Control of feeding motor output by paracerebral neurons in brain of Pleurobranchaea california

Rhanor Gillette, M. P. Kovac, W. J. Davis

Research output: Contribution to journalArticle

Abstract

1. A population of interneurons that control feeding behavior in the mollusk Pleurobranchaea has been analyzed by dye injection and intracellular stimulation/recording in whole animals and reduced preparations. The population consists of 12-16 somata distributed in two bilaterally systemetrical groups on the anterior edge of the cerebropleural ganglion (brain). On the basis of their position adjacent to the cerebral lobes, these cells have been named paracerebral neurons (PCNs). This study concerns one subset of PCNs, the large, phasic ones, which have the strongest effect on the feeding rhythm (21). 2. Each PCN sends a descending axon via the ipsilateral cerebrobuccal connective to the buccal ganglion. Axon branches have not been detected in other brain or buccal nerves and hence the PCNs appear to be interneurons. 3. In whole-animal preparations, tonic intracellular depolarization of the PCNs causes them to discharge cyclic bursts of action potentials interrupted by a characteristic hyperpolarization. In all specimens that exhibit feeding behavior, the interburst hyperpolarization is invariably accompanied by radula closure and the beginning of proboscis retraction (the ite. No other behavioral effect of PCN stimulation has been observed. 4. In whole-animal preparations, the PCNs are excisted by food and tactile stimulation of the oral veil, rhinophores, and tentacles. When such stimuli induce feeding the PCNs discharge in the same bursting pattern seen during tonic PCN depolarization, with the cyclic interburst hyperpolarization phase locked to the bite. When specimens egest an unpalatable object by cyclic buccal movements, however, the PCNs are silent. The PCNs therefore exhibit properties expected of behaviorally specific ommandneurons for feeding. 5. Silencing one or two PCNs by hyperpolarization may weaken but does not prevent feeding induced by natural food stimuli. Single PCNs therefore can be sufficient but are not necessary to induction of feeding behavior. Instead the PCNs presumably operate as a population to control feeding. 6. Isolated nervous system preparations tonic extracellular stimulation of the stomatogastric nerve of the buccal ganglion elicits a cyclic motor rhythm that is similar in general features to the PCN-induced motor rhythm. Bursts of PCN action potentials intercalated at the normal phase position in this cycle intensify the buccal rhythm. Bursts of PCN impulses intercalated at abnormal phase positions reset the buccal rhythm. The PCNs, therefore, also exhibit properties expected of pattern-generator elements and/or coordinating neurons for the buccal rhythm. 7. The PCNs are recruited into activity when the buccal motor rhythm is elicited by stomatogastric nerve stimulation or stimulation of the reidentifiable ventral white cell. The functional synergy between the PCNs and the buccal rhythm is therefore reciprocal. 8. The PCNs form both short and constant latency and long and variable latency synaptic connections with interneurons in the buccal ganglion, which also command motor output. The PCNs also exhibit reciprocal, short and constant latency excitatory connections with coordinating (corollary discharge) interneurons in the buccal ganglion. In addition, the PCNs make excitatory and inhibitory connections with buccal motor neurons. Single PCNs both excite and inhibit different follower motor neurons. 9. It is concluded that the PCNs represent central nervous elements of a reciprocal positive feedback network that controls feeding behavior in pleurobranchaea. The PCNs exert their control by means of synaptic connections with a population of recurrent, oscillatory inhibitory neurons and with identifiable buccal interneurons and motor neurons.

Original languageEnglish (US)
Pages (from-to)885-908
Number of pages24
JournalJournal of neurophysiology
Volume47
Issue number5
DOIs
StatePublished - Jan 1 1982

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Pleurobranchaea
Neurons
Cheek
Brain
Interneurons
Ganglia
Motor Neurons
Feeding Behavior
Population Control

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

Cite this

Control of feeding motor output by paracerebral neurons in brain of Pleurobranchaea california. / Gillette, Rhanor; Kovac, M. P.; Davis, W. J.

In: Journal of neurophysiology, Vol. 47, No. 5, 01.01.1982, p. 885-908.

Research output: Contribution to journalArticle

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N2 - 1. A population of interneurons that control feeding behavior in the mollusk Pleurobranchaea has been analyzed by dye injection and intracellular stimulation/recording in whole animals and reduced preparations. The population consists of 12-16 somata distributed in two bilaterally systemetrical groups on the anterior edge of the cerebropleural ganglion (brain). On the basis of their position adjacent to the cerebral lobes, these cells have been named paracerebral neurons (PCNs). This study concerns one subset of PCNs, the large, phasic ones, which have the strongest effect on the feeding rhythm (21). 2. Each PCN sends a descending axon via the ipsilateral cerebrobuccal connective to the buccal ganglion. Axon branches have not been detected in other brain or buccal nerves and hence the PCNs appear to be interneurons. 3. In whole-animal preparations, tonic intracellular depolarization of the PCNs causes them to discharge cyclic bursts of action potentials interrupted by a characteristic hyperpolarization. In all specimens that exhibit feeding behavior, the interburst hyperpolarization is invariably accompanied by radula closure and the beginning of proboscis retraction (the ite. No other behavioral effect of PCN stimulation has been observed. 4. In whole-animal preparations, the PCNs are excisted by food and tactile stimulation of the oral veil, rhinophores, and tentacles. When such stimuli induce feeding the PCNs discharge in the same bursting pattern seen during tonic PCN depolarization, with the cyclic interburst hyperpolarization phase locked to the bite. When specimens egest an unpalatable object by cyclic buccal movements, however, the PCNs are silent. The PCNs therefore exhibit properties expected of behaviorally specific ommandneurons for feeding. 5. Silencing one or two PCNs by hyperpolarization may weaken but does not prevent feeding induced by natural food stimuli. Single PCNs therefore can be sufficient but are not necessary to induction of feeding behavior. Instead the PCNs presumably operate as a population to control feeding. 6. Isolated nervous system preparations tonic extracellular stimulation of the stomatogastric nerve of the buccal ganglion elicits a cyclic motor rhythm that is similar in general features to the PCN-induced motor rhythm. Bursts of PCN action potentials intercalated at the normal phase position in this cycle intensify the buccal rhythm. Bursts of PCN impulses intercalated at abnormal phase positions reset the buccal rhythm. The PCNs, therefore, also exhibit properties expected of pattern-generator elements and/or coordinating neurons for the buccal rhythm. 7. The PCNs are recruited into activity when the buccal motor rhythm is elicited by stomatogastric nerve stimulation or stimulation of the reidentifiable ventral white cell. The functional synergy between the PCNs and the buccal rhythm is therefore reciprocal. 8. The PCNs form both short and constant latency and long and variable latency synaptic connections with interneurons in the buccal ganglion, which also command motor output. The PCNs also exhibit reciprocal, short and constant latency excitatory connections with coordinating (corollary discharge) interneurons in the buccal ganglion. In addition, the PCNs make excitatory and inhibitory connections with buccal motor neurons. Single PCNs both excite and inhibit different follower motor neurons. 9. It is concluded that the PCNs represent central nervous elements of a reciprocal positive feedback network that controls feeding behavior in pleurobranchaea. The PCNs exert their control by means of synaptic connections with a population of recurrent, oscillatory inhibitory neurons and with identifiable buccal interneurons and motor neurons.

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