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.
The voluntary control of phonation is a crucial achievement in the evolution of speech. In humans, ventral premotor cortex (PMv) and Broca's area are known to be involved in voluntary phonation. In contrast, no neurophysiological data are available about the role of the oro-facial sector of nonhuman primates PMv in this function. In order to address this issue, we recorded PMv neurons from two monkeys trained to emit coo-calls. Results showed that a population of motor neurons specifically fire during vocalization. About two thirds of them discharged before sound onset, while the remaining were time-locked with it. The response of vocalization-selective neurons was present only during conditioned (voluntary) but not spontaneous (emotional) sound emission. These data suggest that the control of vocal production exerted by PMv neurons constitutes a newly emerging property in the monkey lineage, shedding light on the evolution of phonation-based communication from a nonhuman primate species.
The ventral agranular frontal cortex of the macaque monkey is formed by a mosaic of anatomically distinct areas. Although each area has been explored by several neurophysiological studies, most of them focused on small sectors of single areas, thus leaving to be clarified which is the general anatomo-functional organization of this wide region. To fill this gap, we studied the ventral convexity of the frontal cortex in two macaque monkeys (Macaca nemestrina) using intracortical microstimulation and extracellular recording. Functional data were then matched with the cytoarchitectonic parcellation of the recorded region. The results demonstrated the existence of a dorso-ventral functional border, encompassing the anatomical boundary between areas F4 and F1, and a rostro-caudal anatomo-functional border between areas F5 and F4. The ventral subdivision of areas F4 and F1 was highly electrically excitable, represented simple mouth movements and lacked visual properties; in contrast, their dorsal counterpart showed a higher stimulation threshold, represented forelimb and mouth motor acts and hosted different types of visual properties. The data also showed that area F5 was scarcely excitable, and displayed various motor specificity (e.g. for the type of grip) and complex visual (i.e. mirror responses) properties. Overall, the posterior areas F4 and F1 appear to be involved in organizing and controlling goal-directed mouth motor acts and simple movements within different parts of the external (dorsal sector) and internal (ventral sector) space, whereas area F5 code motor acts at a more abstract level, thus enabling the emergence of higher order socio-cognitive functions.
The vast majority of functional studies investigating mirror neurons (MNs) explored their properties in relation to hand actions, and very few investigated how MNs responding to mouth actions or communicative gestures. From an anatomical point of view, hand and mouth MNs were recorded in two partially overlapping sectors of the ventral precentral cortex of the macaque monkey: hand MNs were located more dorsally (area F5), mouth MNs more ventrally, extending over the border between the premotor (F5) and the opercular region (DO and PrCO). Despite this anatomical segregation, there is a general assumption that a same neuroanatomical network, having a main source of visual information deriving from the parietal cortex, supports both hand and mouth MNs. In the current review, we challenge this perspective and describe the connectivity pattern of mouth MNs sector, comparing it with the hand MNs sector of F5. The mouth and hand MNs sectors share part of their connectivity pattern, but each also has distinct and specific connections. In particular, the mouth MNs F5/opercular region is connected with premotor, parietal areas mostly related to the somatosensory and motor representation of the face/mouth (area F4, the region between areas F3 and F6, areas PF and SII) and with area PrCO, involved in processing gustatory and somatosensory intraoral input. Unlike hand MNs, mouth MNs do not receive their visual input from parietal regions. Information related to face/communicative behaviors could come from the ventrolateral prefrontal cortex (areas 12 and 46). Further strong connections derive from limbic structures involved in encoding emotional facial expressions and motivational/reward processing. These brain structures include the anterior cingulate cortex, the anterior and mid-dorsal insula, orbitofrontal cortex and the basolateral amygdala. These anatomical data are in agreement with neurophysiological evidence showing that in the mouth MNs F5/opercular region there are neurons responding to facial communicative gestures and also neurons firing during the production of vocalizations. The mirror mechanism is therefore composed and supported by at least two different anatomical pathways: one is concerned with sensorimotor transformation in relation to reaching and hand grasping within the traditional parietal-premotor circuits; the second one is linked to the mouth/face motor control and is connected with limbic structures, involved in communication/emotions and reward processing. This new view of the mirror mechanism provides a new theoretical account to explain different patterns of brain activation in neuroimaging studies and has also important implications for our comprehension of the developmental factors and evolutionary processes involved in mirror neurons origins and functions.
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