Multisensory Neurons in the Primate Amygdala

Abstract

Animals identify, interpret, and respond to complex, natural signals that are often multisensory. The ability to integrate signals across sensory modalities depends on the convergence of sensory inputs at the level of single neurons. Neurons in the amygdala are expected to be multisensory because they respond to complex, natural stimuli, and the amygdala receives inputs from multiple sensory areas. We recorded activity from the amygdala of 2 male monkeys (Macaca mulatta) in response to visual, tactile, and auditory stimuli. Although the stimuli were devoid of inherent emotional or social significance and were not paired with rewards or punishments, the majority of neurons that responded to these stimuli were multisensory. Selectivity for sensory modality was stronger and emerged earlier than selectivity for individual items within a sensory modality. Modality and item selectivity were expressed via three main spike-train metrics: (1) response magnitude, (2) response polarity, and (3) response duration. None of these metrics were unique to a particular sensory modality; rather, each neuron responded with distinct combinations of spike-train metrics to discriminate sensory modalities and items within a modality. The relative proportion of multisensory neurons was similar across the nuclei of the amygdala. The convergence of inputs of multiple sensory modalities at the level of single neurons in the amygdala rests at the foundation for multisensory integration. The integration of visual, auditory, and tactile inputs in the amygdala may serve social communication by binding together social signals carried by facial expressions, vocalizations, and social grooming. SIGNIFICANCE STATEMENT Our brain continuously decodes information detected by multiple sensory systems. The emotional and social significance of the incoming signals is likely extracted by the amygdala, which receives input from all sensory domains. Here we show that a large portion of neurons in the amygdala respond to stimuli from two or more sensory modalities. The convergence of visual, tactile, and auditory signals at the level of individual neurons in the amygdala establishes a foundation for multisensory integration within this structure. The ability to integrate signals across sensory modalities is critical for social communication and other high-level cognitive functions.