Skip to main content
Log in

Dynamic behaviour of α motoneurone sub-pools subjected to inhomogeneous Renshaw cell inhibition

  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

The spinal α-motoneurone-Renshaw cell system was simulated by a meshed system of three principal negative feedback loops interconnected via “cross”-feedback pathways. Three types of α-motoneurone (MN): S-type, FR-type, and FF-type MNs, and their differing connections to and from Renshaw cells (RCs) were taken into account. The dynamic behaviour of RCs was taken from data provided by Cleveland and Ross (1977) and assumed to be given by a transfer function with one zero and two poles whose time constants τi depended on the overall amount of excitatory input to RCs. Also, the static gain of recurrent inhibition was taken to decrease with increasing excitatory input from α-MN axon collaterals (Cleveland et al., 1981) and to be depressed by spinally descending motor command signals. S-type MNs as well as F-type MNs were assumed to have high-pass characteristics though with slightly different cut-off frequencies. The closed-loop frequency responses of each sub-pool of MNs, S, FR, and FF, at three different levels of recruitment of these sub-pools, were calculated and shown to change significantly with recruitment level. These changes were essentially due to two reasons: firstly, to the general reduction of static gains within the recurrent inhibitory pathways with increasing motor output (recruitment), and secondly, to the increasing complexity of the whole network by recruitment of each new MN type. The particularly strong effect of the latter factor could easily be demonstrated by a comparison of the frequency responses of the MN types when these were, firstly, integrated into the network at their particular level of recruitment, and when they were, secondly, hypothetically assumed “isolated” from the remaining network, i.e., when subjected only to “self-inhibition”, the cross-inhibitory links to other MN types being cut. These results illustrate that the dynamic behaviour of α-MNs submitted to an inhomogeneously distributed recurrent and variable inhibition are not invariant, but depend upon the variable characteristics of a complex MN-RC network. This suggests that an important physiological function of recurrent inhibition via Renshaw cells, particularly of its inhomogeneous distribution, may be to adjust the dynamic MN sensitivity to the particular requirements prevailing at different motor output levels.

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

  • Baldissera, F., Campadelli, P., Piccinelli, L.: Cat motoneurones responsiveness to static and dynamic components of input signals analyzed by intracellular injections of synusoidal currents. Neurosci. Lett. Suppl. 3, 94 (1979)

    Google Scholar 

  • Baldissera, F., Campadelli, P., Piccinelli, L.: Neural encoding of input transients investigated by intracellular injection of ramp currents in cat α-motoneurones. J. Physiol. (London) 328, 73–86 (1982)

    Google Scholar 

  • Baldissera, F., Parmiggiani, F.: Relevance of motoneuronal firing adaptation to tension development in the motor unit. Brain Res. 91, 315–320 (1975)

    Google Scholar 

  • Barrett, J.N., Crill, W.E.: Specific membrane properties of cat motoneurones. J. Physiol. (London) 239, 301–324 (1974)

    Google Scholar 

  • Benecke, R., Boettcher, U., Henatsch, H.-D., Meyer-Lohmann, J., Schmidt, J.: Recurrent inhibition of individual Ia inhibitory interneurones and disinhibition of their target α-motoneurones during muscle stretches. Exp. Brain Res. 23, 13–28 (1975)

    Google Scholar 

  • Burke, R.E.: The role of synaptic organization in the control of motor unit activity during movement. In: Reflex control of posture and movement, Granit, R., Pompeiano, O. (eds.), pp. 61–67. (Progress in brain research, Vol. 50) Amsterdam: Elsevier 1979

    Google Scholar 

  • Burke, R.E.: Motor unit types: functional specializations in motor control. TINS 3, 255–258 (1980)

    Google Scholar 

  • Burke, R.E., Rymer, W.Z., Walsh, J.V., Jr.: Relative strength of synaptic input from short-latency pathways to motor units of defined type in the cat medial gastrocnemius. J. Neurophysiol. 39, 447–458 (1976)

    Google Scholar 

  • Cleveland, S.: Dynamische Eigenschaften der Renshaw-Zellen. Math.-Nat. Diss., Düsseldorf 1977

  • Cleveland, S.: Verarbeitung spinal-motorischer Ausgangssignale durch die Renshaw-Zellen. Med. Habil.-Schrift, Dusseldorf 1980

  • Cleveland, S., Kuschmierz, A., Ross, H.-G.: Static input-putput relations in the spinal recurrent inhibitory pathway. Biol. Cybern. 40, 223–231 (1981)

