Linear and nonlinear auditory response properties of interneurons in a high-order avian vocal motor nucleus during wakefulness.

Motor-related forebrain areas in higher vertebrates also show responses to passively presented sensory stimuli. However, sensory tuning properties in these areas, especially during wakefulness, and their relation to perception, are poorly understood. In the avian song system, HVC (proper name) is a vocal-motor structure with auditory responses well defined under anesthesia but poorly characterized during wakefulness. We used a large set of stimuli including the bird's own song (BOS) and many conspecific songs (CON) to characterize auditory tuning properties in putative interneurons (HVC(IN)) during wakefulness. Our findings suggest that HVC contains a diversity of responses that vary in overall excitability to auditory stimuli, as well as bias in spike rate increases to BOS over CON. We used statistical tests to classify cells in order to further probe auditory responses, yielding one-third of neurons that were either unresponsive or suppressed and two-thirds with excitatory responses to one or more stimuli. A subset of excitatory neurons were tuned exclusively to BOS and showed very low linearity as measured by spectrotemporal receptive field analysis (STRF). The remaining excitatory neurons responded well to CON stimuli, although many cells still expressed a bias toward BOS. These findings suggest the concurrent presence of a nonlinear and a linear component to responses in HVC, even within the same neuron. These characteristics are consistent with perceptual deficits in distinguishing BOS from CON stimuli following lesions of HVC and other song nuclei and suggest mirror neuronlike qualities in which "self" (here BOS) is used as a referent to judge "other" (here CON).

Sensorimotor nucleus NIf is necessary for auditory processing but not vocal motor output in the avian song system.

Sensorimotor integration in the avian song system is crucial for both learning and maintenance of song, a vocal motor behavior. Although a number of song system areas demonstrate both sensory and motor characteristics, their exact roles in auditory and premotor processing are unclear. In particular, it is unknown whether input from the forebrain nucleus interface of the nidopallium (NIf), which exhibits both sensory and premotor activity, is necessary for both auditory and premotor processing in its target, HVC. Here we show that bilateral NIf lesions result in long-term loss of HVC auditory activity but do not impair song production. NIf is thus a major source of auditory input to HVC, but an intact NIf is not necessary for motor output in adult zebra finches.