Empathy: Gender effects in brain and behavior

https://doi.org/10.1016/j.neubiorev.2014.09.001Get rights and content

Highlights

  • Sex differences in empathy have phylogenetic and ontogenetic roots in biology.

  • As primary caregivers females evolved adaptations to be sensitive to infants’ signals.

  • Sex differences in empathy appear to be consistent and stable across the lifespan.

  • In affective empathy, females, compared to men, show higher emotional responsivity.

  • Males show greater recruitment of brain areas for the control of cognitive empathy.

Abstract

Evidence suggests that there are differences in the capacity for empathy between males and females. However, how deep do these differences go? Stereotypically, females are portrayed as more nurturing and empathetic, while males are portrayed as less emotional and more cognitive. Some authors suggest that observed gender differences might be largely due to cultural expectations about gender roles. However, empathy has both evolutionary and developmental precursors, and can be studied using implicit measures, aspects that can help elucidate the respective roles of culture and biology. This article reviews evidence from ethology, social psychology, economics, and neuroscience to show that there are fundamental differences in implicit measures of empathy, with parallels in development and evolution. Studies in nonhuman animals and younger human populations (infants/children) offer converging evidence that sex differences in empathy have phylogenetic and ontogenetic roots in biology and are not merely cultural byproducts driven by socialization. We review how these differences may have arisen in response to males’ and females’ different roles throughout evolution. Examinations of the neurobiological underpinnings of empathy reveal important quantitative gender differences in the basic networks involved in affective and cognitive forms of empathy, as well as a qualitative divergence between the sexes in how emotional information is integrated to support decision making processes. Finally, the study of gender differences in empathy can be improved by designing studies with greater statistical power and considering variables implicit in gender (e.g., sexual preference, prenatal hormone exposure). These improvements may also help uncover the nature of neurodevelopmental and psychiatric disorders in which one sex is more vulnerable to compromised social competence associated with impaired empathy.

Introduction

Empathy – the ability to understand and share in the internal states of others – is a complex, multidimensional phenomenon that includes a number of functional processes, including emotion recognition, emotional contagion, and emotion priming (for recent reviews, see Decety and Jackson, 2006, Singer, 2006, Walter, 2012), as well as the abilities to react to the internal states of others, and to distinguish between one's own and others’ internal states (e.g., Tomova et al., 2014). From the perspective of evolutionary and developmental biology, empathy's purposes, in both humans and nonhuman animals, can be broadly divided into two categories: Promoting prosocial, cooperative behavior, and understanding or predicting the behavior of others (Smith, 2006).

Empathy has been studied from many perspectives (Davis, 1980, Decety and Moriguchi, 2007, Zaki and Ochsner, 2012). For example, social psychology has examined the manifestations of empathy within moral reasoning and social behaviors like mimicry (e.g., Sonnby-Borgström, 2002). In economics, studies have considered empathy's effects on decision-making (e.g., Beadle et al., 2012, Loewenstein, 2005, Ferrari, 2014). Cognitive neuroscience studies of empathy, on the other hand, are mainly divided into two lines of research, one focused on preconscious mechanisms which underlie/facilitate sharing (and mimicry) of others’ behaviors and internal states (we will refer to it as mirroring); the other line of research is focused on a conscious, deliberative process through which inferences can be made about others’ bodily and affective states, beliefs, and intentions (often called mentalizing) (Keysers and Fadiga, 2008, Zaki and Ochsner, 2012). These two aspects of empathy can be roughly mapped onto affective (or pre-reflective) and cognitive (reflective) empathic predispositions, respectively (Smith, 2006). Affective empathy is associated with activity in frontoparietal, temporal, and subcortical regions classically associated with movement, sensation, and emotion, while neural systems involved in cognitive control and decision-making – such as the cingulate, prefrontal, and temporal areas – are often activated during tasks requiring cognitive empathy (see Fig. 1) (Zaki and Ochsner, 2012).

