A model accounting for effects of vibratory amplitude on responses of cutaneous mechanoreceptors in macaque monkey

Abstract

1. A mechanoreceptor model, developed in the preceding paper (Freeman & Johnson, 1982), was used to study the effects of vibratory intensity and frequency on the responses of slowly adapting, rapidly adapting and Pacinian afferents in monkey hairless skin. As in the previous paper almost all of the response properties studied here were accounted for by the equivalent circuit model; changes in membrane time constant and amplitude sensitivity accounted for the differences between the three mechanoreceptive fibre types.2. The stimulus-response function of primary concern was the relationship between impulse rate and vibratory amplitude. This relationship had the same general form in each of the three fibre types. Amplitudes, I, less than I(0) produced no impulse on any stimulus cycles. Amplitudes greater than I(1) produced one impulse on every cycle. As I rose from I(0) to I(1) the impulse rate rose monotonically from 0 to 1 impulse/cycle. For each fibre type the form of this ramp depended on the stimulus frequency.3. At stimulus frequencies low in the frequency range of each fibre type the (I(0), I(1)) ramp tended to be steep and sigmoidal in shape. Two or more impulses occurred on some cycles and none on others.4. At intermediate frequencies the (I(0), I(1)) ramps became linear with at most one impulse on each cycle. A short plateau appeared at 0.5 impulses/cycle (i.e. there was a range of intensities yielding one impulse on alternate cycles). All of these response properties at low and intermediate frequencies were explained by the model.5. At higher frequencies the (I(0), I(1)) ramps became shallower and developed discontinuities in slope at impulse rates of 0.5 impulses/cycle. At stimulus frequencies greater than 20 Hz for SAs and RAs, the upper segment of the (I(0), I(1)) slope became steeper. For frequencies greater than 80 Hz, the upper segments of the Pacinian (I(0), I(1)) slopes were shallower than the lower segments. These effects suggested transient periods of hyperexcitability following each action potential, and reductions in sensitivity due to high impulse rates, respectively.6. The model's membrane time constant was adjusted to match the observed reduction in the (I(0), I(1)) slope with increasing stimulus frequency. The time constants required for least-squares fitting were 58, 29 and 4.2 msec for slowly adapting, rapidly adapting and Pacinian afferents, respectively; these values are of the same order as those obtained in the preceding paper.7. Receptor sensitivity varied across the frequency spectrum, slow adaptors being most sensitive at low frequencies, rapidly adapting units at mid-range, and Pacinians at the high frequencies. According to the model, the high frequency roll-off in a receptor's tuning curve is due to the current integrating properties of receptor membrane, and the low frequency roll-off is due to a high pass filter, presumably mechanical, situated in the tissues between the stimulus probe and receptor membrane.8. Impulse phase advances with increasing stimulus intensity in both receptor and model. The ability of the model to fit both the rate-intensity function and phase advance functions in individual receptors is demonstrated.