Sex-related functional asymmetry in the limbic brain

Abstract

At a macroscopic level, the brains of both men and women are very similar. However, closer inspection shows striking differences between the sexes in the structure–function relationships in the brain. Interpersonal, emotional, and occupational success depends critically on effective navigation of the social world. At the same time, individuals of each sex have different goals—only women bear children, and this basic function likely sets the agenda for the individual and societal goals of many women. Men do not bear children and may be driven by an agenda emphasizing acquiring and maintaining resources and power. Thus, sex differences in social-emotional regions of the brain might be adaptive. The limbic regions of the brain and closely connected regions, especially the ventromedial prefrontal cortex (VMPC) and amygdala, are important for social-emotional processing. Furthermore, as nearly all brain regions have homologous versions in each hemisphere, this may be a substrate on which divergent selection resulted in sex-related functional asymmetry. Studies of neurological patients have shown that the right VMPC and amygdala appear to be critical for social-emotional functioning and decision making in men, whereas the left VMPC and amygdala appear to be more important for these functions in women (Tranel et al, 2005; Tranel and Bechara, 2009). For example, a man with a unilateral right VMPC lesion, who was well educated and had worked successfully as a minister, was entirely unable to return to any form of gainful employment after his brain damage. He requires supervision for daily tasks and demonstrates severe disturbances in behavior and emotional regulation, including impulsivity and poor judgment. By contrast, a man with a unilateral left VMPC lesion was able to return to his job at a grain elevator and remains successfully employed there. He is remarkably free of disturbances to his social life and emotional functioning (Tranel et al, 2005). Moreover, preliminary evidence from the Trust Game, a multiplayer neuroeconomics task, suggests that women with left VMPC lesions and men with right VMPC lesions trust others less (ie, they invest less in others) and display more frequent acts of negative interpersonal reciprocity (ie, they return less than the amount invested). Similarly, women with lesions to the left amygdala and men with lesions to the right amygdala appear less risk averse than do men and women with lesions to the opposite amygdala. This evidence converges with other research, including (1) fMRI studies showing similar patterns of lateralized activations in these regions in response to social and emotional paradigms (eg, Killgore and Yurgelun-Todd, 2001; Cahill et al, 2004); (2) studies showing sex differences in orbitofrontal-dependent behavioral paradigms, such as the Iowa Gambling Task (eg, Overman, 2004); and (3) studies showing increased functional connectivity with the right amygdala of men and with the left amygdala of women (eg, Kilpatrick et al, 2006). Altogether, such evidence suggests that the right VMPC and amygdala in men as well as the left VMPC and amygdala in women are important for social-emotional functions. Potentially, the left limbic dominance observed in women reflects a need for expertise in interpersonal relationships (eg, the need to bear and rear children, maintain in-group cohesion, etc.), whereas the right limbic dominance observed in men could reflect a need for expertise in inter-group relations (eg, warfare, out-group relations, leverage of critical resources, etc.). Sex-related functional asymmetry in the VMPC and amygdala may prove to be at the heart of the complementary social roles that both men and women have in human society. It is incontrovertible that men and women deserve equal opportunities to participate in society; it is also clear that men and women are neither biologically nor behaviorally identical. Sex-related functional asymmetry may be one way that evolution has capitalized on the capacity of homologous brain regions to process information differently and shaped our brains to meet the demands of both the sexes with unique reproductive and social roles.