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The Journal of Neuroscience, August 8, 2007, 27(32):8687-8698; doi:10.1523/JNEUROSCI.2045-07.2007

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Behavioral/Systems/Cognitive
Pallidal Neuron Activity Increases during Sensory Relay through Thalamus in a Songbird Circuit Essential for Learning

Abigail L. Person¹ and David J. Perkel²

¹Graduate Program in Neurobiology and Behavior and ²Departments of Biology and Otolaryngology, University of Washington, Seattle, Washington 98195

Correspondence should be addressed to Dr. David J. Perkel, Departments of Biology and Otolaryngology, University of Washington, 1959 Northeast Pacific Street, HSB BB1165, Box 356515, Seattle, WA 98195. Email: perkel{at}u.washington.edu

Disinhibition of the thalamus remains the primary model of information transfer between the basal ganglia and the cortex. Yet in apparent conflict with this model, the globus pallidus, a GABAergic basal ganglia output structure, often exhibits marked increases in firing rate during movement. To investigate the translation of pallidal activity and its relay through the thalamus, we explored a basal ganglia–thalamic pathway essential for song learning in songbirds. We found that single units in the thalamic nucleus DLM of urethane-anesthetized adult male zebra finches responded selectively to playback of the bird's own song, like neurons in its upstream and downstream nuclei. Because the pallidal input to these neurons forms giant calyx-like synapses, we were able to record extracellular signals from these presynaptic terminals as well. Pallidal units were distinctly excited by song playback, suggesting an increase in GABAergic transmission in the thalamus during sensory processing. However, this overall increased firing rate was phasic, punctuated by rapid decelerations in firing rate. In several cases, we were able to record presynaptic and postsynaptic units simultaneously. Correlating the presynaptic and postsynaptic activity, we found that disinhibition of thalamus may entail pallidal firing rate decelerations rather than simple long pauses in spontaneous activity, as has long been assumed.

Key words: thalamus; songbird; basal ganglia; pallidum; DLM; Area X

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Received Jan. 9, 2007; revised June 23, 2007; accepted June 26, 2007.

Correspondence should be addressed to Dr. David J. Perkel, Departments of Biology and Otolaryngology, University of Washington, 1959 Northeast Pacific Street, HSB BB1165, Box 356515, Seattle, WA 98195. Email: perkel{at}u.washington.edu

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