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The Journal of Neuroscience, February 1, 2003, 23(3):1072

Respiratory and Telencephalic Modulation of Vocal Motor Neurons in the Zebra Finch

Christopher B. Sturdy¹, J. Martin Wild², and Richard Mooney¹

¹ Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710, and ² Division of Anatomy, Faculty of Medical and Health Sciences, University of Auckland, Auckland 92019, New Zealand

Birdsong, like speech, involves coordinated vocal and respiratory activity achieved under telencephalic control. The avian vocal organ, or syrinx, is innervated by motor neurons (MNs) in the tracheosyringeal part of the hypoglossal nucleus (XIIts) that receive their synaptic input from medullary respiratory areas and telencephalic song control areas. Despite the importance of XIIts MNs to learned vocalizations, little is known about their intrinsic electrical properties or their synaptic inputs. Therefore, we made in vitro and in vivo intracellular recordings from XIIts MNs in adult male zebra finches to characterize their intrinsic properties and their synaptic modulation by respiratory and telencephalic areas. In vitro, electrical stimulation of ipsilateral or contralateral medullary respiratory areas (RAm) routinely evoked glycine receptor-mediated inhibition in XIIts. With inhibition blocked, similar stimulation evoked excitatory synaptic responses capable of driving sustained MN firing that was mediated partly by NMDA receptors. These inhibitory and excitatory inputs likely arise from RAm neurons, because chemical or electrical stimulation of RAm evoked similar responses in XIIts. In vivo, XIIts MNs displayed rhythmical, expiratory-related activity. EPSPs were pronounced at expiratory onset, but IPSPs were not apparent during inspiration, although XIIts MN firing was suppressed. However, hyperpolarizations as well as excitation were evoked by playback of the bird's own song, a stimulus that potently excites the telencephalic song nucleus that innervates XIIts. These findings illuminate functional properties of the songbird's brainstem circuitry and its specific activation by telencephalic inputs, which could coordinate vocal and respiratory activity during singing.

Key words: XIIts; RAm; birdsong; vocal learning; respiration; RA

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Copyright © 2003 Society for Neuroscience  0270-6474/03/2331072-15$05.00/0

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