Skip to main content
Log in

Recurrent inhibition: Its influence upon transduction and afferent discharges in slowly-adapting stretch receptor organs

  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

The crayfish stretch receptor organs provide the opportunity to study recurrent inhibition (RI) in pure experimental conditions. The slowly adapting organ (SAO) from the cephalothoraxabdomen joint of Procambarus darkii was isolated and its length set by anchoring one end and clamping the other with a movable forceps. Each impulse from the SAO triggered a shock to the common inhibitory fiber, after an adjustable delay called “phase”. Thus, RI acted upon the SAO. Under steady length conditions, the discharge rate with RI was proportional to the spontaneous discharge rate (i.e. to that without RI), and negatively correlated to the ratio of the phase to the spontaneous interspike interval. Under dynamic conditions, with the SAO submitted to under 0.3 mm length variations, sine-like with or without “white” noise, and periodic at 0.2, 1.0, or 3.0 cps, the effect of RI was basically the same in all conditions. While the lower rates of discharge were unchanged, the higher rates were reduced: thus the overall sensitivity of the SAO was decreased. The RI also decreased the discharge variability at the low rates; variability remained unaffected at the high rates. The general form of the response of the SAO was unaffected by RI, as indicated by displays of rate versus length, of rate versus velocity, or of change in rate versus velocity: only the widness of the loops changed. The effects of RI were compared to those of randomly arriving, Poisson-like IPSP's at the same overall rate: the latter did not exhibit the same dependence on the SAO firing rate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adam, D., Windhorst, U., Inbar, G.F.: The effects of recurrent inhibition on the cross correlated firing patterns of motoneurons (and their relations to signal transmission in the spinal cord-muscle channel). Biol. Cybernetics 29, 229–235 (1978)

    Google Scholar 

  • Alexandrowicz, J.S.: Receptor organs in thoracic and abdominal muscles of crustacean. Biol. Rev. 42, 288–326 (1967)

    Google Scholar 

  • Brooks, V.B., Wilson, V.J.: Recurrent inhibition in the cat's spinal cord. J. Physiol. (London) 146, 380–391 (1959)

    Google Scholar 

  • Buño, W., Fuentes, J., Segundo, J.P.: Crayfish stretch receptor organs: Effects of length-steps with and without perturbations. Biol. Cybernetics 31, 99–110 (1978)

    Google Scholar 

  • Cleveland, S., Ross, H.G.: Dynamic properties of Renshaw cells: Frequency response characteristics. Biol. Cybernetics 27, 175–184 (1977)

    Google Scholar 

  • Eccles, J.C., Fatt, P., Koketsu, K.: Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J. Physiol. (London) 126, 524–562 (1954)

    Google Scholar 

  • Eccles, J.C., Eccles, R.M., Iggo, A., Ito, M.: Distribution of recurrent inhibition among motoneurones. J. Physiol. (London) 159, 479–499 (1961)

    Google Scholar 

  • Eccles, J.C., Eccles, R.M., Iggo, A., Lundberg, A.: Electrophysiological investigation of Renshaw cells. J. Physiol. (London) 159, 461–478 (1978)

    Google Scholar 

  • Eckert, R.O.: Reflex relationships of the abdominal stretch receptors of the crayfish. I Feedback inhibition of the receptors. J. Cell. Comp. Physiol. 57, 149–162 (1961a)

    Google Scholar 

  • Eckert, R.O.: Reflex relationships of the abdominal stretch receptors of the crayfish. II Stretch receptor involvement during the swimming reflex. J. Cell. Comp. Physiol. 57, 163–174 (1961b)

    Google Scholar 

  • Firth, D.R.: Interspike interval fluctuations in the crayfish stretch receptor. Biophys. J. 6, 201–215 (1966)

    Google Scholar 

  • Gelfand, I.M., Gurfinkel, V.S., Kots, Y.M., Tsetlin, M.C., Shik, M.L.: Synchronization of motor units and associated model concepts. Biofizika 8, 475–486 (1963)

    Google Scholar 

  • Granit, R.: Regulation of discharge rate by inhibition, especially by recurrent inhibition. In: Nervous inhibition, Florey, E. (ed.), p. 61. Oxford: Pergamon Press 1961

    Google Scholar 

  • Granit, R.: Recurrent inhibition as a mechanism of control. Progress in Brain Research, Vol. 1: Brain mechanisms, p. 23. Moruzzi, G., Fessard, A., Jasper, H.H. (eds.). Amsterdam: Elsevier 1963

    Google Scholar 

  • Granit, R.: The basis of motor control. London, New York: Academic Press 1970

    Google Scholar 

  • Granit, R., Maase, J., Haase, J., Rutledge, L.T.: Recurrent inhibition in relation to frequency of firing and limitation of discharge rate of extensor motoneurones. J. Physiol. (London) 154, 308–328 (1960)

