Spontaneous fluctuations of excitability in the muscle spindle of the frog

Abstract

The discharge of impulses from the muscle spindle of the frog, when subjected to a constant mechanical stimulus (stretch), may show great irregularity. This is most noticeable when the muscle is near its resting length. The mean rate of impulses is then very low, and successive intervals appear to vary in a random manner. As the muscle is stretched, the rate of afferent discharge increases and irregularities become less obvious (Matthews, 1931).A possible explanation of the random discharge at low frequency has been suggested by Katz (1950a, b), on the basis of observations on single sensory nerve endings. Depolarization of the terminal branches of an axon in a muscle spindle was found to be responsible for the initiation of sensory impulses, the rate of the discharges depending upon the intensity of the local potential change. Fluctuations of the level of depolarization would therefore cause irregularity of the intervals between successive impulses. Such fluctuations of potential might be due directly to thermal agitation of ions in the nerve terminals, or they might be produced indirectly by molecular agitation in the mechanical receptor substance.At present, little is known about the mechanical receptor system, but the effects of thermal agitation in nerve endings can be subjected to a tentative theoretical analysis (see Fatt & Katz, 1952). Thus, the finer the diameter of a fibre, the larger will be the amplitude of 'voltage noise' at the terminal.For example, for an extremely fine ending, 0-1 ,u in diameter, a voltage fluctuation of the order of 0 5 mV r.m.s. has been estimated. The present experiments were planned to investigate whether this simple source of physical random disturbance could explain the observed fluctuations of impulse discharge. The irregularity was measured over a large range of frequencies of firing, applying various amounts of stretch to the muscle. * With a scholarship from the Swedish Medical Research Council.

The influence of certain chemical substances on the initiation of sensory discharges in pulmonary and gastric stretch receptors and atrial receptors

“…10C. Irregularity of discharge is a feature of receptors firing at a low frequency (Buller, Nicholls & Str6m, 1953) and it is also known that increasing the frequency regularizes the discharge; but the frequency at which this occurs is very low when compared with the frequency at which dropping out of impulses was observed in the present experiments.…”

Nerve-Model Experiments on Fluctuation in Excitability

“…It will be noted that these latency distributions bear a close resemblance to the interval distributions studied by Buller et al (1953) and by Hagiwara (1954) for the muscle spindle, by Grossman and Viernstein (1961) for slowly adapting, spontaneously discharging neurons of the cochlear nucleus and by Amassian et al (1961) for the spontaneous activity of neurons in the reticular formation of the midbrain.…”

“…Furthermore, the idea that very brief fluctuations of membrane potential have probably little effect, is advanced by Buller et al (1953). Until now the lower frequency limit of the noise studied in the model has been kept constant at 20 c/s.…”

Adaptation of the discharge of frog muscle spindles following a stretch

“…Whereas the hypothesis of Buller adequately explains the variability of the impulse train, he did not explore its consequences for the adaptation process, nor does it explain the progressive changes in the distribution of intervals during adaptation ( Fig. 5; Buller et al 1953, fig. 2).…”