From Hunger to Satiety: Reconfiguration of a Feeding Network byAplysiaNeuropeptide Y

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.

Functional Characterization of a Vesicular Glutamate Transporter in an Interneuron That Makes Excitatory and Inhibitory Synaptic Connections in a Molluscan Neural Circuit

“…Immunocytochemistry (whole mount) was performed as described previously (Furukawa et al, 2001;Jing et al, 2007). Central ganglia were fixed in 4% paraformaldehyde, 0.2% picric acid, 25% sucrose, and 0.1 M NaH 2 PO 4 , pH7.6, for either 3 h at room temperature or overnight at 4°C.…”

“…The Aplysia feeding circuit generates a rhythmic pattern of repetitive protraction-retraction sequences Jing et al, 2009), with protraction initiated first followed by retraction. Previous work has shown that many critical neurons that play important roles in the generation of protraction are cholinergic.…”

Why is the neurobiology of nausea and vomiting so important?

“…It will be important to distinguish brainstem systems for respiration, cardiovascular control, and swallowing from those involved in nausea and vomiting. Studies in invertebrate systems reveal overlapping neural architecture that simply switches between "behavioral states" (e.g., rejection and ingestion responses in the marine snail Aplysia, Jing et al, 2007) and this also seems operative in mammals (e.g., the role of the respiratory network in the emetic response: Fukuda et al, 2003). The sensory pathways for nausea and vomiting are generally well understood (e.g., vagal and vestibular inputs) but the pivotal problem of defining the convergent neural circuitry that generates nausea and vomiting is still largely unsolved.…”

Genetic analysis of crawling and swimming locomotory patterns in C. elegans

“…D ifferent forms of rhythmic neural output are ubiquitously observed in motor behaviors such as locomotion, respiration, and feeding (1)(2)(3)(4). Extensive research has revealed that a neural network can switch among alternate rhythms by altering the properties of specific intrinsic membrane currents and synapses (5).…”