Self-monitoring of social facial expressions in the primate amygdala and cingulate cortex

Abstract

Keeping track of self-executed facial expressions is essential for the ability to correctly interpret and reciprocate social expressions. However, little is known about neural mechanisms that participate in self-monitoring of facial expression. We designed a natural paradigm for social interactions where a monkey is seated in front of a peer monkey that is concealed by an opaque liquid crystal display shutter positioned between them. Opening the shutter for short durations allowed the monkeys to see each other and encouraged facial communication. To explore neural mechanisms that participate in self-monitoring of facial expression, we simultaneously recorded the elicited natural facial interactions and the neural activity of single neurons in the amygdala and the dorsal anterior cingulate cortex (dACC), two regions that are implicated with decoding of others' gestures. Neural activity in both regions was temporally locked to distinctive facial gestures and close inspection of time lags revealed activity that either preceded (production) or lagged (monitor) initiation of facial expressions. This result indicates that single neurons in the dACC and the amygdala hold information about self-executed facial expressions and demonstrates an intimate overlap between the neural networks that participate in decoding and production of socially informative facial information.face-to-face interaction | spike triggered average | facial-expression production | amygdala-cingulate interaction A ccurate decoding of social interaction requires information about all participants, including one's own behavior. We would interpret differently a smile if we knew that we smiled first (or not) and, similarly, a threatening face has different meaning if we threatened first. Computationally, this ambiguity implies that information about the observed facial expression and one's own expression should converge in the network to incorporate these complementary sources of information. However, little is known about the neural mechanisms that enable such integration.Successful decoding of a facial expression should allow a rapid adequate response to the outcome that is implied by this meaningful expression. Accordingly, the amygdala, a structure associated with representing the learned valence of sensory inputs (1, 2), has been implicated with decoding and processing of various facial expressions (3). Notably, bilateral amygdala lesion selectively impairs recognition of fear expressions (4), which possibly signal the existence of an immediate threat. In addition, amygdala responses to fear and other facial expressions are modulated by social context (5, 6) (e.g., gaze direction), suggesting that the amygdala also participates in the decoding processes of a wider range of emotionally salient facial signals.The dorsal anterior cingulate cortex (dACC) is hypothesized to synthesize information about reinforcers with the current behavioral goal (7) and contributes to the resolution of emotional conflicts (8). Like the amygdala, dACC response to facia...

New perspectives on the neurophysiology of primate amygdala emerging from the study of naturalistic social behaviors

“…Most importantly, these results pave the way for future experiments that will replace videos with live interactions with conspecifics as already pioneered by a few laboratories. 70,78,81,82 The ideal development would be to implement in the laboratory closed-loop social interactions. The social brain evolved to process social signals and make social decisions in closed-loop interactions—and neural activity monitored under such conditions holds the promise of further exciting discoveries.…”

“…Neural responses to tactile stimuli in the primate amygdala have not been previously reported and understanding their function will require further exploration. These neurons may serve as necessary sensory feedback during the production of facial expressions, as suggested by Livneh et al 70 …”

Mirth and laughter elicited by electrical stimulation of the human anterior cingulate cortex

“…Moreover, subcortical connections of the rostral ACC include midline, intralaminar and mediodorsal nuclei , and the lateral and accessory basal nuclei of the amygdala (Ghashghaei and Barbas, 2002;Morecraft et al, 2007). Note that monkey studies showed that neurons in both the anterior cingulate cortex and amygdala respond during production of lip-smacking, that is a typical monkey emotional and affiliative facial expression (Livneh et al, 2012). On the basis of this evidence, Gothard (2014) suggested that this region is in position to coordinate both the behavioral and autonomic expression of emotions.…”

“…shown by single neuron studies (Livneh et al, 2012), and on the other side that rostral ACC, ventral insula and the amygdala are part of the same cortico-subcortical loop (Höistada and Barbas, 2008), one can speculate that they constitute the core structures for the control of positive emotions.…”

The neurobiology of primate vocal communication

“…Macaques, in particular, exhibit prototypical facial movements associated with specific types of vocalizations [82]. Both the pre-frontal mirror neuron system [83] and anterior cingulate cortex [84] exhibit neural activities that reflect an animal’s current facial gestures, making them two possible sites for non-auditory vocal self-monitoring. Further work will be needed to elucidate the role of these pathways in vocalization-associated somatomotor control and in the integration of multiple sensory pathways for feedback vocal control.…”