Phase-Locked Coordination Between Two Rhythmically Active Feeding Structures in the Mollusk<i>Clione limacina</i>. I. Motor Neurons

Malyshev, A. Yu.; Norekian, Tigran P.

doi:10.1152/jn.2002.87.6.2996

Cited by 12 publications

(15 citation statements)

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“…As a consequence of their high feeding specialization, Clione and other mollusks from the order Gymnosomata have a unique feeding structure -chitinous hooks, whose functional role is to grab the soft body of Limacina, and pull it out of its shell and into their buccal cavity. We have shown in a previous study that the rhythmic movements of radula and hooks are highly coordinated in a phasedependent manner (Malyshev and Norekian, 2002). This phasedependent coordination was observed at a behavioral level and was always recorded at the motoneuronal level during spontaneous and induced rhythmic activity.…”

Section: Introductionmentioning

confidence: 76%

“…This phasedependent coordination was observed at a behavioral level and was always recorded at the motoneuronal level during spontaneous and induced rhythmic activity. Hook protractor neurons were active in the same phase as radula retractor neurons, whereas hook retractor neurons burst in phase with radula protractor neurons (Malyshev and Norekian, 2002).…”

Section: Introductionmentioning

confidence: 94%

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Buccal neurons activate ciliary beating in the foregut of the pteropod molluskClione limacina

Malyshev

Balaban

2009

Journal of Experimental Biology

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SUMMARYBeating of cilia lining the foregut of gastropods facilitates the swallowing of food and, therefore, plays a role in feeding behavior. Despite the fact that neural control of feeding is well studied in mollusks, no neurons controlling ciliary beating in the foregut have been identified to date. Here we describe for the first time a pair of buccal neurons innervating the foregut of Clione. Intracellular stimulation of these neurons induced vigorous activation of cilia lining the foregut in a semi-intact preparation. Using immunochemistry labeling, buccal foregut cells were found to contain peptides similar to CNP neuropeptides of the terrestrial snail Helix lucorum. Application of DYPRL-amide, a member of the Helix CNP peptide family, mimicked the effect of buccal foregut cell stimulation on ciliary activity. Induction of fictive feeding in an isolated CNS preparation resulted in the activation of buccal foregut cells suggesting that these cells control ciliary beating in the foregut during feeding. Thus, cilia-activating buccal neurons may represent a new intrinsic element of the neural control of feeding in gastropods.

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Section: Introductionmentioning

confidence: 76%

Section: Introductionmentioning

confidence: 94%

Buccal neurons activate ciliary beating in the foregut of the pteropod molluskClione limacina

Malyshev

Balaban

2009

Journal of Experimental Biology

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“…Hook activity is also rhythmic and consists of protraction and retraction phases. We have shown in the previous investigation that the rhythmic movements of radula and hooks are highly coordinated in a phase-dependent manner (Malyshev and Norekian 2002). This phase-dependent coordination was observed on the behavioral level and was always recorded on the motoneuronal level during spontaneous and induced rhythmic activity.…”

Section: Introductionmentioning

confidence: 80%

Section: Introductionmentioning

confidence: 92%

“…This phase-dependent coordination was observed on the behavioral level and was always recorded on the motoneuronal level during spontaneous and induced rhythmic activity. Hook protractor neurons were active in the same phase with radula retractor neurons, whereas hook retractor neurons were bursting in phase with radula protractor neurons (Malyshev and Norekian 2002).We describe in this study and discuss the role of a bilaterally symmetrical cerebral interneuron, designated Cr-BM cell, which produces a prominent excitatory influence on all neural networks that control three major feeding structures in Clione: buccal cones, chitinous hooks, and the radula. A preliminary general description of some of these effects has been previously published (Norekian 1995).…”

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confidence: 90%

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Coordinated Excitatory Effect of GABAergic Interneurons on Three Feeding Motor Programs in the MolluskClione limacina