    Google Scholar 

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

    Google Scholar 

  • Cullheim, S., Kellerth, J.-O.: A morphological study of the axons and recurrent axon collaterals of cat α-motoneurones supplying different functional types of muscle unit. J. Physiol. (London) 281, 301–313 (1978)

    Google Scholar 

  • De Luca, C.J., LeFever, R.S., McCue, M.P., Xenakis, A.P.: Behaviour of human motor units in different muscles during linearly varying contractions. J. Physiol. (London) 329, 113–128 (1982)

    Google Scholar 

  • Evinger, C., Baker, R., McCrea, R.A.: Axon collaterals of cat medial rectus motoneurons. Brain Res. 174, 153–160 (1979)

    Google Scholar 

  • Ellaway, P.H., Murphy, P.R.: A comparison of the recurrent inhibition of α- and γ-motoneurones in the cat. J. Physiol. (London) 315, 43–58 (1981)

    Google Scholar 

  • Fleshman, J.W., Munson, J.B., Sypert, G.W., Friedman, W.A.: Rheobase, input resistance, and motor-unit type in medial gastrocnemius motoneurons in the cat. J. Neurophysiol. 46, 1326–1338 (1981)

    Google Scholar 

  • Freund, H.J., Buedingen, H.J., Dietz, V.: The activity of single motor units from human forearm muscles during voluntary isometric contractions. J. Neurophysiol. 38, 933–946 (1975)

    Google Scholar 

  • Friedman, W.A., Sypert, G.W., Munson, J.B., Fleshman, J.W.: Recurrent inhibition in type-identified motoneurons. J. Neurophysiol. 46, 1349–1359 (1981)

    Google Scholar 

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

    Google Scholar 

  • Gydikov, A., Kosarov, D.: Some features of different motor units in human biceps brachii. Pflügers Arch. 347, 75–88 (1974)

    Google Scholar 

  • Haase, J., Cleveland, S., ross, H.-G.: Problems of postsynaptic autogenous and recurrent inhibition in the mammalian spinal cord. Rev. Physiol. Biochem. Pharmacol. 73, 73–129 (1975)

    Google Scholar 

  • Hellweg, C., Meyer-Lohmann, J., Benecke, R., Windhorst, U.: Response of Renshaw cell to muscle ramp stretch. Exp. Brain Res. 21, 353–360 (1974)

    Google Scholar 

  • Hultborn, H.: Convergence on interneurones in the reciprocal Ia inhibitory pathway to motoneurones. Acta Physiol. Scand. Suppl. 375, 3–42 (1972)

    Google Scholar 

  • Hultborn, H., Lindstroem, S., Wigstroem, H.: On the function of recurrent inhibition in the spinal cord. Exp. Brain Res. 37, 399–403 (1979)

    Google Scholar 

  • Hultborn, H., Pierrot-Deseilligny, E.: Changes in recurrent inhibition during voluntary soleus contractions in man studied by an H-reflex technique. J. Physiol. (London) 297, 229–251 (1979a)

    Google Scholar 

  • Hultborn, H., Pierrot-Deseilligny, E.: Input-output relations in the pathway of recurrent inhibition to motoneurones in the cat. J. Physiol. (London) 297, 267–287 (1979b)

    Google Scholar 

  • Hultborn, H., Pierrot-Deseilligny, E., Wigstroem, H.: Recurrent inhibition and after hyperpolarization following motoneuronal discharge in the cat. J. Physiol. (London) 297, 253–266 (1979)

    Google Scholar 

  • Kato, M., Fukushima, K.: Effect of differential blocking of motor axons on antidromic activation of Renshaw cells in the cat. Exp. Brain Res. 20, 135–143 (1974)

    Google Scholar 

  • Kernell, D.: Input resistance, electrical excitability, and size of ventral horn cells in cat spinal cord. Science 152, 1637–1640 (1966)

    Google Scholar 

  • Kernell, D., Zwaagstra, B.: Input conductance, axonal conduction velocity, and cell size among hindlimb motoneurones of the cat. Brain Res. 204, 311–326 (1981)

    Google Scholar 

  • Kirkwood, P.A., Sears, T.A., Westgaard, R.H.: Recurrent inhibition of intercostal motoneurones in the cat. J. Physiol. (London) 319, 111–130 (1981)

    Google Scholar 

  • Koehler, W., Schomburg, E.D., Steffens, H.: Switching function of Renshaw cells during fictive locomotion? Pflügers Arch. 389, R26 (1981)

  • Koehler, W., Windhorst, U., Schmidt, J., Meyer-Lohmann, J., Henatsch, H.-D.: Diverging influences on Renshaw cells and monosynaptic reflexes from stimulation of capsula interna. Neurosci. Lett. 8, 35–39 (1978)

