Efficiency of the CMT method was assessed using a large battery of language and reading tests as well as other psychometric tests focusing on rhythm, auditory attention, visuo-spatial attention, sequential visual processing, phonological awareness, speed and quality of reading, audio-vocal loop in working memory. Moreover, the identification and discrimination tasks as well as the syllabic duration task used in Experiment 1 were also presented here. The tests were performed four times: at T1, 6 weeks before the start of the workshops; at T2 and T3, just before and just after the end of the workshops, respectively, and at T4, 6 weeks after the end of the workshops. Due to technical problems, the categorical perception and syllabic duration tasks were only performed twice, at T2 and T3 that is, just before and after CMT training.

## Language and Cognitive Tasks

Three tasks were selected from the NEPSY II Battery ("A Developmental NEuroPSYchological Assessment"; Korkman et al., 2012).

Four tasks were chosen from the BALE battery ("Batterie Analytique du Langage Ecrit"; http://www.cognisciences.com) that allow testing for reading, spelling, and meta-phonological skills in French.

Finally, three standardized task were used to test for reading abilities, rhythm reproduction and writing.

## Data Analysis

To allow for comparisons with Experiment 1, repeated measures ANOVAs were conducted for the categorical perception tasks that included Position or Pair and Session (T2 vs. T3) as within-subject factors. Fischer's PLSD were used for posthoc comparisons. For the syllabic duration task, the ANOVA included Condition (normal vs. lengthened syllables) and Session (T2 vs. T3) as within-subject factors. Student t-tests were used for pre vs. post-test comparisons in the other tests. When possible, scores were transformed into standard deviation units from the norm (as provided by authors of the tests). Means, standard deviations and significance level for each individual measurement are reported in **Tables 3**–**5**. When relevant, effect sizes are also reported as Cohen's d (Cohen, 1988; Soper, 2015). Finally, in order to correct for multiple comparisons and considering that <10 independent planned comparisons were computed, the significance level was set at p < 0.01 rather than p < 0.05.

## Results

### A- Categorical Perception and Syllabic Duration Tasks

#### **Categorical perception**

For the identification task (**Figure 3A**), results revealed that both the main effect of Position and the Session × Position interaction were significant [F(1, 11) = 35.58, p < 0.001 and F(8, 88) = 2.50, p < 0.01, respectively] but the main effect of Session was not significant (F < 1). Post-hoc comparisons showed that the improvement from T2 to T3 was significant for positions B5 and B6 (i.e., around the phonemic [ba]-[pa] boundary with p < 0.03 and p < 0.004, respectively).

For the discrimination task (**Figure 3B**), the main effect of Pair was significant [F(1, 11) = 4.46, p < 0.001] and the main effect of Session was marginally significant [F(1, 11) = 2.88, p < 0.11]. The Session × Position interaction was not significant [F(7, 77) = 1.39, p = 0.21]. However, post-hoc analyses revealed that the improvement from T2 to T3 was significant for the B4/B5 pair (p < 0.02) and for the B5/B7 pair (p < 0.004).

#### **Syllabic duration task**

The main effect of Condition was not significant [F(1, 11) = 1.50, p = 0.24] so that lengthened words were not processed differently than normally spoken words. The main effect of Session was only marginally significant [F(1, 11) = 2.42; p < 0.14]. The Session × Condition interaction was not significant (F < 1) and post-hoc analyses also revealed marginal improvements between T2 and T3 for both normally spoken words (p = 0.10) and words with syllabic lengthening (p = 0.08).

## B- Attentional Processing of Speech and Non Speech Stimuli

#### **Auditory attention**

Results for the two auditory attention subtests from the NEPSY battery showed that total performance (t = −5.72, p < 0.001) and performance in both subtests (A: t = −6.35, p < 0.001) and (B: t = 4.25, p < 0.01) were improved from T2 to T3 with no decrease from T3 to T4 (all p > 0.15) and with no difference between T1 and T2 (all p > 0.70; see **Table 3**).

### **Visuo-spatial attention**

No significant improvement was found from T2 to T3, but performance improved from T1 to T2 when children received no treatment (T1-T2: t = 3.77, p < 0.003; see **Table 3**).

### **Digit repetition task from the battery BALE**

No significant improvement was found whatever the period considered (all p > 0.30, see **Table 3**).

#### **Reproduction of motor rhythmic sequences**

No significant differences were found whatever the period considered (all p > 0.10, see **Table 3**).

#### C- Phonological and Reading Tasks

#### **Pseudo-word repetition**

Results showed improvements from T2 to T3 (t = −2.56, p < 0.026), no decrease from T3 to T4 (p > 0.15) and no difference between T1 and T2 (p > 0.80, see **Table 4** and **Figure 4**).

#### **Reading in 1 min (Khomsi test)**

Results showed improvements from T2 to T3 (t = −5.59, p < 0.001) with no significant decrease from T3 to T4 (p > 0.80) and no significant difference between T1 and T2 (p > 0.20, see **Table 4**).

Children' levels of performance were measured four times (T1, 6 weeks before CMT started; T2, just before CMT; T3, just after CMT; T4, 6 weeks after CMT ended). Mean and standard deviation or s.d. from norms (when indicated) for each task are reported. Student T-tests and p-values were computed; significant improvements are in bold (\*\*\*p < 0.001; \*\*p < 0.01). Effect sizes are also reported when relevant (Cohen's d).

Children' levels of performance were measured at T1 (6 weeks before CMT started) at T2 (just before CMT), at T3 (just after CMT), and at T4 (6 weeks after CMT ended). Mean and standard deviation or s.d. from norm (whenever indicated) are reported for each task. Student T-tests and p-values were computed and significant improvements are in bold (\*\*\*p < 0.001; \*\*p < 0.01; \*p < 0.05). Effect sizes are also reported when relevant (Cohen's d).

#### **Phoneme fusion (BALE)**

Results showed an improvement from T2 to T3 for accuracy (t = −2.90, p < 0.01), with only a tendency for speed (t = 1.94, p = 0.07). No decrease was found from T3 to T4 whether for accuracy or for speed (all p > 0.40) and no difference was found between T1 and T2 (all p > 0.30; see **Table 4** and **Figure 4**).

#### D- Visual and Writing Tasks

#### **Comparison of letter strings (BALE)**

The improvement from T2 to T3 was significant for speed (t = 3.41, p < 0.006) but only marginally significant for accuracy (t = −1.78; p = 0.10). No significant decrease was found from T3-T4 (p > 0.40 in both cases) and no significant difference between T1 and T2 (p > 0.20 in both cases, see **Table 5**).

#### **Contour discrimination (BALE)**

The improvement from T1 to T2 was significant (t = 2.55, p < 0.03) with no change from T2 to T3 or from T3 to T4 (see **Table 5** and **Figure 5**).

#### **BHK (writing)**

The improvement from T3 to T4 was marginally significant (t = −2.17, p < 0.05) with no change from T2 to T3 or from T1 to T2 (p > 0.15, see **Table 5**).

#### TABLE 5 | Visual and writing abilities.

Children' levels of performance were measured at T1 (6 weeks before CMT started) at T2 (just before CMT), at T3 (just after CMT), and at T4 (6 weeks after CMT ended). Standard deviation from norm for each task are reported. Student T-tests and p-values were computed and significant improvements are in bold (\*\*p < 0.01; \*p < 0.05). Effect sizes are also reported when relevant (Cohen's d). n.a.: not available.

syllables [pa] and [ba] within a 9-step acoustical continuum. The hit rate was significantly higher after than before 6-week of CMT for B5 and B6. (B) Discrimination: The hit rate is significantly higher for B4/B5 and B5/B7 pairs (i.e., around the categorical boundary) after than before CMT. \*p < 0.05; \*\*p < 0.01.

Finally, correlational analyses between the different tasks did not reveal any significant results when the significance level is set at p < 0.01.

## Discussion

significant).

The first aim of Experiment 2 was to determine whether results similar to Experiment 1 would be found when CMT was spread over time. The second aim was to assess whether or not this effect also extended to standardized psychometric tests known to be sensitive to learning difficulties encountered by children with dyslexia. Overall, these two objectives were reached. As in Experiment 1, results revealed improved categorical perception of syllables after the period of CMT (significant Session × Condition interaction in both experiments). While improvements were found both for the quality of intracategorical perception and for inter-categorical boundary in Experiment 1 (i.e., at B2, B6 and B9), the improvement was mainly found for inter-categorical boundary in Experiment 2 (i.e., at B5 and B6). Nevertheless, in both experiments and in line with previous results in younger and older adults (Bidelman et al., 2014), music training seemed to positively influence categorical

perception in children with dyslexia. Turning to the perception of syllabic duration, the Session by Condition was marginally significant in both experiments. While the effect of CMT was larger for lengthened than normally spoken words in Experiment 1, the perception of both types of words was marginally improved after the CMT in Experiment 2. Thus, overall results were similar in both Experiments, showing that the CMT program positively influenced categorical perception and the temporal aspects of speech processing. Importantly, these effects were found in Experiment 2 when the CMT program was spread over time and, consequently, more compatible with standard speech therapy practice.

Results of standardized psychometric tests showed that several aspects of the children's behavior that were directly targeted by the CMT program specifically improved during the period of music training. This was clearly the case for auditory attention, pseudo-word repetition, reading words in 1 min, phonological awareness (phonemes fusion), and comparison of letter strings. Specifically, for auditory attention, results showed almost 15% gain in selective attention, 10% in divided attention, and 20% in total score from T2 to T3. Importantly, these improvements persisted in the following period without further training (from T3 to T4: no significant decrease in level of performance). Turning to the reading tests that were probably the most interesting due to their strong relationship to academic performance, the improvement after CMT was almost one standard deviation from the norm, moving from a score lower to -2 s.d. to nearly -1 s.d. from controls scores. Similar to results for auditory attention, pseudo-word repetition and phoneme fusion (scores), these reading improvements persisted unchanged for 6 weeks after the end of the CMT period, thereby pointing to the durability of the CMT program.

Equally important, the effect of the CMT program was not significant between T2 and T3 on the control variables for which we did not a priori predict an effect of this type of treatment, such as visuo-spatial attention, contour discrimination, and writing efficiency. However, some effects, such as the significant improvement between the untrained period from T1 to T2 for visual attention and contour discrimination and from T3 to T4 for writing efficiency, were unexpected and may result from mere repetition effects. They need to be replicated and examined in further experiments. More surprisingly in view of several results in the literature showing strong links between rhythmic and linguistic abilities (Overy, 2000, 2003; Przybylski et al., 2013; Slater et al., 2013; Bishop-Liebler et al., 2014; Flaugnacco et al., 2014; Weiss et al., 2014) and in view of the strong focus of the CMT program on the temporal association between sensory input and motor activities, we found no significant improvements in memory span and in the rhythm reproduction tasks. While these null findings are difficult to interpret, it may be that the specific rhythmic test used here was not best adapted to capture potential improvements or that training temporal processing may generalize to other cognitive functions without perceptible improvement on the trained function itself. Finally, correlational analyses between the different tasks did not reveal any significant results.

## GENERAL DISCUSSION

Overall, our results provide convincing arguments in favor of using musical rehabilitative materials with children with dyslexia. The different aspects of the CMT program were specifically designed to improve sound perception, multiple aspects of temporal processing, and the integration of information from different sensory and motor modalities. In this respect, further experiments are needed to try disentangling the effects of these different components or, at least, to specify the weight of their respective contribution. Moreover, other characteristics of the training were: progressive learning, repetition of exercises, multiple modalities, and small-group workshops. Altogether, our results are in line with the repeated and longstanding observation from teachers, clinicians and scientists, that music in general, and perhaps more specifically learning an instrument, interfere positively with basic scholastic skills. Reading is the area that has been most directly tested probably as the most likely to have a direct impact on academic success. It was thus encouraging to find a significant impact of the CMT on reading ability.

The model most often put forward to account for a possible effect of music on cognitive development, specifically the acquisition of reading, calls upon a possible analogy between music and language. Many authors, most notably Patel (2003, 2011), have discussed this point, noting, in particular, that music and speech share many features such as the sequence of sounds, an alphabet that represents them, and a specific syntax. Patel (2011) hypothesized that music leads to adaptive brain plasticity of the same neural networks which are otherwise involved in language processing. More recently, it has been proposed to rather conceive music and language as sharing common cognitive ressources, especially attentional and memory ressources which could be equally recruited by music and language (Rogalsky et al., 2011; Perruchet and Poulin-Charronnat, 2013).

