Processing vibratory stimuli in isolated frog muscle spindle.

Abstract

Experiments were performed on isolated frog muscle spindle receptors to study the particular transducer and encoder mechanisms involved in the signal transfer of high frequency sinusoids (vibration). In order to systematically investigate the signal transfer over the entire dynamic range of the receptor, vibration stimuli were applied to the intrafusal muscle bundle at different prestretch levels, so that the isolated receptor potential or the afferent impulse train were recorded at different operating points. The vibration-induced receptor potential displayed severe distortion, because the depolarization during stretch rose steeply, whereas the repolarization transient during release of stretch declined more slowly. The positive peak velocity values of the depolarization transient increased with increasing stimulus frequency, although the ac-component of the receptor potential decreased. The negative peak velocity values of the repolarization transient remained constant throughout the frequency range. The amplitude of the receptor potential grew larger when vibration of constant amplitude was applied at increasing levels of prestretch, revealing another non-linearity of the transducer. These two types of non-linearity were influential in determining the afferent discharge pattern. Each fast depolarization transient facilitated the generation of a single action potential, which therefore could be firmly phase-locked to a small segment of the vibratory movement. Due to its short rise-time, the depolarization transient tended to prevent multiple firing during one stimulus cycle. The prolonged depolarizing afterpotential of the evoked action potential operated in the same direction. Increasing prestretch greatly enhanced the responsiveness of the spindle to vibration. Thus, under appropriate conditions, the afferent discharge was driven in 1:1 synchrony with the vibration. An analysis is given of the after-effects of repetitive activity at the receptor site. The progressive decline of the mean membrane voltage during long lasting stimulation and the "post-tetanic" hyperpolarization ("off-effect") on termination of the vibration suggest the action of an electrogenic pumping mechanism. As a consequence, the afferent impulse train possessed a complex structure segmented into several transient and steady states, which differed in impulse rate, phase response, and in the degree of phase-locking.