Value-related neuronal responses in the human amygdala during observational learning

Abstract The amygdala plays an important role in many aspects of social-cognition and reward-learning. Here we aimed to determine whether human amygdala neurons are involved in the computations necessary to implement learning through observation. We performed single-neuron recordings from the amygdalae of human neurosurgical patients (male and female) while they learned about the value of stimuli through observing the outcomes experienced by another agent interacting with those stimuli. We used a detailed computational modeling approach to describe patients’ behavior in the task. Then, using both population-level decoding and single neuron analyses we found evidence to implicate amygdala neurons in two key computations relevant for observational-learning: tracking the expected future reward associated with a given stimulus, and in tracking outcome values received by oneself or other agents. Encoding and decoding analyses suggested observational value coding in amygdala neurons occurred in a different subset of neurons than experiential value coding. Collectively, these findings support a key role for the human amygdala in the computations underlying the capacity for learning through observation.

Significance statement Single neuron studies of the human brain provide a unique window into the computational mechanisms of cognition. In this study, epilepsy patients implanted intracranially with depth microelectrodes performed an observational learning task. We measured activity bilaterally in the amygdala and found a representation for observational rewards as well as observational expected reward values. Additionally, the representation of self-experienced and observational values was performed by distinct subsets of amygdala neurons. This study thus provides a rare glimpse into the role of human amygdala neurons in social cognition.