Abstract
Half a century ago, two independent papers that described unexpected results of experiments on locomotion in insects and crayfish appeared almost simultaneously. Together these papers demonstrated that an animal's central nervous system (CNS) was organized to produce behaviorally important motor output without the need for constant sensory feedback. These results contradicted the established line of thought that was based on interpretations of reflexes and ablation experiments, and established that in these animals the CNS contained neural circuits that could produce complex, periodic, multisegmental patterns of activity. These papers stimulated a flowering of research on central pattern-generating mechanisms that displaced reflex-based thinking everywhere except in medical physiology texts. Here we review these papers and their influence on thinking in the 1960s, 1970s, and today. We follow the development of ideas about central organization and control of expression of motor patterns, the roles of sensory input to central pattern-generating circuits, and integration of continuous sensory signals into a periodic motor system. We also review recent work on limb coordination that provides detailed cellular explanations of observations and speculations contained in those original papers.
Highlights
Fifty years ago, two groups of zoologists working independently on the neural basis of locomotion in arthropods made similar startling observations
Hughes, visiting from Cambridge, found that the deafferented crayfish abdominal nerve cord sometimes continued to produce coordinated bursts of spikes in motor axons that innervated different swimmerets (Hughes and Wiersma, 1960), a motor pattern that drives coordinated swimmeret beating during normal forward swimming(Figure 1). They recognized that this meant the complex motor pattern that coordinated movements of four pairs of limbs (Figure 1B) could not depend on cycle-by-cycle proprioceptive feedback from the limbs themselves because they had severed all connections to those limbs
Wilson’s Discussion ends with “It seems not too early to conclude that central oscillators in arthropods are of such fundamental importance that they are used even when other mechanisms might suffice.”. Wiersma and his students promptly looked more closely at the organization of the neural circuits that coordinated and controlled swimmeret movements (Ikeda and Wiersma, 1964; Wiersma and Ikeda, 1964). They compared the swimmeret motor pattern in intact animals with the patterns recorded from swimmeret nerves when the chain of six abdominal ganglia were isolated in vitro
Summary
Two groups of zoologists working independently on the neural basis of locomotion in arthropods made similar startling observations. The two Lateral Neuropils of each swimmeret ganglion are the anatomical loci of the “centers of coordination,” where alternating bursts of spikes in PS and RS motor neurons are organized by local pattern-generating circuits (Figure 3D).
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