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Inhibitory Network Interactions Shape the Auditory Processing of Natural Communication Signals in the Songbird Auditory Forebrain

¹Department of Brain and Cognitive Sciences, University of Rochester, Rochester, New York; ²Neurological Sciences Institute and ³Center for Research on Occupational and Environmental Toxicology, Oregon Health and Science University, Portland, Oregon; ⁴Department of Psychology, Rutgers University, Piscataway, New Jersey; ⁵Department of Physiology, Faculdade de Medicina de Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil; and ⁶Department of Biology, Sacred Heart University, Fairfield, Connecticut

Submitted 9 November 2007; accepted in final form 13 May 2008

The role of GABA in the central processing of complex auditory signals is not fully understood. We have studied the involvement of GABA_A-mediated inhibition in the processing of birdsong, a learned vocal communication signal requiring intact hearing for its development and maintenance. We focused on caudomedial nidopallium (NCM), an area analogous to parts of the mammalian auditory cortex with selective responses to birdsong. We present evidence that GABA_A-mediated inhibition plays a pronounced role in NCM's auditory processing of birdsong. Using immunocytochemistry, we show that approximately half of NCM's neurons are GABAergic. Whole cell patch-clamp recordings in a slice preparation demonstrate that, at rest, spontaneously active GABAergic synapses inhibit excitatory inputs onto NCM neurons via GABA_A receptors. Multi-electrode electrophysiological recordings in awake birds show that local blockade of GABA_A-mediated inhibition in NCM markedly affects the temporal pattern of song-evoked responses in NCM without modifications in frequency tuning. Surprisingly, this blockade increases the phasic and largely suppresses the tonic response component, reflecting dynamic relationships of inhibitory networks that could include disinhibition. Thus processing of learned natural communication sounds in songbirds, and possibly other vocal learners, may depend on complex interactions of inhibitory networks.

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