Mechanisms of adaptation in a mechanoreceptor : A study of mechanical and ionic factors in the crayfish stretch receptors

Abstract: - The stretch receptor organ of the crayfish, an analog to the human muscle spindle, is a unique preparation for the study of mechanotransduction. The organ consists of a rapidly and a slowly adapting receptor each composed of a receptor muscle fibre into which inserts the dendrites of a multipolar sensory neuron. The present work explored various aspects of the mechanotranduction process with regard to the differences in adaptive properties between the rapidly and the slowly adapting receptors. The rapidly adapting receptor muscle fibre is statically less stiff, and the transient tensiol response more pronounced, as shown by a greater ratio of the peak to steady-state tension, compared to that of the slowly adapting receptor muscle fibre. These facts show that the visco-elastic properties do contribute to receptor adaptation. The presence of the initial stiffness could be considered as an increase in dynamic sensitivity of the receptor at small extension levels. Mechanosensitive (MS) ion channels generate a receptor current in the rapidly and the slowly adapting neuron. In the rapidly adapting neuron the receptor current was larger, decayed faster and llad a steeper slope of the stimulus-response relationship than in the slowly adapting neuron. It is concluded that the adaptive properties of the rapidly adapting receptor neuron depend on the viscoelastic properties of the muscle fibre but that the MS channels also contribute. Gadolinium (Gd3+) blocked the receptor current in the receptor neurons. Decreasing extracellular calcium concentration increased the affinity of Gd3+. However, the Gd3+effect was not selective, sodium and potassium channels were also blocked. The potential-dependent outward current, carried by potassium ions, is present in the rapidly and the slowly adapting receptor neurons. However, some electrical properties of the K+ currents differed between the receptors. Analysis of the dose-response relationship for TEA block indicates the presence of two different K+ channel populations with different relative densities in the two neurons. The action potential was shown to be generated by a potential-dependent inward current carried by sodium ions both in the rapidly and the slowly adapting receptor neurons. However, it was demonstrated that in the rapidly adapting neuron the inactivation kinetics and the current-voltage relationship of the sodium current as well as the changes induced by crude scorpion venom from Leiurus quinquestriatus were different from those observed in the slowly adapting neuron. The action potentials were different in the two neurons in agreement with the differences the sodium current. It is concluded that in the slowly adapting neuron the sodium current may consist of two components located in the axon and soma, whereas one of these current components is either absent or very small in the rapidly adapting neuron. The impulse response adaptation is thus a product of the properties of the receptor muscle fibre, the mechano-gated channels in the neuronal dendrites, the voltage-gated sodium and potassium channels and the ion-pumping mechanisms which all seem to have evolved to favor either the slow or the rapid adaptation seen in the two receptor organs. Keywords: Crayfish, stretch receptor, adaptation, visco-elastic properties, mechanosensitive channels, potassium channels, sodium channels, gadolinium, tetraethylammonium chloride, 4-amino pyridine, scorpion venom Leiurus quinquestrialus ~) Nuhan Purali, 1997 Printed in Sweden by Repro Print AB, Stockholm lSBN 91-628-2386-8