QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

HOME  |   SEARCH  |   ARCHIVE  |   SUBSCRIBE  |   CONTACT  |   HELP

The Journal of Neuroscience, September 21, 2005, 25(38):8794-8806; doi:10.1523/JNEUROSCI.2663-05.2005

This Article Full Text Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (21) Citing Articles via Google Scholar Google Scholar Articles by Beenhakker, M. P. Articles by Nusbaum, M. P. Search for Related Content PubMed PubMed Citation Articles by Beenhakker, M. P. Articles by Nusbaum, M. P.

 Previous Article  |  Next Article 

Behavioral/Systems/Cognitive
Proprioceptor Regulation of Motor Circuit Activity by Presynaptic Inhibition of a Modulatory Projection Neuron

Mark P. Beenhakker,^1 * Nicholas D. DeLong,^1 * Shari R. Saideman,¹ Farzan Nadim,² and Michael P. Nusbaum¹

¹Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104, and ²Department of Biological Sciences, Rutgers University, and Department of Mathematical Sciences, New Jersey Institute of Technology, Newark, New Jersey 07102

Phasically active sensory systems commonly influence rhythmic motor activity via synaptic actions on the relevant circuit and/or motor neurons. Using the crab stomatogastric nervous system (STNS), we identified a distinct synaptic action by which an identified proprioceptor, the gastropyloric muscle stretch receptor (GPR) neuron, regulates the gastric mill (chewing) motor rhythm. Previous work showed that rhythmically stimulating GPR in a gastric mill-like pattern, in the isolated STNS, elicits the gastric mill rhythm via its activation of two identified projection neurons, modulatory commissural neuron 1 (MCN1) and commissural projection neuron 2, in the commissural ganglia. Here, we determine how activation of GPR with a behaviorally appropriate pattern (active during each gastric mill retractor phase) influences an ongoing gastric mill rhythm via actions in the stomato gastric ganglion, where the gastric mill circuit is located. Stimulating GPR during each retractor phase selectively prolongs that phase and thereby slows the ongoing rhythm. This selective action on the retractor phase results from two distinct GPR actions. First, GPR presynaptically inhibits the axon terminals of MCN1, reducing MCN1 excitation of all gastric mill neurons. Second, GPR directly excites the retractor phase neurons. Because MCN1 transmitter release occurs during each retractor phase, these parallel GPR actions selectively reduce the buildup of excitatory drive to the protractor phase neurons, delaying each protractor burst. Thus, rhythmic proprioceptor feedback to a motor circuit can result from a global reduction in excitatory drive to that circuit, via presynaptic inhibition, coupled with a phase-specific excitatory input that prolongs the excited phase by delaying the onset of the subsequent phase.

Key words: central pattern generator; network; gastric mill circuit; stomatogastric; neuromodulation; sensorimotor

---

Received June 28, 2005; revised August 3, 2005; accepted August 5, 2005.

This article has been cited by other articles:

				U. B. S. Hedrich, C. R. Smarandache, and W. Stein Differential Activation of Projection Neurons by Two Sensory Pathways Contributes to Motor Pattern Selection J Neurophysiol, November 1, 2009; 102(5): 2866 - 2879. [Abstract] [Full Text] [PDF]

				N. D. DeLong, M. S. Kirby, D. M. Blitz, and M. P. Nusbaum Parallel Regulation of a Modulator-Activated Current via Distinct Dynamics Underlies Comodulation of Motor Circuit Output J. Neurosci., September 30, 2009; 29(39): 12355 - 12367. [Abstract] [Full Text] [PDF]

				V. Tohidi and F. Nadim Membrane Resonance in Bursting Pacemaker Neurons of an Oscillatory Network Is Correlated with Network Frequency J. Neurosci., May 20, 2009; 29(20): 6427 - 6435. [Abstract] [Full Text] [PDF]

				F. Nadim, V. Brezina, A. Destexhe, and C. Linster State Dependence of Network Output: Modeling and Experiments J. Neurosci., November 12, 2008; 28(46): 11806 - 11813. [Abstract] [Full Text] [PDF]

				D. M. Blitz and M. P. Nusbaum State-Dependent Presynaptic Inhibition Regulates Central Pattern Generator Feedback to Descending Inputs J. Neurosci., September 17, 2008; 28(38): 9564 - 9574. [Abstract] [Full Text] [PDF]

				G. Barriere, J. Simmers, and D. Combes Multiple Mechanisms for Integrating Proprioceptive Inputs That Converge on the Same Motor Pattern-Generating Network J. Neurosci., August 27, 2008; 28(35): 8810 - 8820. [Abstract] [Full Text] [PDF]

				K. J. Rehm, A. L. Taylor, S. R. Pulver, and E. Marder Spectral Analyses Reveal the Presence of Adult-Like Activity in the Embryonic Stomatogastric Motor Patterns of the Lobster, Homarus americanus J Neurophysiol, June 1, 2008; 99(6): 3104 - 3122. [Abstract] [Full Text] [PDF]

				M. P. Beenhakker, M. S. Kirby, and M. P. Nusbaum Mechanosensory Gating of Proprioceptor Input to Modulatory Projection Neurons J. Neurosci., December 26, 2007; 27(52): 14308 - 14316. [Abstract] [Full Text] [PDF]

				M. S. Kirby and M. P. Nusbaum Peptide Hormone Modulation of a Neuronally Modulated Motor Circuit J Neurophysiol, December 1, 2007; 98(6): 3206 - 3220. [Abstract] [Full Text] [PDF]

				S. R. Saideman, D. M. Blitz, and M. P. Nusbaum Convergent Motor Patterns from Divergent Circuits J. Neurosci., June 20, 2007; 27(25): 6664 - 6674. [Abstract] [Full Text] [PDF]

				S. R. Saideman, A. E. Christie, P. Torfs, J. Huybrechts, L. Schoofs, and M. P. Nusbaum Actions of kinin peptides in the stomatogastric ganglion of the crab Cancer borealis J. Exp. Biol., September 15, 2006; 209(18): 3664 - 3676. [Abstract] [Full Text] [PDF]

				J.-M. Goaillard and E. Marder Dynamic Clamp Analyses of Cardiac, Endocrine, and Neural Function Physiology, June 1, 2006; 21(3): 197 - 207. [Abstract] [Full Text] [PDF]

				C. P. Billimoria, R. A. DiCaprio, J. T. Birmingham, L. F. Abbott, and E. Marder Neuromodulation of spike-timing precision in sensory neurons. J. Neurosci., May 31, 2006; 26(22): 5910 - 5919. [Abstract] [Full Text] [PDF]

Home  |   Search  |   Archive  |   Subscribe  |   Contact  |   Help