Synaptic drive contributing to rhythmic activation of motoneurons in the deafferented stick insect walking system

Abstract

A general feature of motor patterns for locomotion is their cyclic and alternating organization. In walking, for example, rhythmic activity in leg motoneurons innervating antagonistic muscles of a joint is primarily antiphasic within each cycle. We investigate which role central pattern generating networks play in the generation of leg motoneuron activity in the absence of sensory feedback. We elicited activity in antagonistic flexor and extensor tibiae motoneurons in the deafferented mesothoracic ganglion of the stick insect by mechanically stimulating the head or abdomen, while recording intracellularly from their neuropilar processes. In most cases, tactile stimulation induced coactivation of tibial motoneurons. However, in ≈ 25% of the trials, tibial motoneurons generated alternating cycles consisting of bursts of action potentials that were terminated by strong inhibitory synaptic inputs. Injection of depolarizing current increased the amplitude of the inhibitory phase of the oscillation, while hyperpolarizing current decreased it and revealed a tonic depolarization of the motor neurons during the bout of rhythmic motor activity. The same results were gathered from recording tibial leg motoneurons during 'twitching' motor activity in decerebrated animals. Our results indicate that alternating rhythmic motoneuron activity in the deafferented stick insect walking system results from phasic inhibitory drive provided by central pattern generating networks. This inhibitory input patterns the firing of the motoneurons that results from a tonic depolarizing drive. This tonic depolarizing drive was also observed in tibial motoneurons of the deafferented mesothoracic ganglion during walking movements of the intact ipsilateral front leg.