    Google Scholar 

  • Granit, R., Renkin, B.: Net depolarization and discharge rate of motoneurones, as measured by recurrent inhibition. J. Physiol. (London) 158, 461–475 (1961)

    Google Scholar 

  • Granit, R., Rutledge, L.T.: Surplus excitation in reflex action of motoneurones as measured by recurrent inhibition. J. Physiol. (London) 154, 238–307 (1960)

    Google Scholar 

  • Harris, D.A.: Data processing in the cat motoneuron system: Averaging functions and rate limitation. Kybernetik 16, 45–52 (1974)

    Google Scholar 

  • Jansen, J.K.S., Njå, A., Walløe, L.: Inhibitory control of the abdominal stretch receptors of the crayfish. II Reflex input, segmental distribution and output relations. Acta Physiol. Scand. 80, 443–449 (1970a)

    Google Scholar 

  • Jansen, J.K.S., Njå, A., Ormstad, K., Walløe, L.: Inhibitory control of the abdominal stretch receptors of the crayfish. III The accessory reflex as a recurrent inhibitory feed-back. Acta Physiol. Scand. 80, 472–483 (1970b)

    Google Scholar 

  • Kuffler, S.W., Eyzaguirre, C.: Synaptic inhibition in an isolated nerve cell. J. Gen. Physiol. 39, 155–184 (1955)

    Google Scholar 

  • MacGregor, R.J., Lewis, E.R.: Neural modelling. London: Plenum Press 1977

    Google Scholar 

  • MacGregor, R.J., MacMullen, T.: Computer simulation of diffusely connected neuronal populations. Biol. Cybernetics 28, 121–127 (1978)

    Google Scholar 

  • Meyer-Lohmann, J., Henatsch, H.D., Beneck, E.R., Hellweg, C.: Muscle stretch and chemical muscle spindle excitation: Effects on Renshaw cells and efficiency of recurrent inhibition. In: Progress in Brain Research, Vol. 44: Understanding the stretch reflex, p. 223. Homma, S. (ed.). Amsterdam: Elsevier 1976

    Google Scholar 

  • Perkel, D.H., Schulman, J., Bullock, T.H., Moore, G.P., Segundo, J.P.: Pacemaker neurons: Effects of regularly spaced synaptic input. Science 145, 61–63 (1964)

    Google Scholar 

  • Rakic, P.: Local circuit neurons. Bull. Neurosci. Res. Prog. 13, 291–446 (1975)

    Google Scholar 

  • Rall, W., Shepherd, G.M., Reese, T.S., Brightman, M.W.: Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp. Neurol. 14, 44–56 (1966)

    Google Scholar 

  • Roberts, W.J., Rosenthal, N.P., Terzuolo, C.A.: A control model of stretch reflex. J. Neurophysiol. 34, 620–634 (1971)

    Google Scholar 

  • Segundo, J.P., Perkel, D.H.: The nerve cell as an analyser of spike train. UCLA Forum in Medical Sciences, No. 11: The interneuron. Brazier, M.A.B. (ed.). Berkeley, Los Angeles: University of California Press 1969

    Google Scholar 

  • Segundo, J.P., Tolkunov, B.F., Wolfe, G.E.: Regulation between trains of action potentials across an inhibitory synapse. Influence of presynaptic irregularity. Biol. Cybernetics 24, 169–179 (1976)

    Google Scholar 

  • Shepherd, G.M.: Synaptic organization of the brain. Oxford: University Press 1974

    Google Scholar 

  • Snedecor, G.W., Cochran, W.G.: Statistical methods. Ames, Iowa: Iowa State University Press 1976

    Google Scholar 

  • Thom, R.: Stabilité structurelle et morphogenèse. Massachussets, WA: Benjamin 1972

    Google Scholar 

  • Tuckwell, H.C.: Recurrent inhibition and after hyperpolarization effects on neuronal discharge. Biol. Cybernetics 30, 115–123 (1978)

    Google Scholar 

  • Vibert, J.F., Segundo, J.P.: Slowly-adapting stretch-receptor organs: Periodic stimulation with and without perturbations. Biol. Cybernetics 33, 81–95 (1979)

    Google Scholar 

  • Windhorst, U., Adam, D., Inbar, G.F.: The effects of recurrent inhibitory feed-back in shapping discharge patterns of motoneurons excited by phasic muscle stretches. Biol. Cybernetics 29, 221–227 (1978)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by grants from NIH and NSF

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vibert, J.F., Davis, M. & Segundo, J.P. Recurrent inhibition: Its influence upon transduction and afferent discharges in slowly-adapting stretch receptor organs. Biol. Cybernetics 33, 167–178 (1979). https://doi.org/10.1007/BF00337295

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00337295

Keywords

Navigation