The response of primary muscle spindle endings to random muscle stretch: a quantitative analysis

In cats the stretch responses of deafferented Ia afferent fibers from gastrocnemius muscle spindles were measured. The response properties were derived by correlating the action potentials to random mechanical stimuli applied to the gastrocnemius muscle. The muscle stretch consisted of band-limited, normally distributed random changes in muscle length. The upper cut-off frequency of the noise stimuli fc (i.e. the -3 dB point of the amplitude spectrum) was varied systematically between 1.5 and 600 Hz and the amplitude of the noise stimuli sigma (i.e. the standard deviation of the distribution of muscle displacements) between 1.5 and 1200 microns. The neuronal responses were analysed by averaging the stimulus signals centered on the Ia action potentials (the "peri-spike average", PSA). The cross-spectrum between stimulus and neuronal response was determined by computing the Fourier expansion of the PSA. Immediately before the action potentials the PSA decreased below mean muscle length and increased thereafter rapidly. As a rule, the action potentials were elicited close to the point of maximum stretch velocity. The cross-spectra revealed a monotonic increase in gain with stimulus frequency, corresponding to a power function with an average exponent of 0.86. The PSA-shape obtained at stimulus cut-off frequencies between 1.5 and 260 Hz remained fairly independent of fc when the abscissa was normalized with 1/fc. In the cross-spectra a maximum gain was always reached near the actual fc-value for upper cut-off frequencies up to 260 Hz. Above 260 Hz maximum gain remained independently of fc at about 260 Hz. The peak-to-peak displacement A of the PSA increased linearly with the logarithm of fc. The shapes of the PSAs and the cross-spectra did not depend on the noise amplitude sigma in the range above 20 microns. A was linearly related to sigma (about 1.6 to 2.4 . sigma for sigma greater than 10 microns and 75 Hz less than fc less than 450 Hz). A unifying mathematical description of the responses, valid for a wide range of stretch parameters, was obtained. We demonstrated that the application of one short run of random muscle stretch of an intermediate noise amplitude and medium cut-off frequency provides substantial information on the spindle stretch response and is recommended for investigations in which stable recordings cannot be obtained for a sufficient length of time.