The contribution of membrane hyperpolarization to adaptation and conduction block in sensory neurones of the leech.

Abstract

The factors underlying sensory adaptation and conduction block have been studied in cutaneous mechanoreceptor neurones of the leech. A touch-sensitive cell was activated by applying mechanical or electrical stimuli to its receptive field on the skin. Impulses were recorded extracellularly from its axons and intracellularly from its cell body, which is situated within the C.N.S.1. Activation of the touch cell by mechanical stimuli revealed two distinct types of adaptation with characteristically different time courses. Sustained pressure on the skin caused a brief burst of impulses at the onset of the stimulus. This rapid adaptation to pressure was restricted to the part of the receptive field that had been stimulated mechanically. A second type of adaptation developed more slowly during the course of repetitive mechanical stimulation. It persisted for many seconds after the end of a train of impulses and appeared as an increase in the threshold to mechanical stimuli not only in the region of skin that had been rubbed but throughout the receptive field of the cell.2. Impulses initiated in the cell body propagated antidromically towards the skin and also raised the threshold to touch, indicating that after-effects of impulse activity were responsible for the long-lasting threshold increase.3. Repetitive mechanical stimulation could also produce a reversible conduction block in branches of the touch cell. The block occurred in discrete regions of low safety factor such as axonal branch points both within the ganglion and in the periphery. In some experiments impulses intermittently failed to reach one axonal branch yet continued to invade a separate branch of the same cell.4. Several lines of evidence indicate that both conduction block and the slow component of adaptation are linked to a prolonged hyperpolarization that follows repetitive stimulation of the touch cell. Strophanthidin, which blocks the after-hyperpolarization in touch cells, reduced the adaptation following trains of impulses and also relieved a conduction block previously established by repetitive stimulation. Furthermore, a comparison of the effects of hyperpolarizations produced by current injection and by repetitive firing showed that most of the threshold increase in the cell body after a train of impulses could be attributed directly to the membrane hyperpolarization.5. These experiments suggest several ways in which repetitive activity can have pronounced and long-lasting effects on the performance of a highly branched sensory cell. Thus a relatively small number of impulses in a touch cell can markedly decrease its sensitivity to touch. The functional role of the conduction block observed during vigorous stimulation is not as clear because activity for many seconds or minutes is usually needed to establish a block in the larger branches of the cell.