From hunger to satiety: reconfiguration of a feeding network by Aplysia neuropeptide Y.
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.
Jing
Jian
J
Department of Neuroscience, Mount Sinai School of Medicine, New York, New York 10029, USA. Jian.Jing@mssm.edu
Vilim
Ferdinand S
FS
Horn
Charles C
CC
Alexeeva
Vera
V
Hatcher
Nathan G
NG
Sasaki
Kosei
K
Yashina
Irene
I
Zhurov
Yuriy
Y
Kupfermann
Irving
I
Sweedler
Jonathan V
JV
Weiss
Klaudiusz R
KR
D000818:Animals; D001048:Aplysia / Q000502:physiology*; D002610:Cheek / Q000502:physiology; D005247:Feeding Behavior / Q000502:physiology; D017952:Ganglia, Invertebrate / Q000378:metabolism; D006815:Hunger / Q000502:physiology*; D007150:Immunohistochemistry; D008297:Male; D009042:Motivation; D009474:Neurons / Q000378:metabolism; D009478:Neuropeptide Y / Q000378:metabolism* / Q000494:pharmacology; D051381:Rats; D017207:Rats, Sprague-Dawley; D012528:Satiety Response / Q000502:physiology*
D009478:Neuropeptide Y