Concerning more specifically the topic of dyslexia, our results stand in favor of a role of music training in improving the phonological deficit widely recognized as causal to the reading problems (Ramus, 2004), although others have questioned such an interpretation (Morais et al., 2010). In an influential theory of the mechanism underlying dyslexia, Goswami (Goswami et al., 2002, 2013) proposed that the dyslexics' cognitive system is specifically unable to process stimuli occurring at a frequency (frequency modulation) of the order of 2–10 cycles per second, which is the approximate frequency of syllables. As a consequence, dyslexics encounter difficulties capturing the segmental features of words and phrases. Thus, a developmental defect in processing the amplitude envelope of speech could lead to defective development of the phonological system in aspects related to the pace and patterns of intonation (prosody). In fact, children with dyslexia have been found to perform poorly on tasks of rhythmic perception and perception of musical meter (Huss et al., 2011). These observations have led researchers to propose rhythmic stimulation as a treatment for these aspects of the dyslexic deficit, and by extension, for the dyslexic disorder itself (Flaugnacco et al., 2015).

One of the strongest effect of the CMT program was on the attentional tests, in particular, the two subtests of the NEPSY auditory attention battery assessing selective and divided attention. An overall improvement of 20% over the 6 weeks of training is a successful outcome, in particular since this effect persisted after a 6 weeks untrained period. A recent brain imaging study (Heim et al., 2015) showed that dyslexics who received three different types of remediation (based on phonology, on attention, or on reading training) ultimately had similar pattern of improvement in terms of brain activation (specifically, an increase in activity in the lower left temporal region). It is thus conceivable that the improvements we have seen in our study on reading and phonology tasks are epiphenomenons, reflecting an impact on the attention system. We could not, however, find evidence of any correlations between the degree of improvement in phono-lexical tasks and attentional tasks. While the improvement was significant on tests of auditory attention, no significant changes were found on tests of visual attention, contrary to what one might expect if the CMT effect was operating through general attentional mechanisms. The fact remains that a positive effect on attention certainly contributed to the overall improvement even if the multi-faceted aspects of the CMT program preclude from concluding that this was the sole factor responsible for the improvements.

The cross-modal aspects of the CMT program may account for the effects found for tasks requiring sharing information between different modalities, such as reading and sequence comparison of letters as well as the phonological task, if one considers that such tasks require mandatory exchanges of information between the acoustic representation of phonemes that can be stored in auditory regions of the left temporal lobe, and the lower frontal areas, involved in phonological processing (Boets et al., 2013). Similarly, categorical perception also probably requires the involvement of structures such as the left frontal premotor areas that was found to be activated in dyslexics during a categorical perception task in a functional MRI experiment (Dufor et al., 2009). Finally, studies of brain plasticity in non musicians have shown that music training may have the largest effects on brain anatomy and function when it combines sensory and motor training (Lappe et al., 2008, 2011). The recent literature on dyslexia and related learning deficits converge to show that the main structural differences in the brains of dyslexics compared to standard brains lie in the nature, integrity and directionality of certain hemispheric white matter bundles. These differences are present before learning to read (Saygin et al., 2013) and therefore can not be the result of a lack of experience with written language (although this may contribute as shown by studies of illiterates: Thiebaut de Schotten et al., 2014). These association bundles are also altered in musicians, both instrumentalists and singers (Halwani et al., 2011) and change in children after only a few months of musical training (Hyde et al., 2009). Although DTI is often regarded as a very indirect measure of white matter integrity (Jones et al., 2013), it remains that the same white matter bundles considered as the hallmark of the dyslexic brain are modified by musical training. Although strictly speculative, this observation deserve future investigation.

Using fMRI, Blau et al. (2009) have shown that dyslexics are characterized by poor integration of oral and written codes of the same phoneme. When these codes are congruent, temporal areas are less activated by combined visual-auditory processing than in controls; when the oral and written codes are incongruent, temporal areas are more strongly activated than in controls. An interpretation in terms of aberrant crossmodal integration can also potentially explain other clinical conditions such as dysgraphia, in which children hardly associate phonemes with their written form, or dyscalculia, in which they hardly relate numerical terms with the mental representation of the corresponding quantity (Noël et al., 2013).

Finally, we shall consider some of the potential caveats of the present study, specifically the absence of a control group, trained for comparison with another, already proven training method comparable in duration and cognitive load. Besides the obvious difficulty of finding such an ideal comparison group, our training protocol in Experiment 2 partly fulfills this objective, providing evidence for the selectivity of improvements, at least for some tasks, during the training period (T3 vs. T2) compared to the non-trained period (T2 vs. T1). Thus, potential motivational bias (so-called Hawthorne effect) can reasonably be ruled out by this design. Overall, we remain convinced that intra-subject approaches and disease progression models could be more convenient than larger samples for building comparison groups (since it is often difficult to recruit large samples in clinical settings). By having a pre-test/post-test design, we examined group improvement within subjects rather than between-subjects. With a lower number of individuals, this may have resulted in more extraneous effects due to individual differences. A second weakness is that improvement of specific cognitive mechanisms can not be distinguished from a purely attentional effect. In face of the consistency of improvement on attentional variables, the possibility of an exclusive or largely predominant impact of attention on executive processes can not be ruled out. Further experiments are needed to compare our results to the effect of a strictly attentional training protocol.

## CONCLUSION

In a recent yet already acclaimed book, suggestively entitled "The Dyslexia Debate," Elliott and Grigorenko (2014), two eminent specialists of the topic, provided arguments questionning the usefulness, or even reality, of the concept of dyslexia. This is based on the observation that various theories are proposed in the literature, none of them being entirely satisfactory and that most of the existing remediation methods are pedagogic rather than properly therapeutical. Accordingly, our conviction is that although the reality of a biological entity is indeed unquestionable, the multifaceted and kaleidoscopic clinical appearance of dyslexia, as suggested by the recent changes made to the DSM classification (APA, 2013), may lead to consider using multiple-component treatments, such as the ones offered by music training, rather than focusing on one single cognitive mechanism as in classical phonological training methods.

Music training may provide an ideal tool for such a new perspective: it allows considering each one of the multiple facets of dyslexia as a potential target to be improved. In this respect, music training may be one of the most complete and rational ways of treating dyslexia. Whatever the exact mechanism(s) subserving the observed improvements, their occurrence after relatively short sessions of musical training opens interesting avenues for future research as well as practical applications. First, our results suggest that several cognitive functions, including reading but not only, may be improved by adding a musical content to classical speech therapy and remediation of dyslexia.

## REFERENCES

Our view is that such training could usefully complement more classical methods, in particular when they have been used extensively but children still need reeducation. Second, as others have also noted (Heim et al., 2015), the improvement may depend upon two main features of the CMT method; an intensive training and that this training is given collectively to small groups of children. Finally, our results open new avenues for future research. For instance, it would be of interest to include recording of electrophysiological or neuroimaging data, to assess the brain changes underlying the observed improvements. Also, direct comparisons with other remediation methods could provide important additional understanding of the exact nature of the improved processes, for example by comparing musical training to more specific attentional or phonological training. Finally, testing the hypothesis of impaired connectivity in other neurodevelopmental disorders such as dyscalculia (Srinivasan and Bhat, 2013) would certainly contribute to enrich the "The Dyslexia Debate" (Elliott and Grigorenko, 2014).

## ACKNOWLEDGMENTS

The authors acknowledge very gratefully the participation of children and teachers from two elementary specialized schools: Carnot Public School in Toulon and Sainte-Marie Madeleine private school in Marseille. This study was made possible thanks to funding from the Labex "Brain and Language Research Institute" (BLRI; ANR-11-LABX-0036) and support from the foundation Resodys.

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language areas in children with dyslexia. Neuroimage 54, 2426–2436. doi: 10.1016/j.neuroimage.2010.10.002

**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2016 Habib, Lardy, Desiles, Commeiras, Chobert and Besson. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Musical plus phonological input for young foreign language readers

#### M. C. Fonseca-Mora<sup>1</sup> \*, Pilar Jara-Jiménez <sup>2</sup> and María Gómez-Domínguez <sup>1</sup>

<sup>1</sup> English Language Department, University of Huelva, Huelva, Spain, <sup>2</sup> Department of Developmental, Educational and Social Psychology and Methodology, Jaume I University, Castellón, Spain

Based on previous studies showing that phonological awareness is related to reading abilities and that music training improves phonological processing, the aim of the present study was to test for the efficiency of a new method for teaching to read in a foreign language. Specifically, we tested the efficacy of a phonological training program, with and without musical support that aimed at improving early reading skills in 7–8-year-old Spanish children (n = 63) learning English as a foreign language. Of interest was also to explore the impact of this training program on working memory and decoding skills. To achieve these goals we tested three groups of children before and after training: a control group, an experimental group with phonological non-musical intervention (active control), and an experimental group with musical intervention. Results clearly point to the beneficial effects of the phonological teaching approach but the further impact of the music support was not demonstrated. Moreover, while children in the music group showed low musical aptitudes before training, they nevertheless performed better than the control group. Therefore, the phonological training program with and without music support seem to have significant effects on early reading skills.

#### Edited by:

Mireille Besson, Institut de Neurosciences Cognitives de la Méditerranée, France

#### Reviewed by:

L. Robert Slevc, University of Maryland, College Park, USA Sylvain Moreno, University of Toronto/Baycrest Hospital, Canada

#### \*Correspondence:

M. C. Fonseca-Mora, Faculty of Humanities, Avda. Tres de Marzo, 21071 Huelva, Spain<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Cognitive Science, a section of the journal Frontiers in Psychology

> Received: 22 July 2014 Accepted: 27 February 2015 Published: 17 March 2015

#### Citation:

Fonseca-Mora MC, Jara-Jiménez P and Gómez-Domínguez M (2015) Musical plus phonological input for young foreign language readers. Front. Psychol. 6:286. doi: 10.3389/fpsyg.2015.00286 Keywords: phonological awareness, literacy, foreign language, reading, working memory, music

## Introduction

A large amount of literature has been published on reading acquisition difficulties in native (L1) or in second language (L2) learning. Several factors, such as phonological and decoding skills have often been described as variables of crucial importance in the learning-to-read process (Brady, 1991; Melby-Lervåg et al., 2012). In their review, Hulme and Snowling's (2014) conclude that deficits in oral language skills as well as deficits in phonological language skills and problems in phoneme awareness, letter–sound knowledge and rapid automatized naming are of primary importance to account for learning to read difficulties. Jongejan et al. (2007) also considered that phonological language skills are important for L1 and L2 acquisition as they provide the necessary tools for lexical access and reading. The lack of oral language input in L2 acquisition is problematic when the pronunciation rules of L1 differ from L2. In this context, finding alternative research-based teaching approaches that could help learners to achieve foreign language literacy skills is very relevant.

Several results in the last two decades points to music as an aid in learning to read (Butzlaff, 2000; Bolduc, 2008; Standley, 2008; Lessard and Bolduc, 2011; Toscano-Fuentes and Fonseca-Mora, 2012) but the nature of this connection still needs to be clarified. Ott et al. (2011) suggest that early phonetic processing of verbal or non-verbal stimuli is differently organized depending on musical expertise. Patel (2011) proposes the OPERA hypothesis with 5 factors that may account for the influence of instrumental music training on brain plasticity and on shared speech processing networks: Overlap in acoustic features in instrumental music and speech; Precision due to the higher demands of music; Emotion, Repetition and focused Attention. Christiner and Reiterer (2013) consider vocal music, singing, as a 'good indicator of the ability to remember new and unintelligible utterances' and conclude that the ability to sing improves auditory memory span. In their review of electrophysiological studies of speech segmentation, Schön and François (2011) conclude that musical expertise facilitates the learning of both linguistic and musical structures. Similarly, Schön et al. (2004) and Marques et al. (2007) demonstrate that musical training increased pitch discrimination in both music and language. Most importantly, children who are more sensitive in discriminating sounds due to music training are better on phonological awareness and reading tests (Lamb and Gregory, 1993; Douglas and Willats, 1994; Anvari et al., 2002; Peynircioglu et al., 2002; Bolduc and Montésinos-Gelet, 2005; Gromko, 2005; Forgeard et al., 2008; Moreno et al., 2009; Degé and Schwarzer, 2011; Herrera et al., 2011; Moritz et al., 2012).

