Mate copying has been hypothesized to save time and cognitive effort through social learning otherwise needed to evaluate the quality of potential mates (Dugatkin, 1992; Pruett-Jones, 1992; Westneat et al., 2000). However, individual-based copying also carries a possibly costly consequence: It places mate seekers especially in the thick of competition (Brennan et al., 2008), specifically when the mates have already been chosen by others. In many species, competition often leads to intrasexual conflict which can induce serious survival costs (Bowers et al., 2011). Therefore, some researchers have suggested that mate copying is a strategic use of public information via social learning (Richerson and Boyd, 2005; Little et al., 2008, 2010). That is, mate copying may be not just a blind copying, but a process involving copiers' recon on trade-offs between personal and public information use (Laland, 2004; Kendal et al., 2005), and how and when the public information will be most useful (Little et al., 2010). Indeed, once social learning evolved, it would pay to be selective about whom to learn from and what cues to learn because some models will be more successful than others (Henrich and Gil-White, 2001). Previous studies have shown this 'selection bias' in mate copying. For example, men and women were influenced in their judgment of attractiveness of potential mates by the apparent choice of attractive members of the same sex (Sigall and Landy, 1973; Yorzinski and Platt, 2010; Little et al., 2011). Another study using images that were presented with a fictitious partner has shown that both men and women find a face paired with an attractive partner to be more attractive than one paired with an unattractive partner for a long-term but not a short-term relationship (Little et al., 2008). In non-human species, bias has been observed in fish that while younger female guppies copy the choice of older females, the latter do not copy the choice of the former (Dugatkin and Godin, 1993).

In addition, copying effects can be trait-based and more general, where individuals learn about the traits of those chosen and find those traits more attractive in other individuals (White and Galef, 2000; Godin et al., 2005; Swaddle et al., 2005). This generalization has also been shown quite complicated. For example, while the generalized change of attractiveness ratings has been found with manipulations of eye-spacing (Little et al., 2010), the other studies indicate that both males and females fail to exhibit trait-based mate copying for facial traits, yet exhibit it for hair and clothing traits (Bowers et al., 2011) and shirt color trait (Place et al., 2010).

In a summary, in the learning process of mate copying, copiers may need to integrate and select information from the observed partners and then make an appropriate response accordingly. This cognitive execution function has been found especially related to the dorsolateral prefrontal cortex (DLPFC) in recent study (Buckholtz and Marois, 2012). For example, the 'integration-and-selection' hypothesis suggests that the role of DLPFC is to guide the selection of a specific response from among possible response options by integrating relevant information with context-specific rules about how to apply this information (Buckholtz and Marois, 2012). Thus, we hypothesized that compared with the condition of models with uninterested attitude toward the target, the DLPFC should be more active in the condition where models are interested in the potential mates because copiers have to integrate information to recon on tradeoffs between personal and public information use (Laland, 2004; Kendal et al., 2005) and which information will be most useful to make an adaptive decision.

Accordingly, we conducted a behavioral and a fMRI experiment to test our hypothesis. The behavioral experiment was conducted to test the effect of mate copying by using a similar paradigm of previous research (Little et al., 2008; Place et al., 2010; Yorzinski and Platt, 2010; Bowers et al., 2011). Specifically, participants were first asked to rate the attractiveness of isolated opposite-sex (potential mates) faces, then shown the targets associating with a neutral-faced model (compound images) with textual cues indicating the models' attitudes (interested vs. notinterested) toward the potential mates, and then asked to reevaluate the potential mates' attractiveness. The effect of mate copying was assessed by calculating the attractiveness ratings assigned to the individual opposite-sex facial photographs before vs. after viewing the compound images in the interested and not-interested conditions. The fMRI experiment was conducted using the similar rating-observation-re-rating procedure. The scanning process was performed while participants viewing the compound images, which has been the key social learning process in mate copying (Richerson and Boyd, 2005; Jones et al., 2007; Little et al., 2008, 2010, 2011; Yorzinski and Platt, 2010; Bowers et al., 2011). The activated brain regions involved in the learning process related to mate copying can be extracted by comparing trials in the interested condition with trials in the not-interested condition. The difference in DLPFC activation was predicted to be captured by the above-mentioned statistical analyses.

# MATERIALS AND METHODS

#### Participants

There were 92 participants (46 of each sex; age range: 18– 24 years; mean age ± standard deviation: 21.56 ± 2.12 years) recruited from a university community with flyers and by word of mouth. All were healthy, self-reported heterosexuals with normal or corrected-to-normal vision, and all provided written informed consent. The study protocols were approved by the ethics committee of the university. Participants were randomly assigned to separate behavioral (N = 60, 30 of each sex) or scanning (N = 32; 16 of each sex) pools at signup. Scanning participants were screened for current psychiatric diagnoses, and right-handedness. Participants were paid and debriefed after they finished the experiment.

# Stimuli

#### Individual Photographs

fpsyg-07-00546 April 16, 2016 Time: 16:18 # 3

Stimuli were color photographs of 64 men and 64 women from the local university student population. All photographs captured a neutral expression and showed a frontal view without makeup, accessories, or glasses. They were cropped at the neck and adjusted to 300 × 300 pixels against a white background in Adobe Photoshop. The lighting conditions were adjusted to a consistent standard. The photographs were rated for attractiveness by other participants from the university using a 1–7 Likert scale (1 = very unattractive, 7 = very attractive). The rater group included 30 males and 35 females (age range, 18–27 years). Mean attractiveness scores for male and female faces were 3.06 ± 0.80 and 3.32 ± 0.78, respectively. We included photographs with mid-range attractiveness scores (M ± 1 SD) to exclude extremely attractive or unattractive individuals. Neither the participants who rated the photographs nor the individuals in the photographs participated in the behavioral/fMRI experiments.

#### Compound Images

Photographs were edited in Adobe Photoshop to create dualimage compounds (300 × 400 pixels). Each compound image included one male and one female photograph, which were chosen randomly and arranged side by side against a gray background (**Figure 1**). The side on which the female face was displayed was counterbalanced across the compounds. In total, 64 compound images were used in the experiment.

#### Textual Cues

All word cues were in Simplified Chinese and placed at the bottom of the compound images. An affirmative sentence " " (The woman/man in the picture is interested in the man/woman) was assigned to half of the compounds, and the annulling sentence " " (The woman/man in the picture is not interested in the man/woman) was assigned to the other half of the compounds. For each sex of the participants, they would only be presented with words indicating the same-sex models' attitude toward the opposite-sex potential mates.

# Procedure

A rating-observation-re-rating procedure was performed. The participants performed the whole process at a computer and finished the re-rating process immediately after each compound image in the behavioral experiment, whereas participants performed the observation process in the scanner and completed the rating and re-rating processes immediately before and after scanning, respectively, outside of the scanner in the fMRI experiment. The task was otherwise identical.

Specifically, in the first rating process, each participant was shown the 64 individual opposite-sex photographs one by one, in a random order on a computer monitor and was asked to rate each face for attractiveness using the 1–7 Likert scale (where 1 = very unattractive, 7 = very attractive) on a self-determined pace.

For the behavioral participants, after the initial rating process, each of the 64 compound images was randomly presented for 2700 ms with an inter-stimulus interval (ISI) of 300 ms and the participants were asked to observe them attentively. As soon as the compound image disappeared, the target (the opposite-sex photograph) in the compound was presented and participants were asked to rate the attractiveness using the 1–7 Likert scale in a self-paced speed.

In the fMRI experiment, we scanned the observation process after the initial rating process out of the scanner. After a structural scan, each participant's assigned series of image compounds was presented and they were asked to observe them attentively. The stimulus presentation, timing, and counterbalancing of the compound images are outlined in **Figure 1**. There were eight blocks. Each block contained eight instances of the same compound type. Each compound image was presented for 2700 ms with an inter-stimulus interval of 300 ms. Images of each type block (interested vs. not interested) were presented in an alternating fashion, with the presentation order of the blocks being counterbalanced across participants. Each block lasted for 24 s with a 24-s rest between blocks, during which a black fixation cross was presented against the gray background. The re-rating process was a repetition of the first one, which was performed immediately after the scanning outside of the scanner.

After finishing the experiment, all participants reported that they were not familiar with any of the individuals pictured.

### Data Acquisition

Imaging was performed with a 3.0-T Siemens Trio Tim Scanner (Erlangen, Germany) with a 32-channel head coil. T1 weighted sagittal structural images were acquired first with the following parameters: TR/TE = 2530 ms/2.34 ms, field of view (FOV) = 256 mm × 256 mm, flip angle = 7 ◦ , and voxel size = 1 mm × 1 mm × 1 mm, 192 slices. The stimuli were presented via the in vivo ESys fMRI system (Gainesville, FL, USA). Functional images were obtained with a gradient echo-planar imaging sequence (TR/TE = 2000 ms/30 ms, FOV = 192 mm × 192 mm, flip angle = 90◦ , voxel size: 3.13 mm × 3.13 mm × 3.5 mm, 32 slices).

