# NEURO-EDUCATION AND NEURO-REHABILITATION

EDITED BY: Eduardo Martínez-Montes, Julie Chobert and Mireille Besson PUBLISHED IN: Frontiers in Psychology

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ISSN 1664-8714 ISBN 978-2-88945-006-0 DOI 10.3389/978-2-88945-006-0

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# **NEURO-EDUCATION AND NEURO-REHABILITATION**

Topic Editors:

**Eduardo Martínez-Montes,** Cuban Neuroscience Center, Cuba **Julie Chobert,** Centre National de la Recherche Scientifique, France **Mireille Besson,** Centre National de la Recherche Scientifique and Aix-Marseille Université, France

Cover figure designed by Claudia Méndez Romero

In the last decade, important discoveries have been made in cognitive neuroscience regarding brain plasticity and learning such as the mirror neurons system and the anatomo-functional organization of perceptual, cognitive and motor abilities.... Time has come to consider the societal impact of these findings. The aim of this Research Topic of Frontiers in Psychology is to concentrate on two domains: neuro-education and neuro-rehabilitation. At the interface between neuroscience, psychology and education, neuro-education is a new inter-disciplinary emerging field that aims at developing new education programs based on results from cognitive neuroscience and psychology. For instance, brain-based learning methods are flourishing but few have been rigorously tested using well-controlled procedures. Authors of this Research Topic will present their latest findings in this domain using rigorously controlled experiments. Neuro-rehabilitation aims at developing new rehabilitation methods for children and adults with learning disorders. Neuro-rehabilitation programs can be based upon a relatively low number of patients and controls or on large clinical trials to test for the efficiency of new treatments. These projects may also aim at testing the efficiency of video-games and of new methods such as Transcranial Magnetic Stimulation (TMS) for therapeutic interventions in children or adolescents with learning disabilities.

This Research Topic will bring together neuroscientists interested in brain plasticity and the effects of training, psychologists working with adults, with normally developing children and children with learning disabilities as well as education researchers directly confronted with the efficiency of education programs. The goal for each author is to describe the state of the art in his/her specific research domain and to illustrate how her/his research findings can impact education in the classroom or rehabilitation of children and adolescents with learning disorders.

**Citation:** Martínez-Montes, E., Chobert, J., Besson, M., eds. (2016). Neuro-Education and Neuro-Rehabilitation. Lausanne: Frontiers Media. doi: 10.3389/978-2-88945-006-0

# Table of Contents

## **PART III. Basic research with implications in both fields**

Christophe Tandonnet, Borís Burle, Franck Vidal and Thierry Hasbroucq

## Editorial: Neuro-Education and Neuro-Rehabilitation

#### Eduardo Martínez-Montes 1 \*, Julie Chobert 2 and Mireille Besson2

1 Neuroinformatics Department, Cuban Neuroscience Center, La Habana, Cuba, 2 Laboratoire de Neurosciences Cognitives, UMR 7291, Centre National de la Recherche Scientifique, Aix-Marseille Université, Marseille, France

Keywords: learning disorders, language, musical training, sensorimotor training, neurofeedback

#### **The Editorial on the Research Topic**

#### **Neuro-Education and Neuro-Rehabilitation**

The latest advances in cognitive psychology, neuropsychology, and cognitive neuroscience has brought from science fiction to reality the possibility of influencing our brain activity (Owen et al., 2010; Glannon, 2014; Gruzelier, 2014a).  The emerging fields of neuro-education and neuro-rehabilitation aim at creating effective and safe programs to improve brain functioning related to specific perceptive, cognitive, emotional, and motor abilities. Some attempts to achieve these goals take advantage of the use of natural mechanisms, such as those mediating the interactions between brain and arts (Särkämö et al., 2008; Bringas et al., 2015). Others use experimental designs to make the brain aware of its own activity, creating the so-called neurofeedback loop (Gruzelier, 2014b). Succeeding in these goals would constitute an achievement of high societal impact (Davidson and McEwen, 2012; Vuilleumier et al., 2014).

This Frontiers Research Topic brings together 16 articles that cover a broad scope of topics in the relatively young but very dynamic fields of neuro-education and neuro-rehabilitation. Contributed by world-renowned scientists in cognitive psychology, neuropsychology, and cognitive neuroscience, often experts in different types of learning disorders, this E-book is organized around three main themes: neuro-education, neuro-rehabilitation and basic research with relevance to both fields. Each theme includes Review articles covering the state-of-the-art of knowledge in a specific sub-domain, Original Research articles reporting new discoveries and Opinion and Hypothesis and Theory articles adding exciting new ideas and approaches for neuro-educational and neuro-rehabilitation methods.

In the first part, dedicated to neuro-education, Ylinen and Kujala review the impact of auditory or phonological training on the level of performance in various tasks and on the neural basis of behavior in children with dyslexia, children with specific language impairment and children with language-learning impairment. François et al. review the efficacy of musical training for language learning. They highlight several studies showing that learning to play a musical instrument can induce substantial neuro-plastic changes in cortical and subcortical regions of motor, auditory and speech processing networks. They show evidence that musical training can be an alternative, low-cost and effective method for the treatment of language-learning impaired populations, as well as for patients with stroke or Parkinson Disease. Direct support for the use of musical training for the rehabilitation of children with dyslexia is reported by Habib et al. who tested the efficacy of a specially-designed Cognitivo-Musical training (CMT) method. Intensive short-term CMT with dyslexic children yielded significant improvements in categorical and auditory perception

#### Edited and reviewed by:

Eddy J. Davelaar, Birkbeck, University of London, UK

> \*Correspondence: Eduardo Martínez-Montes<EMAIL_ADDRESS>
#### Specialty section:

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

Received: 10 June 2016 Accepted: 06 September 2016 Published: 22 September 2016

#### Citation:

Martínez-Montes E, Chobert J and Besson M (2016) Editorial: Neuro-Education and Neuro-Rehabilitation. Front. Psychol. 7:1427. doi: 10.3389/fpsyg.2016.01427 of temporal components of speech, while long-term CMT provided additional improvements in auditory attention, phonological awareness, reading abilities and repetition of pseudo words. Along the same lines, Fonseca-Mora et al. also tested the efficacy of a new phonological training program (with and without music), for teaching to read in a foreign language, demonstrating its beneficial effects on early reading skills but without additional improvements linked to music training. Final but not least, Kraus et al. present the results of a longitudinal study examining the impact of a community music program on language development in children from low socio-economic backgrounds. Children more engaged in the music program developed stronger brain encoding of speech and improved reading scores, thereby suggesting that this kind of program provides children with auditory enrichments that may counteract some of the biological consequences of growing up in poverty. To conclude this section, the reader will find a novel approach to neuro-education, as proposed by Gerdes et al. They view learners in terms of their neurodevelopmental trajectories and propose a groundwork for allostatic neuroeducation (GANE). Illustrative case studies of the use of GANE in children with Asperger's syndrome, attentiondeficit hyperactivity disorder and reading difficulties are presented.

The second part of this E-book is dedicated to neurorehabilitation. Serniclaes et al. review the efficacy of remediation methods that tap into core deficits in dyslexia (phonemic, grapho-phonemic, and graphemic) and examine how some of these methods may contribute to the remediation of allophonic perception. Guilbert et al. describe different procedures for sensory training in unilateral spatial neglect (USN) and present recent scientific evidence that makes music a good candidate for USN patients' rehabilitation. Dhami et al. consider the use of dancing as an intervention tool and as a potential parallel to physical and music therapies, since dancing also engages various perceptive, cognitive, emotional and motor functions. The opinion paper from Stahl and Kotz addresses three relevant issues in current research on singing and aphasia: articulatory tempo, clinical research designs and formulaic language resources. The authors discuss how these issues may reconcile seemingly contradictory findings in the literature and provide guidelines for future research based on holistic and analytic approaches that may help improving the efficacy of music-based aphasia therapy. Finally, in a Hypothesis and Theory article, Elmer and Jäncke consider the use of a neurofeedback approach for auditory rehabilitation. They first stress the advantages of

## REFERENCES

using intracerebral functional connectivity (IFC) instead of quantitative EEG for interventional applications and then propose concrete interventional IFC applications that may improve auditory-related dysfunctions such as developmental dyslexia.

In the third part, we compiled some interesting studies which contribute both to a better comprehension of basic psychophysiological mechanisms and to the development of potential applications for neuro-education and neurorehabilitation. Vidal et al. review the role of sensorimotor information for motor learning. They discuss the effects of several factors known to influence information processing in sensorimotor activities based on the distinction between extrinsic (e.g., quantity and quality of information, level of instruction and motor program learning) and intrinsic factors (e.g., prior information, individual strategies and capabilities for fast error detection). In a more specific context, Berteletti and Booth investigated the extent to which somatosensory information from the fingers contributes to numerical sense in children. Their work provided first neurological evidence for a functional role of the somatosensory finger area in proficient arithmetic problem solving, thereby encouraging educational practices to integrate finger-based strategies as a tool for instilling stronger numerical sense. Still in another context, writing, Danna and Velay review studies that use natural sensory and supplementary feedback to help the writer learn how to write and to control writing. They discuss the role of each sensory modality, how information is used in handwriting control and how this control changes with practice and learning. Turning from writing to reading, Boudelaa reports, in an original research article, that the processing time course in auditory modality is different for consonants and vowels in Arabic. The implications of this work for neuro-education and neuro-rehabilitation in Arabic are discussed. Finally, Tandonnet et al. illustrate how basic approaches in cognitive science may benefit human factors engineering and potentially improve manmachine interfaces.

We hope this compilation of articles describing the latest research in the field of neuro-education and neuro-rehabilitation will be of interest to the readers and will impulse even more research in these fascinating new fields with strong societal impact.

## AUTHOR CONTRIBUTIONS

All authors listed, have made substantial, direct and intellectual contribution to the work, and approved it for publication.

to neurorestoration of children with severe neurological disorders. Front. Neurosci. 9:427. doi: 10.3389/fnins.2015.00427

**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 Martínez-Montes, 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.

## Neuroscience illuminating the influence of auditory or phonological intervention on language-related deficits

## *Sari Ylinen1\* and Teija Kujala1,2*

1 Cognitive Brain Research Unit, Institute of Behavioural Sciences, University of Helsinki, Helsinki, Finland 2 Cicero Learning, University of Helsinki, Helsinki, Finland

#### *Edited by:*

Julie Chobert, Centre National de la Recherche Scientifique, France

#### *Reviewed by:*

April A. Benasich, Rutgers University, USA Anna J. Simmonds, Imperial College London, UK L. Robert Slevc, University of Maryland, College Park, USA Fabio Richlan, University of Salzburg, Austria

#### *\*Correspondence:*

Sari Ylinen, Cognitive Brain Research Unit, Institute of Behavioural Sciences, University of Helsinki, P.O. Box 9, Helsinki, FIN-00014, Finland e-mail<EMAIL_ADDRESS>
Remediation programs for language-related learning deficits are urgently needed to enable equal opportunities in education. To meet this need, different training and intervention programs have been developed. Here we review, from an educational perspective, studies that have explored the neural basis of behavioral changes induced by auditory or phonological training in dyslexia, specific language impairment (SLI), and language-learning impairment (LLI). Training has been shown to induce plastic changes in deficient neural networks. In dyslexia, these include, most consistently, increased or normalized activation of previously hypoactive inferior frontal and occipito-temporal areas. In SLI and LLI, studies have shown the strengthening of previously weak auditory brain responses as a result of training. The combination of behavioral and brain measures of remedial gains has potential to increase the understanding of the causes of language-related deficits, which may help to target remedial interventions more accurately to the core problem.

