Multiple receptors mediate the modulatory effects of serotonergic neurons in a small neural network.

Abstract

The gastropyloric receptor (GPR) cells are a set of cholinergic/serotonergic mechanosensory neurons that modulate the activity of neural networks in the crab stomatogastric ganglion (STG). Stimulation of these cells evokes a variety of slow modulatory responses in different STG neurons that are mimicked by exogenously applied serotonin (5-HT); these responses include tonic inhibition, tonic excitation and induction of rhythmic bursting. We used pharmacological agonists and antagonists to show that these three classes of modulatory response in the STG neurons are mediated by distinct 5-HT receptor subtypes. GPR stimulation or application of 5-HT or 2-me-5HT (a vertebrate 5-HT3 agonist) inhibited the pyloric constrictor (PY) neurons; these actions were selectively antagonized by gramine. GPR stimulation or application of 5-HT induced rhythmic bursting in the electrically coupled anterior burster (AB) and pyloric dilator (PD) neurons; these effects were antagonized by the 5-HT1c/2 antagonist cinanserin and by atropine at concentrations that do not block muscarinic cholinergic receptors in the crab STG. The 5-HT agonists 5-CT (5-HT1) and alpha-me-5HT (5-HT2) also induced AB/PD bursting, which was blocked by cinanserin, but not by atropine. GPR stimulation or application of 5-HT and 5-CT evoked tonic excitation of the lateral pyloric (LP) neuron. These effects were blocked by cinanserin. Several other 5-HT agonists and nearly all the vertebrate 5-HT antagonists we tested had little or no effect on the crab pyloric 5-HT receptors. These results provide further evidence that the modulatory sensory GPR neuron uses serotonin to evoke multiple modulatory responses via multiple 5-HT receptors. However, the 5-HT receptors in the crab STG neurons are not pharmacologically similar to vertebrate 5-HT receptors.