Similarly, the four meta-analyses of Butzlaff (2000), Bolduc (2008), Standley (2008), and Lessard and Bolduc (2011) that reviewed more than 70 different multidisciplinary studies also point to a relationship between musical training and reading skills, mainly reading in L1. Butzlaff's meta-analysis reviewed 24 correlational and 6 experimental studies. The author concluded that results strongly and reliably associate music performance with standardized reading/verbal tests but that the causal nature of the relationship remained to be demonstrated. For instance, the influence of a factor such as teachers' expectancy could not be ruled out. Bolduc (2008) reviewed 13 studies and concluded that emergent literacy of preschoolers with or without learning difficulties is affected positively by musical instruction. Standley (2008) reviewed 30 studies related to musicrelated reading instruction and specific reading skills in order to make pedagogical recommendations about reading failure. The author differentiated two main music education styles underlying these studies: on the one hand, studies including multisensory programs based on Orff, Kodály, or Dalcroze methods that focus on singing, rhythm, instrument playing, or movement to music, and on the other hand, those that rely on extensive practice in choral, band, or orchestral ensembles. Although, the studies in general indicated benefits for reading, the great diversity of intervention programs and of variables such as age and motivation did not allow to draw firm conclusions, except that the younger the child, the stronger the gains from music interventions. According to this analysis, "Music activities that incorporate specific reading skills matched to the needs of children at-risk for reading difficulties (as well as special education, ESOL, early intervention) will enhance reading instruction" (Standley, 2008, p. 29). Finally, Lessard and Bolduc (2011) analyzed 17 studies that added evidence to the link between musical learning and reading among first to third graders. However, causality was not demonstrated due to differences between musical intervention programs, musical, and reading skills, sample sizes and also that many of these studies were unpublished works (doctoral dissertations, master thesis, pilot studies).

Turning to L2 acquisition, Fonseca-Mora and Gómez-Domínguez (in press) reviewed 27 experimental, correlational and quasi-experimental studies on music and language reading published between 2001 and 2013 and concluded that only 7.4% referred to L2 learning, thereby indicating a gap in this field. Marques et al. (2007) showed behavioral and electrophysiological evidence that musical expertise influenced the detection of pitch manipulations on sentence-final words in a foreign language. In this review, Chobert and Besson (2013) proposed that musical training may reduce phonological deficits in second language learning.

From an educational perspective, it remains unclear if the benefits for learning to read in L2 are based on general music instruction or on singing musically-supported phonological input matched to specific reading skills (Standley, 2008, p. 29). In a study with 11-year-old Spanish English Foreign Language (EFL) learners, Toscano-Fuentes and Fonseca-Mora (2012) showed that the use of musical-linguistic activities in the foreign language classroom improved reading skills as well as speaking and listening skills. Herrera et al. (2011) discussed the effects of a phonological and a musical plus phonological training program on the reading readiness of native and L2 Spanish-speaking children and stressed that the musical training approach helped native and foreign Spanish learners to outperform those without musical training in the ability to identify word endings, possibly because children's songs make rhyming words particularly salient (Herrera et al., 2011, p. 78). However, preschoolers who received the phonological training program without musical support obtained better results in phonological awareness and naming speed.

Our concern in this study is based on the fact that poor foreign language readers, in this case Spanish learners of English, lack phonological language skills, phoneme awareness, letter– sound knowledge and rapid automatized naming (Hulme and Snowling, 2014). In addition, the Spanish school curriculum does not include musical training. All second-grade Spanish children who participated in this study were very low-proficiency English language learners with classrooms located in suburban schools. This is important as this implies that there was no initial selection of participants. However, socio-cultural background, reading skills and working memory were assessed before training to ensure that the different groups were homogenous. Learners' musical aptitude was also tested as it has been described as an individual difference in language learning (Slevc and Miyake, 2006).

### Purpose of the Current Study

Based on previous studies showing that phonological awareness is related to reading abilities and that music training improves phonological processing, the aim of the present study was to test for the efficiency of a new method for teaching to read in a foreign language. Specifically, we aimed at testing the efficacy of phonological training programs, with and without musical support that aimed at improving early reading skills in 7–8-year-old Spanish children learning English as a foreign language (EFL). Of interest was also to explore the impacts of these training programs on working memory and decoding skills. To achieve these goals we tested three groups of children: a control group, an experimental group with non-musical intervention (active control), and an experimental group with musical intervention.

A video was selected in both experimental groups to teach early reading skills such as the alphabetic principle, phonological awareness and phonics. The musical experimental group was taught through video-clips that included musical elements such as songs with lyrics. The non-musical experimental group (or active control group) received the same phonological training program as the musical group but the program did not include melodies. The control group was taught in the traditional way without specific phonological awareness training nor musical support.

We hypothesized that the level of performance would be higher for teaching approaches that included phonological training with or without musical support than for traditional teaching methods. Moreover, we also hypothesized that musical support in a phonological training program for beginner EFL students would be an added value when learning to read because simple, rhythmic and repetitive melodies may induce the song-stuckin-my-head phenomenon, a rehearsal loop that may improve sub-vocal rehearsal. The songs, created especially for improving phonetic aspects, were characterized by their slow pace and by the simplicity of their melodic contours. They were easy to memorize and, if activated periodically, they could favor automatized decoding. Finally, to determine the effects of the pedagogical intervention, pre/post tests and regression analyses including knowledge of sounds and letters, reading fluency and their interaction with working memory were computed.

## Materials and Methods

## Participants

A pre-post comparison design was used to examine training effects. Three second grade classes including 63 students (X = 7.6 years old, SD = 0.4; 29 boys and 34 girls) were selected from two primary schools located in the same school district. Mean age between the three groups was not significantly different (F < 1) nor were the gender differences [χ 2 (2, 63) = 1.97, p = 0.374]. At the beginning of the study, the music experimental group (n = 18) comprised 8 females and 10 males (mean age: X = 7.71, SD = 0.40). The non-musical experimental group (n = 22) comprised 11 females and 11 males (mean age: X = 7.58, SD = 0.35) and the control group (n = 23) comprised 15 females and 8 males (mean age: X = 7.67, SD = 0.51).

### Procedure

Prior to the beginning of the study, the school community was informed, organizational aspects were discussed and formal consent was granted. The control group and the non-music experimental group (with phonological training) were located within the same school. The music experimental group was located in a different school to avoid contamination if learners would sing the learned melodies in the playground. Teachers of both experimental groups were trained for several weeks before the start of the experiment. During the 2 weeks prior to the beginning of the training period, trained language graduate assistants and graduate assistants in psychology (supervised by a neuropsychologist and two language researchers) tested the musical abilities, early reading skills, working memory and socio-cultural level of the 63 learners individually in a quiet room at their school. Immediately after the 11-week training period, reading skills and working memory of the young learners were tested again.

## Questionnaires

A battery made up of four questionnaires was used:

## Training Program (Experimental Groups)

Children in both training programs received two 1-h sessions per week, for a period of 11 weeks and a total of 22 sessions. Video-clips were used in both training programs to help learners attach meaning to the minimal units of discursive articulation. Activities focused on the development of phonological awareness and phonics (e.g., auditory exercises that emphasized alliteration, word-onset awareness, and initial sound identification in frequent English words). Other activities focused on the learning of the alphabet (e.g., English letter-names and lettersounds). The teacher in the music group used videos supported by songs with subtitles, characterized by simple and repetitive melodies and rhymes (Gértrudix Barrio and Gértrudix Barrio, 2010). Children in this group were trained in song perception and production and they were encouraged to sing the material learned in the hope that the catchy songs would foster selfinitiated rehearsal. Children in the non-musical group worked on the same reading skills and contents but through attractive and colorful videos, posters, and audio-books without music. Both teachers planned together and simultaneously their lessons so that they were teaching the same thematic units at the same time.

#### Fonseca-Mora et al. Musical plus phonological input

#### Phonological Training Program

The phonological training program included the following tasks that were supported by visual materials (e.g., posters and flashcards):

#### Practicing with Single-Letter Sounds

Children learned the names and sounds of the letters of the English alphabet. Letter-names and letter-sounds were presented using videos, posters, and audio-books in in the non-musical group, and using songs and subtitles the music group.

To establish a relationship between letters and sounds, frequent one-to-three syllable words were spelled and pronounced at the same time the songs and non-musical videos were played. Every word with a common spelling and phonetic pattern was classified into different word-bank lists written on a board. For example, words with the same middle sound as "book" (/u/ sound:book, foot, look, food) or those with the "ph" grapheme (/f/ sound: elephant, phone, dolphin) were included in the same list. This task was used for students to automatize graphemesphonemes matching as well as English pronunciation, structures, and rules. Most of the tasks were designed to foster learners to use their auditory discrimination and production skills, such as:

(a) Onset and rime detection tasks: learners were asked to identify initial and final phonemes in words. For example, "What is the first sound in the word 'fish'? or 'What is the last sound in 'fox'?"

Phonological oddity tasks were also included in which learners were asked to spot the odd word out when listening to three different words, two of them sharing the same initial phoneme (e.g., "which word begins with a different sound: jam, yoghurt, juice?").

(b) Oral blending skills, manipulation of sounds in words and word formation tasks when learning and reading new words. Learners were required to change the initial sound of a word to create a new word. For example, to change the initial sound of the following words (hen, hill, hat, hot, hump) to /p/ or to choose which words could be made with the following initial phonemes: c, b, l, f, v, h, j. Tasks that required learners to change the middle vowel in a word to another that had the same sound to find out the correct spelling that matched a picture presented on a flashcard ("jamper or jumper?," "mauth or mouth?," "food or fud?").

#### Phonics and Spelling

Word choice tasks based on spelling were also instructed: learners made words using various combinations of vowel and consonant letter-cards, putting them on a board for all students to see. Sound matching tasks based on blending words onset graphemes and ending phonemes (rimes), using "the phonic wheel," were to improve learner's spelling skills.

### Traditional Program (Control Group)

The traditional teaching program was based on the idea that phonological decoding skills are learned from direct exposure to foreign language and transfer directly from L1. The teacher used the syllabic and global word approach as classically described in L1 textbooks. The curriculum for teaching English to second graders mainly included vocabulary (numbers, colors, food, animals, parts of the house, verbs), some easy verbal routines (greeting, saying good-bye. . . ) and simple sentences such as "I have/not. . . , I like/ I don't like. . . " Flashcards and games were used to help students to increase motivation for the English lesson.

#### Data Analysis

One-Way repeated measures Analyses of Variance (ANOVAs) were conducted to test for before training differences in sociocultural factors and musical aptitude between groups. Moreover, ANOVAs were also computed to test for differences before and after training that included Group (Control, musical, and nonmusical) as well as Session (pre vs. post training) as factors. Finally, multiple regression analyses with interactions (Aiken and West, 1991; Rosel et al., 2014) were also conducted to test for the effects of the training program in the experimental and control groups. Data analysis was performed using the 21.0 SPSS statistics package.

To determine whether the intervention produces different effects in the 3 groups (non-musical experimental, musical experimental, and control groups), an ANCOVA was conducted on the differences between groups after training, controlling for the level of performance before training (i.e., "prior knowledge") for each one of the three tasks. In addition, we computed a regression analysis for each one of the three tasks. Reading variablespre, WMpre and the interactions with the Group factor (musical, non-musical, and control) were included.

## Results

#### Before Training

The three groups were homogeneous regarding their sociocultural background (see **Table 1**). Learners' musical aptitude was also homogeneous within the three groups before training, with a normal distribution [Kolmogorov-Smirnov's test: K-S = 0.622, p = 0.834 and Levene(2, 60) = 0.495, p = 0.612]. However, results revealed significant differences between groups [F(2, 60) = 14.175, p < 0.001]: mean scores in the non-musical experimental (NME) group (X = 27.2, Sd = 3.7) were significantly higher than in the control group (Cont: X = 22.6, Sd = 3.2;

TABLE 1 | Test for between groups differences on socio-cultural variables.

Bonferroni = −4.62, p < 0.01) and in the musical experimental group (ME: X = 21.3, Sd = 4.4; Bonferroni = −5.89, p < 0.01), with no significant differences between the control and musical group (Bonferroni = 1.27, p < 0.855).

