Analysis of the feeding motor pattern in the pond snail, Lymnaea stagnalis: photoinactivation of axonally stained pattern-generating interneurons

• Published in: The Journal of neuroscience Vol. 14; no. 1; pp. 153 - 166
• Main Authors: Kemenes, G, Elliott, CJ
• Format: Journal Article
• Language: English
• Published: Washington, DC Soc Neuroscience 01.01.1994; Society for Neuroscience
• Subjects: Animals; Axons - ultrastructure; Biochemistry. Physiology. Immunology; Biological and medical sciences; Cheek - innervation; Feeding Behavior - physiology; Fluoresceins; Fundamental and applied biological sciences. Psychology; Ganglia, Invertebrate - cytology; Ganglia, Invertebrate - physiology; Interneurons - physiology; Interneurons - radiation effects; Interneurons - ultrastructure; Invertebrates; Light; Lymnaea - physiology; Mollusca; Motor Activity - physiology; Neurons - physiology; Periodicity; Physiology. Development; Lymnaea stagnalis; Fluorescent labelling; Buccal ganglion; Central nervous system; Electrophysiology; Gastropoda; Laser irradiation; Invertebrata; Mollusca; Inactivation; Feeding; Interneuron
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.14-01-00153.1994

We have photoinactivated identified feeding interneurons known as N1 and N2 neurons. These are pattern-generating neurons that are active in the protraction of the radula and rasping phases, respectively, of the feeding cycle of the pond snail. The N1 or N2 feeding interneurons in the buccal ganglia were filled with the fluorescent dye 5(6)-carboxyfluorescein (5-CF) from the cut end of the nerve that contains their axon. Filling the cerebrobuccal connective (N = 151) stained just one N1 cell in the contralateral buccal ganglion. Filling the postbuccal nerve stained neurons symmetrically in both buccal ganglia (N = 75): only one labeled cell in each ganglion is an N2 interneuron. The feeding rhythm was evoked by depolarizing a modulatory neuron, the SO, located in the buccal ganglia. The axonally filled N1 interneuron was irradiated at its axon in the buccal commissure with blue laser light (intensity of 0.5 MW.m-2). Irradiation of just one N1 completely blocked the feeding rhythm (seven preparations). In seven further preparations, N1 ablation slowed the SO-driven feeding rhythm and weakened the N1 input to the feeding neurons. Irradiation of the cell bodies of both the filled left and right N2 interneurons killed the cells but did not produce any consistent change in the feeding rate (15 preparations). The feeding interneurons and motoneurons still showed the characteristic N2 phase synaptic inputs, so more, as yet unidentified, N2 neurons must be located in other parts of the buccal ganglia. We conclude that the participation of the identified N1 interneurons is essential for the normal feeding pattern while other, still to be identified N2 neurons must be present and must contribute to the feeding rhythm. We suggest that the extra redundancy of the N2 network may be related to the greater necessity of sensory feedback control during rasping than during protraction of the radula.