From hunger to satiety: Reconfiguration of a feeding network by Aplysia neuropeptide Y

Jian Jing, Ferdinand S. Vilim, Charles C. Horn, Vera Alexeeva, Nathan G. Hatcher, Kosei Sasaki, Irene Yashina, Yuriy Zhurov, Irving Kupfermann, Jonathan V. Sweedler, Klaudiusz R. Weiss

Research output: Contribution to journalArticlepeer-review

Abstract

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.

Original languageEnglish (US)
Pages (from-to)3490-3502
Number of pages13
JournalJournal of Neuroscience
Volume27
Issue number13
DOIs
StatePublished - Mar 28 2007

Keywords

  • Egestion
  • Feeding
  • Ingestion
  • Motivational state
  • PYY
  • Satiation

ASJC Scopus subject areas

  • Neuroscience(all)

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