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

Abstract

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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