Selective Neural Responses to Conspecific Vocalizations in Marmoset Area 32

Abstract

Understanding how primate frontal circuits encode socially informative vocalizations is central to elucidating the neural basis of communication. In common marmosets, functional MRI has identified robust selectivity for conspecific vocalizations in the pregenual anterior cingulate cortex (pgACC; area 32), but the underlying neural dynamics driving this response remain unknown. Here, we investigated this by recording single-neuron activity in area 32 of five awake marmosets (three female and two male) using acute and chronic Neuropixels probes and Utah microelectrode arrays during presentation of a standardized cross-species auditory stimulus set comprising marmoset, macaque, and human vocalizations as well as a suite of nonvocal sounds. Of 1,713 neurons recorded across 17 sessions, 945 (55%) showed significant auditory responsiveness, and 362 (21%) were categorically selective. Selective neurons exhibited their strongest responses to marmoset calls, and population preference indices revealed a robust bias toward conspecific vocalizations. Temporal population analyses showed rapid encoding: decoding accuracy for detection of marmoset calls exceeded chance within ∼50–100 ms, and representational similarity analysis demonstrated that marmoset calls formed a distinct cluster separate from macaque, human, and nonvocal stimuli. These results provide the first direct evidence that ACC area 32 contains a specialized neural representation for conspecific vocal signals. By linking fMRI-defined selectivity to single-neuron population dynamics, our findings identify area 32 as a key node in primate vocal communication networks and illuminate how frontal circuits transform auditory input into socially meaningful categorical information.