Functional Analysis of the Sensory Motor Pathway of Resistance Reflex in Crayfish. I. Multisensory Coding and Motor Neuron Monosynaptic Responses

Abstract

Le Ray, Didier, François Clarac, and Daniel Cattaert. Functional analysis of the sensory motor pathway of resistance reflex in crayfish. I. Multisensory coding and motor neuron monosynaptic responses. J. Neurophysiol. 78: 3133–3143, 1997. An in vitro preparation of the fifth thoracic ganglion of the crayfish was used to study in detail the negative feedback loop involved in the control of passive movements of the leg. Release-sensitive primary afferents of from the coxo-basipodite chordotonal organ (CBCO), a proprioceptor whose strand is released by upward movement of the leg, monosynaptically connect to depressor motor neurons (Dep MNs). Extracellular identification of sensory units from the CBCO neurogram allowed us to determine the global coding of a sine-wave movement, imposed from the most released position of the CBCO strand. Intracellular recordings from sensory terminals (CBTs) and ramp movement stimulations applied to the CBCO strand allowed us to characterize two groups of release-sensitive CBCO fibers. The first group, divided into two subgroups (phasic and phaso-tonic), is characterized by discontinuous firing patterns: phasic CBTs fired exclusively during release movements; phaso-tonic CBTs displayed both a phasic firing and a tonic discharge during the more released plateaus. The second group was continuously firing whatever the movement, with higher frequencies during the release phase of the movement stimulation. All CBTs displayed a marked sensitivity for release movements while only the phaso-tonic ones showed a clear sensitivity to maintained positions. Surprisingly, no pure tonic sensory fibers were encountered. Systematic intracellular recordings from all resistant Dep MNs, performed in high divalent cation saline, allowed us to describe two shapes of monosynaptic resistance reflex responses. A phasic response was characterized by bursts of excitatory postsynaptic potentials (EPSPs) occurring exclusively during CBCO strand release movements. A phaso-tonic response was characterized by a progressive depolarization occurring all along the release phase of the stimulation: during maintained released positions, the amplitude of the sustained depolarization was position dependent; in addition, each release movement produced a phasic burst of EPSPs in the MN. The parallel study of the Dep MN properties failed to point out any correlation between the type of reflex response recorded from the MN and the MN intrinsic properties, which would indicate that the type of MN response is entirely determined by the afferent messages it receives.