Multi-dimensional neural selectivity in the primate amygdala

Abstract

The amygdala contributes to multiple functions including attention allocation, sensory processing, decision-making, and the elaboration of emotional behaviors. The diversity of functions attributed to the amygdala is reflected in the response selectivity of its component neurons. Previous work claimed that subsets of neurons differentiate between broad categories of stimuli (e.g., objects vs. faces, rewards vs. punishment) while other subsets are narrowly specialized to respond to individual faces or facial features (e.g., eyes). Here we explored the extent to which the same neurons contribute to more than one neural subpopulation in a task that activated multiple functions of the amygdala. The subjects (Macaca Mulatta) watched videos depicting conspecifics or inanimate objects, and learned by trial and error to choose the individuals or objects associated with the highest rewards. We found that the same neurons responded selectively to two or more of the following task events or stimulus features: (1) alerting, task-related stimuli (fixation icon, video start, and video end), (2) reward magnitude, (3) stimulus categories (social vs. non-social), and (4) stimulus–unique features (faces, eyes). A disproportionate number of neurons showed selectivity for all of the examined stimulus features and task events. These results suggest that neurons that appear specialized and uniquely tuned to specific stimuli (e.g., face cells, eye cells) are likely to respond to multiple other types of stimuli or behavioral events, if/when these become behaviorally relevant in the context of a complex task. This multi-dimensional selectivity supports flexible, context-depending evaluation of inputs and decision-making based activating the same neural ensemble.

Significance statement The primate amygdala contains neurons tuned to stimuli of high behavioral significance such as reward and punishment, faces, eyes, etc. It has been assumed that these specialized responses emerge from domain-specific cortical inputs that are evaluated for affective significance in the amygdala. Here we show that in the context of a task that requires the joint activation of multiple functions of the amygdala, neurons show multi-dimensional response properties, i.e., instead of specialization for relatively narrow domains of stimuli, they respond to multiple types of stimuli and multiple task events. This finding adds to growing experimental and theoretical evidence that that the same neurons in the amygdala can serve, depending on the behavioral context, multiple functions.