Working memory (WM) data showed a normal distribution (K-S = 0.495, p = 0.967), but this was not the case for "Correct Letters read in English" (K-S = 4.069, p < 0.001), "Initial Sound Identification" (K-S = 1.021, p = 0.021) and "Correct Words Read in a Dialog in English" (K-S = 3.659, p < 0.001). Non-significant differences were found between the three groups [F(2, 60) = 0.55, p = 0.58]. The H non-parametric test of Kruskal-Wallis showed no between-groups differences in the "Correct letters read in English" (HK-W(2) = 2.977, p = 0.226) and the "Correct words read in a dialog in English" (HK-W(2) = 5.159, p = 0.076) tasks, but significant differences in the "Initial sound identification" task (HK-W(2) = 6.562, p = 0.038), with higher scores in ME than in NME group (Md<sup>M</sup> = 94, MdN-<sup>M</sup> = 100, 5; UM-<sup>W</sup> = 110, p = 0.016).

In sum, the three groups were similar in terms of sociocultural background and working memory but the non-musical experimental group had significantly higher musical aptitudes than the other two groups and the musical experimental group showed higher scores in the "Initial sound identification" task than the NME group.

#### Before vs. after Training Comparisons

Results of non-parametric Wilcoxon tests for the variables with non-normal distribution were all significant: the level of performance in "Correct letters read in English" (Z<sup>W</sup> − 4.791, p. 001), "Correct words read in English dialogs" (Z<sup>W</sup> − 3.429, p. 001) and "Initial sound identification" (Z<sup>W</sup> − 3679, p. 001) were higher after than before training. By contrast, results for WM (ANOVAs) were not significant [F(2, 61) = 0.001, p = 0.974] and neither was the interaction between Session (WMpre vs. WMpost) and Group [ME, NME and Cont; F(2, 62) = 1.90, p = 0.16]. Thus, we decided to use the results obtained for WMpre to avoid the potential influence of the WISC test on WMpost.

## "Correct Letter Names Read in English" Task

The main effect of Group was significant after training [F(2, 60) = 9.81, p < 0.01, η 2 <sup>p</sup> = 0.247] with a larger effect when "prior knowledge" was controlled for [F(2, 59) = 16.16, p < 0.01, η 2 <sup>p</sup> = 0.354, β = 0.979], explaining 41.5% of the variance (R 2 <sup>c</sup> = 0.415). Planned Bonferroni contrasts revealed that the level of performance increased significantly in both experimental groups compared to the control group (p < 0.01, ICEM-<sup>C</sup> [5.11, 16.56], ICENM-<sup>C</sup> [5.67, 16.44], with no differences between the musical and non-musical experimental groups (p > 0.05, ICEM-ENM [−5.95, 5.50]).

**Table 2** shows the interaction terms between working memory scores in the control group and in the non-musical group through dummy variables, with the musical experimental group as reference. Specifically, the model explained 52.2% variance in number of letters read per minute (R <sup>2</sup> = 0.52). The number of correct letters read was predicted by the combined effect of Group and WM, with significantly lower scores in the control group than in the musical group.

#### TABLE 2 | Regression coefficients for "correct letters read in English" task after training.

As can be seen on **Figure 1**, learners with higher WMpre scores before training improved more in this task with larger improvements in the musical group. After training, the difference between the musical and control group was significant with no difference between the experimental (non-musical and musical) groups.

#### Correct Words Read in a Dialog in English

The main effect of Group was significant after the intervention [F(2, 60) = 5.216, p = 0.008, η 2 <sup>p</sup> = 0.148, β = 0.812]. However, no pre-post differences were found when "prior knowledge" was controlled for [F(2, 59) = 1.018, p = 0.368, η 2 <sup>p</sup> = 0.034]. The model explained 65.6% of the variance (R 2 <sup>c</sup> = 0.656) with confidence intervals at 95% (Bonferroni tests: ICCTR-EM [−3.22, 5.18], ICCTR-ENM [−5.31, 2.36], ICEM-ENM [−6.82, 1.90]).

As can be seen on **Table 3**, scores obtained in both groups, NME group (lower initial value) and Cont group (higher initial value), were based on significantly different initial values than in the ME group. Although, the interaction was not significant, there was a trend for the largest increase in this task to be found

in the NME group (steeper slope), then in the ME group and the slowest evolution to be found in the Cont group. In this case, R <sup>2</sup> = 0.505 is reached.

It can be observed (**Figure 2**) that the non-musical group (lower initial score) and the control group (higher initial score) have significantly different initial values from the musical group. Differences were observed in the intercepts (the value of Y when X = 0).

### Initial Sound Identification

After training, the main effect of Group was significant [F(2, 60) = 3.352, p = 0.042, η 2 <sup>p</sup> = 0.101, β = 0.612]. However, no pre-post differences were found when "prior knowledge" was controlled for [F(2, 59) = 1.47, p = 0.602, η 2 <sup>p</sup> = 0.017]. The model explained 45.3% of the variance (R 2 <sup>c</sup> = 0.453) with confidence intervals at 95% (Bonferroni tests: ICCTR-EM [−1.30, 1.36], ICCTR-ENM [−1.74, 0.81], ICEM-ENM [−1.90, 0.91]. Significance of the interaction terms between working memory and control group scores contrasted with the musical group on the total scores in this task is reported in **Table 4**. In this model R <sup>2</sup> = 0.525 is reached.

As can be seen on **Figure 3**, no improvement was found in the control group. By contrast, the level of performance improved in both experimental groups with higher scores in the musical group. The difference between control and musical group was significant with no difference between the musical and nonmusical experimental groups.

## Discussion

The main objective of this study was to examine the effects of phonological training programs with and without music support on reading abilities in 7–8 year-old Spanish children learning English as a foreign language. A positive outcome would allow us to propose an alternative, research-based, foreign language teaching method. Most studies point to instrumental musical training as an important factor contributing to reading skills (Anvari et al., 2002; Peynircioglu et al., 2002; Bolduc and Montésinos-Gelet, 2005; Gromko, 2005; Forgeard et al., 2008; Moreno et al., 2009; Degé and Schwarzer, 2011; Herrera et al., 2011; Moritz et al., 2012). However, instrumental musical training is often difficult to implement in primary schools when music classes are not included in the curricula. By contrast, singing is often

FIGURE 2 | Working memory and correct words read in a dialog. The number of correct words read in a dialog contains the significance of the working memory score.

TABLE 4 | Regression Coefficients for "initial sound identification in English" post.

practiced in kindergarten and early primary schools. Christiner and Reiterer (2013) pointed out that singing is similar to music at the acoustic-perception level and can also help detecting rhythmic cues in foreign languages. Consequently, singing can contribute to improve speech production and is easier to implement. Thus, rather receiving an instrumental music training, the young foreign language learners involved in this experiment benefitted from a phonological training program based on repeatedly singing rhythmic melodies during the 11-weeks training program.

Results of pre vs. post comparisons showed that children in the musical and non-musical (i.e., active control) training groups performed significantly better than children in the control group regarding the "Correct letters read in English" and the "Initial sound identification" tests. Moreover, a trend was found in the "Correct words read in an English dialog" with larger increase in the non-musical group compared to the musical group and

smallest increase in the control group. Finally, predictive analyses based on regressions with interactions, and taking working memory into account, indicated no significant differences between musical and non-musical groups, both doing better than the control group. These results clearly point to the beneficial effects of the phonological teaching approach but the further impact of the music support was not demonstrated.

Children in the non-musical group performed higher than children in the musical and control groups in the musicality test presented before training. This was possibly linked to these children being from Spanish gypsy families who typically show strong rhythmic abilities (Gil and Azcune, 2012). In this respect, using a longitudinal approach, David et al. (2007) showed that sensitivity to musical rhythm was related to the ability of decoding complex words requiring the use of linguistic stress and they argued that rhythm predicted reading ability from grade 1 to 5 in primary school. Similarly, Moritz et al. (2012) concluded that the rhythmic abilities students developed when they were preschoolers correlated with their phonological abilities in second grade. Thus, the higher level of performance of children in the nonmusical group in both the "correct letters read in English" and the "correct words read in an English dialog" may be linked to English being a stress-timed language (while Spanish is syllabletimed) strongly relying on rhythmic cues. Moreover, early phonetic processing may be organized differently in children with high musical aptitudes, as shown in adults with stronger musical expertise (Ott et al., 2011). In other words, learners with higher musical aptitudes may tend to benefit more from the phonological training program than children with lower musical aptitudes. Importantly, however, while children in the music group showed low musical aptitudes before training, they nevertheless performed better than the control group in the tests described above. Therefore, the phonological training programs with and without music support seem to have significant effects on early reading skills.

Of interest in this study was to examine the influence of working memory and how it interacted with the effects of other factors. Previous reports in the literature have shown that instrumental musical training significantly improved working memory (Ho et al., 2003; Franklin et al., 2008). More recently, Christiner and Reiterer (2013)showed that singing also improved auditory working memory span in Austrian adult singers performing in Hindi. Surprisingly, no such differences between WMpre and WMpost were found in the present study. However, as seen in **Figure 1**, the largest increase in WM scores is found in the music group. Moreover, the higher the scores in WMpre, the larger the increase in "correct letters read" scores after training. This effect was larger in the experimental groups than in the control group with no differences between experimental groups. It may be that the speech sounds as well as the visual and orthographical elements, addressing the phonological loop and the visuo-spatial sketchpad, respectively (Baddeley, 2012), used in the two experimental groups, improved learners' basic reading skills. In addition, and in line with Christiner and Reiterer (2013) results, it may be that the repetitive use of melodies with memorable lyrics allowed young learners to better retain verbal materials and relevant foreign speech sounds. Finally, the lowest level of performance in the control group clearly showed that direct transfer from learners' L1 reading skills to another language should not be taken as granted in the foreign language classroom.

One final aspect that deserves comments is the positive impact of the phonological and musical-phonological programs after a relatively short training duration (11 weeks). This finding is in line with previous results showing significant effects of training after 16, 14, and 4 weeks, respectively in Gromko (2005), Moreno and Besson (2006), and Register et al. (2007). In addition, our results are in line with the conclusions from a metaanalysis conducted by Standley (2008) showing that using music activities that matched the specific reading needs of the children was more important than the duration of training (e.g., training of less than 4 weeks (d = 0.61) were equally effective than training over an entire school year (0.33, p = 0.37). Nevertheless, and in line with previous longitudinal studies over a school year or longer (David et al., 2007; Moreno et al., 2009; Moritz et al., 2012; Chobert et al., 2014), it would be of interest in further experiments to test for the effects of the phonological and phonological plus music training programs on foreign learning abilities when these programs are applied for a longer duration.

## Conclusions

Acquiring good phonological and decoding skills is of uttermost importance for foreign language learners and these abilities are not necessarily directly transferred from L1 knowledge (specifically when L1 and L2 rely on different phonological systems). Nevertheless, these abilities are needed to access lexical content while reading. The phonological training program based on visual support that was used in this study, improved some of the early reading skills in 7–8-year-old Spanish EFL students. Moreover, learners in the phonological plus musical support training program outperformed children in the control group. Thus, simple rhythmic melodies that work as carriers of visual and orthographic perception may stimulate the rehearsal needed for improving specific phonological skills, thereby providing valuable teaching approaches for learning to read in a foreign language.

## References

## Acknowledgments

We would like to thank Dr. Besson, Dr. Arnold and Dr. Herrero for their suggestions. This research was funded by the Spanish Ministry of Science and Innovation [number FFI2010-15738 (subprogram FILO), Music perception and reading skills in foreign language learning project].

Toscano-Fuentes, C. M., and Fonseca-Mora, M. C. (2012). La música como herramienta facilitadora del aprendizaje del inglés como lengua extranjera. Teoría de la Educación. Revista Interuniversitaria 24, 197–213.

