Distinct Functions for Cotransmitters Mediating Motor Pattern Selection

Abstract

Motor patterns are selected from multifunctional networks by selective activation of different projection neurons, many of which contain multiple transmitters. Little is known about how any individual projection neuron uses its cotransmitters to select a motor pattern. We address this issue by using the stomatogastric ganglion (STG) of the crab Cancer borealis, which contains a neuronal network that generates multiple versions of the pyloric and gastric mill motor patterns. The functional flexibility of this network results mainly from modulatory inputs it receives from projection neurons that originate in neighboring ganglia. We demonstrated previously that the STG motor pattern selected by activation of the modulatory proctolin neuron (MPN) results from direct MPN modulation of the pyloric rhythm and indirect MPN inhibition of the gastric mill rhythm. The latter action results from MPN inhibition of projection neurons that excite the gastric mill rhythm. These projection neurons are modulatory commissural neuron 1 (MCN1) and commissural projection neuron 2 (CPN2). MPN excitation of the pyloric rhythm is mimicked by bath application of proctolin, its peptide transmitter. Here, we show that MPN uses only its small molecule transmitter, GABA, to inhibit MCN1 and CPN2 within their ganglion of origin. We also demonstrate that MPN has no proctolin-mediated influence on MCN1 or CPN2, although exogenously applied proctolin directly excites these neurons. Thus, motor pattern selection occurs during MPN activation via proctolin actions on the STG network and GABA-mediated actions on projection neurons in the commissural ganglia, demonstrating a spatial and functional segregation of cotransmitter actions.