# Data Analysis

#### Behavior

The dependent behavioral variable in the two experiments was the attractiveness rating that the participants assigned to the individual opposite-sex facial photographs. A 2 (pre- vs. post-observation) × 2 (interested vs. not-interested) repeated measures of ANOVA (rmANOVA) on the attractiveness rating of opposite-sex faces was conducted to obtain the effects of experimental manipulations on mate copying.

#### Functional Magnetic Resonance Imaging

Imaging data preprocessing was performed using Statistical Parametric Mapping software, version 8 (SPM8; The Wellcome Department of Imaging Neuroscience, London, UK). The first four volumes were discarded to exclude calibration effects. The functional images were realigned to the first image to correct for interscan head movements. Six participants

compound images of the same type. Two kinds of blocks were alternated between each other, with the order of the blocks counterbalanced across participants. A black fixation cross appeared in the center of the screen during the 24-s pre-block rest periods.

(four male, two female) who had excessive head movement (translation ≥ 2 mm, rotation ≥ 2 ◦ ) were excluded from further analysis. The individual T1-weighted, 3D structural image was co-registered to the mean EPI image generated after realignment. The co-registered structural image was then segmented into gray matter (GM), white matter (WM) and cerebrospinal fluid (CSF) using a unified segmentation algorithm (Ashburner and Friston, 2005). The functional images after the realignment procedure were spatially normalized to the Montreal Neurological Institute (MNI) space (resampled to 2 mm ∗ 2 mm ∗ 2 mm) using the normalization parameters estimated during unified segmentation and then spatially smoothed with a Gaussian kernel of 8 mm full-width halfmaximum (FWHM).

Statistical analyses were performed using a general linear model. The two stimulus types (interested, not-interested) were modeled as a boxcar function convolved with the canonical hemodynamic response. The models additionally included six movement parameters derived from realignment as covariates of no interest. We applied a high-pass filter with a cut-off of 128 s to remove low-frequency signal components. For each subject at the first-level analysis, simple main effects for the interested and not-interested conditions were calculated by applying the '1 0' contrasts. The two first-level individual contrast images were then analyzed at the second group level by employing the random-effects model.

The main effect of models' attitude was calculated by contrasting trials in the interested condition with trials in the notinterested condition (interested > not-interested) and the reverse contrast (not-interested > interested) to identify brain regions involved in the learning process of mate copying. Activations were reported significant with a voxel-level threshold of p < 0.001 (uncorrected), and a cluster size of k > 50.

# RESULTS

# Behavioral Results

For the behavioral experiment, a 2 (pre- vs. post-observation) × 2 (interested vs. not-interested) repeated measures of ANOVA (rmANOVA) on the attractiveness rating of opposite-sex faces revealed significant main effects of pre-to-post ratings (F1,59 = 25.88, p < 0.001, η 2 p = 0.31) and attitude (F1,59 = 53.28, p < 0.001, η 2 p = 0.48). The effect of interaction was also significant, F1,59 = 25.32, p < 0.001, η 2 p = 0.30. Simple effects analysis showed that though the post-attractiveness ratings were significantly higher than the pre-ratings for both conditions (interested: Mpost = 3.49, SDpost = 1.26; Mpre = 2.54, SDpre = 1.02; F1,59 = 66.10, p < 0.001, η 2 p = 0.53; not-interested: Mpost = 3.12, SDpost = 1.24; Mpre = 2.52, SDpre = 1.06; F1,59 = 31.92, p < 0.001, η 2 p = 0.35), the post attractiveness rating in the interested condition was significantly higher than that in the not-interested condition, F1,59 = 34.56, p < .001, η 2 p = 0.37 (see **Figure 2**). These combining results confirmed a mate copying effect presented in the interested condition.

For the fMRI experiment, a 2 (pre- vs. post-observation) × 2 (interested vs. not-interested) repeated measures of ANOVA (rmANOVA) on the attractiveness rating of opposite-sex faces revealed significant main effect of pre-to-post ratings (F1,25 = 4.36, p < 0.048, η 2 p = 0.15), but not of the attitude (F1,25 = 1.06, p = 0.31, η 2 p = 0.04). The effect of interaction was also not reaching the significant level, F1,25 = 0.085, p = 0.77, η 2 p = 0.004 (see **Figure 2**).

#### fMRI Results

In the comparison of interested > not-interested condition, the bilateral DLPFCs were observed significantly

activated (**Figure 3**), but not in the reverse comparison (not-interested > interested) (see **Table 1**). These results confirmed our hypothesis that the DLPFC should be involved in the learning process of mate copying.

# DISCUSSION

The present study examined the effect of mate copying while manipulating models' attitude. The mate copying effect was confirmed in our behavioral experiment – greater increased attractiveness ratings for opposite-sex photographs were observed when they were paired with models with interested attitude than with models with not-interested attitude. However, the behavioral results of the fMRI experiment revealed no significant mate copying effect. The only difference between the two experiments was that the re-rating process was performed immediately after the observation of each compound image in the behavioral experiment, while during the fMRI study, participants observed all compound images in the scanner and then completed re-rating processes outside of the scanner. It may be indicated that mate copying did exist when observing models' attitude to potential mates. When asked to re-rate outside of the scanner in the fMRI study, mate copying effect may be weakened due to the time delay and/or the environmental change.

The fMRI data confirmed our hypothesis that the DLPFC is involved in the social learning process in human mate copying. In detail, the bilateral DLPFC were more active when participants observed models with an interested attitude than with a not-interested attitude. The DLPFC has been shown involved in cognitive execution within working memory (Owen, 2000; du Boisgueheneuc et al., 2006) and attention (Fox et al., 2006). It has been found to be particularly involved in integrating information from social context to enable an appropriate social decision. For example, Spitzer et al. (2007) scanned participants (Player A) while they made decisions about how much of a monetary

FIGURE 3 | Greater activations in bilateral DLPFC were found in the interested condition compared to the not-interested condition when participants viewing the compound images. Error bars indicate one SEM. I, interested condition; NI, not-interested condition.

TABLE 1 | Regions associated with the effect of mate copying.

Coordinates (mm) are in MNI space. L, left, R, right. p < 0.001, uncorrected, k > 50. Sample size = 26.

endowment to split with another, anonymous participant (Player B) and found that the DLPFC is essential for integrating information about sanction threats into decision making to

incentivize norm-compliant behavior. The activation of DLPFC in the current study may reflect an involvement of cognitive execution function in the social learning process of mate copying in two aspects. First, it integrates and selects information from the observation, such as the social popularity and prestige of models, the mate values of the model and the target, or even how the model's and target's mate values compared to that of the observer (Vukomanovic and Rodd, 2007). Secondly, it guides to make an appropriate response in mate copying with the ability of DLPFC to maintain stable goal representations over time (Miller and Cohen, 2001).

# CONCLUSION

The present study provided a novel experimental investigation of neural basis involved in the social learning process of human mate copying. The DLPFC was significantly activated in the comparison of interested > non-interested condition, suggesting

# REFERENCES

that a cognitive integration and selection function may be involved when participants process information from conditions related to mate copying.

# AUTHOR CONTRIBUTIONS

J-YZ developed the study concept and design. Testing and data collection were performed by JX, DH, and MF. JX and DH performed the data analysis and interpretation under the supervision of LZ and J-YZ. J-YZ drafted the manuscript, and LZ provided critical suggestions. All authors approved the final version of the manuscript for submission.

#### FUNDING

This research was supported by National Nature Science Foundation of China (31271112).

**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 Zhuang, Xie, Hu, Fan and Zheng. 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.

# How Does Adult Attachment Affect Human Recognition of Love-related and Sex-related Stimuli: An ERP Study

Juan Hou1 \*, Xin Chen1 , Jinqun Liu1 , Fangshu Yao1 , Jiani Huang1 , Yamikani Ndasauka2 , Ru Ma3 , Yuting Zhang3 , Jing Lan4 , Lu Liu4 and Xiaoyi Fang4 \*

1 Department of Philosophy, Anhui University, Hefei, China, 2 School of Humanities and Social Science, University of Science and Technology of China, Hefei, China, 3 CAS Key Laboratory of Brain Function and Disease, School of Life Science, University of Science and Technology of China, Hefei, China, 4 Institute of Developmental Psychology, Beijing Normal University, Beijing, China

Edited by: Zhiling Zou,

Southwest University, China

#### Reviewed by: Zhao Xin,

Northwest Normal University, China Wenbo Luo, Chongqing University of Arts and Sciences, China

#### \*Correspondence:

Juan Hou<EMAIL_ADDRESS>Xiaoyi Fang<EMAIL_ADDRESS>
#### Specialty section:

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

Received: 18 January 2016 Accepted: 11 April 2016 Published: 02 May 2016

#### Citation:

Hou J, Chen X, Liu J, Yao F, Huang J, Ndasauka Y, Ma R, Zhang Y, Lan J, Liu L and Fang X (2016) How Does Adult Attachment Affect Human Recognition of Love-related and Sex-related Stimuli: An ERP Study. Front. Psychol. 7:596. doi: 10.3389/fpsyg.2016.00596 In the present study, we investigated the relationship among three emotion-motivation systems (adult attachment, romantic love, and sex). We recorded event-related potentials in 37 healthy volunteers who had experienced romantic love while they viewed SEX, LOVE, FRIEND, SPORT, and NEUTRAL images. We also measured adult attachment styles, level of passionate love and sexual attitudes. As expected, results showed that, firstly, response to love-related image-stimuli and sex-related image-stimuli on the electrophysiological data significantly different on N1, N2, and positive slow wave (PSW) components. Secondly, the different adult attachment styles affected individuals' recognition processing in response to love-related and sex-related images, especially, to sex-related images. Further analysis showed that voltages elicited by fearful attachment style individuals were significantly lower than voltages elicited by secure and dismissing attachment style individuals on sex-related images at frontal sites, on N1 and N2 components. Thirdly, from behavior data, we found that adult attachment styles were not significantly related to any dimension of sexual attitudes but were significantly related to passionate love scale (PLS) total points. Thus, the behavior results were not in line with the electrophysiological results. The present study proved that adult attachment styles might mediate individuals' lust and attraction systems.

