Pharmacology of ionotropic and metabotropic glutamate receptors on neurons involved in feeding behavior in the pond snail, Helisoma trivolvis

Abstract

Glutamate is a key regulatory neurotransmitter in the triphasic central pattern generator controlling feeding behavior in the pond snail, Helisoma trivolvis. It excites phase two motor neurons while inhibiting those in phases one and three. However, the receptors that mediate this regulation are only partially characterized. The purpose of these experiments was to further characterize the glutamate receptors on three buccal neurons modulated by glutamate. Intracellular recordings from B5, B19 and B27 neurons were taken during the perfusion of isolated buccal ganglia with agonists that are selective for different vertebrate glutamate receptors. The firing rate of all three neurons was inhibited in a dose-dependent manner by glutamate, including that of B27, a phase 2 motor neuron known to be excited by glutamate in vivo. Quisqualate also reduced the firing rate in all three neurons, and (1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid (ACPD), a relatively non-selective metabotropic glutamate receptor (mGluR) agonist, reduced the firing rate in B5 neurons, but not in B19 or B27 neurons. Agonists selective for vertebrate group I, II and III mGluRs did not affect the firing rate in any of the Helisoma buccal neurons tested, suggesting that mGluR agonist binding sites on these neurons do not closely resemble those on any vertebrate mGluR subtypes. An increase in frequency of action potentials was observed in all three cell types in the presence of 100 micromol l(-1) kainate (KA), suggesting the presence of excitatory (S)-alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/KA-like receptors. However, electrotonic coupling between B19 and B27 neurons, and a lack of effect of KA on isolated B19 neurons suggest the excitatory effects of KA on this neuron are indirect. These findings suggest the presence of multiple glutamate receptor subtypes in molluscan neurons that do not always resemble vertebrate receptors pharmacologically.