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The Journal of Neuroscience, February 23, 2005, 25(8):1952-1964; doi:10.1523/JNEUROSCI.3726-04.2005

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Behavioral/Systems/Cognitive
The HVC Microcircuit: The Synaptic Basis for Interactions between Song Motor and Vocal Plasticity Pathways

Richard Mooney and Jonathan F. Prather

Department of Neurobiology, Duke University School of Medicine, Durham, North Carolina 27710

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.

Key words: HVC; in vitro intracellular; paired recordings; zebra finch; songbird; GABA_A; picrotoxin; unitary synaptic coupling

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Received Sep 8, 2004; revised January 7, 2005; accepted January 8, 2005.

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