Functional differences in face processing between the amygdala and ventrolateral prefrontal cortex in monkeys

Abstract

The ability to categorize social information is essential to survive in a primate's social group. In the monkey brain, there are neural systems to categorize social information. Among these, the relationship between the amygdala and the ventrolateral prefrontal cortex (vlPFC) has recently gained focus with regard to emotion regulation. However, the processing of facial information and the functional differences in these two areas remain unclear. Thus, in this study, we examined the response properties of single neurons in the amygdala and vlPFC while presenting video clips of three types of facial emotions (aggressive threat, coo, and scream) in Macaca mulatta. Neurons in the amygdala were preferentially activated upon presentation of a scream facial expression, which is strongly negative, whereas the neurons in the vlPFC were activated upon presentation of coo, a facial expression with multiple meanings depending on the social context. Information analyses revealed that the amount of information conveyed by the amygdala neurons about the type of emotion transiently increased immediately after stimulus presentation. In contrast, the information conveyed by the vlPFC neurons showed sustained elevation during stimulus presentation. Therefore, our results suggest that the amygdala processes strong emotion roughly but rapidly, whereas the vlPFC spends a great deal of time processing ambiguous facial information in communication, and make an accurate decision from multiple possibilities based on memory.

Computational Architecture of the Parieto-Frontal Network Underlying Cognitive-Motor Control in Monkeys

“…The dmPFC cluster also includes area 45A, located in the caudal VLPF cortex. Functional data show that this sector is involved in multisensory processing of communication stimuli ( Romanski and Averbeck, 2009 ) and activates during action and face observation ( Nelissen et al, 2005 ; Tsao et al, 2008 ; Kuraoka et al, 2015 ), suggesting a role in communication behavior. Moreover, this region is activated during eye movement ( Premereur et al, 2015 ).…”

I'll take the low road: the evolutionary underpinnings of visually triggered fear

“…Exposure to fearful visual stimuli leads to changes in electrical activity of the amygdala in humans (Morris et al, 1996 ) and monkeys (Leonard et al, 1985 ; Nakamura et al, 1992 ; Kuraoka and Nakamura, 2006 , 2007 ; Gothard et al, 2007 ; Hoffman et al, 2007 ; Kuraoka et al, 2015 ) although the amygdala does not receive any direct retinal innervation. LeDoux ( 1990 , 1994 ) suggested that visual threats were primarily conveyed to the limbic system via the SC-pulvinar pathway, the so-called “low road” (Figure 1 ).…”

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

“…In fact, the ventrolateral prefrontal cortex (VLPC) is connected both with temporal sectors participating to the visual coding of biological motion (Barbas, 1988; Petrides and Pandya, 2002; Gerbella et al, 2010, 2013; Borra et al, 2011) and, as demonstrated in the present study, with the mouth MNs sector. In addition, VLPC contains neurons responding to visual stimuli of faces and of facial communicative gestures (Ó Scalaidhe et al, 1997, 1999; Sugihara et al, 2006; Romanski and Diehl, 2011; Kuraoka et al, 2015). It is also likely that information related to facial expressions and/or its emotional content could reach the F5/opercular region through other pathways involving the orbitofrontal, insula and the amygdala (see below for further elaboration).…”