Sensorimotor integration in the Mauthner cell system and the role of inhibition

Abstract

A goal in neuroscience is to understand how individual neurons process sensory information, make a decision and generate a motor command. The Mauthner (M-) cell is a giant reticulospinal neuron present as a pair in many fish. When a stimulus excites the M-cell above threshold it fires a single action potential that correlates with a fast startle-escape response. The escape is often appropriately timed and directional. We used electrophysiological and behavioral techniques to investigate the functional organization of the M-cell's neuronal network, and the biophysical mechanisms that endow the system with decision-making capacities. We show that the M-cell initiates the escape behavior in response to diverse multimodal stimuli, and that other reticulospinal neurons, in parallel and in series with the M-cell, specify the trajectory of the C-start escape. Stimulus-evoked inhibition of the M-cell regulates the behavioral threshold and is partially mediated by a rarely described, but potentially widespread, form of neurotransmission known as a field effect. Sound phase encoding, mediated by gap junctions, is evident in the excitatory and inhibitory branches of the M-cell circuit and at the behavioral level, suggesting that the M-cell system implements a time coding algorithm to discriminate the location of underwater sound sources. These results advance the understanding of sensorimotor integration in the M-cell system, and the biophysical basis of decision-making in single neurons.