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The Journal of Neuroscience, March 15, 1999, 19(6):2368-2380

Concurrent Inhibition and Excitation of Phrenic Motoneurons during Inspiration: Phase-Specific Control of Excitability

M. A. Parkis¹, X.-W. Dong², J. L. Feldman³, and G. D. Funk¹

¹ Department of Physiology, Faculty of Medicine and Health Sciences, University of Auckland, Auckland, New Zealand, ² Schering-Plow Research Institute, CNS/CV Research, Kenilworth, New Jersey 07033, and ³ Systems Neurobiology Laboratory, Departments of Neurobiology and Physiological Science, University of California Los Angeles, Los Angeles, California 90095-1763

The movements that define behavior are controlled by motoneuron output, which depends on the excitability of motoneurons and the synaptic inputs they receive. Modulation of motoneuron excitability takes place over many time scales. To determine whether motoneuron excitability is specifically modulated during the active versus the quiescent phase of rhythmic behavior, we compared the input-output properties of phrenic motoneurons (PMNs) during inspiratory and expiratory phases of respiration.

In neonatal rat brainstem-spinal cord preparations that generate rhythmic respiratory motor outflow, we blocked excitatory inspiratory synaptic drive to PMNs and then examined their phase-dependent responses to superthreshold current pulses. Pulses during inspiration elicited fewer action potentials compared with identical pulses during expiration. This reduced excitability arose from an inspiratory-phase inhibitory input that hyperpolarized PMNs in the absence of excitatory inspiratory inputs. Local application of bicuculline blocked this inhibition as well as the difference between inspiratory and expiratory firing. Correspondingly, bicuculline locally applied to the midcervical spinal cord enhanced fourth cervical nerve (C4) inspiratory burst amplitude. Strychnine had no effect on C4 output. Nicotinic receptor antagonists neither potentiated C4 output nor blocked its potentiation by bicuculline, further indicating that the inhibition is not from recurrent inhibitory pathways. We conclude that it is bulbospinal in origin.

These data demonstrate that rapid changes in motoneuron excitability occur during behavior and suggest that integration of overlapping, opposing synaptic inputs to motoneurons is important in controlling motor outflow. Modulation of phasic inhibition may represent a means for regulating the transfer function of PMNs to suit behavioral demands.

Key words: phrenic motoneuron; brainstem; spinal cord; respiration; GABA; neonatal rat

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Copyright © 1999 Society for Neuroscience  0270-6474/99/1962368-13$05.00/0

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