Research ReportThe gender you are and the gender you like: Sexual preference and empathic neural responses
Introduction
Social cognition links together a vast array of abilities that help us function appropriately in interpersonal relationships in our everyday lives. Proper function in social circumstances depends, to a great measure, on our successful understanding of the people around us. Empathy is a central mechanism of understanding the other, which helps us sense the other's feelings and emotions (Rogers, 1957). Empathy is a multidimensional construct and comprises the cognitive as well as the emotional reactions of individuals to events experienced by other individuals. Thus, empathy may involve reactions such as emotion recognition, perspective taking and emotional contagion which may occur simultaneously or separately (Shamay-Tsoory, 2011).
Empathy and its various constructs have been shown to be sensitive to individual differences, particularly to gender related differences (Schulte-Ruther and Markowitsch, 2008, Yang and Decety, 2009, Derntl and Finkelmeyer, 2010, Pavlova and Wecker, 2010). Indeed, several studies have supported the view of female superiority in empathy-related tasks, such as decoding non-verbal communication, picking up subtle nuances from tone of voice or facial expression, and judging a person's character (Klein and Hodges, 2001, Hall and Matsumoto, 2004). Although several studies failed to find gender differences in empathy (Bandstra and Chambers, 2011, Roth-Hanania and Davidov, 2011) it has been reported that women score higher than men on self-report measures of empathy (Davis, 1994, Baron-Cohen and Wheelwright, 2004). The findings regarding sex differences in empathy are in accordance with the fact that various psychiatric disorders, such as autism spectrum disease, conduct disorder, and antisocial personality disorder, which are often characterized by impaired empathy, are far more common among men (Chakrabarti and Baron-Cohen, 2006).
Recent meta-analyses have shown that empathy related activations include a series of different brain regions including the anterior cingulate, supplementary motor area and bilateral anterior insula (Fan and Duncan, 2011, Lamm and Decety, 2011). On the other hand more cognitive aspects of empathy, including metalizing related tasks have repeatedly shown to activate the medial prefrontal cortex (MPFC), the temporo-parietal junction (TPJ), and the superior temporal sulcus (STS) (Frith and Frith, 2003, Vogeley and Fink, 2003, Decety and Lamm, 2007, Schulte-Ruther and Markowitsch, 2008, Van Overwalle, 2009). Specifically, the TPJ is thought to be important in various social behaviors. The TPJ has a critical role in empathic processing (Cheon et al., 2011) and seems to be engaged in self-reference thoughts (Johnson et al., 2002), mentalizing about the other (Lombardo et al., 2010) as well as in emotion evaluation (Zysset and Huber, 2002, Winston and O’Doherty, 2003), and has been shown to respond atypically in autism during mentalizing (Saxe and Wexler, 2005, Lombardo and Chakrabarti, 2011). A common denominator underlying these behaviors may be the integration and comparisons between self and other mental state. Thus, it might be speculated that the TPJ is a key region where the decoupling of self versus other representations occurs. While the TPJ seems to be responsible for self–other decoding, the MPFC appears to be involved in more abstract inferences about self and others. It has been shown that this region is recruited in self-knowledge, person perception, and mentalizing processes, all of which underlie empathy (Decety and Chaminade, 2003, Gallagher and Frith, 2003).
To date, few behavioral and neuroimaging studies (Canli and Desmond, 2002, Bandstra and Chambers, 2011, Lamm and Decety, 2011, Mercadillo and Diaz, 2011, Roth-Hanania and Davidov, 2011, Chun and Park, 2012, Decety and Svetlova, 2012) have investigated gender differences in empathy. While several studies did not find any gender differences (Geangu and Benga, 2010, Bandstra and Chambers, 2011, Roth-Hanania and Davidov, 2011), some functional imaging studies have found evidence for sex related differences in empathy (Schulte-Ruther and Markowitsch, 2008, Derntl and Finkelmeyer, 2010, Chou and Cheng, 2011). For example, Singer et al. (2006) showed that empathy-related activations are differently modulated in men and women by learned preferences, which are gained through social interactions. In line with this finding, it has also been found that women tend to recruit areas containing mirror neurons, such as the inferior frontal region, more prominently than men (Schulte-Ruther et al., 2008). Hence the question whether gender influences empathy skills is an open one which needs more exploration.
However, no study to date has examined sexual preference of the subject relates to different empathic abilities. Although sexual preference has been shown to be critical to social behavior (Liu et al., 2011), little is known about the relationship between sexual orientation and empathy and its underlying neural mechanism.