**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2015 Fonseca-Mora, Jara-Jiménez and Gómez-Domínguez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

## Engagement in community music classes sparks neuroplasticity and language development in children from disadvantaged backgrounds

## *Nina Kraus1,2 \*, Jane Hornickel1,3 , Dana L. Strait1, Jessica Slater1 and Elaine Thompson1*

<sup>1</sup> Auditory Neuroscience Laboratory, Department of Communication Sciences and Disorders, Northwestern University, Evanston, IL, USA <sup>2</sup> Department of Otolaryngology, Neurobiology & Physiology and Northwestern University Interdepartmental Neuroscience Program, Northwestern University,

Chicago, IL, USA <sup>3</sup> Data Sense LLC, Chicago, IL, USA

#### *Edited by:*

Mireille Besson, Centre National de la Recherche Scientifique – Institut de Neurosciences Cognitives de la Méditerranée, France

#### *Reviewed by:*

Lutz Jäncke, University of Zurich, Switzerland Johannes Ziegler, Université Aix-Marseille, France Sumitava Mukherjee, Indian Institute of Management, India

#### *\*Correspondence:*

Nina Kraus, Auditory Neuroscience Laboratory, Department of Communication Sciences and Disorders, Northwestern University, 2240 Campus Drive, Evanston, IL 60208, USA e-mail<EMAIL_ADDRESS>
Children from disadvantaged backgrounds often face impoverished auditory environments, such as greater exposure to ambient noise and fewer opportunities to participate in complex language interactions during development. These circumstances increase their risk for academic failure and dropout. Given the academic and neural benefits associated with musicianship, music training may be one method for providing auditory enrichment to children from disadvantaged backgrounds. We followed a group of primary-school students from gang reduction zones in Los Angeles, CA, USA for 2 years as they participated in Harmony Project. By providing free community music instruction for disadvantaged children, Harmony Project promotes the healthy development of children as learners, the development of children as ambassadors of peace and understanding, and the development of stronger communities. Children who were more engaged in the music program—as defined by better attendance and classroom participation—developed stronger brain encoding of speech after 2 years than their less-engaged peers in the program. Additionally, children who were more engaged in the program showed increases in reading scores, while those less engaged did not show improvements. The neural gains accompanying music engagement were seen in the very measures of neural speech processing that are weaker in children from disadvantaged backgrounds. Our results suggest that community music programs such as Harmony Project provide a form of auditory enrichment that counteracts some of the biological adversities of growing up in poverty, and can further support community-based interventions aimed at improving child health and wellness.

#### **Keywords: low socioeconomic status/poverty, community music training, electrophysiology, reading, speech, auditory training**

## **INTRODUCTION**

Over 16 million children in the US live in families with incomes below the federal poverty level, with a disproportionate number (68%) being members of minority racial and ethnic groups (Jiang et al., 2014). Parental income, occupation, and education are commonly combined to define a child's socio-economic status [SES (Sirin, 2005)]. A child's SES can interact with other personal factors (race, ethnicity, gender, etc.) to lead to weaker academic achievement (Bradley and Corwyn, 2002; Sirin, 2005; Hernandez, 2011; Skoe et al., 2013) and lower high school graduation rates (Ensminger and Slusarcick, 1992; Bradley and Corwyn, 2002), with lower academic achievement persisting even for low SES students who attend college (Walpole, 2003).

Auditory processing skills, known to be important for language development (Benasich et al., 2002, 2008; Boets et al., 2011; Goswami et al., 2011), may contribute to the link between SES and academic achievement. Children from low SES backgrounds have greater daily exposure to noise (Adler and Newman, 2002; Evans and Kantrowitz, 2002) and tend to be less concerned with using hearing protection in excessively noisy contexts like concerts (Vogel et al., 2007). Chronic noise exposure in children has been linked to weaker reading proficiency and cognitive skills (Maxwell and Evans, 2000; Haines et al., 2001; Clark et al., 2005) and can lead to delayed auditory neural development and greater spontaneous neural activity in animals (Chang and Merzenich, 2003; Seki and Eggermont, 2003; Zhu et al., 2014). Additionally, children from low SES backgrounds hear less complex language and fewer words overall during early language development, which contributes to weaker vocabularies when entering school (Bradley and Corwyn, 2002; Hoff, 2003; Cartmill et al., 2013). Similarly, a host of neural systems important for language, memory, and cognition are impacted by SES background (Raizada et al., 2008; Hackman et al., 2010; Noble et al., 2012), including those implicated in auditory attention (D'Angiulli et al., 2008; Stevens et al., 2009) and speech encoding (Skoe et al., 2013). Encouragingly though, community and home based interventions may reverse these effects; children from low SES families participating in Head Start and attention

training with their parents showed improved language, cognition, and neural measures of auditory attention relative to children in Head Start programs alone (Neville et al., 2013).

Musical training is another avenue of enrichment that may counteract some of the auditory deprivation endemic to low SES environments.   The auditory benefits of music training have direct implications for language skills and academic achievement (Hetland and Winner, 2010; Corrigall and Trainor, 2011; see Tierney and Kraus, 2013 for a review); accordingly, music may serve as an effective training tool for children with learning and attention impairments (Overy, 2003; Bhide et al., 2013; Seither-Preisler et al., 2014).

Community music programs, such as El Sistema and Harmony Project, provide students from low SES backgrounds with music opportunities that enrich the students and their communities. El Sistema, founded almost 40 years ago, provides over 500,000 Venezuelan children with free musical training in their community (for a review of the program, see Majno, 2012). Children are commonly enrolled as young as 2 or 3 years old and are supported through their teen years. Graduates of the program commonly return to teach at their community music center and parents are continually educated by the organization on how to support and encourage their child's music as they advance. Since 2009, 62 El Sistema inspired music programs have been started in the United States. Harmony Project (Los Angeles, CA, USA) similarly promotes the development of healthy children and communities by providing free music training to children from low SES backgrounds in gang-reduction zones of Los Angeles, CA, USA (www.harmony-project.org). Children learn basic music skills in a preparatory class, eventually receive a free instrument to participate in group classes, and have opportunities for performance and ensemble playing throughout their enrollment from early grade school to high school. Between 2010 and 2014, 93% of Harmony Project alumni enrolled in postsecondary education, versus 67.6% of students graduating from public schools within Los Angeles County [most recent data from California Department of Education: Educational Demographics Unit (2008–2009) and Harmony Project Whole Notes 2013–2014 (2014)].

Our laboratory has shown that participation in music training through Harmony Project can reinforce literacy skills, enhance the perception of speech in background noise, and strengthen the neural encoding of speech sounds in children from low SES backgrounds (Kraus et al., 2014a,b; Slater et al., 2014a,b; Kraus and Strait, in press). Here we explore how the extent of student*engagement* in instrumental classes mediates music training's effects on neural speech processing. Although we do not employ an active control group, our aim is to show *within a group undergoing musical training* how engagement may influence the benefits seen for students. Music engagement was defined by a student's percent attendance in class and teacher ratings of classroom participation. We investigated whether greater engagement in music instruction can positively impact the neural encoding of speech. We focused on measures of subcortical brain activity reflecting speech harmonics, the consistency of the response, and spontaneous neural activity, all of which are weaker in teens from low SES backgrounds relative to higher-SES peers (Skoe et al., 2013).

#### **MATERIALS AND METHODS PARTICIPANTS**

Twenty-six children participated in the study (13 males, ages 6 years 11 months – 9 years 3 months; *M* = 8 years 5 months). All children were public elementary school students living in the gang reduction zones of Los Angeles, CA, USA. Participants attended schools where ≥90% of students qualify for free or reduced lunch. Families qualify for free or reduced lunch when their income is below 185% of the federal poverty level (U.S. Department of Education, 2014). The average education of the participants' mothers was 10.7 years (SD = 4.2) and the median and modal maternal educational attainment level was completion of high school/GED. Maternal education is one of the strongest predictors of SES (Hoff et al., 2012), and 76% of children whose parents have a high school degree or less live in low-income families (Jiang et al., 2014). Average maternal education was equivalent across the four Harmony Project sites in which students were enrolled (Kruskal Wallis Test: <sup>χ</sup><sup>2</sup> <sup>=</sup> 6.252, *<sup>p</sup>* <sup>=</sup> 0.100).

Participants were excluded if they had a history of neurological disorders, IQ less than 80 [Wechsler Abbreviated Scale of Intelligence (Woerner and Overstreet, 1999)], previous musical training, or failed a hearing screening (air-conduction thresholds above 20 dB HL for octaves 125–8000 Hz). All procedures were approved by the Northwestern University Institutional Review Board and informed parental consent was obtained for all participants.

### **MUSIC INSTRUCTION**

Students werefollowed as they participated in Harmony Projectfor 2 years. The project curriculum started students in music appreciation class, where they learned pitch-matching and rhythm skills, musical styles and notation, and basic vocal performance and recorder playing. Participants attended these classes twice weekly for 3–10 months (*M* = 5).

As musical instruments became available and students were judged to be ready, they progressed to instrumental instruction. Students were given their own instruments and participated in a mix of group-based instrumental classes for approximately 4 h per week. Students in this study participated in one of four Harmony Project sites. The description of weekly classes at each site and the number of students at each site is presented in **Table 1**. Students played a number of different instruments (viola, cello, bass, French horn, clarinet, or trumpet) and the number of students playing each type of instrument is also reported in **Table 1**. Harmony Project has a standard curriculum for each instrument type (woodwinds, brass, and strings), including rigorous mastery benchmarks required for advancement to the next level of the curriculum. For example, Level 1 benchmarks require students to: demonstrate basic knowledge of music concepts such as rhythm and intonation, exhibit instrument specific skills and knowledge such as proper posture and correct clef identification, and present evidence of commitment through practice at home. As students progress, expectations shift to more instrument specific skills (e.g., proper bowing or breathing techniques) and knowledge and use of dynamics, key signatures and deviations, and articulations (e.g., staccato). Students are required to learn to read music and play from memory throughout the program. All students in the study transitioned to instrument use during their first year, so at the end of their second year in Harmony Project, students had an average of 165 h of school-based instrumental training (SD = 40) and over 210 h of music training overall.

#### *Teacher ratings of music engagement*

At the end of each instrumental class, teachers reported the percent attendance for each student (hours attended/total hours possible) and rated the students on their level of participation in class (1-not at all, 2-little, 3-moderate, 4-fairly good, 5 complete). We averaged percent attendance and teacher ratings of class participation across all the instrumental classes taken by each child over the 2 years. Both attendance and teacher perception of student effort predict 'behavioral engagement' in school, reflecting a student's involvement in the participatory aspects of school (Glanville and Wildhagen, 2007). Because neither percent attendance nor participation were significantly correlated with the number of instrumental classes taken (*p*-values > 0.310), we are confident that higher levels of class participation or attendance reflect student motivation and are not simply artifacts of being enrolled in more classes. Additionally, percent attendance

and participation ratings did not differ across Harmony Project sites (Kruskal Wallis Test: <sup>χ</sup><sup>2</sup> <sup>=</sup> 5.366, *<sup>p</sup>* <sup>=</sup> 0.147; <sup>χ</sup><sup>2</sup> <sup>=</sup> 4.781, *p* = 0.189, respectively), suggesting no rating bias among the sites.

#### **READING ASSESSMENT**

Before enrolling in Harmony Project and after 2 years of Harmony participation, students were administered the Test of Oral Word Reading Efficiency (TOWRE; Torgesen et al., 1999). The TOWRE, a measure of reading fluency, comprises word and nonword reading subtests. Children are required to read a list aloud as quickly as possible and the number of words (or non-words) read correctly in 45 s is tallied and combined to form the Total score.

#### **NEUROPHYSIOLOGICAL MEASURES**

Evoked potentials were collected from the auditory brainstem in response to a 40-ms synthesized speech syllable [da], using an Intelligent Hearing Systems SmartEP system equipped with a cABR module (Miami, FL, USA). Stimuli were presented to the right ear at 80 dB SPL at a rate of 10.9 Hz through electromagnetically-shielded earphones (ER-3A, Etymotic Research, Elk Grove Village, IL, USA). Responses to opposing polarities were subtracted and filtered online from 0.1 to 1.5 kHz in the test session before music training began and from 0.05 to 3 kHz in the test session after 2 years of music training. Due to the differences in filter settings, which were expanded as the longitudinal project evolved, within-subject comparisons over the two test dates are not possible.

Neural measures were those previously shown to index SES (Skoe et al., 2013). Measures of response consistency, speech harmonics, and spontaneous neural activity were generated in MATLAB (Mathworks, Natick, MA, USA). Response consistency reflects the replicability of the response over the first half and second half of the recording on a scale from −1 to 1. Values were Fisher-transformed for analyses, but Pearson's *r*-values are shown in **Figures 1** and **2**. Speech harmonics comprise the average amplitude of the frequency following response over the first-formant range of the stimulus

**Table 1 | Student instrument experience by site and by instrument.**

Participants were enrolled in music classes in one of four sites and played one of seven different instruments. Details about the standard class schedule of each site is included.

(264–656 Hz). Spontaneous neural activity reflects the amplitude of brainstem activity in the absence of the stimulus, and likely reflects neural noise. Please see Banai et al. (2009), Hornickel and Kraus (2013), and Skoe et al. (2013) for additional details.

