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The Journal of Neuroscience, March 28, 2007, 27(13):3490-3502; doi:10.1523/JNEUROSCI.0334-07.2007

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Behavioral/Systems/Cognitive
From Hunger to Satiety: Reconfiguration of a Feeding Network by Aplysia Neuropeptide Y

Jian Jing,¹ Ferdinand S. Vilim,¹ Charles C. Horn,^2,3 Vera Alexeeva,¹ Nathan G. Hatcher,⁴ Kosei Sasaki,¹ Irene Yashina,¹ Yuriy Zhurov,¹ Irving Kupfermann,³ Jonathan V. Sweedler,⁴ and Klaudiusz R. Weiss¹

¹Department of Neuroscience, Mount Sinai School of Medicine, New York, New York 10029, ²Monell Chemical Senses Center, Philadelphia, Pennsylvania 19104, ³Center for Neurobiology and Behavior, Columbia University, New York, New York 10032, and ⁴Department of Chemistry and the Beckman Institute, University of Illinois, Urbana, Illinois 61801

Correspondence should be addressed to Dr. Jian Jing, Department of Neuroscience, Mount Sinai School of Medicine, Box 1065, 1 Gustave Levy Place, New York, NY 10029. Email: Jian.Jing{at}mssm.edu

A shift in motivational state often produces behavioral change, but the underlying mechanisms are poorly understood. In the marine mollusc, Aplysia californica, feeding-induced transition from a hunger to satiation state leads to a slowdown and an eventual termination of feeding. Because the multifunctional feeding network generates both ingestion and the competing response, egestion, it is possible that the transition from a hunger to a satiety state is associated with network reconfiguration that results in production of fewer ingestive and more egestive responses. Chronic electrophysiological recordings in free-feeding Aplysia showed that as the meal progressed, food elicited fewer ingestive responses and simultaneously increased the number of egestive responses. Injections of Aplysia neuropeptide Y (apNPY) reduced food intake and slowed down the rate of ingestion. apNPY was localized to buccal-ganglion afferents originating in the gut-innervating esophageal nerve (EN), a nerve involved both in satiation and in the generation of egestive programs. During EN stimulation, apNPY was released in the feeding circuit. Importantly, stimulation of the cerebral-buccal interneuron-2, a command-like interneuron that is activated by food and normally elicits ingestive responses, elicited egestive responses in the presence of apNPY. This was accompanied by increased activity of the egestion-promoting interneuron B20 and decreased activity in the ingestion-promoting interneuron B40. Thus, apNPYergic reconfiguration of the feeding central pattern generator plays a role in the gradual transition from hunger to satiety states. More generally, changes in the motivational states may involve not only simple network inhibition but may also require network reconfiguration.

Key words: PYY; feeding; satiation; ingestion; egestion; motivational state

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Received Jan. 24, 2007; revised Feb. 21, 2007; accepted Feb. 23, 2007.

Correspondence should be addressed to Dr. Jian Jing, Department of Neuroscience, Mount Sinai School of Medicine, Box 1065, 1 Gustave Levy Place, New York, NY 10029. Email: Jian.Jing{at}mssm.edu

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