Tonic Immobility in a Cricket: Neuronal Underpinnings of Global Motor Inhibition

Abstract

Tonic immobility (TI) in the field cricket Gryllus bimaculatus is triggered by physical restraint of the legs, and is locally characterized by resistance upon imposed restraint and its rapid decay that occur regardless of the tibial position for each leg. The neuronal substrate underlying the induction and maintenance of TI was investigated by sensory and motor neuronal recordings in free-moving crickets. Isometric contraction of flexor tibiae muscles that occurred under the condition of leg restraint intensely activated sensory neurons in the femoral chordotonal organ (FCO). The “restraint signals” detected by prothoracic FCOs intersegmentally inhibited active movements of all legs, which was a hallmark of the widespread motor inhibition. In each leg, two neuronal groups in the FCO mediate the tibial resistance reflex and its inhibition in the same leg, respectively. The flexor muscle rigidity unique to TI was maintained by a weak discharge of slow excitatory motor neurons together with suppression of the activity of common inhibitory motor neurons. Taken together with the requirement of the brain for maintaining TI, I propose that a local reflex that mitigates isometric muscle loading is incorporated into a brain-controlled long-lasting immobilization for camouflaging against predators during evolution.