Precise auditory–vocal mirroring in neurons for learned vocal communication

Abstract

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.

Neural Coding of Syntactic Structure in Learned Vocalizations in the Songbird

“…2C). Because previous studies have demonstrated that singing-related activity in HVC X neurons transmits motor-related information (Hahnloser et al, 2002;Kozhevnikov and Fee, 2007;Prather et al, 2008) and precedes the vocal events by approximately several tens of milliseconds (Kozhevnikov and Fee, 2007), the relative latencies were defined as follows: when a burst was observed during a silent period between syllables, the relative latency was measured from the onset of the target syllable just preceded by the silent period to the onset of the burst (Fig. 2C, blue tick marks); if a burst was generated while vocalizing the target syllable, the relative latency was measured from the onset of the target syllable to the onset of the burst (Fig.…”

“…Information processed in HVC is transmitted by two segregated types of projection neurons (Dutar et al, 1998;Mooney, 2000): HVC RA neurons that project to the robust nucleus of the arcopallium (RA), which relay the information to motor neurons for vocal organs (Nottebohm et al, 1976); and HVC X neurons, which innervate to basal ganglia area X (Nottebohm et al, 1982) and are involved in audition-dependent vocal plasticity (Scharff and Nottebohm, 1991;Brainard and Doupe, 2000). Both types of projection neurons generate sparse burst spikes during singing (Hahnloser et al, 2002;Kozhevnikov and Fee, 2007;Prather et al, 2008). In the awake nonsinging state, however, HVC RA neurons are completely inactive (Hahnloser et al, 2002;Kozhevnikov and Fee, 2007;Prather et al, 2008).…”

“…Both types of projection neurons generate sparse burst spikes during singing (Hahnloser et al, 2002;Kozhevnikov and Fee, 2007;Prather et al, 2008). In the awake nonsinging state, however, HVC RA neurons are completely inactive (Hahnloser et al, 2002;Kozhevnikov and Fee, 2007;Prather et al, 2008). In contrast, a subpopulation of HVC X neurons exhibits both motor-related activity and auditory re-sponse to the individual bird's own song (BOS) playback and similar songs of other birds .…”

Failure of operant control of vocal learning in budgerigars

“…Work on songbirds revealed some neurons are activated by both singing and hearing the same part of song (Prather, Peters, Nowicki, & Mooney, 2008) suggesting the existence of mirror (or mirror-like) neurons in a part of the song nervous system (i.e., HVC parallel of NLC: Jarvis, 2006). Perhaps both auditory processing and vocal motor control mechanisms involving calls are shared also in budgerigars.…”

Sensorimotor learning and the ontogeny of the mirror neuron system

“…These intriguing neurons have been recorded in ventral premotor area F5 [52] and inferior parietal lobule (IPL) area PFG [25] in the macaque. Mirror neurons responsive to both the production and perception of song have also been found in the forebrain of the swamp sparrow [54]. Direct recordings in humans are limited, but a recent study found mirror neurons in a wide range of brain areas including supplementary motor area (SMA) and parts of the medial temporal lobe [49].…”