Keywords: adult attachment, love, sex, event-related potentials (ERPs), emotion-motivation system

# INTRODUCTION

Sexual relationship, in the context of human mating, plays an important role in the development as well as the evolution of human beings. There are three primary emotion-motivation systems in human brain during the development of human sexual relationship for mating, reproduction and parenting: lust, attraction, and attachment (Fisher, 1998). Sex drive (also called the libido or lust) is regarded as a craving for sexual gratification while romantic love (attraction, obsessive love, or passionate love) is considered as a powerful energy, feeling of exhilaration and focused attention on someone who catches our attention (Fisher et al., 2002). Attachment, previously regarded only as intensive bond between mother and infant (Bowlby, 1969/1982), now includes adult male-female

attachment and is divided into three types, namely, secure, avoidant, and anxious (Hazan and Shaver, 1987). One of the most difficult dilemmas in relationship science is the interaction between sexual desire and love (Hatfield and Rapson, 1993; Regan and Berscheid, 1999; Diamond, 2004). Our study seeks to assess whether adult attachment could mediate recognition processing of love and sexual desire.

Love involves complex neural mechanisms and is a result of chemical, cognitive and directed behavioral components (Aron and Aron, 1986, 1996; Bartels and Zeki, 2000, 2004; Mashek et al., 2000; Buss, 2003; Aron et al., 2005; Esch and Stefano, 2005; Fisher et al., 2005). A study of relevance found that when individuals viewed pictures of their loved ones, the activity restricted foci in the medial insula and the anterior cingulate cortex, the caudate nucleus, and the putamen (Bartels and Zeki, 2000). A functional Magnetic Resonance Imaging (fMRI) study verified the hypothesis that love is a goal-directed state that leads to a range of emotions, rather than a specific emotion (Aron et al., 2005). Another study found that subliminal presentation of either a beloved's name (love prime) or a passion descriptor (passion prime) enhance reaction times in a similar fashion (Ortigue et al., 2007). These studies showed that, compared to friendship, romantic love is associated with mediating reward, emotion, and motivation systems (Bartels and Zeki, 2000, 2004; Aron et al., 2005; Fisher et al., 2005; Ortigue et al., 2007). Another study found that regional brain activity during early stage intense romantic love predicted relationship outcomes after 40 months (Xu et al., 2012). By using event-related potentials (ERPs), another study found that when participants viewed faces of their beloved, friend and unknown but beautiful people, the late positive potential (LPP) was larger in reaction to the face of the beloved than the other two types of faces (Langeslag et al., 2007). This entails that romantic love enhances one's lasting attention to faces of his/her beloved.

 Sexual arousal in humans is a complex experience, which includes both physiological and psychological processes. Brain activity plays a crucial role in sexual desire. Researchers use fMRI and positron emission tomography (PET), to investigate regions of brain associated with erotic stimuli. These techniques provide high spatial resolution, allowing researchers to study brain regions at a very macroscopic level (Stoléru et al., 1999; Redouté et al., 2000; Bocher et al., 2001; Karama et al., 2002; Mouras et al., 2003; Ferretti et al., 2005). Three PET studies used 15O-H2O to measure responses of regional cerebral blood flow (rCBF) in healthy males elicited by visual erotic film clips. After comparing them with other neutral control clips, the studies found that sexual stimuli were related to activation of some paralimbic areas (like anterior cingulate gyrus, orbitofrontal cortex, right insula and right inferior frontal cortex (Stoléru et al., 1999; Redouté et al., 2000; Bocher et al., 2001). Mouras et al. (2003) found that sexual stimuli were associated with increased activation of the parietal lobes, the right parietooccipital sulcus, the left superior occipital gyrus and the precentral gyri. Another study investigated the effect of emotional valence and arousal value of non-erotic visual stimuli on ERPs and found that positive valence and high arousal resulted in larger P300 and PSW (Lankveld and Smulders, 2008). Based on these results, we can rightly consider sexual arousal as a composite psychophysiological state correlated with activation/deactivation of several brain regions including cognitive, emotional, motivational, and autonomic components (Redouté et al., 2000).

The attachment theory generated by Bowlby (1969/1982) was conceived after observing separation between infants and their primary caregivers. The study found that infants' reaction could be predictable in three ways- protest, despair and detachment. After including adult male-female attachment the three ways have been re-termed as- secure, avoidant, and anxious, indicating that attachment is not only limited to childhood but also could be translated to romantic love process (Hazan and Shaver, 1987). Bartholomew and Horowitz (1991) proposed a creative 4-group model of adult attachment style- secure, preoccupied, dismissing and fearful. Compared to insecure attachment, secure individuals are much more easily engaged in stable relationships (Hazan and Shaver, 1987; Kirkpatrick and Hazan, 1994). Feeney and Noller (1990) reported that adult attachment was intensively associated with various forms of love and beliefs of relationship. Another study reported that avoidant people could mistrust others and engage in less intensive romantic love (Sepah-Mansour et al., 2009). Ahmadi et al. (2013) reported that ambivalent attachment style could significantly predict obsessive love.   For instance, avoidant attachment was associated with engagement in casual sex and anxious attachment was related to more unwanted but consensual sexual experiences. Birnbaum (2007) found that all attachment orientations were related to aversive sexual affect and cognitions within romantic relationships. Different adult attachment is also related to perception of emotional-laden stimuli, especially when the stimuli contain social information (Vrticka et al., 2012 ˇ ). From the above, we can conclude that adult attachment may affect various forms of love and sexual attitudes.

As mentioned above, the processing of romantic love stimuli and sexual stimuli were generally depicted by using fMRI and PET in the human sexual relationship, which involved the high spatial resolution but were limited in the temporal resolution. It is obvious that the limited of temporal resolution cannot measure the early stage of processing at the precise millisecond level. The present study aimed to use the method of ERPs, which have the high temporal resolution and could be time-locked to the onset of different categories stimuli. Therefore, ERP-measurement is suitable for measuring the early stage processing features of love-related stimuli and sex-related stimuli.

The first purpose of this study was to investigate ERPs in response to love-related images and sex-related images using electrophysiological data. Secondly, we also tested whether

adult attachment styles affect one's recognition processing in response to love-related images and sex-related images. Thirdly, based on behavioral data, we tested whether individuals with different attachment styles show significant difference in levels of passionate love and sexual attitudes. Taking into consideration previous studies, high temporal resolution of ERPs would provide a valuable tool to investigate early stages of processing loverelated stimuli and sex-related stimuli. Our study is the first to simultaneously investigate three primary emotion-motivation systems in human's brain- lust, romantic love and attachment, by using high temporal resolution ERP technology. We tested the following hypotheses: H1- response to love-related images will significantly differ from response to sex-related images on electrophysiological data. H2- different adult attachment styles will affect one's recognition processing in response to love-related images and sex-related images. H3- adult attachment style will affect individual's passionate love level and sexual attitudes based on behavior data as well as electrophysiological data.

# MATERIALS AND METHODS

## Participants

Participants were recruited using a poster at the university campus and on the Internet. Forty-five undergraduate and graduate students at Anhui University in China volunteered to participate in this study. Finally, 8 invalid data were discarded because of artifact rejection from EEG while 37 valid data remained for further analysis. The remaining 37 participants (17 males, 20 females; mean age 22.8, range 20– 32) were all heterosexual and reported to either being in love or to have previously been in love using the questionnaire like. All participants were healthy, with normal or correctedto-normal vision, no history of neurological or psychiatric disorder. Furthermore, all 37 participants were right-handed. Each participant signed a written informed consent before taking part in the experiment and received 50 RMB (approximately US \$8) as compensation.

#### Ethics Statement

Each participant to the study provided written informed consent after receiving an explanation of the study's purpose and procedure. The study was approved by the Human Research Ethics Committee of Anhui University of China according to the principles expressed in the Declaration of Helsinki. Participants were undergraduate and postgraduate students. We did not obtain informed consent from guardians of participants whose age was under 18. These young college students were considered to have comparable intelligence and ability to adult students, and able to take charge of their behaviors. According to the General principles of the Civil Law of the People's Republic of China; "A minor aged 10 or over shall be a person with limited capacity for civil conduct and may engage in civil activities appropriate to his age and intellect; in other civil activities, he shall be represented by his agent ad litem or participate with the consent of his agent ad litem" (Article 12, Chapter II).

