Decorrelating actions of renshaw interneurons on the firing of spinal motoneurons within a motor nucleus: A simulation study

Journal of Neurophysiology

Volumn 80, Issue 1, 1998, Pages 309-323

  Maltenfort, Mitchell G ^a,c   Heckman, C J ^b   Rymer, W Zev ^a  

^a Northwestern University   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c BARROW NEUROLOGICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CORTICAL SYNCHRONIZATION; INTERNEURON; MOTONEURON NUCLEUS; NERVE CELL EXCITABILITY; PRIORITY JOURNAL; RENSHAW CELL; SIMULATION; SPINAL CORD MOTONEURON;

EID: 0031869648     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1998.80.1.309     Document Type: Article

References (79)

1. ADAM, D., WINDHORST, U., AND INBAR, G. F. The effects of recurrent inhibition on the cross-correlated firing patterns of motoneurones (and their relation to signal transmission in the spinal cord-muscle channel). Biol. Cybern. 29: 229-235, 1978.
2. AKAZAWA, K. AND KATO, K. Neural network model for control of muscle force based on the size principle of motor unit. Proc. IEEE 78: 1531-1535, 1990.
3. ALLUM, J.H.J., DIETZ, V., AND FREUND, H.-J. Neuronal mechanisms underlying physiological tremor. J. Neurophysiol. 41: 557-571, 1978.
4. ANDREASSEN, S. AND ROSENFALCK, A. Regulation of the firing pattern of single motor units. J. Neurol. Neurosurg. Psychiatry 43: 897-906, 1980.
5. BALDISSERA, F., HULTBORN, H., AND ILLERT, 1. Integration in spinal neuronal systems. In: Handbook of Physiology. The Nervous System. Motor Control. Bethesda, MD: Am. Physiol. Soc., 1981, sect. 1, vol. II, chapt. 12, p. 509-595.
6. BENDAT, J. S. AND PIERSOL, A. G. Random Data (2nd ed.). New York: John Wiley, 1986.
7. BROOKS, V. B. AND WILSON, V. J. Recurrent inhibition in the cat's spinal cord. J. Physiol. (Lond.) 146: 380-391, 1959.
8. BURKE, R. E. Motor units: anatomy, physiology and functional organization. In: Handbook of Physiology. The Nervous System. Motor Control. Bethesda, MD: Am. Physiol. Soc., 1981, sect. 1, vol. II, chapt. 10, p. 345-422.
9. CHRISTAKOS, C. N. The mathematical basis of population rhythms in nervous and neuromuscular systems. Int. J. Neurosci 29: 103-107, 1986.
10. CHRISTAKOS, C. N., WINDHORST, U., RISSING, R., AND MEYER-LOHMANN, J. Frequency response of spinal Renshaw cells activated by stochastic motor axon stimulation. Neuroscience 23: 613-623, 1987.
11. CLEVELAND, S., KUSCHMIERZ, A., AND ROSS, H.-G. Static input-output relations in the spinal recurrent inhibitory pathway. Biol. Cybern. 40: 223-231, 1981.
12. CULLHEIM, S. AND KELLERTH, J.-O. A morphological study of the axons and recurrent collaterals of cat α-motoneurones supplying different functional types of muscle unit. J. Physiol. (Lond.) 281: 301-313, 1978.
13. CULLHEIM, S. AND KELLERTH, J.-O. Two kinds of recurrent inhibition of cat spinal α-motoneurones as differentiated pharmacologically. J. Physiol. (Lond.) 312: 209-224, 1981.
14. CURTIS, D. R. AND ECCLES, R. M. The excitation of Renshaw cells by pharmacological agents applied electrophoretically. J. Physiol. (Lond.) 141: 435-445, 1958.
15. CURTIS, D. R., GAME, C.J.A., LODGE, D., AND MCCULLOCH, R. M. A pharmacological study of Renshaw cell inhibition. J. Physiol. (Lond.) 258: 227-242, 1976.
16. CURTIS, D. R. AND RYALL, R. W. The excitation of Renshaw cells by cholinomimetics. Exp. Brain Res. 2: 49-65, 1966a.
17. CURTIS, D. R. AND RYALL, R. W. The acetylcholine receptors of Renshaw cells. Exp. Brain Res. 2: 66-80, 1966b.