#### **STATISTICAL ANALYSES**

The relationships among instrumental class attendance, class participation, and neural measures were evaluated at each of the two test dates using Spearman's correlations due to the non-normal distributions of the music engagement variables. Spearman's correlations are more conservative than Pearson's correlations because they reduce the impact of outlying data points and are most appropriate for smaller sample sizes. Similar to Pearson's correlations, Spearman's rho is a

direct measure of effect size, reflecting the proportion of variance in the dependent variable (neural measures) accounted for by the independent variable (music engagement variables). Correlation coefficients with magnitudes of 0.1 are considered small effect sizes, 0.3 medium, and 0.5 large (Cohen, 1992). Reading fluency scores were compared using a paired *t*-test.

#### **RESULTS**

Children who had better attendance in instrumental music classes over 2 years had stronger neural encoding of speech harmonics and better response consistency, two measures previously linked to SES (see **Figure 1**; **Table 2A**). Additionally, there was a positive association between class participation and response consistency (see **Figure 2** for two representative participants

**had stronger neural encoding of speech after 2 years, particularly for measures of speech harmonics and response consistency.** Neural measures before music training began did not predict attendance or level of class participation, suggesting greater engagement in music classes may lead to stronger neural encoding

the average amplitude of harmonic encoding in the frequency following response (μV), Response Consistency is measured as the Pearson's correlation coefficient between response replications (r), and Spontaneous Neural Activity is measured as the root-mean-square magnitude of the pre-stimulus (μV).

**had more consistent neural responses to speech after 2 years. (A)** (red/maroon), a representative subject who had "complete" participation as rated by multiple teachers. The [da] stimulus is plotted in black in top panel of A for reference, shifted in time to account for neural delay. **(B)** (black/gray), a representative subject who had "moderate" participation as rated by multiple teachers. Both students completed four instrumental classes over differ greatly in the consistency of their neural response to speech. After 2 years of music training (bottom), however, the child who participated more in class has a more consistent response to speech than the child who participated less. The two traces in each panel represent the two replications of the response, collected as the recording procedure dictates. The time region of the analysis is marked with vertical hashed lines in each panel.

and **Table 2A**). Interestingly, the least engaged participants in the study still had "moderate" class participation, suggesting that even small variations in student engagement can have implications for success with music training. No relationship was found between music engagement and spontaneous neural activity.

Importantly, our results suggest that greater engagement in music classes predicts stronger speech encoding, not vice versa. Neural measures before music training did not predict subsequent attendance or class participation (*p*-values > 0.126, see **Table 2B**), which suggests that participants with strong speech encoding to begin with did not necessarily go on to be the most engaged students in the study. Additionally, the small variation in years of maternal education did not predict attendance or class participation (ρ = −0.302, *p* = 0.142; ρ = 0.126, *p* = 0.548).

Participants overall showed a subclinical yet statisticallysignificant decline in reading fluency over the 2 years [M1(SD1) = 109.27(12.76), M2(SD2) = 106.04(15.22), *t*<sup>25</sup> = 2.456, *p* = 0.021]. However, change in reading fluency scores was strongly correlated with engagement in instrumental classes. Children who participated more in class were more likely to show an improvement in reading fluency, while those who participated less were more likely to show a decrease in reading fluency (ρ = 0.443, *p* = 0.023).

## **DISCUSSION**

Here we found that greater engagement in group music instruction by children from low SES backgrounds predicted stronger neural encoding of speech for measures negatively influenced by low SES. Children who attended class more regularly and had better classroom participation had stronger neural encoding of speech after 2 years of music training than did their less-engaged peers. These results were found *within* a group of children undergoing music training, and without an active control group. It is likely that greater engagement in other extracurricular activities could also yield stronger neural outcomes. Perhaps the novel experience of

**Table 2 | (A)** Children who are more engaged in music classes have stronger neural encoding of speech after music training for measures previously linked to SES (speech harmonics and response consistency). **(B)** Neural measures before beginning musical training do not predict subsequent engagement in music classes.

Values are Spearman's rho (p-value). Significant relationships are bolded.

participating in an extracurricular activity, interacting with the researchers, etc., influenced our findings. However, previous studies that have employed active control groups indicate that music training but not art training strengthens auditory skills (Moreno et al., 2009, 2011). Moreover, child musicians differ from nonmusician children on auditory working memory and attention but not visual analogs (Strait et al., 2014). Similar to our analyses within a group of children participating in music, Hyde et al. (2009)found that the quality of musical training is critical for neuroplasticity. Children participating in private keyboard lessons for 15 months showed structural growth in primary auditory cortex, correlated with their improvement in melody and rhythm perception tasks; however, a second group of children who participated in school music classes each week learning basic singing and drumming skills did not show the same neural growth (Hyde et al., 2009). Our results suggest that engagement is an important factor mediating the benefits seen from musical training. It's important to note that we found these relationships between engagement and neural function within a group of students whose attendance was relatively high on average (88%), who were rated as having 'moderate' or better class participation, and whose families were highly motivated for them to participate. The limited variance in music engagement and probable influence of other factors such as personality on student engagement may have contributed to the modest statistical significance of our tests. Nevertheless, we do see moderately strong relationships between engagement and neural measures, suggesting that even if well-motivated to begin music training, students may not make gains unless they are actively engaged in the process. In the same vein, previous studies of musicians have revealed the important role of continued practice in maintaining the benefits of musicianship (Pantev et al., 1998; Ho et al., 2003; Norton et al., 2005; Forgeard et al., 2008b; see Strait and Kraus, 2014 for a review).

Greater attendance and class participation were not predicted by neural measures before musical training. This suggests that children with the strongest neural function before beginning musical practice did not go on to be those most engaged in music classes. Instead, it appears that greater engagement in music may have resulted in stronger neural encoding. Cohort research revealing neural differences between musicians and non-musicians is unable to definitively say whether those differences were pre-existing, although the oft observed relationship between length of practice and benefits of musicianship supports music experience as the cause (Pantev et al., 1998; Ho et al., 2003; Norton et al., 2005; Forgeard et al., 2008b; Seither-Preisler et al., 2014; see Strait and Kraus, 2014 for a review). A host of recent longitudinal studies report that musical training can selectively enhance auditory function in children without pre-existing differences. When children are randomly assigned to music or art training, only those in musical training show enhancements in auditory neurophysiology and attention (Moreno et al., 2009, 2011; Chobert et al., 2014). Additionally, children who elect to participate in music do not have inherent differences in neural structure or function from their peers (Norton et al., 2005; Hyde et al., 2009; Tierney et al., 2013), but show enhancements in auditory system structure and function after 1–2 years of musical training (Hyde et al., 2009; Tierney et al., 2013; Kraus et al., 2014b). We were not able to conduct paired

pre-post comparisons due to alterations to our recording scheme as the study progressed. However, the lack of relationship between pre-test neural measures and subsequent classroom engagement in our study suggests our results are independent of pre-existing differences in neural function.

Although some studies report no differences in cognition for children who elect to participate in music versus those who do not (Schlaug et al., 2005; Hyde et al., 2009), personality and preexisting skill may nevertheless influence a student's engagement and persistence in music. For example, using duration of music lessons as the outcome variable, Corrigall et al. (2013) showed that cognitive skills (along with parental income) predicted how long students continued with music. They additionally showed that children exhibiting high Openness to experience (part of the Big Five personality traits) were more likely to continue with music lessons after taking into account cognition and parental income (Corrigall et al., 2013). In our group of students, personality factors may have influenced attendance and participation in music classes. Those who were highly engaged in music classes may have been highly engaged throughout their school day, had a more encouraging home environment, may have been more motivated individuals, etc. Indeed, Openness as a personality trait is linked to factors reflecting academic engagement and achievement in college students, such as enjoying thinking and analyzing, enjoying connecting with others in class, and enjoying working hard (Komarraju and Karau, 2005). One limitation of our study is the lack of measures to investigate which of these personality factors may predict engagement in music. Importantly though, duration of musical experience also predicts cognition and language skills (Schellenberg, 2006; Forgeard et al., 2008b), suggesting the presence of a reinforcing loop. Children more open to new experiences may elect to begin music lessons and continue to participate longer, which leads to larger cognitive benefits, predicting continued retention in music, etc.

In addition to enhancing cognitive skills, music training can lead to stronger reading, language, and academic skills in children (Schellenberg, 2004, 2006; Hetland and Winner, 2010; Corrigall and Trainor, 2011; Dege and Schwarzer, 2012; Francois et al., 2013; Seither-Preisler et al., 2014; Slater et al., 2014a; see Tierney and Kraus, 2013 for a review), including those with reading impairments (Overy, 2003; Bhide et al., 2013). As a group our participants showed a small decline in reading fluency scores, which likely reflects a trend for the achievement gap to widen for children from low SES backgrounds as they age (Sirin, 2005). However, the change in reading scores varied with music engagement; reading fluency improved in children with greater class participation. That this relationship was seen despite the small variance in class participation ratings speaks to the importance of active engagement in music for engendering benefits. Students who had the highest class participation rankings were more likely to show an increase in reading score after 2 years of participation in Harmony Project. On the other hand, participants who had 'moderate' class participation on average were likely to show a decrease in reading score. As the consistency of the auditory brainstem response to speech and the strength of representations of the speech harmonics have been repeatedly linked to reading ability (Banai et al., 2009; Hornickel et al., 2011, 2012a; Hornickel and Kraus, 2013;White-Schwoch and

Kraus, 2013), and musical aptitude can predict reading ability (Ho et al., 2003; Forgeard et al., 2008a; Huss et al., 2011; Strait et al., 2011), it is possible that stronger speech encoding arising from greater participation in music classes contributed to improved reading scores.

Animal models of auditory deprivation and enrichment yield insight into the potential mechanisms involved in the neuroplasticity observed here. Similar to humans exposed to chronic noise, animals reared in noisy environments show detrimental effects on auditory processing, such as broader neural frequency selectivity (Zhou et al., 2011; Zhu et al., 2014), greater spontaneous neural activity (Seki and Eggermont, 2003), and weaker neural speech processing (Reed et al., 2014). Additionally, rats with a knock-down of a dyslexia-linked gene show more variable cortical responses to speech and weaker neural differentiation of speech (Centanni et al., 2014a). These deficits are thought to be due to imbalances in excitatory and inhibitory neurotransmitters, also shown to be negatively affected by noise exposure during development (Guo et al., 2012; Zhu et al., 2014). Auditory enrichment and behavioral training can reverse these effects, yielding better neural frequency selectivity, more consistent neural responses to speech, better neural differentiation of speech sounds, and can re-establish excitatory/inhibitory balances in rats with early auditory deprivation (Guo et al., 2012; Centanni et al., 2014b; Zhu et al., 2014). Although these exact mechanisms have not been investigated in humans, it is very likely that similar ones are at play. Like the auditory enrichment paradigms in animal studies, music training is a social, multisensory process that activates multiple neural networks during repeated exposure to the enriching "environment" [please see Patel (2011) for a review of the multi-faceted nature of music training].

We failed to find significant relationships between spontaneous neural activity and musical engagement. Previous studies of auditory training in humans, such as music training, computerbased training games, foreign language learning, and classroom acoustic modification, have shown improvements in the evoked response to speech, but none have reported changes in spontaneous neural activity (Besson et al., 2007; Song et al., 2008; Stevens et al., 2008; Russo et al., 2010; Hornickel et al., 2012b; Strait et al., 2013). Animals that are subjected to noise during development have increased spontaneous neural activity, likely due to decreased neural inhibition as a result of abnormal excitatory/inhibitory neurotransmitter ratios (Seki and Eggermont, 2003; Zhu et al., 2014). However, auditory enrichment can alleviate imbalances in excitatory and inhibitory neurotransmitters (Guo et al., 2012; Zhu et al., 2014) and possibly reduce noise-induced spontaneous neural activity. Spontaneous cortical activity thought to reflect a functional "resting-state network" can be altered with training in humans (Lewis et al., 2009; Taubert et al., 2011). The present findings show that the extent of music engagement tracks with changes in stimulusevoked, but not spontaneous background activity; trainingrelated influences on spontaneous activity should be explored further.

