Representation of conspecific vocalizations in amygdala of awake marmosets

Abstract

Human speech and animal vocalizations are important for social communication and animal survival. Neurons in the auditory pathway are responsive to a range of sounds, from elementary sound features to complex objects such as voices. For social communication, the responses to distinct patterns of vocalization are usually highly specific to an individual conspecific call in some species, including the specificity of sound patterns and embedded biological information. To address this question, we conducted single-unit recordings in the amygdala of awake marmosets and presented calls used in marmoset communication, calls of other species and specific marmoset individuals. We found that some neurons (47/262) in the amygdala distinguished ‘Phee’ calls from vocalizations of other animals and other types of marmoset vocalizations. Interestingly, a subset of Phee-responsive neurons (22/47) also exhibited selectivity to one out of the three Phees from two different ‘caller’ marmosets. Our findings suggest that, while it has traditionally been considered as the key structure in the limbic system, the amygdala also represents a critical stage of socially relevant auditory perceptual processing.

Neural activity for complex sounds in the marmoset medial prefrontal cortex

“…Independent lines of evidence have associated the amydala with the regulation of emotional processes such as anxiety 11 21 , modulation of social behaviors such as grooming 22 , and cognitive processes including reward processing 23 . Recently, vocalization-related activity has been identified in the marmoset BLA and BMA 24 . Based on this, an intriguing possibility is that area 32 is a site of convergence of such signals with incoming auditory stimuli, and indeed this would be consonant with the role of this area in emotional communication proposed previously 18,25 .…”

Editorial of non-human primate research

“…In addition to the cortices, subcortical areas are likely to play an important role in processing emotional aspects of vocalization. By recording single neuron activities in awake marmosets, Lixia Gao, Xinjian Li and colleagues reported in this issue [ 4 ] that many neurons in the amygdala, a subcortical nucleus known to be involved in processing emotion, could respond selectively to calls made by the same marmoset species as well as calls by specific individual marmosets. These findings point to the amygdala as an area involved in socially relevant perceptual processing of call signals.…”