**Keywords: language deficit, dyslexia, neuroscience, training, remediation, intervention**

## **INTRODUCTION**

Finding the most effective techniques to remediate languagerelated impairments, such as dyslexia, specific language impairment (SLI), or language-learning impairment (LLI, cf. Tallal, 2001), would be of crucial importance to educators, who try to help children struggling with these learning difficulties. This raises a question, whether understanding the neurobiological underpinnings of language impairments facilitates their efficient treatment. In this review, we discuss how neuroscience illuminates the effects of auditory or phonological intervention on dyslexia, SLI, and LLI. We focus on auditory or phonological interventions, because in many cases dyslexia, SLI, and LLI are all characterized by phonological (or auditory) deficits (Tallal, 2001; Shaywitz and Shaywitz, 2005; Pennington and Bishop, 2009; Ramus et al., 2013), despite their complex etiology. Whereas detailed brain areas influenced by reading interventions can be found in a recent meta-analysis by Barquero et al. (2014), here we address whether neuroscientific research on the remediation of language-related deficits is useful for educators and whether it has something to add over behavioral research from an educational perspective.

In the current review, the selection of publications was based on the following criteria: the research should concern dyslexia, SLI, or LLI, include testing before and after an auditory or phonological intervention or training, involve brain research measures [(functional) magnetic resonance imaging (MRI/fMRI),magnetic source imaging (MSI) or magnetoencephalography (MEG), event-related potentials (ERP), or electroencephalography (EEG)], and compare two or more groups of participants to control for the effects of repeated testing and maturation (McArthur, 2009). Searches from Web of Science and PubMed (keywords dyslexia/SLI/LLI, intervention/remediation/training, fMRI/MEG/ERP) were used in finding literature. Additional publications were found in the reference lists of relevant studies.

## **IS NEUROSCIENTIFIC RESEARCH USEFUL FOR EDUCATORS?**

Research on remedial interventions for learning deficits may have important applicability to education (Tallal, 2012). In this area, collaboration between education and neuroscience could result in mutual benefits (Sigman et al., 2014). However, the value of the neuroscientific approach in such research has been questioned by Bishop (2013) because of methodological and interpretive reasons. She argued that neuroscientific studies often use small subject groups, which may decrease their reliability and result in small statistical power (cf. Button et al., 2013). Furthermore, Bishop (2013) noted that some studies lack an adequate control group, which is important to control for the effects of repeated testing and maturation (see also McArthur, 2009). Indeed, future intervention studies should not only aim at having larger subject groups (Bishop, 2013) and adequate control groups (McArthur, 2009; Bishop, 2013), but also control for placebo effects (Boot et al., 2013).

Bishop (2013) also argued that the critical test of the effectiveness of interventions is the change of behavior rather than that of brain function; changes in the brain should not be considered more important than changes in behavior. However, rather than emphasizing the brain over behavior, neuroscientific intervention studies typically aim to determine the links between brain function and behavior. Importantly, understanding the link or correlation between brain activation and skills as a result of training may help to explain how and why remedial gains take place. Since the combination of neuroscientific and behavioral measures has been shown to be a better predictor of reading skills than behavioral measures alone (Hoeft et al., 2007; Maurer et al., 2009), this combination has potential to outperform mere behavioral measures in the study of remedial gains. Cognitive neuroscience has, in our opinion, also some advantages over behavioral research that were not mentioned by Bishop (2013). Especially when working with children whose motivation and skills can affect their performance considerably, a possibility to study the effects of intervention without subject's active effort or attention is a clear advantage. This is possible, for example, by recording mismatch negativity (MMN) brain response (Näätänen et al., 2007; Kujala and Näätänen, 2010).

From educators' perspective, neuroscientific research is seldom directly applicable in the assessment of remedial interventions. Importantly, however, educators may benefit from neuroscientific research by obtaining a more detailed picture of relevant processes underlying behavior. For example, brain measures may help to disentangle whether behaviorally observed improvement is due to the normalization of the core deficit or some compensatory strategy (e.g., Eden et al., 2004; Shaywitz et al., 2004), which is not evident in behavioral data. If, hypothetically, some intervention resulted in the formation of a compensatory function to solve some task, it may improve behavior to a certain degree but might not compete in effectiveness with the optimal function for solving that task. Still, in a large subject group, this compensatory improvement in behavior may be taken to reflect a successful intervention, if statistically significant improvement is achieved. Thus, neuroscientific research can potentially give some valuable information to educators about the deficits, which may help to target the contents of interventions more accurately.

### **OVERVIEW OF STUDIES ON NEUROBIOLOGICAL CHANGES FOLLOWING PHONOLOGICAL OR AUDITORY INTERVENTIONS**

As shown by **Tables 1** and **2,** the majority of studies on phonological or auditory interventions focused on dyslexia or related problems in reading, writing, or spelling. Furthermore, the majority of studies have focused on children. Older age groups should not be neglected in remediation and its research, however: as noted by Eden et al. (2004), most dyslexics are adults, who may suffer from the socio-economic consequences of their reading deficit. There seem to be no constraints with respect to brain plasticity that would hinder remediation in adults or older children (Simos et al., 2002; Eden et al., 2004). Nevertheless, the earlier the interventions are conducted, the more benefit to individuals is gained, because learning is cumulative. The early gains may help to prevent difficulties not only in academic but socio-emotional domain. The optimal timing of intervention is, however, determined by maturity and acquired skills. For example, if a new skill is scaffolded by previous skills, it cannot be adapted before they are mastered (cf. Jolles and Crone, 2012).

The studies listed in **Tables 1** and **2** suggest that in addition to behavior, the remedial gains of phonological or auditory interventions are consistently reflected in different aspects of brain functioning. These include increased or normalized brain activation as a result of training in previously hypoactive areas as measured with fMRI (Aylward et al., 2003; Temple et al., 2003; Eden et al., 2004; Shaywitz et al., 2004; Gaab et al., 2007; Meyler et al., 2008; Heim et al., 2014) and MSI or MEG (Simos et al., 2002; Pihko et al., 2007) during different cognitive tasks.  Training-induced changes in strength and timing of neural responses to stimulation have been demonstrated with ERPs (Kujala et al., 2001; Hayes et al., 2003; Stevens et al., 2008, 2013; Jucla et al., 2010; Lovio et al., 2012; Hasko et al., 2014). Also the time-frequency analysis of EEG has revealed amplitude increases in the oscillatory brain activity after training (Heim et al., 2013). In addition to brain function, interventions have been found to change brain anatomy, such as white matter integrity (Keller and Just, 2009). **Tables 1** and **2** also show that remedial gains, if any, consistently manifest in both behavioral and brain measures: in 16 out of 17 studies of **Table 1** and in all four studies of **Table 2**, remedial gains were found in both brain activation and skills targeted by intervention (note that Jucla et al., 2010, failed to find different behavioral improvement and similar brain response patterns between their treatment group and controls). The strong coupling of training gains in behavior and brain activation suggests that most likely the observed changes in the brain drive the changes in the behavior. As neuroscientific research may reveal the neural dynamics of processes related to behavioral performance and allows localize the deficient brain functions, it may enable to specify the neural mechanisms underlying languagerelated impairments and to determine brain functions and areas altered by interventions, which surface in behavior as improved skills. However, it is noteworthy that **Tables 1** and **2** lists published studies, whereas studies failing to find changes in behavior or brain activation may remain unpublished. This may cause bias toward systematically finding the coupling between neural and behavioral gains.

A recent meta-analysis of neuroscientific research exploring reading networks in the brain has suggested that dyslexia is characterized by the dysfunction of left occipito-temporal cortex, left inferior frontal gyrus, and the inferior parietal lobule (Richlan, 2012; see also Richlan et al., 2011). These brain areas are involved in phonological encoding, phonological representations, and attention, respectively (Richlan, 2012). Barquero et al.'s (2014) meta-analysis of the neuroimaging of reading interventions, in turn, suggests intervention-induced functional changes in the left thalamus, left middle occipital gyri, bilateral inferior frontal gyri, right insula, and right posterior cingulate gyrus. Thus, both Richlan's (2012) and Barquero et al.'s (2014) findings point toward the central role of inferior frontal and occipitotemporal/occipital dysfunction in dyslexia. Correspondingly, the neuroscientific dyslexia studies included in **Table 1**, involving auditory or phonological intervention, have shown normalized brain activation, metabolism, or anatomy as a result of interventions in the occipito-temporal (Aylward et al., 2003; Heim et al., 2014) and inferior frontal (Richards et al., 2000, 2002; Aylward et al., 2003; Shaywitz et al., 2004; Heim et al., 2014) areas.  Although inferior frontal and

**|Publicationsincludingneuroscientificresearchonphonologicalorauditoryremediationof**

(Continued)

phoneme

discrimination,

 phoneme

identification,

 phonic match, phonic word,

understanding

 instructions,

 grammatical

 structures and rules.

occipito-temporal/occipital dysfunctions, linked with phonological representations and processes (Richlan et al., 2011; Richlan, 2012), seem to be the robustest effects in dyslexia, the effects in the other areas need not to be spurious. The fact that studies use different training techniques and experimental tasks in the scanner during neuroimaging may account for finding remedial changes in different brain functions and areas (Heim et al., 2014).

Neuroimaging research on the effects of auditory and phonological intervention is complemented by ERPs, reflecting the dynamics of neural responses.  Lovio et al. (2012) observed also a treatment-induced shortening of the MMN latency across groups receiving grapheme-phoneme or numberknowledge training. In SLI and LLI (**Table 2**), the remedial gains of interventions have been observed as the strengthening of oscillatory brain activity (Heim et al., 2013) and auditory cortical responses, including MMN (Pihko et al., 2007) and attentionrelated ERPs (Stevens et al., 2013), which are accompanied by improved performance in behavioral language tasks. Training has also been shown to shorten the latency of auditory P1-N2 complex, resulting in a more mature response pattern (Hayes et al., 2003). As the MMN study by Pihko et al. (2007) involved passive listening, where participants' attention was directed elsewhere, enhanced MMN responses indicate remedial effects on low-level, pre-attentive auditory processing that is modified by phonetic representations.

#### **DOES THE CONTENT OF THE INTERVENTION MATTER?**

From educators' perspective, it would be important to conduct interventions that tap the core deficit rather than induce compensatory improvements. Direct comparisons using the same experimental tasks but different interventions could clarify, whether the optimal method of remediating language-related deficits can be found. To this end, Shaywitz et al. (2004) have compared the effects of a targeted experimental intervention and a community intervention on behavioral performance and brain activation in children with reading difficulties. The experimental intervention focused specifically on phonological skills with different kinds of tasks, whereas community intervention consisted of activities commonly provided in school, such as remedial reading (see Shaywitz et al., 2004, for details). As a result of interventions, the experimental intervention group had achieved significant gains in reading fluency and showed an increased activation of left-hemisphere brain regions, whereas no such gains were observed after community intervention. This result emphasizes that the nature of intervention is critical for its success (however, see Boot et al., 2013, for discussion on the expectations about improvement).

Besides showing a correspondence between improvements in skills and changes in neural function, neuroscientific measures can illuminate the specific effects of interventions on brain areas subserving distinct cognitive functions. Heim et al. (2014) compared three different kinds of training that focused on phonology, attention, and visual word recognition (reading). They divided school-aged dyslexic children into three training groups according

to their cognitive profiles. All training methods improved children's reading skills to a similar degree. During a reading task in an fMRI scanner, all training programs resulted in the increased activation of the visual word form area, located in the left fusiform gyrus. In some other brain areas, however, the training programs had different effects on brain activation: phonological and reading training increased activation in bilateral parietal areas, whereas attention training increased activation in the left temporal cortex. Thus, different training programs had both shared and specific effects on brain activation, which would not have been evident on the basis of behavior alone.

In line with Heim et al.'s (2014) conclusions on shared effects induced by different training types, very different kinds of interventions have resulted in significant behavioral and neural gains in individuals with language-related deficits. For example, many studies (see **Tables 1** and **2**) have shown the remedial gains of phonological training with FastForWord, including auditory discrimination, phoneme discrimination, phoneme identification, phonic match, phonic word, understanding instructions, and grammatical structures and rules. Significant remedial gains in brain activation and behavior have, however, been obtained also with non-linguistic tasks that, at first sight, might seem to have a less obvious link to language-related deficits. Kujala et al. (2001) presented dyslexics with an intervention with nonlinguistic audiovisual training, including matching a sequence of non-speech sounds with a sequence of visual shapes. As a result of intervention, reading accuracy had improved and MMN brain responses to tone-order reversals had increased. The change in reading skills and MMN amplitude significantly correlated, suggesting an association between reading abilities and non-linguistic processing. In a similar vein, Gaab et al. (2007) used non-speech stimuli with rapid transitions to remediate dyslexia. After training, language and reading skills had improved and prefrontal regions associated with the processing of rapid transitions were more strongly activated than before training. The remedial gains for reading skills from very different kinds of intervention tasks allude to the possibility that they tap some common, domain-general process involved in, and perhaps necessary for, reading and language skills and contribute to remedial gains along with domain-specific effects.

