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 I0 produced no impulse on any stimulus cycles. Amplitudes greater than I1 produced one impulse on every cycle. As I rose from I0 to I1 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 (I0, I1) 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 (I0, I1) 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 (I0, I1) 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 (I0, I1) slope became steeper. For frequencies greater than 80 Hz, the upper segments of the Pacinian (I0, I1) 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 (I0, I1) 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.
Full text
PDF





















Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Brugge J. F., Anderson D. J., Hind J. E., Rose J. E. Time structure of discharges in single auditory nerve fibers of the squirrel monkey in response to complex periodic sounds. J Neurophysiol. 1969 May;32(3):386–401. doi: 10.1152/jn.1969.32.3.386. [DOI] [PubMed] [Google Scholar]
- Freeman A. W., Johnson K. O. Cutaneous mechanoreceptors in macaque monkey: temporal discharge patterns evoked by vibration, and a receptor model. J Physiol. 1982 Feb;323:21–41. doi: 10.1113/jphysiol.1982.sp014059. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gregory J. E., Harvey R. J., Proske U. A 'late supernormal period' in the recovery of excitability following an action potential in muscle spindle and tendon organ receptors. J Physiol. 1977 Oct;271(2):449–472. doi: 10.1113/jphysiol.1977.sp012008. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HARMON L. D. Studies with artificial neurons. I. Properties and functions of an artificial neuron. Kybernetik. 1961 Dec;1:89–101. doi: 10.1007/BF00290179. [DOI] [PubMed] [Google Scholar]
- HUBBARD S. J. A study of rapid mechanical events in a mechanoreceptor. J Physiol. 1958 Apr 30;141(2):198–218. doi: 10.1113/jphysiol.1958.sp005968. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holden A. V. The response of excitable membrane models to a cyclic input. Biol Cybern. 1976 Jan 2;21(1):1–7. doi: 10.1007/BF00326666. [DOI] [PubMed] [Google Scholar]
- Hughes G. W., Maffei L. Retinal ganglion cell response to sinusoidal light stimulation. J Neurophysiol. 1966 May;29(3):333–352. doi: 10.1152/jn.1966.29.3.333. [DOI] [PubMed] [Google Scholar]
- Johnson K. O. Reconstruction of population response to a vibratory stimulus in quickly adapting mechanoreceptive afferent fiber population innervating glabrous skin of the monkey. J Neurophysiol. 1974 Jan;37(1):48–72. doi: 10.1152/jn.1974.37.1.48. [DOI] [PubMed] [Google Scholar]
- Knight B. W. Dynamics of encoding in a population of neurons. J Gen Physiol. 1972 Jun;59(6):734–766. doi: 10.1085/jgp.59.6.734. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LIPPOLD O. C., REDFEARN J. W., VUCO J. The effect of sinusoidal stretching upon the activity of stretch receptors in voluntary muscle and their reflex responses. J Physiol. 1958 Dec 30;144(3):373–386. doi: 10.1113/jphysiol.1958.sp006108. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LOEWENSTEIN W. R., COHEN S. After-effects of repetitive activity in a nerve ending. J Gen Physiol. 1959 Nov;43:335–345. doi: 10.1085/jgp.43.2.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LOEWENSTEIN W. R., COHEN S. Post-tetanic potentiation and depression of generator potential in a single non-myelinated nerve ending. J Gen Physiol. 1959 Nov;43:347–376. doi: 10.1085/jgp.43.2.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lindblom U. Properties of touch receptors in distal glabrous skin of the monkey. J Neurophysiol. 1965 Sep;28(5):966–985. doi: 10.1152/jn.1965.28.5.966. [DOI] [PubMed] [Google Scholar]
- Loewenstein W. R., Skalak R. Mechanical transmission in a Pacinian corpuscle. An analysis and a theory. J Physiol. 1966 Jan;182(2):346–378. doi: 10.1113/jphysiol.1966.sp007827. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matthews P. B., Stein R. B. The sensitivity of muscle spindle afferents to small sinusoidal changes of length. J Physiol. 1969 Feb;200(3):723–743. doi: 10.1113/jphysiol.1969.sp008719. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakajima S., Takahashi K. Post-tetanic hyperpolarization and electrogenic Na pump in stretch receptor neurone of crayfish. J Physiol. 1966 Nov;187(1):105–127. doi: 10.1113/jphysiol.1966.sp008078. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rescigno A., Stein R. B., Purple R. L., Poppele R. E. A neuronal model for the discharge patterns produced by cyclic inputs. Bull Math Biophys. 1970 Sep;32(3):337–353. doi: 10.1007/BF02476873. [DOI] [PubMed] [Google Scholar]
- Sokolove P. G., Cooke I. M. Inhibition of impulse activity in a sensory neuron by an electrogenic pump. J Gen Physiol. 1971 Feb;57(2):125–163. doi: 10.1085/jgp.57.2.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stevens C. F. Inferences about membrane properties from electrical noise measurements. Biophys J. 1972 Aug;12(8):1028–1047. doi: 10.1016/S0006-3495(72)86141-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Talbot W. H., Darian-Smith I., Kornhuber H. H., Mountcastle V. B. The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. J Neurophysiol. 1968 Mar;31(2):301–334. doi: 10.1152/jn.1968.31.2.301. [DOI] [PubMed] [Google Scholar]
- Verveen A. A., DeFelice L. J. Membrane noise. Prog Biophys Mol Biol. 1974;28:189–265. doi: 10.1016/0079-6107(74)90019-4. [DOI] [PubMed] [Google Scholar]
