Brain mechanisms for communication must establish a correspondence between sensory and motor codes used to represent the signal. One idea is that this correspondence is established at the level of single neurons that are active when the individual performs a particular gesture or observes a similar gesture performed by another individual. Although neurons that display a precise auditory-vocal correspondence could facilitate vocal communication, they have yet to be identified. Here we report that a certain class of neurons in the swamp sparrow forebrain displays a precise auditory-vocal correspondence. We show that these neurons respond in a temporally precise fashion to auditory presentation of certain note sequences in this songbird's repertoire and to similar note sequences in other birds' songs. These neurons display nearly identical patterns of activity when the bird sings the same sequence, and disrupting auditory feedback does not alter this singing-related activity, indicating it is motor in nature. Furthermore, these neurons innervate striatal structures important for song learning, raising the possibility that singing-related activity in these cells is compared to auditory feedback to guide vocal learning.

Synaptic interactions between telencephalic neurons innervating descending motor or basal ganglia pathways are essential in the learning, planning, and execution of complex movements. Synaptic interactions within the songbird telencephalic nucleus HVC are implicated in motor and auditory activity associated with learned vocalizations. HVC contains projection neurons (PNs) (HVC RA ) that innervate song premotor areas, other PNs (HVC X ) that innervate a basal ganglia pathway necessary for vocal plasticity, and interneurons (HVC INT ). During singing, HVC RA fire in temporally sparse bursts, possibly because of HVC INT -HVC RA interactions, and a corollary discharge can be detected in the basal ganglia pathway, likely because of synaptic transmission from HVC RA to HVC X cells. During song playback, local interactions, including inhibition onto HVC X cells, shape highly selective responses that distinguish HVC from its auditory afferents. To better understand the synaptic substrate for the motor and auditory properties of HVC, we made intracellular recordings from pairs of HVC neurons in adult male zebra finch brain slices and used spike-triggered averages to assess synaptic connectivity. A major synaptic interaction between the PNs was a disynaptic inhibition from HVC RA to HVC X , which could link song motor signals in the two outputs of HVC and account for some of the song playback-evoked inhibition in HVC X cells. Furthermore, single interneurons made divergent connections onto PNs of both types, and either PN type could form reciprocal connections with interneurons. In these two regards, the synaptic architecture of HVC resembles that described in some pattern-generating networks, underscoring features likely to be important to singing and song learning.

The division of continuously variable acoustic signals into discrete perceptual categories is a fundamental feature of vocal communication, including human speech. Despite the importance of categorical perception to learned vocal communication, the neural correlates underlying this phenomenon await identification. Here we report that individual sensorimotor neurons in freely behaving swamp sparrows express categorical auditory responses to changes in note duration, a learned feature of their songs, and that the neural response boundary accurately predicts the categorical perceptual boundary measured in field studies of the same sparrow population. Furthermore, swamp sparrow populations that learn different song dialects exhibit different categorical perceptual boundaries, consistent with the boundary being learned. Our results extend the analysis of the neural basis of perceptual categorization into the realm of vocal communication, while advancing the learned vocalizations of songbirds as a model for investigating how experience shapes categorical perception and the activity of categorically responsive neurons.