A candidate function that may, in concert with others, participate in domain-general remedial gains is attention. Stevens et al. (2008) studied whether linguistic intervention would improve selective attention in children with SLI. As a result of training, measures of receptive language had improved and previously attenuated event-related brain responses reflecting selective attention had normalized. Stevens et al. (2013) have also suggested that children at risk for reading difficulty show atypical brain measures of selective attention, which can be remediated by reading intervention. These findings suggest that language skills and auditory attention are strongly connected, complementing the earlier findings on the role of visual attention in dyslexia (Facoetti et al., 2000; Valdois et al., 2004; Shaywitz and Shaywitz, 2008; Vidyasagar and Pammer, 2010; Franceschini et al., 2012; Vogel et al., 2012). This is in line with models of dyslexia proposing the dysfunction of the inferior parietal lobule, which has

been linked to attention (Richlan, 2012), and the observations of normalized training-induced activation in the inferior parietal areas (Temple et al., 2003; Eden et al., 2004; Meyler et al., 2008).

## **HOW LONG-LASTING ARE THE REMEDIAL GAINS IN THE BRAIN?**

Interventions aim at long-lasting gains. The dynamics of neural changes induced by intervention can be explored with follow-up neuroimaging studies, which enable to specify brain functions that show long-term effects. Shaywitz et al.'s (2004) experimental intervention group of dyslexic children returned to an fMRI scan 1 year after the intervention. The normalization of activation pattern was seen both immediately after intervention as well as 1 year after it, suggesting long-lasting remedial effects. Similarly, Meyler et al. (2008) observed hypoactivation of parietal areas before intervention in poor readers and increased activation of these areas immediately after intervention. Interestingly, when they conducted a follow-up 1 year after the intervention, they found that the activation of the parietal areas had continued to increase. Thus, the activation pattern of previously hypoactive areas had normalized, probably reflecting cumulative learning effects following intervention. These follow-up studies thus show that treatment-induced neurobiological changes, coupled with improvement in behavioral performance, can be long-lasting and may enable cumulative gains in language-related skills.

### **CONCLUSION**

Interventions and training programs involving phonological and auditory tasks have repeatedly gained remedial effects in dyslexia, SLI, and LLI. Neuroscientific research has demonstrated that improved behavioral performance is coupled with changes in both brain function and brain anatomy. Neuroimaging has revealed normalized training-induced brain activation patterns, whereas electrophysiological measures have demonstrated the normalization of strength and timing of brain responses and oscillatory activity after training. Training effects have been observed also in white matter. Especially in the study of dyslexia, neuroscientific studies have illuminated the location of aberrant brain functions, which has enabled to specify the models of the impairment. Neuroimaging studies have also highlighted partly similar and partly specific patterns of neural activation as a result of different training programs. Gains from very different phonological and auditory tasks as well as training effects in the parietal cortex support the models that propose the involvement of some domaingeneral neural mechanisms, such as attention, in language-related impairments.

In our opinion, neuroscientific studies thus give an important contribution to the treatment of language-related impairments. Specifically, we argue that the use of both neuroscientific and behavioral measures in intervention studies can increase the understanding of how and why interventions change the deficient neural networks, if methodological requirements are met (cf. Bishop, 2013). From educators' perspective, neuroscientific research methods are seldom directly applicable to the assessment of remedial interventions. However, keeping up-to-date in such

research can provide educators with better understanding of the causes of language-related impairments and help them to target interventions more accurately.

#### **ACKNOWLEDGMENT**

This work has been funded by the Academy of Finland (projects 131963, 274058, and 276414).

#### **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: 25 September 2014; accepted: 26 January 2015; published online: 17 February 2015.*

*Citation: Ylinen S and Kujala T (2015) Neuroscience illuminating the influence of auditory or phonological intervention on language-related deficits. Front. Psychol. 6:137. doi: 10.3389/fpsyg.2015.00137*

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

*Copyright © 2015 Ylinen and Kujala. 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 training as an alternative and effective method for neuroeducation and neuro-rehabilitation**

*Clément François 1,2 \*, Jennifer Grau-Sánchez 1,2 \*, Esther Duarte 3 and Antoni Rodriguez-Fornells 1,2,4*

*1 Department of Basic Psychology, University of Barcelona, Barcelona, Spain, 2 Cognition and Brain Plasticity Group, Bellvitge Biomedical Research Institute, Barcelona, Spain, 3 Department of Physical Medicine and Rehabilitation, Parc de Salut Mar, Hospitals del Mar i de l'Esperança, Barcelona, Spain, 4 Catalan Institution for Research and Advanced Studies, Barcelona, Spain*

#### *Edited by:*

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

#### *Reviewed by:*

*Yun Nan, Beijing Normal University, China Salomi S. Asaridou, University of California, Irvine, USA Maria L. Bringas, International Center for Neurological Restoration, Cuba*

#### *\*Correspondence:*

*Clément François and Jennifer Grau-Sánchez, Department of Basic Psychology, University of Barcelona, Campus de Bellvitge, Pavelló de Govern, L'Hospitalet de Llobregat, 08908 Barcelona, Spain<EMAIL_ADDRESS><EMAIL_ADDRESS>
#### *Specialty section:*

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

*Received: 03 December 2014 Accepted: 02 April 2015 Published: 28 April 2015*

#### *Citation:*

*François C, Grau-Sánchez J, Duarte E and Rodriguez-Fornells A (2015) Musical training as an alternative and effective method for neuro-education and neuro-rehabilitation. Front. Psychol. 6:475. doi: 10.3389/fpsyg.2015.00475* In the last decade, important advances in the field of cognitive science, psychology, and neuroscience have largely contributed to improve our knowledge on brain functioning. More recently, a line of research has been developed that aims at using musical training and practice as alternative tools for boosting specific perceptual, motor, cognitive, and emotional skills both in healthy population and in neurologic patients. These findings are of great hope for a better treatment of language-based learning disorders or motor impairment in chronic non-communicative diseases. In the first part of this review, we highlight several studies showing that learning to play a musical instrument can induce substantial neuroplastic changes in cortical and subcortical regions of motor, auditory and speech processing networks in healthy population. In a second part, we provide an overview of the evidence showing that musical training can be an alternative, low-cost and effective method for the treatment of language-based learning impaired populations. We then report results of the few studies showing that training with musical instruments can have positive effects on motor, emotional, and cognitive deficits observed in patients with non-communicable diseases such as stroke or Parkinson Disease. Despite inherent differences between musical training in educational and rehabilitation contexts, these results favor the idea that the structural, multimodal, and emotional properties of musical training can play an important role in developing new, creative and cost-effective intervention programs for education and rehabilitation in the next future.

**Keywords: neuro-rehabilitation, neuro-education, music training, music therapy, stroke rehabilitation, language development disorders**

## **Introduction**

Recently, the Organisation for Economic Co-operation and Development published the "2012 PISA report" providing strong evidence of the dramatic drop in the scholar level of 15-year-old French pupils over the past 10 years (OECD, 2014). Compared to data collected in 2003, 15 years old French children exhibited a drop of 15 points (from 511 to 495) in mathematics and the number of pupils in difficulty increased dramatically. In addition, learning disorders are very frequently diagnosed during childhood with the prevalence of developmental dyslexia being of 7–10% of the general population (Démonet et al., 2004; Collective expertise INSERM, 2007). These data point toward the urge of building and testing efficient learning tools to optimize the learning trajectories of typically developing young pupils and even more importantly to remediate specific disabilities found in children with language-based learning impairments. In addition to the burden in the young population, the demographic changes in life expectancy will lead to a significant increase of the population aged over 65 years old in Europe. This population is at high risk of suffering from neurologic age-related diseases (Salomon et al., 2012). For instance, the incidence of stroke is expected to grow by 36% from 2000 to 2025 (Truelsen et al., 2006). The last study of the World Health Organization Global Burden of Disease project is eloquent in showing that stroke remains the second cause of worldwide mortality (Lozano et al., 2012). Although advances in the acute medical management of stroke patients have reduced mortality in high-income countries (Feigin et al., 2014), stroke is still a major cause of disabilityadjusted life-years (Murray et al., 2012). Beyond cardiovascular diseases, the rapid aging in Europe will also increase other noncommunicable disorders such as neurodegenerative diseases. For instance, Parkinson's disease affects 2.4 per 100 inhabitants of more than 65 years and its prevalence is expected to double by year 2030 (Dorsey et al., 2007). In this context, the need to develop innovative and effective rehabilitation evidence-based techniques is a challenge for the next years in the field of neuro-rehabilitation.

During the last decade, the neuroscientific community has developed a line of research on music perception and on the musician's brain. Results obtained have largely contributed to increase our knowledge on the brain functioning in general and have allowed delineating the positive impact of playing a musical instrument on brain plasticity. In the first part of the review, we report evidence from cross-sectional and longitudinal studies showing that learning to play a musical instrument can induce substantial neuro-plastic changes in cortical and subcortical regions of motor, auditory and speech processing networks. The second part focuses on music to language transfer effect and on the necessary conditions for enhancing language processing in healthy participants. We follow by reporting an overview of the evidence showing that musical training can be an alternative, low-cost, and effective method for the remediation of languagebased learning impaired populations. We then focus on neurorehabilitation by presenting the results of studies showing that music interventions can enhance motor recovery and neuroplasticity after stroke and can ameliorate motor deficits observed in Parkinson disease. Finally we discuss some of the important similarities and differences between musical training for neuroeducation and for rehabilitation purposes.

## **Musical Practice Fosters Neuroplasticity**

In the last decade, the neuroscientific community has concentrated a great amount of effort to explore the positive impact of playing a musical instrument on the brain. Those efforts have provided converging evidence that the musician's brain is an excellent model of neuroplasticity, specifically in the sensory-motor system (Münte et al., 2002; Zatorre, 2013). Indeed, playing in a symphony orchestra requires a large amount of practice: 20-year-old orchestra musicians typically spend more than 10,000 h of musical practice (Krampe and Ericsson, 1996). During all those hours, the musician will develop and ultimately master many different competences involving sensory-motor, mnesic, cognitive control, and attentional processes. As a consequence of the repetition of this complex activity, the underlying neural substrates will be eventually modified due to functional and structural neuroplastic mechanisms (see for a recent review, Kolb and Muhammad, 2014).

## **Neuroplastic Changes in the Sensory-Motor Network**

The neuroplastic changes induced by specific training can be studied using both cross-sectional and longitudinal approaches. While longitudinal studies generally use a test-training-retest procedure with naïve participants before training, cross-sectional studies compare a group of experts to a group of laymen participants. In the case of cross-sectional studies in which eventual pre-existing inter-individual differences might account for the differences observed between the groups (Zatorre, 2013) so that causality between music training and the observed effects cannot be demonstrated. By contrast, longitudinal studies with pseudorandom assignment of the participants to a training group and a non-training group allow determining that musical training is the cause of the differences (Schellenberg, 2004). Using a crosssectional approach, Bangert and Schlaug (2006) conducted a study comparing the anatomical structure of the primary motor cortices in professional musicians and non-musicians. Using magnetic resonance imaging (MRI) these authors compared a group of nonmusicians to pianists and violinists. While pianists showed similar structural modifications over both hemispheres, violinists showed a modification only over the right hemisphere. Indeed, playing the piano or the violin involves different type of bimanual control: pianists require fast and accurate finger movements of both hands whereas violinists use both hands asymmetrically favoring fine motor control of left hand fingers and gross motor control of the right hand thus leading to such a structural asymmetry. It is interesting to note that these studies provided evidence on how practicing particular cognitive and motor induce structural plastic brain alterations and improved level of performance for instance in motor areas (Schlaug et al., 1995a; Schlaug, 2001; Schmithorst and Wilke, 2002; Gaser and Schlaug, 2003; Hutchinson et al., 2003; see also Elbert et al., 1995; Draganski et al., 2004; Bengtsson et al., 2005).