#### Measures

Attachment to romantic partners: participants completed the Chinese version of Experiences in Close Relationships (ECR) Questionnaire (Li and Kato, 2006). This 36-item questionnaire includes 18 items measuring avoidance attachment, the other 18 items measuring anxiety attachment about romantic relationships. Each item was rated on a 7-point Likert scale (ranging from 1 = strongly disagree to 7 = strongly agree). The Cronbach's alphas for the avoidance and anxiety scales were high (0.832 for both scales). According to the method of Griffin and Bartholomew (1994a,b), we divided the participants into four attachment styles groups (secure, preoccupied, dismissing and fearful).

Passionate love level: in order to test this, we used the short version of PLS, developed by Hatfield and Sprecher (1986). This scale consists of 30 items and each item is rated on a 9-point Likert scale (ranging from 1 = strongly disagree to 9 = strongly agree), higher scores indicating higher levels of love. The Cronbach's alpha of this scale was 0.857.

Sexual attitude: participants completed the Brief Sexual Attitudes Scale (BSAS), which has four subscales of Permissiveness, Birth Control (formerly called Sexual Practices), Communion, and Instrumentality. This scale includes 23 items and each item is rated on a 5-point Likert scale (ranging from 1 = strongly disagree to 5 = strongly agree). Higher scores indicated higher open sexual attitude. The Cronbach's alpha of this total scale was 0.851.

We engaged two colleagues to translate the above two scales from English to Chinese and engaged another pair of colleagues to translate it back to English. We compared the translations and came up with the best translation.

#### Materials

Materials for the experiment included video clips and visual images. We obtained three different copyright-free video clips (erotic, non-erotic love, and friendship) from publicly shared online videos. Erotic video clip showed heterosexual couples engaged in intercourse, non-erotic love video clip showed heterosexual couples in romantic love without any sexual behavior and friendship video clip showed male-female friendship. Each video clip lasted for not more than 6 min and all participants used earphones to listen to the sound of the videos during the experiment. We used the video clips as cues for imagestimuli that followed and were not analyzed in detail. The three types of video clips were used for creating three different states and making subjects a better understanding of the followed three image-stimuli (erotic, non-erotic love and friendship).

As mentioned in the introduction, previous related ERPs studies used faces of beloved or friends, erotic sex pictures, sports pictures, and neutral pictures as experimental materials (Langeslag et al., 2007; Lankveld and Smulders, 2008). The previous love-related ERP studies chose the love-related and friend-related facial stimuli as the experimental materials for control some other confounded variables such as familiarity and perceived beauty (Langeslag et al., 2007). As to the sexrelated study, researchers chose the sport stimuli as the contrast

stimuli for separating the ERP-contributions of erotic content from that of arousal value and hedonic valence, that is the erotic picture was equivalent to the category of high-energy sports pictures on the dimensions of valence and arousal (Lankveld and Smulders, 2008). In order to compare love-related stimuli and sex-related stimuli simultaneously, we divided the original visual images of our study into five categories. (1) 20 SEX images (nude heterosexual couples engaging in intercourse while showing female breasts, but without showing female or male genital areas in close-up). (2) 20 LOVE images (heterosexual couples dating, kissing and hugging without any erotic behavior).   Images from the first three categories (LOVE, FRIEND, and SEX) were taken from erotic, non-erotic love and friendship video clips (as mentioned in the above paragraph) respectively, while images from the other two categories (SPORT and NEUTRAL) were downloaded from free sites on the Internet. We chose the SPORT images to match possible motion factors in the SEX images during the ERP experiment whilst FRIEND images were chosen to match possible friendship factors in the LOVE images during the ERP experiment.  All images were standardized for brightness, saturation and size (600 pixels × 450 pixels) with Photoshop CS4. Before the experiment began, eight males and eight females, not involved in the study, independently rated these images on levels of quality (1-extremely bad to 7-extremely good), sexual arousal (1- no arousal to 7- highest arousal level) and love arousal (1- no arousal to 7-highest arousal level). According to their mean scores, 40 images were selected for the formal experiment, each category included eight images. In addition, the center of each image had a cross-shaped image (65 pixels × 65 pixels; white background and black foreground) which contained two shapes in which horizontal line was longer than vertical line or vertical line was longer than horizontal line. Two crossshaped images occurred in the five categories randomly. When the shape changed, participants were instructed to press "1" on the keyboard, using the right hand. The task was used to keep participants focused on the images.

#### Procedure

After arriving at the laboratory, participants read and signed an informed consent form, which included a brief description of the procedure. Participants then filled in questionnaires and provided information about the duration of their recent romantic relationships as well as other demographic variables. Next, we placed electrodes on participants' heads and instructed them to limit movements and eye blinks during experiment. The participants sat in a comfortable chair in a soundproof, dimly lit room and put on their earphones. Images were displayed on a 49-cm monitor, with a maximum size of 27 cm × 37 cm, presented approximately 1.25 m from the participant's eyes with a visual angle of 16◦ horizontally and 12◦ vertically. Stimuli were presented in two blocks of 24 images each and each block contained 8 images from three different categories.  The order of two blocks was counter-balanced across participants to control for any sequence or carryover effects. Stimuli of the same categories appeared in random order within each block. Stimuli presentation was controlled by E-Prime software.

Before each block, we showed participants a video clip (erotic; before the SEX block) or two video clips (friendship and non-erotic love; before the LOVE block) to make participants understand the relationship between the two persons of the following stimuli, which could render the love-related or sexualrelated emotions. We did not analyze the recorded EEG during the video time. There was a 1-min break after video clip(s). Each block started with a black fixation cross (5 cm × 5 cm) in the center of the white computer screen and lasted for 500 ms. Then stimuli were presented for 350 ms. Specifically, the stimuli were presented in the order of FRIEND-NEUTRAL-LOVE (in LOVE block) or SPORT-NEUTRAL-SEX (in SEX block). Images in the same categories appeared in random order within each block. Each category (SEX, LOVE, FRIEND, SPORT, and NEUTRAL) contained eight images and each image was presented 50 times in one block, thus, the study consisted 2400 trials. Furthermore, once participants found the cross-shaped image in the center of each stimuli and pressed "1" on the keyboard using the right hand, the shape changed. There were several times for resting during the experiment.

# Electroencephalogram (EEG) Recording and Signal Processing

The electroencephalogram (EEG) was recorded using a 64 channel amplifier (SynAmps 2, Neuroscan) and data acquisition software (SCAN4.3, Neuroscan). The 64 Ag–AgCl active electrodes were placed on the scalp by means of a head cap, according to the 10–20 International System. Scalp impedance for each electrode was kept below 5 k. Vertical electrooculogram (VEOG) was recorded by attaching additional electrodes above and below the left eye. The REF electrode served as reference and the forehead GND electrode was used as ground. All signals were digitized with a sample rate of 500 Hz, a 24-bit A/D conversion and a 0.05–100 Hz band pass filter.

The offline analysis of ERP data was performed with Neuroscan 4.3 software. Data were filtered using a band pass filter of 0.5–25 Hz with zero phase shifts (24 dB/octave slope). Ocular artifact correction was applied according to the Gratton and Coles algorithm. Data epochs were extracted from a time window between 200 ms before and 750 ms after the stimuli onset. The mean 200 ms pre-stimuli period was used for baseline correction. Artifact rejection criteria were minimum and maximum baselineto-peak −50 to +50 µV. According to previous studies and the purpose of current study, average ERPs were then computed for each participant and the five images categories (SEX, LOVE, NEUTRAL, SPORT, and FRIEND). The following nine electrode

positions were analyzed: F3, Fz, F4, C3, Cz, C4, P3, Pz, and P4 (cf. Langeslag et al., 2007; Lankveld and Smulders, 2008). The voltages and waves that were elicited by SEX, LOVE, SPORT and FRIEND stimuli images during the experiment were recorded.

#### Analysis

The questionnaire and ERP data were analyzed using SPSS 11.0 for Windows, the mean ERP voltages in the time windows 100–200 ms (referred to as N1 component), 200–300 ms (referred to as N2 component), and 500–750 ms (referred to as PSW component) were tested at several electrodes (frontal: F3, Fz, F4; central: C3, Cz, C4; parietal: P3, Pz, P4). The considered two difference waves were created through the SEX minus SPORT (referred to as SEX-MINUS-SPORT wave) and LOVE minus FRIEND (referred to as LOVE-MINUS-FRIEND wave). The minus waves were created for further analysis. Using repeated measures ANOVAs with the within-subject factors categories (SEX-MINUS-SPORT, LOVE-MINUS-FRIEND) and nine electrodes (frontal: F3, Fz, F4; central: C3, Cz, C4; parietal: P3, Pz, P4), and with N1, N2, and PSW as dependent variables. The interaction effects between difference waves (SEX-MINUS-SPORT wave, LOVE-MINUS-FRIEND wave) and the between-subject factors four attachment styles (secure, preoccupied, dismissing, and fearful) were tested using the method of repeated measures ANOVAs. Only effects involving the factor condition of interest were reported. Greenhouse-Geisser correction for violations of the sphericity assumption in repeated measures analyses was used when appropriate. Effects were considered significant when p < 0.05. Significant interaction effects were followed-up by paired-samples t-tests.