    Google Scholar 

  • Kukulka, C.G., Clamann, H.P.: Comparison of the recruitment and discharge properties of motor units in human brachial biceps and adductor pollicis during isometric contractions. Brain Res. 219, 45–55 (1981)

    Google Scholar 

  • Lindstroem, S.: Recurrent control from motor axon collaterals of Ia inhibitory pathways in the spinal cord of the cat. Acta Physiol. Scand. Suppl. 392, 1–43 (1973)

    Google Scholar 

  • Lindstroem, S., Schomburg, E.D.: Recurrent inhibition from motor axon collaterals of ventral spinocerebellar tract neurons. Acta Physiol. Scand. 88, 505–515 (1973)

    Google Scholar 

  • McCrea, D.A., Pratt, C.A., Jordan, L.M.: Renshaw cell activity and recurrent effects on motoneurons during fictive locomotion. J. Neurophysiol. 44, 475–488 (1980)

    Google Scholar 

  • Miller, S., Scott, P.D.: The spinal locomotor generator. Exp. Brain Res. 30, 387–403 (1977)

    Google Scholar 

  • Milner-Brown, H.S., Stein, R.B., Yemm, R.: Changes in firing rate of human motor units during linearly changing voluntary contractions. J. Physiol. (London) 230, 371–390 (1973)

    Google Scholar 

  • Pompeiano, O., Wand, P., Sontag, K.-H.: Response of Renshaw cells to sinusoidal stretch of hindlimb extensor muscles. Arch. Jtal. Biol. 113, 92–117 (1975a)

    Google Scholar 

  • Pompeiano, O., Wand, P., Sontag, K.-H.: The sensitivity of Renshaw cells to velocity of sinusoidal stretches of the triceps surae muscle. Arch. Jtal. Biol. 113, 280–294 (1975b)

    Google Scholar 

  • Ross, H.-G.: Experimentelle Untersuchungen und Modellvorstellungen zur quantitativen Charakterisierung der rekurrenten Inhibition spinaler α-Mononeurone. Med. Habil.-Schrift, Düsseldorf 1976

  • Ross, H.G., Cleveland, S., Haase, J.: Contribution of single motoneurons to Renshaw cell activity. Neurosci. Lett. 1, 105–108 (1975)

    Google Scholar 

  • Ryall, R.W.: Renshaw cell mediated inhibition of Renshaw cells: patterns of excitation and inhibition from impulses in motor axon collaterals. J. Neurophysiol. 33, 257–270 (1970)

    Google Scholar 

  • Ryall, R.W.: Patterns of recurrent excitation and mutual inhibition of cat Renshaw cells. J. Physiol. (London) 316, 439–452 (1981)

    Google Scholar 

  • Ryall, R.W., Piercey, M.F., Polosa, C., Goldfarb, J.: Excitation of Renshaw cells in relation to orthodronic and antidromic excitation of motoneurons. J. Neurophysiol. 35, 137–148 (1972)

    Google Scholar 

  • Sasaki, K.: Electrophysiological studies on oculomotor neurons of the cat. Jpn. J. Physiol. 13, 287–302 (1963)

    Google Scholar 

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

    Google Scholar 

  • van Keulen, L.: Autogenetic recurrent inhibition of individual spinal motoneurons of the cat. Neurosci. Lett. 21, 297–300 (1981)

    Google Scholar 

  • Wenstoep, F., Rudjord, T.: Recurrent Renshaw inhibition studied by digital simulation. In: Proceedings of the first European Biophysics Congress, Vol. 5, Broda, E., Locker, A., Springer-Lederer, H. (eds.), pp. 365–369. Wien: Verlag der Wiener Medizinischen Akademie 1971

    Google Scholar 

  • Windhorst, U.: Auxiliary spinal networks for signal focussing in the segmental stretch reflex system. Biol. Cybern. 34, 125–135 (1979)

    Google Scholar 

  • Windhorst, U., Ptok, M., Meyer-Lohmann, J., Schmidt, J.: Effects of conditioning stimulation of the contralateral N. ruber on antidramic Renshaw cell responses and monosynaptic reflexes. Pflügers Arch. 373, R 70 (1978)

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Windhorst, U., Koehler, W. Dynamic behaviour of α motoneurone sub-pools subjected to inhomogeneous Renshaw cell inhibition. Biol. Cybern. 46, 217–228 (1983). https://doi.org/10.1007/BF00336803

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00336803

Keywords

Navigation