Interestingly, the level of musical practice seems to be positively correlated with the increase in gray matter (GM) over motor regions (Gaser and Schlaug, 2003). Nonetheless, a recent study using particularly well controlled and highly selected pianists challenged the results mentioned above by showing a more complex pattern with decreasing GM density in peri-rolandic and striatal areas together with increasing GM density over areas involved in higher order processing such as the right fusiform gyrus, the right mid orbital gyrus, and the left inferior frontal gyrus (James et al., 2014). Increases in GM volume in the putamen have also been associated with timing variability and irregularity of scale playing in professional pianists (Granert et al., 2011). In this study, it was also observed that patients with musical dystonia presented more volume of GM in the right middle putamen. These surprising results may relate to the age of onset of musical practice and to excessive training, a potentially important factor for influencing plastic mechanisms and neural efficiency (Amunts et al., 1997). For instance, the age of onset of musical training is correlated with the level of motor performance in a rhythm synchronization task (Bailey et al., 2014) and may be decisive for the non-linear dynamic of structural brain changes induced by musical practice (Steele et al., 2013; Groussard et al., 2014).

Musical practice can also modify the strength of the connections between distant areas via white matter modifications. Compared to non-musicians, professional pianists exhibit a larger anterior portion of the Corpus Callosum, the main white matter fiber bundle connecting the two hemispheres (Schlaug et al., 1995b). Using diffusion tractography imaging method (DTI), it has been recently reported that musicians exhibit stronger white matter connectivity in the left and right supplementary motor areas (Li et al., 2014), in the corticospinal tract (Imfeld et al., 2009) and importantly, between auditory and motor areas (Oechslin et al., 2010; Halwani et al., 2011). The strong coupling of motor and auditory networks has been confirmed by further functional imaging studies showing activation of motor areas during the listening to musical rhythms in musicians (Haueisen and Knösche, 2001; Grahn and Brett, 2007; Bengtsson et al., 2009; Grahn and Rowe, 2009). Nevertheless, non-musicians also show such audio–motor co-activation (Baumann et al., 2007).

Moreover, short-term training programs also induce functional plastic changes. When beginners learn to play simple melodies (Bangert and Altnemüller, 2003). For instance, Lahav et al. (2007) trained non-musicians to play melodies by ear during five consecutive days and found activations in premotor regions when participants passively listened to the trained melodies (see also Meister et al., 2005). By contrast, Chen et al. (2012) observed a reduction of activation in both dorsal and ventral premotor cortices during musical training of naïve participants. This pattern of reduced activation over motor areas in musicians may reflect functional efficiency changes induced by musical training (Jäncke et al., 2000). In this context, Pascual-Leone et al. (1995) were the first in observing functional reorganization during piano learning using transcranial magnetic stimulation (TSM). After 4 weeks of training, participants showed a reduction of the motor map while showed an increase during the first week. This reorganization process over cortical motor maps highlight three important aspects. Firstly, rapid functional changes can occur after a rather short period of training. Secondly, the plastic changes induced by shortterm training disappear when the training ends (see for example also Draganski et al., 2004). Thirdly, long-term training can lead to more efficient reduced patterns of activation. Aside from motor regions, plastic changes have also been reported at the level of the somatosensory cortices: musicians are more sensitive to tactile stimulations of the fingers than non-musicians, suggesting that musical practice can modify the size of the somatosensory receptive fields (Elbert et al., 1995).

Playing a musical instrument requires a clear motor component for a good performance. Nonetheless, the auditory dimension is also crucial in order to generate error feedback that might correct or adjust movements in case of errors (Maidhof, 2013; Maidhof et al., 2013; Pfordresher and Beasley, 2014) and to accurately perceive the pertinent acoustical parameters of the auditory input. Therefore, music induced plastic modifications over auditory areas might also be expected to occur.

### **Neuroplastic Changes in the Auditory Pathway**

The positive effects of musical practice on auditory processing have been evidenced by several studies showing lower discrimination thresholds for frequency, duration, silences, or time intervals in experts than in laymen (Jones et al., 1995; Kishon-Rabin et al., 2001; Micheyl et al., 2006; Rammsayer and Altenmüller, 2006; Mishra et al., 2014). In terms of structural plasticity, as in the case of the motor system, musical practice induces structural changes in the cortical auditory network: GM changes have been observed in both longitudinal and cross-sectional studies with musicians exhibiting enlarged AC compared to non-musicians (Schlaug et al., 1995a; Keenan et al., 2001; Schneider et al., 2002, 2005; Bermudez and Zatorre, 2005; Hyde et al., 2009). Moreover, compared to non-musicians, musicians also show more developed superior longitudinal fasciculus and arcuate fasciculus, the fiber bundles connecting the AC to Broca's area (Oechslin et al., 2010; Wan and Schlaug, 2010; Halwani et al., 2011).

In line with these findings, functional changes have been reported in musicians at almost every single step of the auditory pathways: from the cochlea to the inferior colliculus (IC) and finally to the auditory cortices (AC). Musicians show functional changes already at the very peripheral level with enhanced activity of the Medial olivocochlear complex, responsible for controlling the cochlear micromechanics (Perrot et al., 1999; see for a review Perrot and Collet, 2014). Since almost 10 years, the systematic work of Nina Kraus and her group have provided exciting evidence that musical practice also induces substantial neuroplastic changes over subcortical structures. The IC, a subcortical structure in the brainstem receiving both bottom-up inputs from the cochlea and top-down inputs via the corticofugal pathway (Kraus and Chandrasekaran, 2010), encodes specific characteristics of the auditory input (Russo et al., 2004). For instance, very brief acoustic events such as stop consonants ("b," "p," "g," "d," "t") are reflected by the transient response of the auditory brainstem responses (ABRs) whereas sustained acoustic events such as vowels are reflected by the frequency following response (FFR). Compared to non-musicians, adult musicians show more robust transient response and FFR to both musical and speech sounds (Musacchia et al., 2007; Parbery-Clark et al., 2012) suggesting that at the level of the brainstem, the representations of the sounds are more elaborated and more accurate in musicians than in non-musicians. The enhancement of ABRs is already visible at age three suggesting that very few years of musical training might be sufficient to elicit such consistent plastic changes in the IC (Strait et al., 2013). Moreover, the benefit of musical training received during childhood appears to remain during adulthood as revealed by a correlation between ABR amplitude and how recently participants quitted the training (Skoe and Kraus, 2012; see also Strait and Kraus, 2011).

Finally, musical practice fosters functional brain plasticity in cortical areas: compared to non-musicians, adult and child musicians show enhanced response of the AC as reflected by larger N1/P2 amplitude to complex sounds (Shahin et al., 2003, 2004; Trainor et al., 2003). Moreover, this enhanced N1/P2 is particularly visible when the stimulus presented is the instrument played by the participants (Pantev et al., 1998, 2001). Again, these results suggest that musicians have a more elaborated representation of the auditory input and better encode fine-grained features of sounds than non-musically trained individuals.

Interestingly, musical practice also increases the neural sensitivity to the statistical regularities found in the auditory input (François and Schön, 2014). For instance, a deviant sound rarely occurring within a sequence of repeated standard sounds elicit a specific event-related potential (ERP) component, the mismatch negativity (MMN), reflecting the pre-attentive detection of an auditory change (Näätänen et al., 2005; Grimm and Escera, 2011). Adult and child musicians often show larger and/or earlier MMNs to changes in several features of the sounds such as frequency, duration, intensity, or spatial localization than non-musicians (Tervaniemi et al., 2001, 2005; Van Zuijen et al., 2005; Vuust et al., 2005, 2011; Brattico et al., 2009; Marie et al., 2011; Putkinen et al., 2014). Additional evidence shows that musicians exhibit enhanced MMN to change in longer sequences of structured sounds (Tervaniemi et al., 2001; Trainor et al., 2002; Fujioka et al., 2004; Habermeyer et al., 2009).

## **Neuro-Education: Music Training as an Alternative Tool to Promote Literacy Skills**

After having delineated the positive effects of playing music on brain plasticity in the auditory and motor networks, we now turn to the topic of neuro-education We aim to give an overview of evidence showing that language-based learning impaired children often show deficits in the specific processes that are boosted by musical practice. We then present the hypothesis of music to language transfer effect, which allow grounding the subsequent evidence from both cross-sectional and longitudinal studies showing the beneficial effects of musical practice on speech processing in typically developing children. We finally summarize the few studies testing music-training programs in language-based learning impaired populations.

## **Speech Processing in Children with Language Impairment**

Children with language based learning impairments such as developmental dyslexia present a specific deficit in reading despite conventional instruction, socio-cultural level, normal intelligence and the absence of sensory deficits (Lyon et al., 2003; Vellutino et al., 2004; Collective expertise INSERM, 2007). Phonological awareness is crucial for normal language development (Ramus, 2003; Serniclaes et al., 2004) and relies on the ability to categorize speech sounds on the basis of extremely short timing differences. The voice onset time (VOT) is an acoustic parameter largely used to study phonological awareness as it allows differentiating the sound "ba" from the sound "pa," a task in which dyslexic children have difficulties (Serniclaes et al., 2004). In line with these findings, Chobert et al. (2012) were able to demonstrate that children with dyslexia are impaired in the pre-attentive processing of VOT and duration in syllables based on MMN data. Children with language learning difficulties have also difficulties in extracting speech sounds when presented in a background noise (Ziegler et al., 2005, 2009) and show degraded neural responses to speech in noise stimuli (Warrier et al., 2004; Wible et al., 2004; Anderson et al., 2010).

These children might present a general deficit in the processing of timing information (Goswami et al., 2011). This timing hypothesis would explain why they exhibit impaired phonological processing (Ziegler and Goswami, 2005) and impaired general rhythmic processing (Thomson and Goswami, 2008; Corriveau and Goswami, 2009). Huss et al. (2011) showed that children with dyslexia present a deficit in the perception of rise time, an acoustic parameter important to extract the periodic and eventually metrical structures of speech (Cummins and Port, 1998; Quené and Port, 2005; Goswami, 2010; Huss et al., 2011). Growing evidence converge on the idea that rhythmic skills are crucial for the development of literacy skills in typically developing children (Tierney and Kraus, 2013; Woodruff Carr et al., 2014) and that children with dyslexia are impaired at tapping to a rhythm, and in perceiving tempo (Thomson and Goswami, 2008; Corriveau and Goswami, 2009). These results also confirm findings showing a link between literacy skills, phonological abilities, and musical aptitudes in typically developing child and in adult participants (Anvari et al., 2002; Slevc and Miyake, 2006; Tierney and Kraus, 2013). Following this line, a recent study with 48 children with dyslexia shows that temporal auditory processing strongly predicts phonological processing and reading abilities (Flaugnacco et al., 2014).

## **Music to Language Transfer of Competences: Why and How Music Can Transfer to Language**

Transfer of skills generally occurs when a specific skill acquired in one specific domain influences processes in another supposedly unrelated domain. Several observations have lead to the hypothesis that musical practice could transfer to language and more specifically to speech processing (Kraus and Chandrasekaran, 2010; Besson et al., 2011; Patel, 2011, 2014). Firstly, as presented above, there is a whole body of literature showing enhanced auditory processing in musicians. Secondly, music and speech share similarities: both involve the processing of similar acoustic cues (such as pitch, intensity, timbre, and duration) and both involve maintaining sequences of sounds that are unfolding in time in a structured manner. Thirdly, music and speech processing show a clear overlap in their cortical and subcortical neural substrates (Koelsch et al., 2005; Vigneau et al., 2006; Schön et al., 2010), suggesting shared neural resources (Patel, 2011, 2014).