# RESULTS

# Electrophysiological Data

Dependent variables were area measures under the two ERP difference waveforms (SEX-MINUS-SPORT wave, LOVE-MINUS-FRIEND wave) in the latency windows of interest. **Figure 1** shows the grand average waveforms per difference image stimuli at frontal (F3, Fz, F4), central (C3, Cz, C4), and parietal (P3, Pz, P4) electrode sites. Apparently, the amplitude of SEX-MINUS-SPORT wave was larger than the LOVE-MINUS-FRIEND wave especially at parietal. **Figure 2** shows the voltage scalp distributions for the two minus-difference waveforms between 100 and 200 ms, 200 and 300 ms, and 500 and 750 ms after image-stimuli onset.

 Both the main effect of two difference waves [F(1,36) = 31.30, p < 0.00] and nine electrodes [F(8,288) = 7.236, p < 0.00] were significant. The interaction between stimuli categories and electrode was also significant [F(8,288) = 11.972, p < 0.00].

 Both the main effect of two difference waves [F(1,36) = 50.25, p < 0.00] and nine electrodes [F(8,288) = 9.96, p < 0.00] were significant. The interaction between stimuli categories and electrode was also significant [F(8,288) = 40.58, p < 0.00].

 Both the main effect of two difference waves [F(1,36) = 39.42, p < 0.00] and nine electrodes [F(8,288) = 18.67, p < 0.00] were significant. The interaction between stimuli categories and electrode was also significant [F(8,288) = 10.11, p < 0.00].

#### Effects of Image Stimuli Categories and Attachment Style

According to the ECR Questionnaire, we divided participants into four attachment style groups- secure (n = 7), fearful (n = 17), preoccupied (n = 9), and dismissing (n = 4).

We performed a two-way repeated measure ANOVA to test whether four adult attachment styles (secure, preoccupied, dismissing, and fearful) could have interaction effects with the grand average voltages of SEX-MINUS-SPORT wave and LOVE-MINUS-FRIEND wave on N1, N2, and PSW components at each electrode. The interaction effects results are shown in **Table 1**. Results showed that adult attachment styles had significant interaction effects with difference waves at electrodes (F3, FZ, and F4) on N1 and N2 components, at electrodes (CZ, C4, and PZ) on N2 component, at electrode C4 on PSW component.

We further tested multiple comparisons in order to understand specific differences among the four adult attachment styles at the above significant electrodes on N1.

∗p < 0.05, ∗∗p < 0.01.

∗p < 0.05.

We found that voltages that were elicited by secure attachment style individuals were larger than those elicited by fearful attachment style individuals on SEX-MINUS-SPORT wave at electrodes F3 (p < 0.05) and F4 (p < 0.01). Voltages elicited by secure attachment style individuals were larger than those elicited by preoccupied attachment style individuals on SEX-MINUS-SPORT wave at electrode F4 (p < 0.05). Voltages elicited by dismissing attachment style individuals were larger than those elicited by preoccupied attachment style individuals on SEX-MINUS-SPORT wave at electrode F4 (p < 0.05).

We also tested multiple comparisons to assess differences among the four adult attachment styles at the above significant electrodes on N2.  Voltages elicited by secure attachment style individuals were larger than voltages elicited by preoccupied attachment style individuals on SEX-MINUS-SPORT wave at electrode FZ (p < 0.05), F4 (p < 0.01) and CZ (p < 0.05). Voltages elicited by dismissing attachment style individuals were larger than voltages elicited by fearful attachment style individuals on SEX-MINUS-SPORT wave at electrode FZ (p < 0.05), F4 (p < 0.05), and C4 (p < 0.05). Voltages elicited by dismissing attachment style individuals were larger than both preoccupied and fearful attachment style individuals on LOVE-MINUS-FRIEND wave at electrode FZ (p < 0.05).

In summary, our results showed that adult attachment styles are related to recognition of different stimuli (SEX or LOVE) especially at frontal sites on N1 and N2 ERP components. Further comparisons showed that voltages elicited by secure attachment style individuals are significantly larger than voltages elicited by fearful and preoccupied attachment style individuals on SEX-MINUS-SPORT wave, at frontal sites, on N1 and N2 components. Finally, voltages elicited by dismissing attachment style individuals are larger than voltages elicited by fearful attachment style individuals on SEX-MINUS-SPORT wave at frontal sites, on N2 components.

# Behavior Data and Electrophysiological Data

We used One-Way ANOVA analyses to test whether the four adult attachment styles (secure, preoccupied, dismissing, and fearful) are significantly different among between loverelated and sexual-related behavior variables (i.e., PLS total points, sexual attitude dimensions: permissiveness, birth control, communion, and instrumentality). Results showed that the four adult attachment styles were significantly different in PLS and total points [F(3,33) = 3.34, p < 0.05].  See **Table 2** for detailed results.

Results from electrophysiological data showed that adult attachment styles were related to recognition of different stimuli (SEX or LOVE) especially at frontal sites on the N1 and N2 ERP components. Further, electrophysiological voltage differences of adult attachment styles were more significant on the recognition of sex-related stimuli images, while behavior data found that adult attachment styles were not significantly related to all dimensions of sexual attitudes. Thus, results from behavior data were different from electrophysiological data.

## DISCUSSION

In the present study, we found some interesting results. Firstly, based on our electrophysiological data, response to love-related image-stimuli and sex-related image-stimuli significantly differed on N1, N2, and PSW components. Secondly, different adult attachment styles significantly affected individuals' recognition processing in response to love-related images and sex-related images, especially response to sex-related image-stimuli. Thirdly, adult attachment styles were significantly different in passionate love.

As discussed in the introduction, we tested attachment style, level of passionate love and sexual attitudes to understand mediation effect of adult attachment style on individuals' processing of love-related variable (passionate love level) and sex-related variable (sexual attitudes). Our results showed that the four adult attachment styles (secure, preoccupied, dismissing, and fearful) were significantly different in PLS total points. Further analysis showed that preoccupied attachment style was significantly higher than secure and fearful attachment styles in PLS total points. This implies that preoccupied attachment individuals are extremely passionate in romantic relationships (Hatfield and Sprecher, 1986). Bartholomew and Horowitz

(1991) reported that preoccupied attachment individuals are associated with more expressiveness and less coldness. Further, ambivalent attachment style can significantly predict obsessive love (Ahmadi et al., 2013). Thus, attachment style can influence individuals' performance in sexual relationship, particularly, unsecure attachment individuals are considered more likely to fall in obsessive love.

As shown in **Figure 1**, we found that N1 (from 100 ms after stimuli onset) was more pronounced in sex-related stimuli than love-related stimuli at frontal and parietal sites. This suggests that cortical neural response was activated more by sexrelated stimuli than by love-related stimuli. In the present study, sexual-related stimuli induced lager N1 components than the other categories, which, just like other emotional expressions, gets prior and more attention at early stages of cognition processing. Sex-related pictures are not only considered as one category of emotional pictures but also as a biological stimulus (Anokhin et al., 2006), which are crucial for human survival and reproduction. This helps us better understand why brain activities pay more attention to sex-related stimuli than loverelated stimuli. Evolutionary and biological information from visual scenes may hence affect human brain mechanism of processing these relevant visual stimuli. Such brain mechanism could preferentially discriminate sex-related stimuli from stimuli from other categories in early stage processing. Early ERP components contain top-down regulation of sensory processing (Foxe and Simpson, 2002). These brain activities may modulate the processing in order to facilitate discerning information of biological stimuli.

Between 200 and 300 ms after stimuli onset, N2 was less pronounced in sex-related stimuli than love-related stimuli and neutral stimuli at three prefrontal electrodes. The ERP components included N1, P2, N2, and P3. N1 and P2 are regarded as early components of brain processes in response to stimuli, relying on physical properties of stimuli (strength, type, frequency, etc.), which are called exogenous components. N2 and P3 are related to human perception, recognition, attention and memory, named endogenous components. Thus, current finding of a decreased N2 for sex-related stimuli may be due to physical properties of stimuli. Besides, N2 has been found to be smaller for emotional facial stimuli than neutral facial stimuli at prefrontal electrodes (Eimer and Holmes, 2002, 2007). As such, sexual-related stimuli may be a special emotional category, which could influence this early component. Discriminative response to different picture categories starts in anterior regions of the scalp, suggesting that an involvement of the prefrontal cortex in the discrimination of specific contents.

