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Cholinergic suppression: A postsynaptic mechanism of long-term associative learning

Morielli, Anthony D. and Matera, Eugene M. and Kovac, Mark P. and Shrum, Richard G. and McCormack, Kenneth J. and Davis, W. Jackson (1986) Cholinergic suppression: A postsynaptic mechanism of long-term associative learning. Proceedings of the National Academy of Sciences of the United States of America, 83 (12). pp. 4556-4560. ISSN 0027-8424. http://resolver.caltech.edu/CaltechAUTHORS:MORpnas86

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Abstract

Food avoidance learning in the mollusc Pleurobranchaea entails reduction in the responsiveness of key brain interneurons in the feeding neural circuitry, the paracerebral feeding command interneurons (PCNs), to the neurotransmitter acetylcholine (AcCho). Food stimuli applied to the oral veil of an untrained animal depolarize the PCNs and induce the feeding motor program (FMP). Atropine (a muscarinic cholinergic antagonist) reversibly blocks the food-induced depolarization of the PCNs, implicating AcCho as the neurotransmitter mediating food detection. AcCho applied directly to PCN somata depolarizes them, indicating that the PCN soma membrane contains AcCho receptors and induces the FMP in the isolated central nervous system preparation. The AcCho response of the PCNs is mediated by muscariniclike receptors, since comparable depolarization is induced by muscarinic agonists (acetyl-ß -methylcholine, oxotremorine, pilocarpine), but not nicotine, and blocked by muscarinic antagonists (atropine, trifluoperazine). The nicotinic antagonist hexamethonium, however, blocked the AcCho response in four of six cases. When specimens are trained to suppress feeding behavior using a conventional food-avoidance learning paradigm (conditionally paired food and shock), AcCho applied to PCNs in the same concentration as in untrained animals causes little or no depolarization and does not initiate the FMP. Increasing the concentration of AcCho 10-100 times, however, induces weak PCN depolarization in trained specimens, indicating that learning diminishes but does not fully abolish AcCho responsiveness of the PCNs. This study proposes a cellular mechanism of long-term associative learning -- namely, postsynaptic modulation of neurotransmitter responsiveness in central neurons that could apply also to mammalian species.


Item Type:Article
Additional Information:© 1986 by the National Academy of Sciences. Communicated by Kenneth V. Thimann, December 23, 1985. We are indebted to Dr. Francoise Dubas for technical assistance and to Ms. Tracy Karrer and Mr. Paul Volk for reading and criticizing the manuscript. This research was supported by National Institutes of Health Research Grant NS09050 and Department of Defense University Equipment Grant DAAG29-83-G-0071 to W.J.D. The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Subject Keywords:acetylcholine; food avoidance learning; muscarinic; gastropod
Record Number:CaltechAUTHORS:MORpnas86
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:MORpnas86
Alternative URL:http://www.pnas.org/cgi/content/abstract/83/12/4556
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:9270
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:05 Dec 2007
Last Modified:26 Dec 2012 09:47

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