## **Music to Language Transfer Effects, Evidence in Healthy Children**

In the specific context of education, it is now clearly demonstrated that noisy environments in classroom settings with higher than normal ranges level of noise negatively impacts pupils' performance (Knecht et al., 2002; Shield and Dockrell, 2008). Indeed, the level of performance in a syllable discrimination task dramatically drops as the level of noise increases (Neuman et al., 2010). The amplitude and latency of ABRs are also clearly reduced in the

presence of acoustic noise (Burkard and Sims, 2002; Russo et al., 2004). Children with language based learning impairment show impaired speech in noise perception and altered neural responses to speech sounds presented in a background noise. Musical practice seems to be a good tool to prevent this deleterious effect of noise as adult musicians exhibit more preserved ABRs in noise than non-musicians (Parbery-Clark et al., 2009a,b; Bidelman and Krishnan, 2010; Strait et al., 2012). Furthermore, a recent longitudinal study has revealed that musical training in high school music classes can induce these changes (Tierney et al., 2013), which appear to maintain during lifespan (Zendel and Alain, 2012, 2013).

If musicians are better in perceiving speech in noise they also have refined representations of syllables (Degé and Schwarzer, 2011; Zuk et al., 2013; see also Moreno et al., 2009) at both subcortical and cortical levels (Chobert et al., 2011, 2014; Strait et al., 2012; see **Figure 1** for an illustration of the experimental design). All together, these results show that musicians have better neural encoding of speech sounds, which might help to develop a greater sensitivity to the metrical structure of speech (Port, 2003). Compared to non-musicians, adult and child musicians showed increased sensitivity to subtle pitch modifications inserted in the prosodic contour of sentences being uttered in their native or in a foreign language (Schön et al., 2004; Magne et al., 2006; Marques et al., 2007). Adult musicians are also more sensitive to the metrical structures of speech and to anomalous durational modifications in sentences (Marie et al., 2011).

Further evidence of better speech processing skills in musicians than in non-musicians was also provided by cross-sectional and longitudinal studies exploring speech segmentation ability in adults and children (François and Schön, 2011; François et al., 2013, 2014). Speech segmentation is one of the mandatory steps for acquiring a new language, which requires the ability to extract words from continuous speech. When presented with 2 min of an artificial stream of statistically structured syllables, infants and adults are able to segment and discriminate syllables sequences that are part of the stream (i.e., familiar sequences) from new sequences (i.e., unfamiliar sequences; Saffran et al., 1996; Aslin et al., 1998). While adult musicians barely outperformed nonmusicians (François and Schön, 2011), musically trained children largely outperformed their non-musician counterparts after 1 year and even more after 2 years of musical training (François et al., 2013). Moreover, neural responses in both adult and child musicians differentiated familiar from unfamiliar sequences during the behavioral test. In a further study, François et al. (2014) provided evidence that the ability to differentiate familiar from unfamiliar items was correlated with how fast a fronto-central negative ERP component emerged during the exposition to the artificial speech stream.

The mounting evidence of the beneficial effects of musical training on speech auditory processing in typically developing children as well as the timing deficits found in children with language based learning impairments led researchers to test the idea that musical training could be used as a remediation tool.

## **Music Training Programs in Language Impaired Populations**

Overy (2000, 2003) were the first evaluating the efficiency of playing music in children with dyslexia. Despite a small group and no clear matched-control, the results showed improved phonological awareness and spelling performance after a rhythmic training program. Along these lines, short rhythmic priming sequences have be used to enhance phonological processing in typically developing children and in prelingually deaf children (Cason and Schön, 2012; Cason et al., 2015) and to improve syntactic processing in children with language impairments (Przybylski et al., 2013). Despite a clear lack of controlled trials in children and adolescents with dyslexia (Cogo-Moreira et al., 2012), a recently published study confirms that musical training can improve reading skills and educational achievement in those children (Cogo-Moreira et al., 2013). Moreover, a recent study from Bishop-Liebler et al. (2014) provides clear evidence of the positive influence of musical practice on the timing deficits found in dyslexics.

Finally, recent data suggest that an adapted musical training program can enhance auditory, phonological, and cognitive processes in 8-year-old deaf children (Rochette et al., 2014) and that musical rhythmic priming can enhance phonological production in prelingually deaf children (Cason et al., 2015). These results are important for future studies in cochlear-implanted users who show profound deficits in speech in noise perception, in the perception of complex rhythms, timbres, and melodies with somewhat preserved tempo and simple rhythms perception (McDermott, 2004; Drennan and Rubinstein, 2008).

## **Neuro-Rehabilitation: Music-Based Therapies in Neurologic Population**

Music playing requires the processing of multimodal information and entails high neural demands. Multimodality is an excellent opportunity to adapt different musical activities such as playing an instrument, moving in synchrony along a rhythm or listening to music with a therapeutic purpose (Pantev and Herholz, 2011). In this section, we present rehabilitative techniques using music as a key feature to remediate motor deficits in neurological conditions.

## **Playing Music to Overcome Motor Deficits in Stroke**

Motor impairment after stroke refers to a weakness of the muscles mainly affecting the control and performance of voluntary movements (Mohr et al., 2011). This deficit is the most common outcome after stroke with paresis of the upper and lower extremities being found in almost 70% of cases (Rathore et al., 2002). While paresis of the legs impedes functional mobility such as walking, the limitations of arm and hand paresis extend to several daily-living activities (Langhorne et al., 2011).

Music-supported therapy (MST) aims to restore paresis of the upper limb through musical instrument playing (Schneider et al., 2007; see **Table 1**). In order to enhance fine and gross movements, patients are trained on playing melodies on a midi piano and/or electronic drum pads. MST relies on four basic principles: massive repetition, audio–motor coupling, shaping, and emotionmotivation effects (Rodríguez-Fornells et al., 2012). Firstly, MST requires massive repetition of simple sequences of movements through the intervention. Importantly, high-intensity practice is a basic and well-accepted principle in neuro-rehabilitation (Langhorne et al., 2009, 2011). Secondly, multimodal integration may enhance audio–motor coupling where the musical sound serves as a feedback to reinforce the movement, to correct the errors, to adjust the timing and to refine motor representations. Thirdly, the therapy is adapted to the level of impairment and to the progression of the patient. Fourthly, the emotionalmotivational aspects of music may regulate emotional responses through the playfulness of learning a new skill.

Music-supported therapy is successful in reducing the motor deficits in subacute stroke patients. Altenmüller et al. (2009) and Schneider et al. (2007) compared the effectiveness of MST to conventional treatment. Only patients in the MST group improved in frequency, velocity and smoothness of fingers and hand tapping movements. Moreover, those patients obtained greater scores over time on standardized clinical tests assessing motor functions. However, to what extent is the presence of music responsible for the observed gains and associated plasticity? In a single-case study (Rojo et al., 2011), a patient performed a passive listening task with unfamiliar and trained melodies. Interestingly, while before the application of MST the patient exhibited only activation of the AC, the motor regions were also activated after the training. This phenomenon of audio–motor coupling provided evidence that the auditory feedback is an essential part of the therapy by contributing to enhance activations over motor regions (Rodríguez-Fornells et al., 2012). In a further study, Amengual et al. (2013) used TMS to demonstrate changes in the excitability of the sensorimotor cortex due to MST. Participants recovered from their motor deficits and exhibited an increased excitability of the sensorimotor cortex in the affected hemisphere after 4 weeks of MST. Moreover, a lateral shift in the motor map of chronic patients was evidenced after the training and was associated with motor gains. Interestingly, similar results have been recently reported in subacute patients (Grau-Sánchez et al., 2013). Taken together these studies suggest that MST can induce functional changes associated to brain reorganization processes.

Recent studies aimed at modifying different aspects of the MST protocol. Van Vugt et al. (2014) implemented MST in two groups of subacute stroke patients in which participants received the therapy in pairs instead of individual sessions. One group had to play together while the other group played in turns. Although both groups improved their performance in a motor task, results indicated a positive trend favoring the in-turn group. Besides, the in-turn group improved more their mood as well as their feelings about their partner. The idea that music playing is a shared experience (Overy, 2012) is interesting to consider because patients can feel emphatic and understood by others individuals presenting similar difficulties. This could in turn enhance the mood and reduce depressive symptoms (Gillen, 2010). MST has also been evaluated in a home-training protocol (Villeneuve et al., 2014) showing improvements in the paresis of chronic patients that were maintained over time. During nine 1-h sessions, patients played musical sequences using Synthesia (Synthesia LLC) a software that provides visual cues to guide them. The sessions were complemented with at home exercises on a roll-up piano. Home sessions in chronic stages may be an appropriate cost-effective approach once patients have gained a certain degree of improvements and stabilization. In this vein, the use of new technologies and adapted software with rehabilitative purposes opens new directions in the field of neuro-rehabilitation. The recently developed MusicGlove (Friedman et al., 2014) may be an alternative tool to treat paresis in chronic stages. The MusicGlove is an instrumented glove that produces notes during gripping movements while being guided with visual stimuli displayed on a screen. An exploratory study with 12 chronic patients has revealed improvements in motor functions compared to conventional therapy or isometric training (Friedman et al., 2014).

*The abbreviations in the participants column correspond to: MST, music-supported therapy; CT, conventional treatment. The abbreviations in the results' column refers to the following motor tests: ARAT, Action Research Arm Test (Carroll, 1965; Lyle, 1981); BBT, Box and Blocks Test (Mathiowetz et al., 1985); 9HPT, 9 Hole Pegboard Test (Parker et al., 1986); APS, arm paresis score (Wade et al., 1983); FTN, Finger To Nose Test; FTT, Finger Tapping Test; Jebsen, Jebsen Hand Function Test (Jebsen et al., 1969).*

Importantly, all subacute patients involved in theses studies receive a rehabilitation program in a hospital or outpatient setting that includes physiotherapy and occupational therapy to train the affected extremity (Gillen, 2010). This may limit the interpretation of the positive effects of MST over conventional treatments because participants cannot be excluded from the standard rehabilitation program (Oremus et al., 2012). Moreover, natural brain processes of recovery take place in acute and subacute stages which may be a confounding factor (Cramer et al., 2011; Johansson, 2011; Zeiler and Krakauer, 2013). In order to control for spontaneous recovery, it is important to have comparable groups in terms of age, severity of the deficits and time since stroke. Chronic stages are characterized by a stabilization of the deficits via compensatory mechanisms at both the behavioral and neural levels (Cramer et al., 2011; Langhorne et al., 2011) and thus, it might be more appropriate to perform proper randomized controlled trials (RCT) using

within-participant designs combined together with disease progression models.

## **Using Music Listening to Improve Gait in Parkinson's Disease and Other Neurological Diseases**

The main symptom in Parkinson's disease is motor impairment in gait, which is characterized by a decreased speed, shorter stride length, and asymmetries in stride times for both lower limbs, all in turn increasing cadence of steps. This pronounced reduction in speed and amplitude is accompanied by a difficulty in initiating voluntary movements in later stages of the disease, with patients experiencing a freezing of the movements (Okuma and Yanagisawa, 2008). This limitation in walking will in turn impair balance and postural control and lead patients to a reduced activity and high risk of falls (Kim et al., 2013). A dysfunction of the basal ganglia is responsible for the mentioned symptoms (Stoessl et al., 2014) and the efficacy of pharmacological treatment reduces with time. Thus, the development of behavioral therapies may help in coping with the impairment and may be an alternative to be combined with pharmacological therapy.

One approach to enhance intrinsically rhythmical movements consists in using external sensory cues to entrain the movements (Thaut and Abiru, 2010; Thaut et al., 2014). Rhythm auditory stimulation (RAS, Thaut et al., 1996) aims to facilitate gait using metronome beats. The patient is first trained to move to the beat and then the tempo is increased from 5 to 10% over the baseline to accomplish faster movements. A first study observed that 3 weeks of RAS could improve gait velocity, stride length, and step cadence more than no treatment or self-paced training program (Thaut et al., 1996). Further studies have confirmed the positive effects of RAS on gait parameters such as overcoming freezing of gate (McIntosh et al., 1997, 1998; Thaut et al., 1997; Freedland et al., 2002; Fernandez del Olmo and Cudeiro, 2003, 2005; Arias and Cudeiro, 2010; for a review, see Nombela et al., 2013). It also improves stride length, gait velocity, cadence, and asymmetry in patients with stroke (Thaut et al., 1997, 2007; for a review in other neurological conditions, see Wittner et al., 2013). The neuroplastic mechanisms beyond the effectiveness of RAS may be due to an increased activity in the cerebellum, trying to compensate the dysfunctional pathway of the basal ganglia to regions of the premotor cortex (Fernandez del Olmo and Cudeiro, 2003). However, two studies have showed more benefits in the advanced than in the early stages of the disease suggesting that the effectiveness of RAS depends on the stage of the disease (Willems et al., 2006; Arias and Cudeiro, 2008). Moreover, some studies have explored variations in RAS, manipulating the tempo (Fernandez del Olmo and Cudeiro, 2003, 2005) as well as the rhythm with respect to the individual's baseline (Willems et al., 2006; Ledger et al., 2008). These studies have evidenced that beats presented at 20% slower than the baseline cadence does not benefit gait (Willems et al., 2006). Although other types of therapy have examined the use of other sensorial modalities (visual and proprioceptive cues), the auditory modality seems to be the best to improve gait in Parkinson's disease (Nombela et al., 2013).

