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