How are these two primary modes of empathizing – cognitive empathy and affective empathy – related? While affective empathy involves pre-reflective processes, humans seem nevertheless capable of consciously and unconsciously modulating it. Furthermore, humans are capable of internally evoking emotions, behaviors, and sensations of an absent other, or even of ourselves at another point in time. We are also capable of inhibiting our internal states and reflexive responses to others. Indeed, numerous studies have shown that mirroring is modulated by numerous contextual factors, such as social distance, status, trustworthiness, group membership, and attention (Bernhardt and Singer, 2012, Gu and Han, 2007, Guo et al., 2012, Hogeveen et al., 2014, Lamm et al., 2007, Liew et al., 2011, Loggia et al., 2008, Singer et al., 2006), and is controlled by systems involved in cognitive empathy (Spengler et al., 2010). Conversely, some authors propose that mentalizing and social decision-making may employ information derived from mirroring (Iacoboni et al., 2005, Obhi, 2012, Zaki and Ochsner, 2009) (Fig. 2).

Recent studies suggest that a large portion of the ability to read intentions derive from pre-reflective mechanisms for processing biological motion (Obhi, 2012), and studies of empathic accuracy have shown that accurately discerning the internal states of others, as well as inferring intentions from observed behavior, relies on the interaction between mirroring and mentalizing processes (Liew et al., 2011, Zaki and Ochsner, 2012). There is also evidence that our immediate affective responses to others’ pain and distress can increase prosocial decision-making (Christov-Moore and Iacoboni, under revision; Hein et al., 2010, Masten et al., 2011, Ma et al., 2011, Smith, 2006). Indeed, it is likely that, without the interactive participation of both modes of empathizing, social interactions would be impaired, potentially impacting the health and wellbeing of the individual as well as those around him/her (Gallese, 2003).

While we now associate the mentalizing system with decision-making, musing about others etc., this system may have arisen in part as a form of contextual control for mirroring. In our view, this seems likely for two reasons: compared to the mirroring system, both the mentalizing system's cognitive functions and the brain areas that underlie mentalizing (i.e., temporal and prefrontal cortices), (1) developed more recently in our evolution and (2) are the last to mature during ontogeny (Preston and De Waal, 2002). Furthermore, neural systems associated with mentalizing have been implicated in the control of behavioral mirroring (mimicry) (Spengler et al., 2010). Indeed, recent evidence from our group (Christov-Moore and Iacoboni, under revision) suggests that mirroring areas and mentalizing areas exist in interaction rather than as independent systems. Rather than just using the mirroring system when we view others in pain, feeling emotion, or having fast social interactions that are typically thought to bypass mentalizing (Bohl and van den Bos, 2012), and using the mentalizing system when we need to consciously make decisions in a social setting, guess the beliefs and intentions of others, or take another person's perspective, we may use both at all times. Obviously, one system may take the lead over the other, depending on the situation's demands. This larger dynamic system formed by the interactions between mirroring and mentalizing may allow individuals to revisit past experience and behavior, predict the consequences of their own behaviors, both for themselves as well as for others, and to selectively share in the behavior and affective states of others in response to context (such as common group affiliation).

An understanding of empathy would be incomplete without a consideration of individual differences. Popular conceptions of gender1– defined here as reflecting both self-identification (i.e., females, males) as well as biological classification (i.e., female, male) – contain expectations about empathy and empathic behavior, many of which have been borne out by extant research. However, empathy and gender remain difficult to define, in part because the disciplines that study them use distinct and often non-overlapping methods and terminology. While this difficulty is not something we can address in this article, we should keep it in mind when considering the evidence reviewed here.

In reviewing gender differences in empathy, we propose to address two questions: first, how deep do gender differences in empathy go? Cultural and societal effects on gender differences are most pronounced in explicit measures in which adults are asked to describe themselves or produce a behavior which is clearly related to “empathy” or “sympathy” (Eisenberg and Lennon, 1983, Gleichgerrcht and Decety, 2013). However, meta-analyses examining gender and sex differences in empathy provide results supporting fairly stable gender differences across a broad range of measures (e.g., Cohn, 1991, Eisenberg and Lennon, 1983, Feingold, 1994, Hall, 1978, Hall, 1984, Hoffman, 1977, O’Brien et al., 2013, Thompson and Voyer, 2014; although, for null results see Lamm et al., 2007). Additionally, empathy has developmental precursors in early infancy (Alexander and Wilcox, 2012, McClure, 2000) as well as evolutionary precursors in other social animals (Preston and De Waal, 2002). Indeed, there is considerable overlap between empathetic behaviors demonstrated in young humans early in development and in nonhuman animals. Thus, in addition to examining implicit measures of empathy, we can look to developmental and evolutionary precursors of empathy for a more complete view of sex differences.