## **Music Therapy and Emotion in Neuro-Rehabilitation**

Beyond motor impairment, neurological patients are at high risk for suffering psychological consequences. Around one third of stroke patients suffer from depression in the following months and years (Hackett et al., 2005; Ayerbe et al., 2013) and apathy and anxiety can also be found as a frequent neuropsychiatric consequence (Campbell Burton et al., 2011; Caeiro et al., 2013). These neuropsychiatric symptoms are thought to impact healthrelated quality of life, increase morbidity and worsen the cognitive impairments (Whyte and Mulsant, 2002; Aarsland et al., 2012; Ayerbe et al., 2013). Psychological factors can also have a negative effect on recovery and can affect the engagement in the rehabilitation program. Pharmacological interventions have small effects on treating depression and reducing its symptoms in stroke and Parkinson's disease and can also lead to negative side effects (Hackett et al., 2008, 2010; Aarsland et al., 2012). Some studies have reported that MST can reduce depression and fatigue and can improve the quality of life in stroke patients (Grau-Sánchez et al., 2013; Van Vugt et al., 2014). Music playing could be an alternative approach to target depression and neuropsychiatric symptoms through emotion regulation. However, there is little research studying the effectiveness of music therapy in the emotional domain. Compared to listening to audio books or auditory intervention, the daily listening to self-selected music during 2 months improves mood in the following months. Listening to music can also improve verbal memory and focused attention (Särkämö et al., 2008). Importantly, listening to music also induced structural changes with an increase of GM in frontal and limbic structures (Särkämö et al., 2014). Participants reported that music was helpful for relaxing and sleeping, influenced their mood and evoked memories and reflexive thoughts (Forsblom et al., 2009). Musical activities may be a tool to modulate the emotional reactions and cope with them through playfulness activity.

## **Future Research in the Field of Music Therapy in Neuro-Rehabilitation**

We focused our review on MST, RAS, and listening to music as standardized therapies to treat motor deficits and improve mood. Further research should aim to standardize interventions to build a strong dataset in this field. Moreover, the majority of studies refer to conventional treatment as the current rehabilitation program provided by the hospital. However, the content of the rehabilitation program may vary depending upon the facilities or the countries. Thus, an accurate description of the exercises performed by the control group is needed. Randomization of participants and blind evaluations of the treatment constitute RCTs and are necessary to implement interventional programs in clinical practice.

## **Musical Training for Neuro-Education and Neuro-Rehabilitation: Differences and Similarities in Conceptual and Practical Aspects**

Fundamental differences may exist between musical training for education or rehabilitation. Firstly, conceptual differences on the aim of musical training remain in the two cases. In neuro-education, musical training generally aims to boost a "typical" developmental trajectory (Kraus and Chandrasekaran, 2010), whereas in neuro-rehabilitation, musical training is rather used to normalize or compensate sensory, motor or cognitive deficits induced by a pathological condition (Cramer et al., 2011). Nonetheless, in the case of children with dyslexia, musical training will also aim to normalize the learning trajectories in order to facilitate speech and language processing which in turn may have a positive impact on educational achievement (Tierney and Kraus, 2013).

Secondly, the neuro-plastic mechanisms induced by musical training during childhood or in neurological population may be different. This might be due to the intrinsic physiological differences at play in these two cases. Animal and human studies showed that auditory stimulation received early in life enhances both sub-cortical and cortical electrophysiological responses to sounds (Sanes and Constantine-Paton, 1985; Kraus and Chandrasekaran, 2010) and persist in adult development (Zhang et al., 2001; Skoe and Kraus, 2012; White-Schwoch et al., 2013). Early in life, the neural system is immature and capitalizes on plastic changes such as myelination, neurogenesis, or dendritic growth (Kolb and Telskey, 2012; Kolb et al., 2012). On the contrary, stroke generally occurs in a mature neural system in which the insult has induced the death of neurons from a specific region and the disruption of neural networks. The plastic mechanisms underpinning recovery after stroke rely on different processes than in typical development such as restitution and substitution (Albert and Kesselring, 2012). Studies exploring the benefits of MST have shown that musical training induced functional reorganization of cortical motor maps (Amengual et al., 2013). In Parkinson disease, the aim of the therapy is to compensate the deficits in internally generated movements using music as an external cue that engages a different motor pathway to achieve the same goal, which is the initiation and normalization of gait (Nombela et al., 2013).

Thirdly, qualitative and quantitative practical differences in the type of training administered also remain. In neuro-rehabilitation settings, the training is generally provided during a relatively short period of time together with a high intensity (Albert and Kesselring, 2012). Interestingly, the use of the affected upper extremity during sessions of conventional stroke rehabilitation is minimal (Birkenmeier et al., 2010; Krakauer et al., 2012), suggesting that rehabilitation protocols should increase the doses of practice. In this context, musical training protocols for motor rehabilitation may be a good choice as they involve the massive repetition of movements with a high-intensity. Moreover, MST and RAS are most of the time individually administered and the complexity of the tasks is adapted to the progression of each patient. In the case of MST and particularly in middle to low-income countries, the training may become rather expensive due to the individualized administration of the therapy. However and importantly, when patients are discharged from the rehabilitation unit, they are most of the time physically inactive, exhibiting sedentary behaviors and have poor social interactions (Särkämö et al., 2008; Dontje et al., 2013; Tieges et al., 2015). The use home-based MST and RAS therapies may be important to encourage these patients to continue the rehabilitation and to maintain active. Moreover, listening to music could be good alternative not only to be applied at home but also in the rehabilitation unit, where most of the time patients remain in their rooms with no social interaction (Särkämö et al., 2008). Music making in neuro-education settings is generally provided in group settings with a lower intensity than in neuro-rehabilitation but importantly, the training is administered during longer periods of time thus allowing reaching a higher degree of musical complexity than in the context of rehabilitation. The group settings used with children may be more cognitively demanding than the ones used with neurologic patients. Most of the time, children have to play in synchrony with each other and ultimately create new musical pieces whereas patients will generally listen and reproduce simple familiar musical pieces.

Despite obvious differences, fundamental similarities might relate to the emotional, sensory, motor, cognitive, and social demands of music making *per se* (Herholz and Zatorre, 2012). In both fields, musical training is selected for its unique characteristics involving complex interactions between different domains and systems. Due to its multimodal aspect, musical training represents a good activity to develop audio–motor interactions, for cognitive stimulation and mood regulation. Moreover, music making as well as music listening are generally pleasant activities that are most likely to induce motivated behaviors. This is particularly the case for patients who may be more committed toward an enjoyable activity with a specific purpose rather than to a repetitive training with different rehabilitative tools. Musical training is also able to reinforce social cohesion or bonding through repetitive interindividual interactions (Huron, 2001). Another similarity may also reside on the fact that musical practice will induce positive side effects: by enhancing language processing for the educational side and by boosting spared functions for the rehabilitation side. Finally, the permanence in time of the benefits of music making is clearly observed and is probably the most meaningful aspect for both purposes.

## **Conclusion**

The neural mechanisms of music-induced plasticity are still not perfectly understood (Fukui and Toyoshima, 2008), but the evidence for a positive effect of musical practice are growing and could justify the use of music both in the context of neuroeducation (Caine and Caine, 1990) and of neuro-rehabilitation (Särkämö et al., 2014). The findings showing that the age of onset of musical training influences the dynamic of training induced plastic changes (Steele et al., 2013; Groussard et al., 2014) leads to the idea that multiple sensitive periods for specific functions and specific brain networks may co-exist in typical development (Penhune, 2011). This opens interesting perspectives to study the benefit of musical training in the developing brain as well as to study its consequences on speech perception and scholar achievement. The recent findings showing that listening to music is a rewarding experience for most of the people (Mas-Herrero et al., 2014) and that simple music listening activates the rewarding dopaminergic system (Salimpoor et al., 2013) give even more support to the idea that musical practice may be the perfect tool for neuro-education and Rehabilitation by fostering plastic changes in the healthy or pathological brains. Despite these growing evidence, the educational and health systems generally seem to be refractory to the idea of developing musical training programs. We hope that both teachers and therapists will keep on believing and applying alternative methods based on musical practice.

## **Acknowledgments**

Financial support for the present project has been received by the Spanish government (Ministry of Economy and Competitiveness [MINECO] Grant PSI2011-29219 to AF) and from the Fyssen Foundation to CF (http://www.fondationfyssen.fr/). We are grateful to three reviewers and to Dr. Mireille Besson for helping us improving the quality of the manuscript. The research leading to these results has received funding from RecerCaixa.

## **References**

Gillen, G. (2010). *Stroke Rehabilitation*. St. Louis: Mosby, Elsevier.

**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 François, Grau-Sánchez, Duarte and Rodriguez-Fornells. 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.*

# Music and Dyslexia: A New Musical Training Method to Improve Reading and Related Disorders

Michel Habib1, 2 \*, Chloé Lardy 1 , Tristan Desiles 1 , Céline Commeiras 1 , Julie Chobert 2 and Mireille Besson2

1 Résodys et Service d'Éducation Spéciale et de Soins à Domicile Résodys, Agence Régionale de la Santé, Marseille, France, 2 Laboratoire de Neurosciences Cognitives, Centre National de la Recherche Scientifique and Aix-Marseille Université, Marseille, France

Numerous arguments in the recent neuroscientific literature support the use of musical training as a therapeutic tool among the arsenal already available to therapists and educators for treating children with dyslexia. In the present study, we tested the efficacy of a specially-designed Cognitivo-Musical Training (CMT) method based upon three principles: (1) music-language analogies: training dyslexics with music could contribute to improve brain circuits which are common to music and language processes; (2) the temporal and rhythmic features of music, which could exert a positive effect on the multiple dimensions of the "temporal deficit" characteristic of some types of dyslexia; and (3) cross-modal integration, based on converging evidence of impaired connectivity between brain regions in dyslexia and related disorders. Accordingly, we developed a series of musical exercises involving jointly and simultaneously sensory (visual, auditory, somatosensory) and motor systems, with special emphasis on rhythmic perception and production in addition to intensive training of various features of the musical auditory signal. Two separate studies were carried out, one in which dyslexic children received intensive musical exercises concentrated over 18 h during 3 consecutive days, and the other in which the 18 h of musical training were spread over 6 weeks. Both studies showed significant improvements in some untrained, linguistic and non-linguistic variables. The first one yielded significant improvement in categorical perception and auditory perception of temporal components of speech. The second study revealed additional improvements in auditory attention, phonological awareness (syllable fusion), reading abilities, and repetition of pseudo-words. Importantly, most improvements persisted after an untrained period of 6 weeks. These results provide new additional arguments for using music as part of systematic therapeutic and instructional practice for dyslexic children.