As expected, we found that PSW (between 500 and 750 ms after stimuli onset) was lager for sex-related stimuli than loverelated stimuli and neutral stimuli at frontal and parietal sites. This finding is in line with earlier studies, both in females and males (Anokhin et al., 2006). Van-Lankveld and Smulders (2008) compared difference among males in response to erotic pictures and sport pictures and found that erotic pictures induced lager P300 and PSW components. PSW is treated as the index of attention maintenance (Bradley, 2000; Schupp et al., 2003), which meanings need much more attention materials. Anokhin et al. (2006) investigated difference in neuroelectric response between erotic pictures and other picture categories and found that emotionally arousing pictures, regardless of their content, produce a larger late positive wave than neutral pictures. As we know, sex-related stimuli contain more biology information than love-related pictures and neural pictures, which are crucial for human's survival and reproduction. Whether in early or late processing stages, sex-related stimuli always catch more attention and need more processing materials in our brain.

In our study, we tested the mediation effect of adult attachment on individuals' processing of stimuli from different categories on ERP components (N1, N2, and PSW). Results showed that adult attachment styles were related to recognition of difference stimuli (SEX or LOVE) especially a frontal site on N1 and N2 ERP components. Further analyses showed that voltages elicited by secure attachment style individuals were significant larger than voltage elicited by fearful and preoccupied attachment style individuals on SEX-MINUS-SPORT at frontal sites, on N1 and N2 components. Voltages elicited by dismissing attachment style individuals were larger than voltages elicited by fearful attachment style individuals on SEX-MINUS-SPORT wave at frontal sites, on N2 components. Compared to individuals of the other three adult attachment styles, fearful attachment style individuals are usually frightened and anxious during sexual relationship, which explains the decreased response to sex-related image-stimuli.

In addition, adult attachment styles may influence level of obsessive love, sexual attitude and sexual experiences in common romantic relationships (Hazan and Shaver, 1987; Kirkpatrick and Hazan, 1994; Feeney et al., 2000; Gentzler and Kerns, 2004). Importantly, individuals with dismissing attachment style have been found to be cold and less expressive (Bartholomew and Horowitz, 1991). In present study, the electrophysiological voltage differences in adult attachment styles were significantly related to recognition of sex-related images while behavior data found that adult attachment styles were not significantly related to any dimension of sexual attitudes. The difference in results between behavior data and electrophysiological data helps to prove that implicit ERP technology results may not be the same with explicit questionnaire behavior data. However, Chinese people's view of sex is relatively conservative, so self-reported behavior questionnaire method may have many weaknesses for such variables, as individuals tend to report the more reasonable and socially desirable responses. Thus, compared to behavior method, ERP technology can be used widely in future studies to investigate the most spontaneous and real potential reactions of the human brain.

One limitation of the present study merits consideration. In order of presentation of stimuli, in the LOVE block; stimuli were presented in FRIEND-NEUTRAL-LOVE, order while in the SEX block; stimuli were presented in SPORT-NEUTRAL-SEX, order. The fixed order may have affected participants' attention to different image-stimuli. Future studies should balance the order to capture full attention of participants during the experiment.

#### CONCLUSION

fpsyg-07-00596 April 28, 2016 Time: 12:52 # 9

From electrophysiological data, the current study found that response to love-related image-stimuli and sex-related imagestimuli were significantly different on N1, N2, and PSW components. Our results suggest that different adult attachment styles may affect one's recognition processing in response to love-related images and sex-related images, especially, to sexrelated images. Further, from behavior data, we found that adult attachment styles were not significantly related to any dimension of sexual attitudes but showed significant difference in PLS total points. These behavior results were not in line with electrophysiological results. The present study provides evidence that during development of sexual relationship for mating, reproduction, and parenting, there are three primary emotionmotivation systems in human brains, called lust, attraction, and attachment. Using electrophysiological technology, our study also found that adult attachment styles may influence human lust and attraction systems.

#### REFERENCES

#### AUTHOR CONTRIBUTIONS

Conceived and designed the experiments: JH, XC, JL, FY, JNH, and XF. Performed the experiments: JH, XC, JL, FY, and JNH. Analyzed the data: JH, XC, JL, FY, JNH, RM, YZ, JL, and LL. Contributed reagents/materials/analysis tools: JH, XC, JL, FY, JNH, RM, YZ, JL, and LL. Wrote the paper: JH, XC, YN, RM, YZ, and XF. Discussed the result: JH, ZH, YN, RM, YZ, JL, LL, and XF. Final approval of the version to be published: JH, YN, JL, LL, and XF.

#### ACKNOWLEDGMENTS

This work was supported by grants from the National Social Science Foundation for the education of young people of China, "Family Group Intervention Model in Network Moral Education of Adolescent" (CEA150174); the National Natural Science Foundation of China (31571157); Anhui Provincial Key Science Foundation for Outstanding Young Talent (2013SQRW007ZD); Academic and Technology Leaders Introduction project of Anhui University<PHONE_NUMBER>63); Scientific Research Training Program of Anhui University (KYXL2014084); and Open Key Laboratory Project of Brain function and Brain Diseases in Chinese Academy of Sciences (2014–2015).

magnetic resonance imaging study. J. Cogn. Neurosci. 19, 1218–1230. doi: 10.1162/jocn.2<IP_ADDRESS>8

**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 Hou, Chen, Liu, Yao, Huang, Ndasauka, Ma, Zhang, Lan, Liu and Fang. 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.

# Decreased Empathic Responses to the 'Lucky Guy' in Love: The Effect of Intrasexual Competition

Li Zheng1† , Fangxiao Zhang2† , Chunli Wei2 , Jialin Xu3 , Qianfeng Wang3 , Lei Zhu4 , Ian D. Roberts5 and Xiuyan Guo6,1 \*

1 Key Laboratory of Brain Functional Genomics, Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Psychology and Cognitive Science, East China Normal University, Shanghai, China, 2 School of Psychology and Cognitive Science, East China Normal University, Shanghai, China, 3 Shanghai Key Laboratory of Magnetic Resonance and Department of Physics, East China Normal University, Shanghai, China, 4 Department of Psychology, Fudan University, Shanghai, China, 5 Department of Psychology, The Ohio State University, Columbus, OH, USA, 6 Shanghai Key Laboratory of Magnetic Resonance and School of Psychology and Cognitive Science, East China Normal University, Shanghai, China

#### Edited by:

Xiaochu Zhang, University of Science and Technology of China, China

#### Reviewed by:

Bin Xuan, Anhui Normal University, China Zhihao Li, Shenzhen University, China

#### \*Correspondence:

Xiuyan Guo<EMAIL_ADDRESS><EMAIL_ADDRESS>
†These authors have contributed equally to this work.

#### Specialty section:

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

Received: 30 December 2015 Accepted: 21 April 2016 Published: 11 May 2016

#### Citation:

Zheng L, Zhang F, Wei C, Xu J, Wang Q, Zhu L, Roberts ID and Guo X (2016) Decreased Empathic Responses to the 'Lucky Guy' in Love: The Effect of Intrasexual Competition. Front. Psychol. 7:660. doi: 10.3389/fpsyg.2016.00660 People have a greater desire to date highly attractive partners, which induces intrasexual competition between same-sex individuals. The present study used functional magnetic resonance imaging to explore whether and how intrasexual competition modulates pain empathy for a same-sex rival and the underlying neural mechanism. Participants were scanned while processing the pain of a same-sex 'lucky guy' who had an attractive partner and one with a plain partner. The results revealed that participants reported lower pain intensity for the lucky guy. Neurally, reduced pain-related activations in anterior insula and anterior mid-cingulate cortex and increased activations in right superior frontal gyrus (SFG) and medial prefrontal gyrus (MPFC) were found for the lucky guy compared to the one with a plain partner. Right SFG and MPFC activations could predict participants' subsequent pain intensity ratings for the lucky guy. These findings suggest intrasexual competition can modulate normal empathic responses.

Keywords: pain empathy, intrasexual competition, fMRI, AI, aMCC, MPFC

# INTRODUCTION

Evolutionarily speaking, physical attractiveness is linked to youth, health, and female fertility (Sugiyama, 2005). Physical attractiveness also provides information about mate-relevant economic or social factors, such as income or hunting ability (Harper, 2000) and plays an important role in mate selection (Grammer et al., 2003; Gangestad and Scheyd, 2005). Both males and females have a greater desire to date highly attractive partners (Greitemeyer, 2010). The common motive to obtain and maintain access to partners, especially highly desirable partners, can often induce intrasexual competition (Buunk and Massar, 2012). Emerging evidence has demonstrated that intrasexual competition can affect people's attitudes. That is, people tend to dislike same-sex rivals, exhibiting negative evaluations and hostile behaviors toward them (Fisher, 2004; Griskevicius et al., 2009). Previous studies have revealed that the attitudes held toward others impact empathy for their suffering and pain (Singer et al., 2006; Cheng et al., 2010). This leads to the question: are empathic responses to the same-sex rival, especially when the rival is a 'lucky guy' who obtains the love of a highly attractive partner, modulated by intrasexual competition? The goal of the present study

was to investigate the impact of intrasexual competition on empathy and the underlying neural mechanisms.

