Readiness discharge for spontaneous initiation of walking in crayfish

Animals initiate behavior not only reflexively but also spontaneously in the absence of external stimuli. In vertebrates, electrophysiological data on the neuronal activity associated with the self-initiated voluntary behavior have accumulated extensively. In invertebrates, however, little is known about the neuronal basis of the spontaneous initiation of behavior. We investigated the spike activity of brain neurons at the time of spontaneous initiation of walking in the crayfish Procambarus clarkii and found neuronal signals indicative of readiness or preparatory activities in the vertebrate brain that precede the onset of voluntary actions. Those readiness discharge neurons became active >1 s before the initiation of walking regardless of stepping direction. They remained inactive at the onset of mechanical stimulus-evoked walking in which other descending units were recruited. These results suggest that the parallel descending mechanisms from the brain separately subserve the spontaneous and stimulus-evoked walking. Electrical stimulation of these different classes of neurons caused different types of walking. In addition, we found other descending units that represented different aspects of walking, including those units that showed a sustained activity increase throughout the walking bout depending on its stepping direction, as well as one veto unit for canceling out the output effect of the readiness discharge and three termination units for stopping the walking behavior. These findings suggest that the descending activities are modularized in parallel for spontaneous initiation, continuation, and termination of walking, constituting a sequentially hierarchical control.