Keywords: dyslexia, music therapy, phonology, reading, attention, learning disorders

## INTRODUCTION

There is worldwide agreement for estimating between 5 and 15% the school-age population that fails to get into initial learning that is, to acquire reading, writing, and/or calculation correctly, despite normal intelligence and in the absence of gross psycho-affective or socioeducative deficiency. This deficit corresponds to the "specific learning disorder" section of the latest

## *Edited by:*

Eddy J. Davelaar, Birkbeck, University of London, UK

#### *Reviewed by:*

Karsten Specht, University of Bergen, Norway Michelle Hood, Griffith University, Australia

*\*Correspondence:* Michel Habib<EMAIL_ADDRESS>
#### *Specialty section:*

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

*Received:* 17 March 2015 *Accepted:* 07 January 2016 *Published:* 22 January 2016

#### *Citation:*

Habib M, Lardy C, Desiles T, Commeiras C, Chobert J and Besson M (2016) Music and Dyslexia: A New Musical Training Method to Improve Reading and Related Disorders. Front. Psychol. 7:26. doi: 10.3389/fpsyg.2016.00026 international classification (DSM-5, 2013). Among these disorders, dyslexia has been the subject of numerous studies in recent years with results clearly demonstrating functional and structural brain abnormalities from both genetic and cultural origins. In short, experiments using brain imaging have shown abnormal activation in several cortical and subcortical brain regions and cerebellum (Démonet et al., 2004) as well as a lack of connectivity between these different areas in children or adults with dyslexia (Finn et al., 2014). This last group of results opens promising new perspectives for understanding the mechanisms underlying dyslexia and related disorders, as well as to guide remediation (van der Mark et al., 2011; Vandermosten et al., 2012). For instance, results of a recent study combining multiple imaging methods (functional magnetic resonance imaging—fMRI—, functional and structural connectivity) revealed that phoneme discrimination impairments, one of the halmarks of cerebral dysfunction in dyslexia, reflect a failure to access otherwise intact phonemic representations via the subcortical white matter bundles (including the so-called "arcuate fasciculus," which links Broca's area to the temporoparietal regions; Boets et al., 2013). The direct implication of this finding is that rehabilitation methods of dyslexia should not only focus on restoring phonological representations, as is the case of most remediations currently used with these children, but also on restoring functional connections between frontal and temporal language areas. More generally, rehabilitation should aim at increasing the integration of information typically processed by different brain areas. As we will argue below, one way to reach this aim is through music training.

Active research in the domain of the neuroscience of music has demonstrated that the brain of professional musicians is an excellent model of brain plasticity (e.g., Münte et al., 2002) both at the subcortical and cortical levels (e.g., Kraus and Chandrasekaran, 2010; Besson et al., 2011). The musician's brain is ideally suited to study brain changes induced by intensive training and the effects of a targeted and repeated cognitive activity on brain morphology, as suggested for the rehabilitation of dyslexia (Keller and Just, 2009). Interestingly, some white matter subcortical tracts, including the arcuate fasciculus mentioned above and long-known as a crucial element within the left hemisphere language network, are particularly sensitive to learning to play a musical instrument or singing (Halwani et al., 2011), both skills requiring intense and fine coordination between sensory (visual, auditory, and somatosensory) and motor processes. Previous results also demonstrated structural differences in interhemispheric fibers of the anterior region of the corpus callosum connecting motor cortical regions of the right and left hands (e.g., Schlaug et al., 1995). This finding may be related to structural abormalities of such interhemispheric fibers in children and adults with dyslexia, suggesting that interhemispheric communication failure may be one of the possible mechanisms underlying this disorder (Welcome and Joanisse, 2014).

Using musical training for the remediation of dyslexia and language disorders is based on both theoretical considerations and experimental results. If there are common underlying processes between music and language, especially between music perception and speech perception, one might assume that improving some of the processes involved in the perception of music can also improve speech perception and reading skills (e.g., Goswami et al., 2002; Patel, 2003, 2012; Kraus and Chandrasekaran, 2010; Besson et al., 2011; Corrigall and Trainor, 2011). In one of the first studies aimed at testing this hypothesis, Overy (2000, 2003) proposed a series of music games gradually increasing in difficulty and focusing on pace and "timing" skills to dyslexic children over a period of 15 weeks. Results showed significant improvements, not in reading skills, but in two related areas: phonological processing and spelling. More recently, Cogo-Moreira et al. (2012, 2013) reported that musical training had positive effects on reading skills and educational achievement in children and adolescents with dyslexia and Weiss et al. (2014) showed that adult musician dyslexics performed better than nonmusician normal readers on various pitch interval discrimination tasks, finger rhythmic tapping, and speech in noise perception tasks.

The importance of word metric structure and, specificially, rise-time perception for speech processing has been stressed by Goswami et al. (2002). They proposed that misalignments between neuronal excitability fluctuations in the auditory regions and maximum amplitudes in the speech signal may be related to phonological disabilities in children with dyslexia (Power et al., 2013). In line with this view, Bishop-Liebler et al. (2014) recently reported that adult musician dyslexics were better than non-musician dyslexics on various tests of temporal auditory processing and specifically for processing temporal envelope and "rise time." In addition, musician dyslexics outperformed their non-musician peers on reading scores and also, to a lesser extent, on phonological awareness. Similarly, Flaugnacco et al. (2014) showed that, among other rhythm production and perception tasks, the level of performance on a metric perception task (i.e., perceiving changes in note duration within recurrent series) specifically predicted both reading speed and accuracy as well as phonological processing in Italian dyslexics. The authors concluded that their results strongly encourage the use of music training in dyslexia rehabilitation, and specifically recommended to "focus on rhythm rather than on pitch accuracy as is often the case in classical music pedagogy." This recommendation is in line with recent work from the Kraus group (Slater et al., 2013), examining the effect of 1 year musical training based on the perception of pitch, rhythm (tapping in synchrony with a given tempo) and improvisation. The level of performance of 8 year-old children considered "at risk" for learning disability and who received this musical training was significantly higher than matched controls in the synchrony tapping task. Going one step further, Przybylski et al. (2013) examined the influence of rhym perception on syntactic processing. They presented to language and reading impaired chidren a rhythmic prime (a succesion of notes played either regularly or irregularly), immediately followed by a spoken sentence that was syntactically correct or incorrect (e.g., "Laura has/have forgotten her violin"). Results showed a clear superiority for regular over irregular rhythmic primes on the chidren's performance in the syntactic task. Based on these results, the authors proposed to use rhythmic stimulation in remediation protocols designed for chidren with oral and written language developmental disorders (see also Cason and Schön, 2012; Cason et al., 2015, for similar results with prelingually deaf children).

In a previous work from our group (Chobert et al., 2012), we recorded the Event-related brain Potentials in an original mismatch negativity (MMN) protocol to test for the pre-attentive perception of syllables varying in pitch, duration or voice-onset time. We found that dyslexic children differed from matched controls in the MMN to voice-onset time and to duration but not to pitch variations; that is, to the two time-related among the three variables examined. Directly related to this issue, Bidelman et al. (2014) conducted a series of experiments examining categorical perception, the cornerstone of speech perception, in younger and older adult musicians and nonmusicians. Results consistently showed improved categorical perception in musicians than in non-musicians in both younger and older adults. Based on these results and others showing that categorical perception is often impaired in children with dyslexia (Serniclaes et al., 2004), the first aim of the experiments reported here was to further test for categorical perception of voice-onset time (identification and discrimination) in children with dyslexia compared to control normal-readers.

The second aim was to examine perception of word metric structures in children with dyslexia and in normal-readers. We used the materials built by Magne et al. (2007) and comprising trisyllabic words spoken at a normal speech rate or with an unusual lengthening of the penultimate syllable. We hypothesized that children with dyslexia would perform lower than normal readers in the detection of unusual syllabic lengthening.

The third aim was to further test pitch discrimination in dyslexic children since results reported in the literature are quite variable showing both normal or abormal pitch processing in different studies (e.g., Baldeweg et al., 1999; Santos et al., 2007; Chobert et al., 2012). We included a pitch discrimination task with changes in melodic contour, harmony or both contour and harmony in simple nursery rhymes.

The last and most important aim was to determine whether a specifically-designed Cognitive-Musical Training (CMT) method can improve categorical perception as well as perception of the metric structure of words and possibly pitch discrimination in children with dyslexia. Based on the literature review above, we reasoned that the CMT method should include at least three components: (1) an auditory component targetting the language-music similarity in auditory perception, (2) a motor component, mainly focusing on rhythm production and imitation, and (3) a cross-modal component, making special demands on simultaneous processing of information from different modalities including auditory, visual, sensory, and motor modalities as well as their combinations. To this end and in order to stimulate auditory attention and working memory abilities, the CMT program comprises a battery of musical tasks and exercises based on these components and on the active listening to various sorts of musical stimuli. Multimodal training combining different modalities, as is typically the case in real life, was achieved through tasks that simultaneously involve visual, auditory, and sensory-motor processing. Simplified visual and gestural supports were provided that were adapted to each child's level of performance. For instance, a very simple musical notation system was purposefully devised, made of only 3 or 5 strokes to represent pitch and duration of sounds. The rhythmic aspect of each task was emphazised (for details regarding the content of exercises and tasks, see the Methods Section below and Habib and Commeiras, 2014).

Two experiments were conducted with two different populations of dyslexic children, using similar tasks and materials and only differing in the duration of the musical training period. Thus, we compared the effects of the CMT program when training sessions were clustered on 3 consecutive days and when they were distributed over a period of 6 weeks.

## STUDY 1: INTENSIVE COGNITIVE-MUSICAL TRAINING (CMT) CLUSTERED ON 3 CONSECUTIVE DAYS

## Methods Participants

A group of 12 children from 8.2 to 11.7 years (mean 10 years 7 months, s.d. = 17 months) participated in the study. They all received a common diagnosis of severe dyslexia leading to their admission in specialized classes with multi-disciplinary support for dyslexic children. Thus, all children were already involved in intensive conventional rehabilitation methods, but during this 3-day CMT period, they did not receive speech therapy. The clinical characteristics of the children are reported in **Tables 1, 2**. A reading-age matched normal-reading group of 22 children (30 months younger on average), served as a control population for normative data. As seen from **Tables 1, 2**, the diagnosis of severe dyslexia rests on the presence of significant delay in terms of reading age as well as reading isolated words. General intelligence was largely preserved, as shown by scores on the similarities and matrices substests of the WISC-IV scale. Spelling and auditory-verbal short-term and working memory were more variably altered.

## Training Procedure Description of the CMT Method

The CMT method was designed by speech therapists based on widely recognized principles of effective intervention (i.e., goal-directed, systematic, and coherent progression along a hierarchical structure; Shaywitz, 2005). Several exercises were built that covered various dimensions and components of music: pitch, duration, tempo, pulsation, and rhythm and that aimed at developing both the perception and the production sides. Exercises also comprised both sensory (visual and auditory) and motor components, engaging the child into transcoding processes from one modality to another (e.g., tapping in synchrony with a heard sequence, tapping the written notation of a rhythm; learning to play a small melody and to correct errors in other children's performance; etc...). The use of a piano keyboard was systematically added to provide children with the visuo-spatial organization of the white and black keys, as a reinforcement for the sequential nature of the musical

TABLE 1 | Level of performance of dyslexics and control normal-readers (with indication of two standard deviations below norm) in several standard psychometric tests.

Significant control/patient differences are in bold (T-test, \*p < 0.05). Reading ages are in months.

scale. Also and as often as possible, exercises required body movements to be performed in line with the musical excerpts. Finally, the connection between music and language was used through exercises implicating both speech and music (e.g., nursery rhymes, tracing the prosody of a sentence on a sheet of paper...). During the CMT sessions, no speech therapy was used and no conventional exercises (e.g., related to phonology reading or writing) were performed. However, most children were also involved in their usual weekly treatment, more or less half an hour, one or two times per week with a speech therapist.

The CMT program started on the first day of winter vacation in an outbuilding of the University Hospital, after the children and their legal representatives had agreed to participate in this experiment that was approved by the ad-hoc local ethics committee. They were fully informed of the aim and content of the research program. The training workshop lasted for 3 whole days, 6 h per day, for a total of 18 h. Children were divided into three groups of four and they all participated in three training sessions including (1) specific musical exercises given by a speech therapist, (2) music education with piano instruction with a piano professor, and (3) percussion and rhythmic bodily exercises with a psychomotor therapist. Each session lasted 45 min, with a 15 min break before moving onto the next training session. Each of the 3 days included the same sequence of sessions, only varying in level of difficulty. At the end of each day, all children met in a dance hall, where they practiced folk dancing with a specialized teacher. Children were informed that they will perform in front of their parents and teachers at the end of the third and final day to give a more recreational and challenging aspect to the whole training and to increase their motivation.

