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J Neurophysiol 84: 1186-1193, 2000;
0022-3077/00 $5.00
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The Journal of Neurophysiology Vol. 84 No. 3 September 2000, pp. 1186-1193
Copyright ©2000 by the American Physiological Society

Intrinsic and Extrinsic Modulation of a Single Central Pattern Generating Circuit

Peter T. Morgan,1 Ray Perrins,2 Philip E. Lloyd,3 and Klaudiusz R. Weiss1

 1Department of Physiology and Biophysics, Mount Sinai School of Medicine, New York, New York 10029;  2Department of Biological Science, University of Bristol, Bristol, Avon BS8 1U9, United Kingdom; and  3Committee on Neurobiology and Department of Pharmacological Sciences, University of Chicago, Chicago, Illinois 60637

Morgan, Peter T., Ray Perrins, Philip E. Lloyd, and Klaudiusz R. Weiss. Intrinsic and Extrinsic Modulation of a Single Central Pattern Generating Circuit. J. Neurophysiol. 84: 1186-1193, 2000. Intrinsic and extrinsic neuromodulation are both thought to be responsible for the flexibility of the neural circuits (central pattern generators) that control rhythmic behaviors. Because the two forms of modulation have been studied in different circuits, it has been difficult to compare them directly. We find that the central pattern generator for biting in Aplysia is modulated both extrinsically and intrinsically. Both forms of modulation increase the frequency of motor programs and shorten the duration of the protraction phase. Extrinsic modulation is mediated by the serotonergic metacerebral cell (MCC) neurons and is mimicked by application of serotonin. Intrinsic modulation is mediated by the cerebral peptide-2 (CP-2) containing CBI-2 interneurons and is mimicked by application of CP-2. Since the effects of CBI-2 and CP-2 occlude each other, the modulatory actions of CBI-2 may be mediated by CP-2 release. Although the effects of intrinsic and extrinsic modulation are similar, the neurons that mediate them are active predominantly at different times, suggesting a specialized role for each system. Metacerebral cell (MCC) activity predominates in the preparatory (appetitive) phase and thus precedes the activation of CBI-2 and biting motor programs. Once the CBI-2s are activated and the biting motor program is initiated, MCC activity declines precipitously. Hence extrinsic modulation prefacilitates biting, whereas intrinsic modulation occurs during biting. Since biting inhibits appetitive behavior, intrinsic modulation cannot be used to prefacilitate biting in the appetitive phase. Thus the sequential use of extrinsic and intrinsic modulation may provide a means for premodulation of biting without the concomitant disruption of appetitive behaviors.




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