18. CURTIS, D. R. AND RYALL, R. W. The synaptic excitation of Renshaw cells. Exp. Brain Res. 2: 81-86, 1966c.
19. DELUCA, C. J. AND ERIM, Z. Common drive of motor units in regulation of muscle force. Trends Neurosci. 17: 299-305, 1994.
20. DIETZ, V., BISCHOFBERGER, E., WITA, C., AND FREUND, H.-J. Correlation between the discharges of two simultaneously recorded motor units and physiological tremor. EEG Clin. Neurophysiol. 40: 97-105, 1976.
21. ECCLES, J .C., ECCLES, R. M., IGGO, A., AND ITO, M. Distribution of recurrent inhibition among motoneurones. J. Physiol. (Lond.) 159: 479-499, 1961.
22. ECCLES, J. C., FATT, P., AND KOKETSU, K. Cholingergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J. Physiol. (Lond.) 126: 524-562, 1954.
23. FRIEDMAN, W. A., SYPERT, G. W., MUNSON, J. B., AND FLESHMAN, J. W. Recurrent inhibition in type-identified motoneurones. J. Neurophysiol. 46: 1349-1359, 1981.
24. FYFFE, R.E.W., ALVAREZ, F. J., AND HARRINGTON, D. Differential distribution of glycine receptors on interneurones. Proc. 23rd Annu. Meet. Soc. Neurosci. Washington, DC, 1993, p. 983.
25. GRANIT, R., HAASE, J., AND RUTLEDGE, L. T. Recurrent inhibition in relation to frequency of firing and limitation of discharge rate of extensor motoneurones. J. Physiol. (Lond.) 158: 461-475, 1960.
26. GRANIT, R. AND RENKIN, B. Net depolarization and discharge rate of motoneurones, as measured by recurrent inhibition. J. Physiol. (Lond.) 158: 461-475, 1961.
27. GUSTAFFSON, B. AND PINTER, M. J. An investigation of threshold properties among cat spinal α-motoneurones. J. Physiol. (Lond.) 357: 453-483, 1984.
28. HAASE, J. AND VAN DER MUELEN, J. P. Effects of supraspinal stimulation on Renshaw cells belonging to extensor motoneurones. J. Neurophysiol. 24: 510-520, 1961.
29. HAMM, T. M., SASAKI, S., STUART, D. G., WINDHORST, U., AND YUAN, C.-S. Distribution of single-axon recurrent inhibitory post-synaptic potentials in the cat. J. Physiol. (Lond.) 388: 631-651, 1987a.
30. HAMM, T. M., SASAKI, S., STUART, D. G., WINDHORST, U., AND YUAN, C.-S. The measurement of single motor-axon recurrent inhibitory post-synaptic potentials in a single spinal motor nucleus in the cat. J. Physiol. (Lond.) 388: 653-664, 1987b.
31. HARRISON, L. M., IRONTON, R., AND STEPHENS, J. A. Cross-correlation analysis of multi-unit EMG recordings in man. J. Neurosci. Methods 40: 171-179, 1991.
32. HECKMAN, C. J. AND BINDER, M. D. Computer simulation of the steady-state input-output function of the cat medial gastrocnemius motoneuron pool. J. Neurophysiol. 65: 952-967, 1991.
33. HECKMAN, C. J. AND BINDER, M. D. Computer simulation of motor unit firing rate modulation. J. Neurophysiol. 69: 1005-1008, 1993.
34. HENNEMAN, E. AND MENDELL, L. M. Functional organization of motoneuron pool and its inputs. In: Handbook of Physiology. The Nervous System. Motor Control. Bethesda, MD: Am. Physiol. Soc., 1981, sect. 1, vol. II, part 1, p. 423-507.
35. HOUR, J. C. AND RYMER, W. Z. Neural control of muscle length and tension. In: Handbook of Physiology. The Nervous System. Motor Control, Bethesda, MD: Am. Physiol. Soc., 1981, sect. 1, vol. II, chapt. 8, p. 257-323.
36. HOUNSGAARD, J., HULTBORN, H., JESPERSEN, B., AND KIEHN, O. Bistability of α-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J. Physiol. (Lond.) 405: 345-367, 1988.
