A tonically active master neuron continuously modulates mutually exclusive motor states at two-time scales

Behaviors consist of distinct states and state transitions. How a neural system continuously modulates each state, which underlies smooth state transitions, is not well understood. C. elegans spontaneously switches between two mutually exclusive motor states, forward and backward movements, a behavior long thought to reflect the reciprocal antagonism between interneurons that separately gate the forward and backward motor circuits. We report here that during spontaneous locomotion, the two motor states are not separately controlled, and these interneurons are neither functionally equivalent nor strictly reciprocally inhibitory. AVA, the premotor interneuron previously thought to exclusively gate the backward motor circuit, regulates both motor states with opposite polarities at two-time scales. AVA’s transient, fast activation inhibits the forward circuit while initiating the backward movement; in parallel, AVA maintains a slow, but constitutive excitation of the forward circuit to transit from reversals into maintained forward movement. This excitation results from AVA’s sustained depolarized membrane potential, which makes its chemical synapse tonically active. A tonically active master neuron breaks the symmetry between the forward and backward motor circuits. It offers an elegant circuit solution for smooth transitions when animals switch between two mutually exclusive motor states. Highlights Two mutually exclusive, forward and backward motor states, are inherently asymmetric The forward and backward motor states are not separately controlled A master neuron underlies continuous modulation and transitions of two motor states A tonically active premotor interneuron of the reversal circuit is the master neuron