## Assessment Tests

As described below, three tasks tapping into different aspects of auditory and speech perception, were used: categorical perception (identification and discrimination tests), syllabic duration and pitch variations. The level of performance in each task was measured in children with dyslexia both before and after training. For comparison purposes, the level of performance in each task was also measured in control normal-readers who did not follow the CMT program as they were not impaired in the perceptual, cognitive, and motor abilities that the CMT aimed at improving.

## Categorical Perception of the Phoneme "b" in the Syllable [Ba] Identification Task

A 9-step continuum between two phonemes (i.e., "b" in syllable "Ba" from B1 to B4 and "p" as in syllable "Pa" from B5 to B9) was used with voicing delays varying between −52 and +20 ms. The identification rate of Ba (that of Pa being represented by the

## Discrimination Task

reverse curve) was computed.

Eight pairs were formed (from Ba1–Ba2 to Pa8–Pa9) using the nine syllables of the continuum. The rate of correct discrimination (same-different) was computed.

### Syllabic Duration Task

Children listened to 42 tri-syllabic words (e.g., "canapé") and they had to decide whether the word was spoken normally or with an incongruous lenghtening of the penultimate syllable (e.g., "ca**naa**pé"). The percentage of correct responses was measured. **Pitch discrimination task**: children listened to five nursery rhymes played on the piano (e.g., "Sur le pont d'Avignon"; each around 20 s duration) that were recorded in four different versions: exact version, pitch change within the melodic contour, pitch change out of melodic contour, pitch change out of melodic contour and out of harmony, for a total of 20 trials. Children were asked to decide whether each fragment was the normal version or not.

## Data Analysis

First, we compared dyslexics and normal-readers in the different tasks (identification and discrimination tasks for categorical perception, metric, and pitch discrimination tasks) using Analyses of Variance (ANOVAs) including Group (Dyslexics vs. Controls) as a between-subject factor and Position on the continuum (nine Positions; identification task), Pairs (eight different pairs; discrimination task), Syllabic duration (normal vs. lengthened; metric task), or Pitch (normal pitch, pitch change preserving melodic contour, pitch change out of melodic contour, and out of harmony) as within-subject factors in separate ANOVAs. To test for the effects of the CMT program in dyslexic children, we also computed ANOVAs including Session (before vs. after CMT) as well as the within-subjects factors described above for each task. Simple effects were analyzed using posthoc Fischer's PLSD tests. All analyses were computed using the Statistica program.

## Results

#### Categorical Perception

As shown in **Figure 1A**, the percentage of syllables identified as "Ba" differed between children with dyslexia before CMT and normal-readers. However, while, the main effect of Group was not significant [F(1, 29) = 2.16, p = 0.15], the main effect of Position [F(8, 29) = 193.61, p < 0.001] and the Group × Position interaction [F(8, 232) = 6.97, p < 0.001] were significant. Posthoc analyses showed that the between-group differences were significant for position B2 (p < 0.007), with a higher percentage of "Ba" identification for dyslexics than controls as well as for B5 (p < 0.03), B8 (p < 0.02), and B9 (p < 0.002), with a lower percentage of "Ba" identification for dyslexics than for controls.

For the discrimination task (see **Figure 1B**), both inter- and intra-categorical pairs were presented (the latter being harder to discriminate). Neither the between-group difference (F < 1) nor the Group × Pairs interaction (F < 1) were significant. Only the main effect of Pairs was significant [F(7, 33) = 5.56, p < 0.001] with the highest percentage of correct discrimination for the B4–B5 pair (Pair 4 on **Figure 1B**) for all children.

Testing for the effect of the CMT program, results of separate ANOVAs for dyslexics in the identification task showed significant improvements after 3 days of CMT with no main effect of Session (F < 1) but a significant main effect of Position [F(1, 11) = 68.94, p < 0.001] and a significant Session × Condition interaction [F(8, 88) = 2.41, p < 0.021]. Post-hoc analyses showed that both within-category and inter-category perceptions were modified after training (B2: p < 0.03; B6: p < 0.03; and B9: p < 0.04).

Results for dyslexics in the discrimination task revealed that the main effect of Session was marginally significant [F(1, 11) =

between the syllables [ba] and [pa]. In the identification test (A) dyslexic children before CMT (red) showed less steep intercategorical boundary than normal readers (blue) but a "normalization," specifically for B5 and B6 after CMT (green). In the discrimination task (B), dyslexics before CMT (red) seemed to differ from normal readers (blue) for items at or close to the inter-categorical border (median peak in the figure) but these differences vanished after CMT (green).

3.61, p < 0.08] but the main effect of Pairs as well as the Session by Pairs interaction were significant [F(1, 11) = 16.32, p < 0.001 and F(7, 77) = 3.28, p < 0.004]. The improvement in phonetic discrimination after CMT was largest for the pairs 4 and 5. Posthoc analyses confirmed both intra (pairs B1-B2; p < 0.02) and inter (B5-B6, p < 0.007) category perception improvement.

#### For the Syllabic Duration Task (Figure 2)

The level of performance of dyslexics before training was significantly lower than for normal readers [main effect of Group: F(1, 33) = 4.97, p < 0.03]. Moreover, all children performed lower for words with lengthening of the penultimate syllables than for normally spoken words [main effect of Condition: F(1, 33) = 27.21, p < 0.001] and the Group × Condition interaction was also significant [F(1, 33) = 4.2, p < 0.05]. Post-hoc comparisons showed that dyslexics (52%) performed lower than controls (64%) for words with lengthening of the penultimate syllables with no differences for normally spoken words (dyslexics: 73% and controls: 78%).

Importantly, results of separate ANOVA for dyslexics, showed that the main effects of Session and Syllabic duration were significant [F(1, 11) = 16.62, p < 0.001 and F(1, 11) = 8.96, p < 0.01 respectively]. The Condition × Session interaction was only marginally significant [F(1, 11) = 3.15, p = 0.10]: the level of performance of dyslexics was higher after CMT than before for both normally spoken words (after: 81% and before: 73%) and for lengthened words (after: 69% and before: 52%). Nevertheless, results of post-hoc tests showed that the improvement was larger for lengthened words (p < 0.002) than for normally spoken words (p < 0.02).

#### For the Pitch Discrimination Task (Nursery Rhymes)

Results revealed that dyslexics did not differ from controls before CMT [main effect of Group: F(1, 32) = 1.36, p > 0.25]. The main effect of Condition was significant [F(3, 96) = 89.35, p < 0.001] but the Group × Condition interaction was only marginally significant [F(3, 96) = 2.34, p = 0.07]. The differences between dyslexics and controls were larger for the exact version condition (p < 0.05) than for the other three conditions (all p > 0.50).

Results of separate ANOVA comparing dyslexic children before and after the CMT program showed no main effect of Session (F < 1) and no Session × Condition interaction (F < 1). The overall percentage of correct responses of dyslexic children was not higher after (56, 30, 26, 30%) than before CMT (54, 30, 30, 29%). By contrast, the main effect of Condition was significant [F(3, 33) = 18.06, p < 0.001]. Results of post-hoctests showed that the level of performance was highest for the "normal" condition (p < 0.002).

## Discussion

Results of this first experiment that aimed at testing the effects of an intensive use of the CMT method over 3 consecutive days in children with dyslexia, revealed two findings of main interest. First, compared to normal-readers, dyslexics were impaired in the identification test of categorical perception but their level of performance reached the level of control children after 3 days (18 h) of the CMT program. That dyslexics and controls were significantly different in the identification task before training suggests an excessive intra-categorical and less clear intercategorical perception. Importantly, intensive music training positive influenced categorical perception by facilitating syllabic identification based on differences in VOT between the "b" and "p" phonemes. Likewise, there was a significant improvement in the discrimination test of categorical perception wherein intra-categorical pairs were more often perceived as different by dyslexics than by normal-readers, possibly reflecting some type of allophonic perception (Serniclaes et al., 2004). Overall, these results are in line with improved perception of VOT with music training in normal readers (e.g., Chobert et al., 2014) and with vowel identification in young and older musician compared to non-musician adults (Bidelman et al., 2014).

The present results also showed that while the level of performance of children with dyslexia before CMT was lower than normal readers in the syllabic lengthening task, it was significantly improved after 3 days of CMT. These findings are in line with those of a previous study using the same stimuli and showing that musicians were more sensitive than nonmusicians to the abnormal lengthening of the penultimate syllable of trisyllabic words (Marie et al., 2011). More generally, these results support the view that deficits in children with dyslexia are linked to temporal processing of speech insofar as time-dependent variables such as VOT and duration are the most altered (Goswami et al., 2002, 2013). In this respect, the improvement found after music training in the children tested here possibly resulted from the CMT focusing on the manipulation of the temporal characteristics of sounds: rhythm and tempo for non-speech sounds and duration or voicing for speech sounds. Finally, the present results showed no deficits in pitch discrimination in dyslexics (e.g., Chobert et al., 2012), unlike previous evidence of the contrary (e.g., Baldeweg et al., 1999; Santos et al., 2007), and no improvement after CMT. However, this is to be expected since the CMT focussed on the rhythmic and temporal aspects of music training.

In sum, these results were encouraging in showing a positive effect of the CMT program on auditory-verbal variables that were not specifically trained after 3 days (18 h) of intensive intervention. While the several caveats present in this experiment (e.g., lack of an appropriate control group, multi-dimensionality of the MT program. . . ) will be considered in the general discussion, we first present the second experiment aimed at testing the effects of this type of intervention conducted over a longer period. To this aim, the CMT program was used with a different group of children with dyslexia trained over 6 weeks. We used the same tasks as in Experiment 1 together with several standardized psychometric tests of various cognitive functions.

## STUDY 2: COGNITIVE-MUSICAL TRAINING OVER 6 WEEKS: ANALYSIS OF THE EFFECTS ON A BATTERY OF COGNITIVE AND SPEECH TESTS

Many questions remained unanswered after Experiment 1. First, it was of importance to determine whether the effects observed after three CMT training days could be replicated in conditions more compatible with regular primary school schedule, so that it can be applied in current practice by speech therapists or other specialists. Second, it was of interest to test whether the observed effects generalized to variables directly involved in the nature of learning difficulties such as phonology, reading, or spelling. Third, one could question the sustainability of the observed effect since it would lose interest if it only proved ephemeral.

To answer these questions, we used a CMT similar in content and total duration but spread over 6 weeks and in a different context, that of a classroom of 12 dyslexic children, all of them with a main diagnosis of severe dyslexia. We took advantage of the existence, in the Marseille area, of schools providing special classrooms for dyslexic children (i.e., "CLIS-DYS": sections for school inclusion of dyslexics). In contrast to the previous study, the experimental design involved three 6-week periods, including two untrained periods, one before (between T1 and T2) and one after (between T3 and T4) the CMT period (between T2 and T3). Measurements were taken four times, before and after each period (i.e., T1, T2, T3, and T4).

We hypothesized that the children's level of performance in auditory, phonological, and reading tasks, but not in writing and visual tasks, would specifically improve during the CMT period that is between T2 and T3. Any improvement between T1 and T2 (i.e., before the start of CMT) would suggest the influence of other, confounding factors. Moreover, the lack of significance for T4 vs. T3 comparisons would be compatible with the persistence of the beneficial effects beyond the end of CMT.

## Methods

### Participants

A total of 12 children were grouped according to the intensity of their problems and not on age. Indeed, their age difference prompted us to work on homogeneous groups of four children based upon school criteria provided by the teaching team:

## Training Protocol

All children were participating in workshops that took place during school time as detailed below, 3 h per week for 6 weeks. Within each of the 6 weeks, four interventions took place: two workshops of 1 h of CMT in full class (12 children) provided by a speech therapist and two musical workshops in smaller groups (4 children) for half an hour, including piano and percussion practice. Although they differed in mean age, the four groups basically received the same type of intervention, with similar content but with the easiest exercises for the youngest children. The content of the training was similar to Experiment 1, except for the dancing activity which was not proposed in Experiment 2.

## Assessment Battery