Crayfish stretch-receptor organs: Effects of length-steps with and without perturbations

Abstract

Isolated slowly and fast adapting stretch receptor organs (SROs) of crayfish were submitted to step-like length changes separated by prolonged stations with constant lengths. At times they were perturbed by a small-amplitude, fast length variation representing natural pertubations and referred to as “jitter”. Stimulus “cycles” depended on the sequence of lengths and on whether jitter was present. First-order afferent discharges were recorded from the dorsal nerve. Firing intensity, measured by the rate over bins of about 1 s, was displayed along ongoing time. Quantification involved estimation of cycle histograms, and trend tests for fully adapted discharges and preparation stability. The behaviour perturbed by jitter differed quantitatively in both organs from that without jitter, apart from more intense and irregular firing. Differences were also qualitative in the rapidly adapting organ (RAO), that jitter kept firing almost unccasingly and changed from a “transient detector” to a “tonic receptor”. Jitter effects varied with background stretch. The slowly adapting organ (SAO) and the perturbed RAO behaved quite similarly and exhibited features of lead-lag linear systems that implied joint sensitivity to length and velocity, like lively accelerations after stretches and lively slowings after relaxations with subsequent adaptation to steady discharges. Shortenings provided as important stimuli as lengthenings. At constant lengths, discharges eventually reached “full adaptation”: full adaptation cannot be proven experimentally, but can be accepted in practice using statistically sound and physiologically pragmatic criteria. When fully adapted, the SAO and the perturbed RAO had length-dependent discharges. Both SROs exhibited also prominent non-linear features besides the expected limiter behavior. Responses to symmetric stimuli were asymmetric: e.g. lengthenings produced greater rate changes and more durable transients than shortenings. The coding from steady lengths to fully-adapted discharges was multivalued (except in the unperturbed RAO): discharges were more or less intense depending on whether the particular length had been reached through lengthening or shortening, respectively (“hysteresis”). The anatomical and physiological reasons for many of these linear or nonlinear features are not yet identified fully. Discharge profiles deviated (in mean squared error) from the corresponding stimuli less with jitter than without. This happened, in spite of increased fluctuations in successive bins, because of reductions in transient effects and in delays to full adaptation. Length identification on the basis of the afferent discharges was improved by jitter, because of the above and because of reduction of the multivaluedness. The consequences of this more faithful representation are contingent on the neuronal analyzer to which the discharges are presented. The issues discussed, like full adaptation, multivaluedness, and the implications of the perturbations are relevant to mechanoreceptors in general, and even to all receptors.