Shared yet dissociable neural codes across eye gaze, valence and expectation

Area of Science:

• Neuroscience
• Primate behavior
• Social cognition

Background:

• Eye gaze direction is a crucial social cue in primates, influencing communication and emotional responses.
• While gaze can signal threat and anxiety, its neural overlap with stimulus value (valence) is not fully understood.
• Gaze predicts social encounter outcomes, which can be positive or negative, but the underlying neural mechanisms are unclear.

Purpose of the Study:

• To investigate the neural overlap between eye gaze processing and stimulus valence in primates.
• To identify distinct neural mechanisms for processing gaze outcomes versus expectations.
• To explore the implications for understanding social anxiety and related disorders.

Main Methods:

• Monkeys underwent the human intruder test with direct or averted gaze stimuli.
• Aversive and appetitive conditioning paradigms were interleaved with gaze stimuli.
• Single-neuron recordings were conducted in the amygdala and anterior cingulate cortex.

Main Results:

• Amygdala neurons encode eye gaze direction, while anterior cingulate cortex neurons encode social context.
• A shared neural population in the amygdala showed responses to direct/averted gaze mirroring aversive/appetitive stimuli.
• Two distinct neural mechanisms were identified: overall activity for gaze/unconditioned stimulus and correlated selectivity for gaze/conditioned stimulus.

Conclusions:

• Neural codes for gaze and valence significantly overlap in the primate amygdala.
• Distinct neural mechanisms underlie the processing of gaze outcomes and expectations.
• Findings provide insights into the neural basis of social interactions, valence computation, and social anxiety.