37. HULTBORN, H., KATZ, R., AND MACKEL, R. Distribution of recurrent inhibition within a motor nucleus. II. Amount of recurrent inhibition in motoneurones to slow and fast units. Acta Physiol. Scand. 134: 363-374, 1988a.
38. HULTBORN, H., LINDSTRÖM, S., AND WIGSTRÖM, H. On the function of recurrent inhibition in the spinal cord. Exp. Brain Res. 37: 399-403, 1979a .
39. HULTBORN, H., LIPSKI, J., MACKEL, R., AND WIGSTRÖM, H. Distribution of recurrent inhibition within a motor nucleus. I. Contribution from slow and fast motor units to the excitation of Renshaw cells. Acta Physiol. Scand. 134: 347-361, 1988b.
40. HULTBORN, H. AND PEIRROT-DESEILLGNY, E. Input-output relations in the pathway of recurrent inhibition to motoneurones in the cat. J. Physiol. (Lond.) 297: 267-287, 1979.
41. HULTBORN, H., PEIRROT-DESEILLGNY, E., AND WIGSTRÖM, H. Recurrent inhibition and afterhyperpolarization following motoneuronal discharge in the cat. J. Physiol. (Lond.) 297: 253-266, 1979b.
42. ILLERT, M., KUMMEL, H., AND SCOTT, J. J. Beta innervation and recurrent inhibition: a hypothesis for manipulatory and postural control. Pflügers Arch. 432: R61-67, 1996.
43. JANKOWSKA, E. AND SMITH, D. O. Antidromic activation of Renshaw cells and their axonal projections. Acta Physiol. Scand. 88: 198-214, 1973.
44. KANEKO, T., HIDEKI, O., AND FUKUDA, H. Enhancement of recurrent inhibition of the spinal monosynaptic reflex by preceding stimulation of the medullary raphe in rats. Brain Res. 417: 403-407, 1987.
45. KERNELL, D. Rhythmic properties of motoneurones innervating muscle fibres of different speed in m. gastrocnemius medialis of the cat. Brain Res., 160: 159-162, 1979.
46. KERNELL, D. Functional properties of spinal motoneurones and gradation of muscle force. In: Advances in Neurology, Motor Control Mechanisms in Health and Disease, edited by J. E. Desmedt. New York: Raven Press, 1983, vol. 39, p. 213-216.
47. KOEHLER, W. AND WINDHORST, U. Responses of the spinal α-motoneuron-Renshaw cell system to various differentially distributed segmental afferent and descending inputs. Biol. Cybern. 51: 417-426, 1985.
48. KOKKOROYANNIS, T., LAOURIS, Y., MEYER-LOHMANN, J., AND WINDHORST, U. Early and late components in cat Renshaw cell responses to random stimulation of motor axons: their differential sensitivity to preceding activation. Neuroscience 30: 651-661, 1989.
49. LAGERBÄCK, P.-Å. AND KELLERTH, J.-O. Light microscopic observations on cat Renshaw cells after intracellular staining with horseradish peroxidase. I. The axonal systems. J. Comp. Neurol. 240: 359-367, 1985a.
50. LAGERBÄCK, P.-Å. AND KELLERTH, J.-O. Light microscopic observations on cat Renshaw cells after intracellular staining with horseradish peroxidase. II. The cell bodies and dendrites. J. Comp. Neurol. 240: 368-376, 1985b.
51. LINDSAY, A. AND BINDER, M. D. Distribution of effective synaptic currents underlying recurrent inhibition in cat triceps surae motoneurones. J. Neurophysiol. 65: 168-177, 1991.
52. MACGREGOR, R. J. Neural and Brain Modeling. San Diego, Academic Press, 1987.
53. MACGREGOR, R. J. AND OLIVER, R. M. A model for repetitive firing in neurons. Kybernetik 16: 53-64, 1974.
54. MARMARELIS, P. Z. AND MARMARELIS, V. Z. Analysis of Physiological Systems: The White Noise Approach. New York: Plenum Press, 1978.
55. MORALES, F. R., ENGELHARDT, J. K., PEREDA, A. E., YAMUY, J., AND CHASE, M. H. Renshaw cells are inactive during motor inhibition elicited by the pontine microinjection of carbachol. Neurosci. Lett. 86: 289-295, 1988.