Empathy refers to the ability to understand and experience the emotional and affective states of another person (Decety and Jackson, 2004; Singer and Lamm, 2009; Decety, 2011). Recently, a number of neuroimaging studies on pain empathy have demonstrated that the perception or imagining of others' pain activates a pain matrix similar to what is engaged in the first-hand experience of pain (Derbyshire, 2000; Price, 2000; Jackson et al., 2006), including the bilateral anterior insula (AI), anterior cingulate cortex (ACC), and anterior mid-cingulate cortex (aMCC; e.g., Singer et al., 2004; Jackson et al., 2006; Lamm et al., 2007, 2011; Saarela et al., 2007; Fan et al., 2011; Guo et al., 2012, 2013; Zheng et al., 2016). In addition, activation in medial prefrontal cortex (MPFC) was associated with decreased empathic responses to others' pain (Cheng et al., 2007). Converging with evidence showing the role of MPFC in cognitive inhibitory control and emotion regulation (Floden and Stuss, 2006; Banks et al., 2007; Phillips et al., 2008), activation in MPFC during empathy for others' pain may reflect a downregulation of empathic pain (Cheng et al., 2007).

Although, a key feature of empathy is the observer's experience of an affective state that is isomorphic to another person's affective state, empathy is not simply an automatic resonance of the target's state (De Vignemont and Singer, 2006). Previous neuroimaging studies have revealed that individuals' attitudes toward empathy targets influence empathy for their pain. Decety et al. (2010) found that, compared with healthy controls, the more participants blamed targets for contracting AIDS from illegal intravenous drug use, the less empathy participants had for the target's pain, indicating that empathic responses were modulated by an a priori negative attitude toward the empathy target. In a study conducted by Singer et al. (2006), participants, especially males, showed decreased responses in brain regions associated with empathy when observing an unfair person who they disliked receiving pain. Given that intrasexual competition leads to negative attitudes toward same-sex rivals (Fisher, 2004; Griskevicius et al., 2009), we predicted that observers would show reduced behavioral and neural empathic responses to their pain.

To test this prediction, an functional magnetic resonance imaging (fMRI) study was designed. Before the experiment, four plain models (two females and two males) and two attractive models (one female and one male) were selected. Participants were informed that one of two plain same-sex models had an attractive partner (PlainAtt), i.e., the 'lucky guy' in love in the experiment; another had a plain partner (PlainPlain). Then participants were scanned while viewing a series of pictures showing PlainPlain or PlainAtt (targets were always the same-sex as the participants) in painful or non-painful situations (**Figure 1**). We predicted that participants would report more negative attitudes and decreased pain intensity ratings for PlainAtt than for PlainPlain. At the neural level, decreased pain-related brain activations in AI and ACC/aMCC and increased activation in MPFC, which has been associated with the regulation of empathic pain, would be observed for PlainAtt relative to PlainPlain.

# METERIALS AND METHODS

### Participants

Twenty right-handed participants (12 females, mean age = 21.70, SD = 1.89) were recruited from the university community to participate in this experiment. None of the participants had a history of neurological or psychiatric disorders. All participants received monetary compensation for their participation. All of them had normal or corrected-to-normal vision. All participants gave informed consent before scanning. The study was approved by the local ethics committee.

# Materials

A total of 192 pictures collected from two females and two males volunteers were used as stimuli. For each volunteer, 24 painful pictures, depicting their bilateral ears (not including faces), palms, and index fingers in four kinds of nociceptive situations (cutting with a knife or a pair of scissors and pricking with a needle or an awl), were paired with a corresponding nonpainful situation, in which the nociceptive tool did not touch the ear, palm, or finger, but was placed next to the body part (in total, 48 pictures for each volunteer). All of the pictures were 500 × 350 pixels in size. Ninety-six pictures from the two males volunteers were used as stimuli for male participants, while ninety-six other pictures from the two females volunteers were used as stimuli for female participants.

# Procedure

Before the experiment, we collected 38 free face pictures (19 females and 19 males) from the Internet. From 19 females candidates, one attractive female model and two plain females models were selected according to the attractiveness and liking ratings of 10 males (not participants). The attractive model got the highest attractiveness and liking ratings, while the two plain models were ranked in the last quarter of the ratings. There were significant differences between the attractiveness and liking ratings of the attractive model and the plain models (ts > 3.46, ps < 0.01), but no significant attractiveness or liking rating differences between the two plain models. From 19 male candidates, one attractive male model and two plain male models were selected in the same way, with significant differences between the attractive model and plain models (ts > 6.20, ps < 0.01) and no significant differences between the two plain models. For each participant, face pictures of two couples were presented during the fMRI scan. The first couple was composed of one of the two plain same-sex models paired with the attractive opposite-sex model. The second couple was composed of the other plain same-sex model paired with one of the two plain opposite-sex models. Which plain model was paired with the attractive opposite-sex model was counterbalanced between participants.

Before scanning, participants were informed that they would view pictures of two couples and that the same-sex models from these couples would be their empathy targets. They were told they would view a series of pictures depicting the empathy target in painful or non-painful situations.

During the experiment, six blocks were set for each plain same-sex model (PlainAtt or PlainPlain; **Figure 1**). Before each block, a 6-s cue trial (i.e., a picture of one of the couples) was presented to inform the participants which plain samesex model was the target in the following block. Each block consisted of four painful pictures and four non-painful pictures of the model indicated by the cue with null events (only fixation cross) randomly interspersed. Each trial was presented for 3.5 s followed by a jittered fixation cross from 0.5 to 1.5 s. PlainAtt and PlainPlain blocks were alternated. The presentation orders of the different blocks were counterbalanced across the participants. Each block lasted for 48.5 s, followed by a 5-s rest. The participants were asked to view the pictures attentively. The manipulation of grouping events into different blocks aimed to reduce the possible influence of participants' cognitive loads to switch between two empathy targets on the modulation of neural empathic responses by intrasexual competition.

After scanning, participants were presented with the same stimuli that they viewed in the scanner again and asked to rate how much pain they felt in each situation (0–9 point Likert-type scale where 0 indicated no pain and 9 indicated extreme pain). Then, they were presented with the same cue pictures as in the scanner and asked to rate the attractiveness of the empathy targets who had an attractive or plain partner and how much they envied and liked the empathy targets with 1 point (not at all)-7 point (extreme) Likert-type scales.

#### fMRI Image Acquisition and Analysis

Imaging was performed on a 3T Siemens Trio system (East China Normal University, Shanghai) with a standard head coil. Functional images were obtained using a gradient echo echoplanar imaging (GRE-EPI) sequence. Thirty-five transversal slices with 3 mm slice thickness and a 0.3-mm spatial gap were acquired (TR = 2200 ms, TE = 30 ms, FOV = 220 mm, flip angle = 90◦ , matrix size = 64 × 64). There was only one run of functional scanning which was about 13 min (346◦ EPI volumes). Before the functional imaging, a high-resolution structural image was acquired using a T1-weighted, multiplanar reconstruction sequence (MPR; 1 mm× 1 mm× 1 mm).

Participants' data were analyzed separately using SPM8 (Statistical Parametric Mapping, Wellcome Department of Imaging Neuroscience, London, UK). During data preprocessing, the first five volumes were discarded to allow for T1 equilibration effects. The functional images were corrected for the delay in slice acquisition and were realigned to the first image to correct for interscan head movements. The individual T1-weighted, 3D structural image was co-registered to the mean EPI image generated after realignment. The co-registered structural image was then segmented into gray matter (GM), white matter (WM), and cerebrospinal fluid (CSF) using a unified segmentation algorithm (Ashburner and Friston, 2005). The functional images after slice timing and realignment procedures were spatially normalized to the Montreal Neurological Institute (MNI) space (resampled to 2 mm × 2 mm × 2 mm) using the normalization parameters estimated during unified segmentation and then spatially smoothed with a Gaussian kernel of 8 mm full-width half-maximum (FWHM).

Statistical analyses were then carried out with the general linear model (GLM) implemented in SPM8. At the first-level analysis, four types of conditions were defined based on the

attractiveness of the empathy target's partner and painful or non-painful stimuli the target received: (1) PlainAtt in the painful situations (PlainAttP); (2) PlainAtt in the non-painful situations (PlainAttN); (3) PlainPlain in the painful situations (PlainPlainP); (4) PlainPlain in the non-painful situations (PlainPlainN). All the conditions were modeled as 3.5 s long from the onset time of the pictures and convolved with a canonical hemodynamic response function (HRF). The models additionally included cues (also convolved with a canonical HRF) and six movement parameters derived from realignment as covariates of no interest. High pass temporal filtering with a cutoff of 180 s was also applied in the models. For each participant, simple main effects for each of the four conditions were computed with the '10' contrast, respectively, at the first-level analysis. The resulting four first-level individual contrast images for each participant were then fed into a second-level full factorial ANOVA.

The main effect of pain was defined using the (PlainAttP + PlainPlainP) – (PlainAttN + PlainPlainN) and the reverse contrasts. The interaction between pain and partner's attractiveness defined by the (PlainPlainP – PlainPlainN) – (PlainAttP – PlainAttN) and the reverse contrasts were also computed to explore how the empathic brain responses changed. A cluster-level threshold of p < 0.05 (FWE) and a voxel-level threshold of p < 0.001 (uncorrected) were used to define activations.