Sexual orientation is defined as the degree of sexual attraction to either men or women (Ellis and Ames, 1987). Studies on sexual preference have focused mainly on genes (Liu et al., 2011), prenatal hormones, and brain neuroanatomy (Bem, 1996, Rahman, 2005). It has been suggested that in homosexual men, the interstitial nucleus 3 of the human anterior hypothalamus is more female-like (Le Vay, 1991) and that in homosexual women, the grey matter in the perirhinal cortex, a region associated with social bonding, displays a more male-like structural pattern (Ponseti et al., 2007). Recently, Savic and Lindstrom (2008) demonstrated differences in brain asymmetry and connectivity related to sexual preference. They found that homosexual men showed similar amygdala connectivity patterns to heterosexual women (i.e., connections with the caudate, putamen, and prefrontal cortex), while the pattern of connectivity of homosexual women resembled that of heterosexual men (i.e., connection with the cingulate cortex).
In accordance with these anatomical findings, a considerable amount of personality and behavioral findings have demonstrated that homosexual men are more feminine than heterosexual men and that homosexual women are more masculine than heterosexual women (Haslam, 1997). Homosexual and heterosexual individuals are also found to differ on measures of masculine instrumentality and feminine expressiveness (Lippa, 2000). Furthermore, investigations of cognitive skills have shown that homosexual men demonstrate female-typical responses in cognitive-related tasks, such as spatial location memory, recall of spatial landmarks during navigation, and phonological and semantic fluency (Rahman, 2005), indicating similarities between the brains of heterosexual women and homosexual men.
Collectively, these findings support the possibility that individual differences in empathy may be related not only to gender, but also to sexual preference. If indeed women show higher levels of empathy and homosexual men show similar neural and behavioral patterns, then it is possible that individuals attracted to men (homosexual men, heterosexual women) would show higher levels of empathy than individuals attracted to women (homosexual women, heterosexual men). To the best of our knowledge, no brain imaging study has investigated sexual preference differences in social behavior and empathy. Therefore, the aim of the present study was to examine differences in the neural empathic responses of individuals attracted to men versus individuals attracted to women. Given that gender differences have been reported for the neural correlates of emotional perspective taking (Schulte-Ruther et al., 2008), in the current study we used an emotional mentalizing task in which subjects rated the emotional magnitude of events happening to another protagonist (“OTHER” condition) or to themselves (“SELF” condition, Fig. 1). It was speculated that individuals attracted to men would show higher behavioral and neural empathic responses toward the protagonist as compared to subjects attracted to women. Specifically, it was hypothesized that both the gender and the sexual orientation of the subjects would interact so that heterosexual women will show the highest empathy followed by homosexual men, homosexual women and heterosexual men. Finally, we predicted that the levels of sexual orientation tendencies, as assessed by the Klein Sexual Orientation Grid (KSOG) (Klein, 1993) would predict the levels of empathy in the task.
Section snippets
Behavioral results
To examine the empathic abilities of the participants an empathy index was calculated as the ratio between the ratings for SELF and OTHER protagonists. For purposes of convenience, the index was multiplied by −1, indicating that higher index scores represent higher empathy and vice versa. The index was calculated for each subject.
A univariate ANOVA of the empathy index, with gender (women, men) and attraction (attracted to men, attracted to women) as the between-subject factors was performed.
Discussion
The present study investigated the behavioral and neural characteristics of empathy as manifested by subjects from different sexual orientation groups. Brain-related empathy activations were measured in women and men with a clear homosexual or heterosexual preference who were undergoing a mentalizing task comprising of emotional mentalizing about the self versus another protagonist.
Our data show that at the behavioral level, individuals attracted to men (homosexual men and heterosexual women)
Conclusion
We show here that subjects differ on their empathic abilities depending on their sexual preference such that subjects attracted to men empathize to a higher degree than subjects attracted to women. These results indicate that individual differences in empathy may be modulated by one's sexual preference. Hence, sexual orientation and preference are important when examining individual differences in empathy.
Participants
Participants were 52 healthy individuals, ranging in age from 22–36 (mean age: 28.46, SD=3.4). The recruitment of subjects was carried out through an ad and was based on a screening which included a self-report questionnaire involving direct questions regarding the sexual orientation of the participant (heterosexual/homosexual). Following the screening, the participants were grouped into two sexual preference groups and were invited to the scanning session. Subjects were included only if they
Author contributions
The authors declare no conflict of interest.
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