Time-course of vibratory adaptation and recovery in cutaneous mechanoreceptive afferents

Abstract

Extended suprathreshold vibratory stimulation applied to the skin results in a desensitization of cutaneous mechanoreceptive afferents. In a companion paper, we describe the dependence of the threshold shift on the parameters of the adapting stimulus and discuss neural mechanisms underlying afferent adaptation. Here we describe the time-course of afferent adaptation and recovery. We found that absolute and entrainment thresholds rise and fall exponentially during adaptation and recovery with time constants that vary with fiber type. slowly adapting type I (SA1) afferents adapt most rapidly, and pacinian (PC) afferents adapt most slowly, whereas rapidly adapting (RA) afferents exhibit intermediate rates of adaptation; SA1 fibers also recover more rapidly from adaptation than RA and PC fibers. We also showed that threshold adaptation is accompanied by a shift in the timing of the spikes within individual cycles of the adapting stimulus (i.e., a shift in the impulse phase). We invoked an integrate-and-fire model to explore possible mechanisms underlying afferent adaptation. Finally, we found that the time-course of afferent adaptation is more rapid than that of its psychophysical counterpart, as is the time-course of recovery from adaptation, suggesting that central factors play a role in the psychophysical phenomenon.

Fig. 1

Time-course of adaptation and recovery for 2 typical SA1 afferents. Stimulus parameters and time constants are shown above each plot. Thin lines, thresholds estimated from the tracking algorithm; thick dotted and solid lines, fitted exponential functions. F_t, test frequency; F_a, adaptation frequency; A_a, adaptation amplitude; τ_a, adaptation time constant; τ_r, recovery time constant.

Fig. 2

Time-course of adaptation and recovery for 2 typical RA afferents. Conventions as in Fig. 1.

Fig. 3

Time-course of adaptation and recovery for 2 typical PC afferents. Conventions as in Fig. 1.

Fig. 4

Cumulative histograms of adaptation (left) and recovery (right) threshold time constants for all SA1, RA, and PC afferents and all stimulus conditions.

Fig. 5

Correspondence between the initial and final (recovered) I₀ and I₁ thresholds. I₀ correspondence seems more variable because the scale is generally magnified by a factor of 3 or more relative to the I₁ scale.

Fig. 6

Cumulative histograms of adaptation and recovery time constants for I₀ (left) and I₁ (right) thresholds for all 3 types of afferents. Conventions as in Fig. 4, in which the same data are presented in different pairings.

Fig. 7

Impulse phase as a function of time for 1 afferent of each type. Each data point corresponds to the phase of the 1st impulse evoked during a cycle of the adapting stimulus. Dark trace shows the exponential fit to the data. All 3 neurons were nearly perfectly entrained with the stimulus. Digitization in the data reflects temporal resolution of the spike collection system.

Fig. 8

Cumulative histogram of phase adaptation time constants for the 3 types of fibers. SA1 and RA phase adaptation time constants were similar to their threshold adaptation counterparts, whereas PC time constants were substantially shorter.

Fig. 9

Decay of the response of an SA1 afferent (averaged in 500-ms bins) to a 1-mm indentation applied over 30 s. Rate of decay of SA1 response is the same as that of SA1 vibratory adaptation, supporting the hypothesis that the same mechanism underlies the 2 phenomena.