The second question this review will address is the nature of empathy itself, that is, what are its core biological and neural underpinnings? More specifically: are individual differences in cognitive and affective subcomponents of empathy independent or tightly integrated (or somewhere in between)? Are individual differences in the behavioral manifestations of empathy, such as social competence or prosocial behavior, due to differences in low-level processes like emotional reactivity, or higher level functions like spatial reasoning or theory of mind (ToM)? Which components of empathy emerge first during ontogeny, and does each component accomplish a specific proximate or ultimate function throughout development? To what extent, and in what way, is empathy modulated and controlled by higher cognitive functions? As recent cognitive neuroscience reviews have suggested (Zaki and Ochsner, 2012), the relationship between the principal components of empathy, as they are currently studied, remains unclear. Although several scholars agree that emotional and cognitive component of empathy underpin a broad range of empathic responses, a global concept of empathy remains elusive, and this is in large part due to a lack of cross-talk among the disparate fields that study it. Studying gender differences in empathy might provide insights to understanding empathy by observing whether such differences covary across different measures. For example, if we were to find consistent gender differences in both affective empathy and prosocial behavior, but less consistent differences in cognitive empathy, we might infer that affective empathy drives prosocial behavior.

To address these issues, we structured this review into four parts. First, we will examine the evolutionary precursors of empathy. Then, we will review gender differences related to the psychological and behavioral processes associated with empathy. Sex differences in empathy will be also evaluated from an ontogenetic point of view. Lastly, we will review evidence suggesting that gender differences assessed at behavioral and psychological level are supported by specific neural substrates.

Section snippets

Evolutionary precursors of empathy

In the last few decades, as outlined above, it has become evident that empathy is not limited to the cognitive manifestation of the capacity to take the perspective of another, putting oneself in others’ shoes. Instead, empathic responses are often revealed by immediate responses of the body (e.g., Levenson and Ruef, 1992), suggesting that the brain mechanisms mediating such responses are often devoid of cognitive efforts (Shamay-Tsoory, 2014, Shamay-Tsoory et al., 2009).

Empathy should

Emotion recognition, priming, and emotion contagion

In humans, the ability to recognize other people's emotions varies among individuals (Martin et al., 1996). Throughout the nonverbal perception literature there appears a consistent pattern of interindividual differences: a female advantage in nonverbal emotion recognition, in both visual and auditory modalities (Hall, 1990, McClure, 2000, Schirmer et al., 2007; for recent reviews, see Kret and De Gelder, 2012, Stevens and Hamann, 2012, Thompson and Voyer, 2014). Though an extensive review of

Precursors to empathy in infancy: Emotion contagion, mimicry, and social interest

Rudimentary forms of empathy may exist in infants – perhaps facilitated by the matching and synchronization of emotional facial expression – behaviors that appear to promote emotional closeness of mothers and infants (e.g., Murray et al., 1996). The degree of emotional synchrony can be determined by monitoring mother–infant physiology (e.g., heart rate: Feldman et al., 2011), or behavior (de Waal, 1989, Sagi and Hoffman, 1976). For instance, contagious crying is a phenomenon in which human

Mirror neurons

In emphasizing that empathy is a multilayered phenomenon, several scholars converge in considering an action–perception mechanism as central for automatically reproducing others’ affective states (Preston and De Waal, 2002, Iacoboni, 2009). Much theoretical discussion has been stimulated by the discovery of mirror neurons in the ventral premotor cortex and the inferior parietal lobule of the monkey (Di Pellegrino et al., 1992, Gallese et al., 1996, Rizzolatti et al., 1996). These neurons have

Conclusions

The construct of empathy is relevant to several disciplines, from psychology and neuroscience, to behavioral economics and animal behavior. For years, theories on altruism and kin selection have emphasized the selfish nature of humans and other animals. However, the ‘selfish gene’ paradigm faced serious challenges to the idea that individuals are complex organisms whose activities ultimately function to increase reproductive success, and do so through careful calculations of costs and benefits.

Acknowledgements

This work was supported by NICHD P01HD064653 to P. F.F., by NIH grant 1R21MH097178 to M.I., and by NSF Graduate Fellowship DGE-1144087 to L.C.-M.

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