Norekian¹,

Malyshev²

2005

Journal of Neurophysiology

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Norekian, Tigran P. and Aleksey Y. Malyshev. Coordinated excitatory effect of GABAergic interneurons on three feeding motor programs in the mollusk Clione limacina. J Neurophysiol 93: 305-315, 2005. First published August 25, 2004; doi:10.1152/ jn.00722.2004. Coordination between different motor centers is essential for the orderly production of all complex behaviors. Understanding the mechanisms of such coordination during feeding behavior in the carnivorous mollusk Clione limacina is the main goal of the current study. A bilaterally symmetrical interneuron identified in the cerebral ganglia and designated Cr-BM neuron produced coordinated activation of neural networks controlling three main feeding structures: prey capture appendages called buccal cones, chitinous hooks used for prey extraction from the shell, and the toothed radula. The Cr-BM neuron produced strong excitatory inputs to motoneurons controlling buccal cone protraction. It also induced a prominent activation of the neural networks controlling radula and hook rhythmic movements. In addition to the overall activation, Cr-BM neuron synaptic inputs to individual motoneurons coordinated their activity in a phase-dependent manner. The Cr-BM neuron produced depolarizing inputs to the radula protractor and hook retractor motoneurons, which are active in one phase, and hyperpolarizing inputs to the radula retractor and hook protractor motoneurons, which are active in the opposite phase. The Cr-BM neuron used GABA as its neurotransmitter. It was found to be GABA-immunoreactive in the double-labeling experiments. Exogenous GABA mimicked the effects produced by Cr-BM neuron on the postsynaptic neurons. The GABA antagonists bicuculline and picrotoxin blocked Cr-BM neuron-induced PSPs. The prominent coordinating effect produced by the Cr-BM neuron on the neural networks controlling three major elements of the feeding behavior in Clione suggests that this interneuron is an important part of the higher-order system for the feeding behavior. I N T R O D U C T I O NAny complex behavior requires a specific coordination between various neural networks controlling its different aspects to achieve a meaningful behavioral output. Such coordination ensures the orderly production of a complex behavior and represents a universal principle of CNS functioning in both vertebrate and invertebrate animals. The focus of the current study is the feeding behavior of the carnivorous pteropod mollusk Clione limacina and the neuronal mechanisms of coordination between the main elements of this complex behavior.Clione is a highly specialized carnivore, which feeds only on two species of shelled pteropod mollusks of the genus Limacina (Lalli 1970;Lalli and Gilmer 1989; Wagner 1885). To seize its prey, Clione rapidly protracts tentacle-like oral appendages, called buccal cones, which surround the Limacina shell and hold it during the subsequent phases of feeding. Once buccal cones have gripped the prey, they begin to manipulate it so that the shell aperture is pressed against the mo...

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Phylogenetic and individual variation in gastropod central pattern generators

Sakurai

Katz

2015

J Comp Physiol A

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Gastropod molluscs provide a unique opportunity to explore the neural basis of rhythmic behaviors because of the accessibility of their nervous systems and the number of species that have been examined. Detailed comparisons of the central pattern generators (CPGs) underlying rhythmic feeding and swimming behaviors highlight the presence and effects of variation in neural circuits both across and within species. The feeding motor pattern of the snail, Lymnaea, is stereotyped, whereas the feeding motor pattern in the sea hare, Aplysia, is variable. However, the Aplysia motor pattern is regularized with operant conditioning or by mimicking learning using the dynamic clamp to change properties of CPG neurons. Swimming evolved repeatedly in marine gastropods. Distinct neural mechanisms underlie dissimilar forms of swimming, with homologous neurons playing different roles. However, even similar swimming behaviors in different species can be produced by distinct neural mechanisms, resulting from different synaptic connectivity of homologous neurons. Within a species, there can be variation in the strength and even valence of synapses, which does not have functional relevance under normal conditions, but can cause some individuals to be more susceptible to lesion of the circuit. This inter- and intra-species variation provides novel insights into CPG function and plasticity.

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Phase-Locked Coordination Between Two Rhythmically Active Feeding Structures in the MolluskClione limacina. I. Motor Neurons

Cited by 12 publications

References 22 publications

Buccal neurons activate ciliary beating in the foregut of the pteropod molluskClione limacina

Buccal neurons activate ciliary beating in the foregut of the pteropod molluskClione limacina

Coordinated Excitatory Effect of GABAergic Interneurons on Three Feeding Motor Programs in the MolluskClione limacina

Phylogenetic and individual variation in gastropod central pattern generators

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