SYNAPTIC CONNECTIVITY OF THE CIRCUMFERENTIAL MOTONEURONS IN THE BUCCAL GANGLIA OF NAVANAX AND ITS ROLE IN THE FEEDING BEHAVIOR

Abstract

The present work is a description of the cellular connectivity of a population of at least 12 motoneurons which control constriction of the pharynx in Navanax inermis, a cephalaspidean opisthobranch mollusc, and the functional significance of this connectivity. Cellular connectivity, and cellular activity during pharyngeal movement were assayed with up to four simultaneous intracellular recordings in identified cells of intact ganglion-muscle preparations of over 300 specimens of Navanax inermis. Feeding behavior was observed in dissected animals during intra-cellular recording from identified neurons, and in whole animals under natural conditions in the field.;The principal findings are as follows: (1) Circumferential motoneurons are electrotonically coupled to each other and to two distinct identifiable groups of interneurons, the C and Z groups. Circumferential motoneurons receive inhibitory chemical synaptic input from the C group interneurons; and expansion motoneurons, motoneurons which control muscles which oppose circumferential muscles, receive inhibitory chemical synaptic input from the Z group interneurons. (2) Reversed coupling whereby hyper- and depolarization of a circumferential motoneuron leads to depolarization and hyperpolarization of a coupled companion circumferential motoneuron favors the antero-posterior direction and appears to be a functionally significant network property for the peristaltic swallowing motor pattern. (3) Anterior circumferential motoneurons form a group of electrotonically coupled neurons involved in prey capture and the start of swallowing. They receive chemical inhibitory and excitatory synaptic input from mechanosensory cells which innervate the lips and inner pharyngeal wall. They may also receive chemical inhibitory synaptic input from the same low threshold interneuronal pathway (L group) that inhibits many of the expansion motoneurons. (4) C and Z neurons are electrotonically coupled to each other. Hyperpolarization of the Z group may turn off the synchronously active C group IPSPs in the CMNs. Firing in the C group may depolarize the Z group. Electrotonic coupling between these interneurons could provide a simple mechanism for avoiding the simultaneous discharge of incompatible motor patterns: prey capture and swallowing.