Our results support the importance of active experience and meaningful engagement with sound to engender neural changes. Even in a group of highly motivated students, small variations in music engagement (attendance and class participation) predicted the strength of speech encoding after music training. These measures of neural encoding are known to be weaker in children from low SES backgrounds. Although personality features likely played a large role in students' levels of engagement in class, our results do support that greater levels of engagement are not prompted by pre-existing differences in neural encoding. In our group of participants from low SES backgrounds, those who were the most engaged in music classes had the strongest neural responses and were most likely to show improvements in reading ability. Community music programs such as Harmony Project and El Sistema have proven success in bolstering academic achievement in children from disadvantaged backgrounds. We have also shown that participation in Harmony Project reinforces literacy skills and enhances the neural encoding of speech cues important for reading and the perception of speech in noisy backgrounds (Kraus et al., 2014a,b; Slater et al., 2014a; Kraus and Strait, in press). Taken together, we suggest that motivated engagement in community music programs may counteract some of the auditory impoverishment that children from low SES backgrounds commonly experience.

#### **AUTHOR CONTRIBUTIONS**

Nina Kraus and Dana L. Strait designed the study; Dana L. Strait, Jessica Slater, and Elaine Thompson collected the data; Jane Hornickel analyzed the data; Jane Hornickel and Nina Kraus prepared the manuscript; all authors contributed to the final version of the manuscript.

#### **ACKNOWLEDGMENTS**

We thank Samantha R. O'Connell, Shivani Bhatia, Jason V. Thompson, Emily Spitzer, Erika Skoe, Jen Krizman, Travis White-Schwoch, and Trent Nicol for their contributions throughout the project. We are grateful to Harmony Project (www.harmonyproject.org) administrators and staff for facilitating this research, especially Harmony Project founder Dr. Margaret Martin, Executive Director Myka Miller, Monk Turner, Sara Flores, and Jeremy Drake. We thank the children and their families for participating. This work was supported by the National Association of Music Merchants, the GRAMMY Foundation, and the Knowles Hearing Center of Northwestern University.

#### **REFERENCES**

**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

*Received: 21 August 2014; accepted: 17 November 2014; published online: 16 December 2014.*

*Citation: Kraus N, Hornickel J, Strait DL, Slater J and Thompson E (2014) Engagement in community music classes sparks neuroplasticity and language development in children from disadvantaged backgrounds. Front. Psychol. 5:1403. doi: 10.3389/fpsyg.2014.01403*

*This article was submitted to Cognitive Science, a section of the journal Frontiers in Psychology.*

*Copyright © 2014 Kraus, Hornickel, Strait, Slater and Thompson. This is an openaccess article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.*

# A groundwork for allostatic neuro-education

## *Lee Gerdes1, Charles H. Tegeler2 and Sung W. Lee1,3\**

*<sup>1</sup> Brain State Technologies LLC, Scottsdale, AZ, USA, <sup>2</sup> Department of Neurology, Wake Forest School of Medicine, Winston-Salem, NC, USA, <sup>3</sup> Running River School, Sedona, AZ, USA*

We propose to enliven educational practice by marrying a conception of education as guided human development, to an advanced scientific understanding of the brain known as allostasis (stability through change). The result is a groundwork for allostatic neuro-education (GANE). Education as development encompasses practices including the organic (homeschooling and related traditions), cognitive acquisition (emphasis on standards and testing), and the constructivist (aimed to support adaptive creativity for both learner and society). Allostasis views change to be the norm in biology, defines success in contexts of complex natural environments rather than controlled settings, and identifies the brain as the organ of central command. Allostatic neuro-education contrasts with education focused dominantly on testing, or neuroscience based on homeostasis (stability through constancy). The GANE perspective is to view learners in terms of their neurodevelopmental trajectories; its objective is to support authentic freedom, mediated by competent, integrated, and expansive executive functionality (concordant with the philosophy of freedom of Rudolf Steiner); and its strategy is to be attuned to rhythms in various forms (including those of autonomic arousal described in polyvagal theory) so as to enable experiential excitement for learning. The GANE presents a variety of testable hypotheses, and studies that explore prevention or mitigation of the effects of early life adversity or toxic stress on learning and development may be of particular importance. Case studies are presented illustrating use of allostatic neurotechnology by an adolescent male carrying diagnoses of Asperger's syndrome and attention-deficit hyperactivity disorder, and a grade school girl with reading difficulties. The GANE is intended as a re-visioning of education that may serve both learners and society to be better prepared for the accelerating changes of the 21st century.

Keywords: allostasis, neuro-education, neurodevelopment, RDoC, executive function, polyvagal theory, toxic stress, neurotechnology

## Introduction and Orientation

One should not ask, 'What does a person need to know and be able to do for the existing social order?' but rather, 'What gifts does a person possess and how may these be developed?' Then it will be possible to bring to society new forces from each succeeding generation. Then the social order will always be alive with that which fully developed individuals bring with them into life, rather than that each succeeding generation be made to conform to an existing social organization – Rudolf Steiner, Founder of Waldorf Schools.

Fenner and Rapisardo (1999)

#### *Edited by:*

*Eduardo Martínez-Montes, Cuban Neuroscience Center, Cuba*

#### *Reviewed by:*

*Sandrine Rossi, Université de Caen Basse-Normandie, France Jean-Luc Velay, Aix-Marseille Université, France Lorie A. Hammond, Peregrine School, USA*

*\*Correspondence:*

*Sung W. Lee, Brain State Technologies LLC, 15150 North Hayden Road, Suite 106, Scottsdale, AZ 85260, USA<EMAIL_ADDRESS>
#### *Specialty section:*

*This article was submitted to Cognitive Science, a section of the journal Frontiers in Psychology*

*Received: 01 October 2014 Accepted: 03 August 2015 Published: 17 August 2015*

#### *Citation:*

*Gerdes L, Tegeler CH and Lee SW (2015) A groundwork for allostatic neuro-education. Front. Psychol. 6:1224. doi: 10.3389/fpsyg.2015.01224* Today, clinicians are accused of overdiagnosing and overmedicating children with behavioral problems. It is time to shift from an exclusive focus on behavior and symptombased diagnosis to incorporate a deeper understanding of neurodevelopmental trajectories with interventions that can support the healthy development of brain and behavior – Thomas Insel, Director of the US National Institute of Mental Health.

Insel (2014)

Educational practice is as old as human civilization. Modern understanding of the brain, supported by innovations in technology, has developed over approximately the last 100 years. The proposition of this paper is that a recent innovation in scientific understanding of the brain known as *allostasis* ("stability through change") has potential to support a constructive re-visioning of education as stewardship of emergent, individualized, and advanced brain functionality. The progeny of the union between education and allostasis is an approach to the developing and multi-faceted learner that we call allostatic neuro-education. To characterize this conceptualization we outline a perspective, an objective, and a strategy for educators which collectively constitute a *groundwork for allostatic neuroeducation* (GANE). The ultimate benefit we conceive from the GANE is to support the profession of education to reach its own highest potential, to be a match for the meaning reflected in its Latin etymology *educere*, to *lead out* the expression of that which is within. To support understanding of the terms, concepts, and abbreviations presented in this paper, a glossary is provided in **Figure 1**.

For purposes of introducing the reconstructed view of education entailed by the GANE, we recapitulate a taxonomy outlined by Lawrence Kohlberg, the pioneer of moral psychology, and Rochelle Mayer in a paper titled "Development as the Aim of Education" (Kohlberg and Mayer, 1972). In this work, Kohlberg and Mayer categorized educational practice in the Western world to consist of three broadly different streams or typologies – the romantic, the transmission of culture, and the progressive. To update their labels, we substitute the words *organic* for their *romantic*, *cognitive acquisition* for their *cultural transmission*, and *constructivist* for their *progressive*.

The *organic* type of educational practice is intended to nurture that which is already within the child. Cognitive development is encouraged (rather than instructed) to proceed along lines of pre-programmed unfolding and in parallel with physical and emotional development. Organic education is philosophically descended from Jean Jacques Rousseau (1712–1778) and others who exalt the natural and express concern over the corrupting influences of society. Formal and didactic aspects of education tend to be de-emphasized in favor of child-centric practices including homeschooling, de-schooling, and other strategies aimed to enable flourishing of innate potential. Education for *cognitive acquisition* is rooted in classical traditions of Western civilization, aiming to impart literacy, mathematical competence, and other forms of knowledge that relate to prevalent norms. Education for cognitive acquisition is largely society-centric, and it is largely synonymous with education as instruction (from the Latin *instruere*, to build up or pile on) that includes emphases on standardized testing. In the USA, coalescence around standards of cognitive skill acquisition has occurred in various ways including federal legislation known as No Child Left Behind as well as the more recent initiative known as the Common Core. In East Asian cultures, cognitive acquisition takes on even greater importance in that educational striving is commonly used as a tool for character building or as a high-stakes funnel for social advancement (Chua, 2011; Ripley, 2014). *Constructivist* education, represented by John Dewey (1859–1952) and others, posits that the goal of education is to facilitate guided development of the learner through proactive experiences and interactions with society and the natural environment at large, such that knowledge and skills are actively created through engagement with living and changing contexts. Dewey in particular considered that education to nurture such development should have implications for both the learner and for healthy participatory democracy.

Kohlberg and Mayer associated the first two educational streams with different metaphors for learning. Organic education compares the learner to a plant or blossoming flower. For education in the service of cognitive acquisition, the learner has inputs and outputs, comparable to a machine or other functional instrument. For the constructivist, the learner is understood to be engaged in a constant dialectic with the environment. She or he generates and applies an initial idea, experiences its consequences, and subsequently revises the idea or its application in a continuous procession. Kohlberg and Mayer were proponents of constructivism, proposing that this approach was the only one adequate to "prepare free people for factual and moral choices which they will inevitably confront in society." Their sentiment is echoed in other recent writing that has warned against the societal impacts of educational systems that begin and terminate with unbridled focus on cognitive acquisition. Such approaches can fail to recognize fundamental misalignments between learner needs and teacher efforts, ultimately resulting in wasted resources and distorted understanding, akin to "lecturing birds how to fly" (Taleb, 2012).

The GANE in contrast recognizes important roles for all three educational streams or traditions, and the dialectical appreciation that Kohlberg and Mayer assigned exclusively to the constructivist can be understood to apply to all three traditions aligned in a larger unfolding. The child-centric view of organic education can be understood, normatively, as a robust starting point for the learner, as a way to nurture the innate capacities of a young life form. The society-centric view of education for cognitive acquisition may serve to equip and ballast developing learners with a common set of shared skills and knowledge which enable clear and robust communal interaction, without which self-centered individuals may descend into narcissism or chaos. Though constructivism may represent the highest educational ideal, in its goal of enabling perpetual renewal and re-creation for both individual and society, actual constructivist practice may need a foundation of nurturing, experience, skills, and knowledge that are the province of organic and cognitive acquisitional approaches. The GANE thus aims for a re-visioning of education that is inclusive of a breadth of traditions.

The GANE is motivated by a sense of urgency for educators to consider seriously the need for innovation in educational

FIGURE 1 | Glossary of terms, concepts, and abbreviations presented in the paper, listed in the order in which they are principally discussed in the text.

principles and practice. Because of the acceleration of changes that we are now experiencing in multiple realms – socioeconomic, cultural, geo-political, and technological – educational systems must better prepare 21st century learners to be adaptable and genuinely constructivist, so they may thrive in a world that is manifesting increasing degrees of variability and unpredictability. To further explicate the background of the GANE and how it differs from other approaches to neuroeducation, the ensuing section of the paper introduces the advanced model of physiological regulation known as *allostasis*. Allostasis is proposed as a necessary advance on the paradigm of homeostasis, that has limitations associated with its origins in pre-evolutionary 19th century biology. The third section defines and characterizes the GANE by outlining its perspective, objective, and strategy. Fourth, the paper considers a range of testable hypotheses that stem from the GANE. To emphasize that the brain-centrism of the GANE is not metaphorical or only implied, two case studies are presented that illustrate use of allostatic neurotechnology by learners with special needs.

## Homeostasis, Allostasis, and Education

The advanced understanding of brain functionality that is central to the GANE is contained in the paradigm of *allostasis* (Sterling and Eyer, 1988), defined as "stability through change." In comparison to the idea of homeostasis, or "stability through constancy," allostasis presents a more biologically accurate understanding of the role and functionality of the brain itself (Sterling, 2004, 2012). There are three main insights from the paradigm of allostasis that enable it to serve as a robust scientific foundation for neuro-education. First, it recognizes that change and not constancy is the fundamental character of biological regulation. Second, it views life and the definition of success against the background of complex natural contexts rather than controlled settings. Third, allostasis identifies the brain as the organ of central command.

