Two different mirror neuron networks: The sensorimotor (hand) and limbic (face) pathways

Abstract

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.

Congenital facial palsy and emotion processing: The case of Moebius syndrome

“…It is possible that the congenital absence of facial mimicry that implies the inability to simulate the facial expressions of others has determined alterations in the visceral responses associated with emotions. The link between motor simulation and ANS reactivity is supported by several neuroimaging studies demonstrating motor pathways activation and brain structures (eg, amygdala, insula) regarded as part of the extended MNS both during execution and observation of emotional facial expressions. Thus, it would be interesting to explore whether people with MBS show reduced autonomic responses such as skin conductance response, finger temperature and heart rate, pupil diameter or hormonal levels .…”

“…Notably, neuroimaging studies in humans have shown that the observation and performance of facial expressions of emotions activate not only motor regions, typically activated during the observation of hand actions, but also regions of the limbic system, such as the anterior cingulate cortex, the amygdala and the anterior insula . Thus, in addition to the classic mirror circuits, emotional brain regions also seem to be vicariously activated while participants perceive the emotional states of others . Together, these findings provide a new picture on how MNs operate within a larger network (now called “Extended Mirror Neuron Network”), with clear implications on the multiple functions to which they might contribute.…”

“…15,16,127 Thus, in addition to the classic mirror circuits, emotional brain regions also seem to be vicariously activated while participants perceive the emotional states of others. 128 Together, these findings provide a new picture on how MNs operate within a larger network (now called "Extended Mirror Neuron Network"), 128,129 with clear implications on the multiple functions to which they might contribute. This is consistent with recent neuroanatomical meta-analyses in the monkey in which the authors reported connections between the mouth region of the ventral premotor cortex (F5) and brain regions involved in emotion processing, such as the basolateral amygdala, the anterior cingulate cortex and the anterior insula.…”

“…Through an embodied simulation mechanism, individuals implicitly and automatically (ie, not mediated by inferential or metalizing processes) can access to the meaning of others' emotions in terms of somatomotor experience and of the bodily changes (eg, heart rate activity, pupil dilation and other visceral responses) typically associated to a specific emotion. Given the complexity that such simulation process entails, it is not surprising that the neural networks involved in perceiving others' facial expressions would be distributed across several cortical and subcortical networks …”

“…This is consistent with recent neuroanatomical meta-analyses in the monkey in which the authors reported connections between the mouth region of the ventral premotor cortex (F5) and brain regions involved in emotion processing, such as the basolateral amygdala, the anterior cingulate cortex and the anterior insula. 128 These functional connections between the motor/premotor regions and limbic system would be considered a core neural system for emotion processing which, through a sensorimotor matching mechanism, provides to the observer a direct understanding of others' emotional experience.…”