Tonic inhibition alternates in paired neurons that set direction of fish escape reaction

Crossed antagonism between activities in neurons subserving alternating movements such as swimming or walking has been described in a number of systems. The role of reciprocal inhibition has been implicated in these activities, but involvement of rhythmic ongoing fluctuations of membrane potential, called synaptic “noise,” has not been examined. In the Mauthner (M) cells, which control the direction of escape, this activity is inhibitory. We report that in the zebrafish (Danio rerio), inhibitory synaptic noise exhibits prolonged bursts of rhythmic, inhibitory postsynaptic potentials, which attenuate the M cell’s sensibility to excitatory sensory drives. Furthermore, paired intracellular recordings have shown that inhibitory synaptic noise alternates between two distinct states, noisy and quiet, which are out of phase in the two cells. Firing of either M cell resets this pattern by reducing the inhibition in the contralateral one. This suggests that an avoidance reflex in one direction may favor initiation, by the opposite M cell, of a subsequent escape toward a more appropriate location.