#### RESULTS

#### Behavioral Results

The means and standard deviations of participants' pain intensity, liking, attractiveness, and envy ratings were shown in **Table 1**. A 2 (pain: painful vs. non-painful) × 2 (partner's attractiveness: PlainPlain vs. PlainAtt) repeated-measures ANOVA on pain intensity ratings revealed significant main effects of pain and partner's attractiveness [Fs(1,19) > 23.89, ps < 0.01]. The interaction was also significant [F(1,19) = 17.31, p < 0.01]. Post hoc analyses revealed significantly higher pain intensity ratings for painful situations than non-painful situations in both PlainPlain and PlainAtt conditions [ts(19) > 13.17, ps < 0.001]. Further analyses showed higher pain intensity rating difference (painful–non-painful) for PlainPlain than PlainAtt [t(19) = 4.16, p = 0.001].

Participants reported significantly less liking and higher envy [t(19) = 12.22, p < 0.01] for PlainAtt than for PlainPlain [t(19) = 5.41, p < 0.01]. No significant difference on the attractiveness ratings was found between PlainAtt and PlainPlain.

# fMRI Results

#### Main Effects

Brain regions related to painful stimuli vs. non-painful stimuli [(PlainAttP + PlainPlainP) – (PlainAttN + PlainPlainN)] were bilateral AI, aMCC, supplementary motor area, bilateral supramarginal gyrus, right inferior occipital gyrus, and cerebellum. The reverse contrast revealed significant activations in right superior occipital gyrus, right angular gyrus, left precuneus, aMCC, right middle frontal gyrus, right middle orbital gyrus, bilateral middle temporal gyrus, and left angular gyrus (**Table 2**). We did not report the main effect of partner's attractiveness for it was of no interest in the current study.

#### Interactions

The interaction between pain and partner's attractiveness identified by the (PlainPlainP – PlainPlainN) – (PlainAttP – PlainAttN) contrast revealed significant activations in right AI, aMCC, left thalamus, left precuneus, and left precentral gyrus, while the reverse contrast revealed significant activations in MPFC, right superior frontal gyrus (SFG) and right angular gyrus (**Table 3**). Percent signal changes were extracted from all the significant voxels in the 6 mm-radius spherical regions centered on the peak or local maximum coordinates identified in the interactions (coordinates can be found in **Table 3**). Further post hoc analyses revealed that, when watching painful pictures, greater percent signal changes in aMCC, right AI, left thalamus, left precuneus, and left precentral gyrus were detected for PlainPlain than for PlainAtt [ts(19) > 3.48, ps < 0.01], whereas in MPFC, right SFG and right angular gyrus, greater percent signal changes was observed for PlainAtt than for PlainPlain [ts(19) > 5.98, ps < 0.01; **Figure 2**]. When watching nonpainful pictures, no significant difference was found between PlainAtt and PlainPlain in any brain regions (**Figure 2**). Interestingly, for both MPFC and right SFG, we found that the difference in percent signal change between PlainAttP condition and PlainAttN condition was negatively correlated with the corresponding pain intensity rating difference (MPFC: r = –0.56, right SFG: r = –0.52, both p < 0.05), whereas similar analyses found no significant correlation for PlainPlain trials.

# DISCUSSION

The present study investigated how the empathic responses were modulated by intrasexual competition. Results showed that, at the behavioral level, participants reported less liking, lower empathic pain intensity, and higher envy for PlainAtt, the lucky guy with an attractive partner, than PlainPlain, the one with a plain partner.

#### TABLE 1 | Mean ( ± SD) for envy, attractiveness, liking, and pain intensity ratings.

#### TABLE 2 | Brain regions showing a significant main effect of pain.

Coordinates (mm) are in Montreal Neurological Institute (MNI) space. L = left hemisphere; R = right hemisphere. Cluster-level, p < 0.05, FWE corrected; voxel-level, p < 0.001, uncorrected.

TABLE 3 | Brain regions showing significant interactions.

Coordinates (mm) are in MNI space. L = left hemisphere; R = right hemisphere. Cluster-level, p < 0.05, FWE corrected; voxel-level, p < 0.001, uncorrected.

At the neural level, increased activations in AI and aMCC were observed in the painful situations relative to the non-painful situations. More importantly, decreased pain-related AI and aMCC activations and stronger MPFC and right SFG activations were found for PlainAtt than for PlainPlain, indicating behavioral and neural empathic responses to others' pain were modulated by intrasexual competition.

Anterior insula and ACC/aMCC have been considered to be involved in encoding the affective dimension of first-hand pain and to play a key role in empathy for others' pain (Singer et al., 2004). In the present study, AI and aMCC responded more strongly to the painful relative to the non-painful stimuli, which was consistent with the findings of previous studies that these areas were critically involved in empathic pain processing (Fan et al., 2011; Lamm et al., 2011). Furthermore, it has been shown that empathic neural responses in AI and aMCC are modulated by many situational factors (e.g., Xu et al., 2009; Guo et al., 2012, 2013; Feng et al., 2016). For example, a recent study found that social hierarchies established based on incidental skill in a perceptual task affected AI and aMCC activations during empathy for pain. Specifically, empathic brain activations in AI and aMCC were reduced when responding to the pain of superior-status targets relative to that of inferiorstatus targets (Feng et al., 2016). Interestingly, our data revealed that AI and aMCC were also involved in the modulation of pain empathy by intrasexual competition. Compared with the

guy with a plain partner, when participants saw the lucky guy suffering pain, reduced AI and aMCC activations and lower pain intensity ratings were observed, indicating that the normal empathic response for the lucky guy was suppressed. It should be noted that, accompanying the decrease of empathic responses, participants reported more negative attitudes (i.e., less liking and higher envy) toward the lucky guy, suggesting that intrasexual competition altered their attitudes, which might have affected the empathy for others' pain. This converging evidence may indicate that AI and aMCC activities are not just responsible for automatic bottom–up processing of others' pain, but are also sensitive to the top–down regulation of pain empathy by various situational factors, such as intrasexual competition and social hierarchies.

Interestingly, the present study also found greater activation in MPFC for PlainAtt than for PlainPlain. Previous studies have demonstrated that MPFC plays an important role in cognitive inhibitory control and emotion regulation (Floden and Stuss, 2006; Banks et al., 2007; Phillips et al., 2008). Recent brain imaging studies also revealed the engagement of MPFC in the empathy for others' pain (Cheng et al., 2007; Rameson et al., 2012).

Cheng et al. (2007) observed increased MPFC activation and also negative functional connectivity between MPFC and AI when physicians who practice acupuncture (versus matched controls) viewed painful stimuli, which was interpreted as reflecting cognitive inhibition of the affective processing in the pain matrix, revealing that MPFC was related to the down-regulation of empathy for pain. The data of the present study revealed greater MPFC activation for PlainAtt than for PlainPlain during the painful (relative to non-painful) situations. Further evidence from correlation analyses showed that when participants saw the lucky guy in pain, stronger activation in MPFC was observed and lower pain intensity ratings were reported, providing support for the argument that MPFC was associated with the evaluation of others' physical pain. Additionally, we also found that MPFC activation in the present study was accompanied by activity in right SFG. In addition to MPFC activity, Cheng et al. (2007) also observed increased right SFG activation and negative functional connectivity between right SFG and AI when physicians (versus controls) viewed painful stimuli. In the present study, right SFG was more active while processing the painful stimuli for the lucky guy and its activation predicted participants' pain intensity ratings for the lucky guy. This evidence suggests that right SFG may have a similar function to MPFC in evaluating others' physical pain.

The present study used fMRI to explore pain empathy for the lucky guy in love. The results revealed that individuals had

#### REFERENCES

more negative attitudes and reported lower pain intensity for the lucky guy with an attractive partner compared to the one with a plain partner. Neurally, reduced responses in AI and aMCC and increased activations in MPFC and right SFG were observed for the pain of the lucky guy compared to the one with a plain partner. These findings indicate intrasexual competition can affect attitudes toward same-sex rivals and modulate normal empathic responses to their suffering.

#### AUTHOR CONTRIBUTIONS

XG conceived of the project; XG, Li Zheng, and Lei Zhu designed the experiments; Li Zheng programmed the experimental scenario; Li Zheng and QW performed the experiments; JX analyzed the data with the help of Li Zheng; FZ and CW wrote the paper; all authors read and approved the manuscript. Li Zheng and FZ contributed equally to this work.

#### FUNDING

National Nature Science Foundation of China (31271090); National Natural Science Foundations of China (71371180); Key Program of the National Social Science Foundation of China (14AZD106); Outstanding Doctoral Dissertation Cultivation Plan of Action (PY2015042); Shanghai Leading Talent Plan.

experienced pain and empathy for pain. Neuroimage 54, 2492–2502. doi: 10.1016/j.neuroimage.2010.10.014

**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 Zheng, Zhang, Wei, Xu, Wang, Zhu, Roberts and Guo. 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.