The innovative view of allostasis may be better understood by an overview of the paradigm it aims to subsume. The foundations of modern experimental physiology were laid by Claude Bernard (1813–1878) and Walter Cannon (1871–1945) through the use of laboratory-based animal experimentation methods and reasoning based on reductive materialism. Bernard posited that physiological systems are designed to preserve a constant interior environment – that is to say, that the goal of life forms is to defend their internal biological operations against changes wrought by the environment. Central to the paradigm was the presumption that differences between species were not of great significance, and thus inferences about the functioning of physiological systems drawn from experiments on one species could be applied to others. Homeostasis recognizes the individual as a collection of multiple and distinct systems – the heart and circulatory system, the gut and digestive system, and others – and that illumination of the operative mechanisms of these systems is the basis for therapeutics.

In contrast, the paradigm of allostasis was born from recognition that social and environmental variables have critical influence on biological functioning, and that life is not fundamentally oriented toward "defense" of a constant internal environment (Sterling, 2004, 2012). Rather, in alignment with evolutionary theory, biological systems are understood to function in such way that they normatively change their operational set points to be optimally fit for the context of the natural environment, which is essentially complex, variable, and unpredictable. *Under evolutionary theory, the ultimate goal of life is not to defend against changes but rather to create more life*, and this objective is achieved through adaptation to present and anticipated needs. Critically, allostasis recognizes that to coordinate and adjudicate among the competing demands of different organ systems or functionalities, life requires a higherorder faculty for organization and regulation, and the organ for such faculty is the brain. The brain is the seat of central command, guiding the organism as a unit to adapt to new circumstances, and to prepare for changes yet to come.

Biological systems under conditions of environmental monotony (including the controlled settings of a laboratory) may appear to be homeostatic because their set points are not challenged to need modification. Nonetheless homeostasis and allostasis present different understandings of the underlying drivers of physiological regulation and their implications. Homeostasis implies the existence of normal and normative set points, whereas allostasis does not (Sterling, 2012, 2014). Under allostasis, recognition that brain activity is fundamentally context-dependent is critical to understanding health or disease across systems, whereas under homeostasis the focus is on identifying disturbances in molecular mechanisms. Homeostatic modeling invites strategies to modify mechanisms and their set points toward the putative norms. Allostatic modeling recognizes the need for variability in biological expression and specifically aims to support the brain's native ingenuity for central command (Sterling, 2004, 2014). Notably it is not the anatomical focus *per se* of a particular strategy that makes it homeostatic or allostatic, and interventions directed toward the brain can be of either type.

Dominance of the homeostatic paradigm in physiology and biomedical health care can be considered the neuroscientific analog of the dominance of standardized cognitive acquisition as the mode of educational practice in the modern era. Just as the modern biomedical system views the individual as so many distinct organ systems, so does educational practice for cognitive acquisition view the learner in terms of a collection of different and distinct systems for cognitive, emotional, and behavioral functionalities, and others. As with homeostatic reductionism, these systems are held to have independent mechanisms of operation, and in general only the cognitive is under the purview of the secular educator. Other systems are allocated to an array of specialists– psychologists, psychiatrists, other behavioral specialists, physical education instructors, speech or language therapists, music or art specialists, and others. Modern educators are largely not trained to interact with learners as whole and integrated beings, and even less are they trained to consider that the learner's various domains may have a common upstream source of regulation in the brain.

The allostatic educator is dynamically flexible and uses different educational approaches in ways that fit the need. During the earliest phases of life, there is major biological development in neural systems that may be well supported by organic educational practices. Education for cognitive acquisition or cultural transmission supports learners to "stand on the shoulders of giants" with respect to established questions. In its essence, allostasis is especially aligned with constructivist educational practices – when learners are ready to question the question itself – which are attuned to the contingent and changing nature of skills and knowledge. By the lights of allostatic neuroeducation, the most well educated student is not the one with the highest scores on fixed and standardized tests, but the one who is most robustly positioned to create successful interactions with complex, variable, and unpredictable environments. Capacity for such success has evolutionary consequences for both the individual and society.

At this juncture we consider whether the proposition to use allostasis as the basis for a new vision of education represents a form of the naturalistic fallacy. That is to say, though change may be the norm of nature, and though the brain's biological role may be to serve as the organ of central command, it may not necessarily be warranted to presume that educators should use these concepts as normative guidelines for educational practice. For example, biological evolutionary theory has been used notoriously, and fallaciously, to justify policies that are intrinsically political (and often repressive), including social darwinism and eugenics. To this question, the authors answer (with further discussion in the following section) that the GANE has an explicitly philosophical dimension, and it specifically aims for attainment of a state of advanced executive functionality associated with authentic *freedom*. Freedom is represented by maximal *optionality* for both the learner and educator. Allostatic neuro-education is based on the power to *opt*, not the imperative of the *ought*. Optionality includes the freedom to place a relative emphasis on cognitive acquisitional educational practices that are themselves essentially homeostatic. It is rather the homeostatic paradigm that tends to commit the naturalistic fallacy, in conceiving that the constant (or typically average) set points for biological regulation should be considered normative, and therefore defended by means of therapeutic or otherwise normalizing interventions.

## Perspective, Objective, and Strategy of the GANE

We define allostatic neuro-education as *activity intended to educe (lead out) the full potentiality of learners, with respect for the integrated developmental trajectory of their multi-faceted brains, to support their successful engagement with complex, changing, and unpredictable environments.* Allostatic neuro-education may derive, now or in the future, from a range of principles and practices in education, child development, neuroscience, brainfocused technologies, or other fields. In this section we give initial substance to the GANE under the rubric of a perspective, an objective, and a strategy.

## The GANE Perspective is the Learner's Extended Neurodevelopmental Trajectory

In bringing a developmental perspective to the foreground, the GANE aligns with pedagogical strategies introduced by a series of educators and psychologists beginning in the late 19th century. Rudolf Steiner (1861–1925) founded the Waldorf School in 1919, based on an appreciation of multiple domains of the human being that develop over the course of 7-years periods. Waldorf teachers progress with the same students from year to year so they can carefully steward the child's long-term process for completing these tasks, and educational practices are designed to encompass organic, cognitive acquisitional, and constructivist objectives. John Dewey (1859–1952) proposed that education should be experiential and guide learners to develop constructive engagement with their surroundings including their larger societal context. Jean Piaget (1896–1980) modeled human cognitive development as proceeding through stages, from basic sensory impressions and motor activities, to a preoperational stage that includes language acquisition, to concrete operations which include a capacity for logic, and finally to a formal-operational stage marked by abstract reasoning. Lawrence Kohlberg (1927–1987) showed that learners developed moral reasoning in a sequence of stages from self-interest (pre-conventional morality), to social consensus (conventional morality), to universal principles (post-conventional morality). Erik Erikson (1902–1994) conceptualized the life cycle to include a series of thematic tasks whose successive completion was required for subsequent stages of development.

Broadly, considerations for the educator as steward of development are threefold. Probably the most important consideration, the one that has historically been appreciated as maternal wisdom but which is now receiving extensive empirical validation, is that early life exposure to adversity or toxic stress levels confers a major risk for negative outcomes in childhood and beyond, due to disruptive impacts on systems for learning, health, and behavior (Shonkoff et al., 2012). Deleterious effects of repeated biochemical stress reactions have been referred to as allostatic load (McEwen, 1998; Juster et al., 2010), and the effects of childhood adversity on adult outcomes are independent of established adult-status risk factors (Danese and McEwen, 2012). Secondly and from a pedagogical perspective, the educator as steward of development should be sensitive to exposing learners to challenges prematurely. For example, attempts to impart abstract concepts too soon may yield poor grasp of those concepts, while robbing the learner of opportunities for experiences salient to their stage. Thirdly, incomplete maturation or failure to complete a task at a given stage (often in association with adversity or toxic stress) may hinder subsequent progress, just as a weak foundation is problematic for constructing higher floors of a building.

On the basis of scientific consensus and in alignment with the paradigm of allostasis, the importance of a developmental perspective is supported by the Research Domain Criteria (RDoC) initiative of the US National Institutes of Mental Health (NIMH). Decades of research have elucidated relationships between brain functionality and behavior, and the NIMH introduced the RDoC in 2009 as a way to advance understanding of mental and behavioral health by transitioning from symptom and behavior-based diagnostic systems to a framework that focuses on underlying brain biology (Cuthbert and Insel, 2013). The initial core domains of brain functionality identified by RDoC are arousal (including sleep), positive valence (including appetitive or reward-oriented behaviors), negative valence (including fear or anxiety), cognitive systems (for attention, memory, language), and systems for social processes (including affiliation and social communication). These core domains are operative in both health and disease, and they cut across different diagnostic categories. RDoC is poised to support advance in mental and behavioral health by suffusing the approach of researchers and practitioners with conceptualizations and interventions – even those that are entirely psychosocial in character – that are based on appreciations of brain functionality. Critically, developmental trajectories exist for all the major brain domains defined by the RDoC (Casey et al., 2014). These trajectories are impacted by use and environmental influences, and they can be presumed to influence one another.

Like behavioral health research and care, the field of education may also be poised to benefit from conceptualizing the learning child as a unique being with a unique brain, with core domains in various stages of development. As alluded to in Homeostasis, Allostasis, and Education, the human brain undergoes massive changes from embryogenesis to the postnatal period, and it remains plastic throughout the lifespan, presenting an array of conjecturable implications for educators as stewards of development. Neural systems for executive function and cognitive control do not fully mature until the third decade (Hsu et al., 2014), lending credence to organic educational views that use metaphors of blooming or pruning through late adolescence and beyond. Adolescence is characterized by a marked (quadratic) increase in incentive motivation (Luciana, 2013) that bears upon the developing reward system with implications that have been studied for mental health, but this trajectory might also be explicitly considered and leveraged by educators. Though the existence of a critical period for second language acquisition has been questioned (Vanhove, 2013), early education for bilingualism may confer a variety of benefits for cognitive development, including increased cognitive control and possibly generation of cognitive reserve (Bialystok et al., 2012). Alteration of circadian rhythm or sleep, an aspect of arousal, is common in adolescence and may disrupt executive functionality and reward processing (Hasler et al., 2012; Telzer et al., 2013), and advancing strategy and policy to support optimal sleep across the life span is a sensible priority for any approach to neuroeducation (Sigman et al., 2014).

To further illustrate the contrasting approaches of cognitive acquisition-focused education and the neurodevelopmental perspective of the GANE, we consider the hypothetical case of a child who is found to be consistently inattentive, distractible, and fidgety. In a homeostatic, cognitive acquisition learning context, this child may be recommended or referred, by an educator, a physician, or parents themselves, to undergo consultation with a behavioral health specialist. If the child falls outside consensus criteria for normal attention and behavior including executive functionality, he or she may be given a diagnosis of attention deficit-hyperactivity disorder (ADHD). Non-normality may be attributed to a variety of disturbances in underlying neural mechanisms that, though possibly understood to have phenotypic expression along a continuum, nonetheless result in categorical assignment to a status of disease versus non-disease. This evaluation has taken place in a *spatial* dimension, wherein fundamentally the individual is compared, at a given moment in time, to other individuals.

The GANE instead evaluates the child's behaviors or tendencies primarily as a snapshot within a longitudinal frame of complex neurodevelopmental trajectories. That is to say, the GANE is critically sensitive to the *temporal* dimension in its evaluation, such that the individual is appreciated primarily with respect to his or her own past and potential futures. Differences in the stepwise unfolding of brain domain functionalities may have consequences across trajectories. The pioneering work of Harry Harlow, for example, showed the importance of healthy attachment for later life development as a whole, and a recent report (Roskam et al., 2014) has shown an association between duration of exposure to early attachment deprivation (likely impacting brain domains for social affiliation, arousal, and affective valence) and degree of ADHD symptoms in adolescence. These data reinforce that brain domains interact with one another over time, and that ADHD cannot be conceptualized exclusively as a disorder of executive functioning. Furthermore while individuals with attention deficits may have altered sensitivity in the reward system that may confer a later risk for addictive disorders (Blum et al., 2008), it is possible that this same difference may, for some, contribute to success in risk-related endeavors that can have higher-order societal impact, including entrepreneurship. The GANE developmental view requires a willingness to use the biological imagination, for educators to create mental pictures related to the learner's neural past and future. Such an approach promotes greater respect for the learner's full life, both backward and forward in time, and appreciation of both risks and opportunities.