Widespread implementations of interactive social gaze neurons in the primate prefrontal-amygdala networks

Neuron. 2022 Jul 6;110(13):2183-2197.e7. doi: 10.1016/j.neuron.2022.04.013. Epub 2022 May 10.

Abstract

Social gaze interaction powerfully shapes interpersonal communication. However, compared with social perception, very little is known about the neuronal underpinnings of real-life social gaze interaction. Here, we studied a large number of neurons spanning four regions in primate prefrontal-amygdala networks and demonstrate robust single-cell foundations of interactive social gaze in the orbitofrontal, dorsomedial prefrontal, and anterior cingulate cortices, in addition to the amygdala. Many neurons in these areas exhibited high temporal heterogeneity for social discriminability, with a selectivity bias for looking at a conspecific compared with an object. Notably, a large proportion of neurons in each brain region parametrically tracked the gaze of self or other, providing substrates for social gaze monitoring. Furthermore, several neurons displayed selective encoding of mutual eye contact in an agent-specific manner. These findings provide evidence of widespread implementations of interactive social gaze neurons in the primate prefrontal-amygdala networks during social gaze interaction.

Keywords: anterior cingulate cortex; basolateral amygdala; dorsomedial prefrontal cortex; mutual eye contact; naturalistic behavior; non-human primates; orbitofrontal cortex; prefrontal-amygdala networks; real-life social gaze interaction; social gaze monitoring.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amygdala* / physiology
  • Animals
  • Gyrus Cinguli
  • Neurons / physiology
  • Prefrontal Cortex* / physiology
  • Primates