56. PAPOULIS, A. Probability, Random Variables, and Stochastic Processes. New York: McGraw-Hill, 1984.
57. POWERS, R.K.D.B. AND BINDER, M. D. Experimental evaluation of input-output models of motoneuron discharge. J. Neurophysiol. 75: 367-379, 1996.
58. PROCHAZKA, A. Proprioceptive feedback and movement regulation. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, chapt. 3, p. 89-127.
59. RACK, P.M.H. AND WESTBURY, D. R. The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J. Physiol. (Lond.) 204: 443-460, 1969.
60. REDMAN, S. J. AND LAMPARD, D. G. Monosynaptic stochastic stimulation of spinal motoneurones in the cat. Nature 216: 921-922, 1967.
61. RENSHAW, B. Central effects of centripetal impulses in axons of spinal ventral roots. J. Neurophysiol. 9: 191-204, 1946.
62. ROMANES, G. J. The motor cell columns of the lumbo-sacral spinal cord of the cat. J. Comp. Neurol. 94: 313-363, 1951.
63. ROSS, H.-G., CLEVELAND, S., AND HAASE, J. Quantitative relation of Renshaw cell discharges to monosynaptic reflex height. Pflügers Arch. 332: 73-79, 1972.
64. ROSS, H.-G., CLEVELAND, S., AND KUSCHMIERZ, A. Dynamic properties of Renshaw cells: equivalence of responses to step changes in recruitment and discharge frequency of motor axons. Pflügers Arch. 394: 239-242, 1982.
65. 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.
66. RYALL, R. W. Patterns of recurrent excitation and mutual inhibition of cat Renshaw cells. J. Physiol. (Lond.) 316: 439-452, 1981.
67. RYALL, R. W., PIERCEY, M. F., AND POLOSA, C. Intersegmental and intrasegmental distribution of mutual inhibition of Renshaw cells. J. Neurophysiol. 34: 700-707, 1971.
68. RYALL, R. W., PIERCEY, M. F., POLOSA, C., AND GOLDFARB, J. Excitation of Renshaw cells in relation to orthodromic and antidromic excitation of motoneurones. J. Neurophysiol. 35: 137-148, 1972.
69. SCHWINDT, P. C. Membrane-potential trajectories underlying motoneuron rhythmic firing at high rates. J. Neurophysiol. 36: 434-439, 1973.
70. SCHWINDT, P. C. AND CALVIN, W. H. Nature of conductances underlying rhythmic firing in cat spinal motoneurons. J. Neurophysiol. 36: 955-973, 1973.
71. STEIN, R. B. AND OGUZTÖRELI, M. N. Motoneuron: modification of muscle responses by spinal circuitry. Neuroscience 11: 231-240, 1984.
72. VAN KUELEN, L.C.M. Autogenetic recurrent inhibition of individual spinal motoneurones of the cat. Neurosci. Lett. 21: 297-300, 1981.
73. WALMSLEY, B. AND TRACEY, D. J. An intracellular study of Renshaw cells. Brain Res. 223: 170-175, 1981.
74. WINDHORST, U. How Brain-Like is the Spinal Cord? New York: Springer-Verlag, 1988.
75. WINDHORST, U. Do Renshaw cells tell spinal neurones how to interpret muscle spindle signals? Prog. Brain Res. 80: 283-294, 1989.
76. WINDHORST, U. Activation of Renshaw cells. Prog. Neurobiol. 35: 135-179, 1990.
77. WINDHORST, U., ADAM, D., AND INBAR, G. F. The effects of recurrent inhibitory feedback in shaping discharge patterns of motoneurones excited by phasic muscle stretches. Biol. Cybern. 29: 221-227, 1978.
78. WINDHORST, U. AND KOKKOROYIANNIS, T. Interaction of recurrent inhibitory and muscle spindle afferent feedback during muscle fatigue. Neuroscience 43: 249-259, 1991.
79. ZENGEL, J. E., REED, S. A., SYPERT, G. W., AND MUNSON, J. B. Membrane electrical properties and prediction of motor-unit type of medial gastrocnemius motoneurones in the cat. J. Neurophysiol. 53: 1323-1344, 1985.