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. 1993 Apr;463:307–324. doi: 10.1113/jphysiol.1993.sp019596

Matching between motoneurone and muscle unit properties in rat medial gastrocnemius.

R Bakels 1, D Kernell 1
PMCID: PMC1175345  PMID: 8246185

Abstract

1. Electrical and contractile (isometric) properties were studied for sixty-six motoneurone-muscle unit combinations from rat medial gastrocnemius (MG). The animals were anaesthetized with pentobarbitone. 2. The muscle units were classified into S (slow) and F (fast) on the basis of measurements of speed and fatigue resistance: the 'slow' category comprised units with an initial twitch contraction time exceeding those found among fatigue-sensitive units (border value 20 ms). 3. Twitch speed was assessed by three different measures: (i) contraction time (time to peak, range 11.4-28.0 ms), (ii) half-relaxation time (8.4-56.5 ms), and (iii) total twitch duration (34-116 ms). All three measures were mutually highly correlated and their respective values showed a continuous and unimodal distribution across the unit population. 4. The motoneurones were investigated with regard to their time course and amplitude of post-spike after-hyperpolarization (AHP; range of total durations 30-116 ms, amplitudes 0.9-8.0 mV), rheobase (0.8-17.1 nA), input resistance (0.8-5.1 M omega) and axonal conduction velocity (33-85 m/s). 5. Motoneurones of slow-twitch muscle units (type S) had, on average, a significantly slower time course of AHP, a smaller rheobase, a higher input resistance and more slowly conducting axons than those innervating fast-twitch muscle units. 6. Across the whole neuronal sample, input conductance (reciprocal of input resistance) correlated well with rheobase (r = 0.74). However, the differences in rheobase did not seem to be caused exclusively by the associated differences in input conductance. 7. Throughout the sampled population, the relative slowness of AHP showed a continuous and highly significant correlation with the relative slowness of the corresponding unit twitch. The absolute duration of AHP was close to that of the twitch. In the Discussion it is argued that this 'speed match' between motoneurone and muscle unit would help ensure that barely recruited motoneurones start firing at a frequency that is optimally suited for the subsequent rate gradation of force. 8. AHP amplitude was, on average, significantly smaller for fast-twitch than for slow-twitch motoneurones. Calculations indicated that these differences were almost completely caused by the associated differences in input resistance; the computed value for the conductance change underlying the AHP was nearly the same for fast- and slow-twitch motoneurones. 9. A simple neurone model was used to calculate the consequences of the differences in AHP amplitude and duration for repetitive discharge properties of fast and slow cell categories.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Ariano M. A., Armstrong R. B., Edgerton V. R. Hindlimb muscle fiber populations of five mammals. J Histochem Cytochem. 1973 Jan;21(1):51–55. doi: 10.1177/21.1.51. [DOI] [PubMed] [Google Scholar]
  2. Barrett E. F., Barrett J. N., Crill W. E. Voltage-sensitive outward currents in cat motoneurones. J Physiol. 1980 Jul;304:251–276. doi: 10.1113/jphysiol.1980.sp013323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burke R. E., Levine D. N., Tsairis P., Zajac F. E., 3rd Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol. 1973 Nov;234(3):723–748. doi: 10.1113/jphysiol.1973.sp010369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burke R. E., Strick P. L., Kanda K., Kim C. C., Walmsley B. Anatomy of medial gastrocnemius and soleus motor nuclei in cat spinal cord. J Neurophysiol. 1977 May;40(3):667–680. doi: 10.1152/jn.1977.40.3.667. [DOI] [PubMed] [Google Scholar]
  5. Carp J. S., Powers R. K., Rymer W. Z. Alterations in motoneuron properties induced by acute dorsal spinal hemisection in the decerebrate cat. Exp Brain Res. 1991;83(3):539–548. doi: 10.1007/BF00229832. [DOI] [PubMed] [Google Scholar]
  6. Dum R. P., Kennedy T. T. Physiological and histochemical characteristics of motor units in cat tibialis anterior and extensor digitorum longus muscles. J Neurophysiol. 1980 Jun;43(6):1615–1630. doi: 10.1152/jn.1980.43.6.1615. [DOI] [PubMed] [Google Scholar]
  7. Emonet-Dénand F., Hunt C. C., Petit J., Pollin B. Proportion of fatigue-resistant motor units in hindlimb muscles of cat and their relation to axonal conduction velocity. J Physiol. 1988 Jun;400:135–158. doi: 10.1113/jphysiol.1988.sp017115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. FRANK K., FUORTES M. G. Stimulation of spinal motoneurones with intracellular electrodes. J Physiol. 1956 Nov 28;134(2):451–470. doi: 10.1113/jphysiol.1956.sp005657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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. 1981 Dec;46(6):1326–1338. doi: 10.1152/jn.1981.46.6.1326. [DOI] [PubMed] [Google Scholar]
  10. Gardiner P. F., Kernell D. The "fastness" of rat motoneurones: time-course of afterhyperpolarization in relation to axonal conduction velocity and muscle unit contractile speed. Pflugers Arch. 1990 Mar;415(6):762–766. doi: 10.1007/BF02584018. [DOI] [PubMed] [Google Scholar]
  11. Grottel K., Celichowski J. Division of motor units in medial gastrocnemius muscle of the rat in the light of variability of their principal properties. Acta Neurobiol Exp (Wars) 1990;50(6):571–587. [PubMed] [Google Scholar]
  12. Gustafsson B., Pinter M. J. An investigation of threshold properties among cat spinal alpha-motoneurones. J Physiol. 1984 Dec;357:453–483. doi: 10.1113/jphysiol.1984.sp015511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Harada Y., Takahashi T. The calcium component of the action potential in spinal motoneurones of the rat. J Physiol. 1983 Feb;335:89–100. doi: 10.1113/jphysiol.1983.sp014521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hashizume K., Kanda K., Burke R. E. Medial gastrocnemius motor nucleus in the rat: age-related changes in the number and size of motoneurons. J Comp Neurol. 1988 Mar 15;269(3):425–430. doi: 10.1002/cne.902690309. [DOI] [PubMed] [Google Scholar]
  15. Kanda K., Hashizume K. Changes in properties of the medial gastrocnemius motor units in aging rats. J Neurophysiol. 1989 Apr;61(4):737–746. doi: 10.1152/jn.1989.61.4.737. [DOI] [PubMed] [Google Scholar]
  16. Kanda K., Hashizume K. Factors causing difference in force output among motor units in the rat medial gastrocnemius muscle. J Physiol. 1992 Mar;448:677–695. doi: 10.1113/jphysiol.1992.sp019064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kernell D., Eerbeek O., Verhey B. A., Donselaar Y. Effects of physiological amounts of high- and low-rate chronic stimulation on fast-twitch muscle of the cat hindlimb. I. Speed- and force-related properties. J Neurophysiol. 1987 Sep;58(3):598–613. doi: 10.1152/jn.1987.58.3.598. [DOI] [PubMed] [Google Scholar]
  18. Kernell D., Eerbeek O., Verhey B. A. Motor unit categorization on basis of contractile properties: an experimental analysis of the composition of the cat's m. peroneus longus. Exp Brain Res. 1983;50(2-3):211–219. doi: 10.1007/BF00239185. [DOI] [PubMed] [Google Scholar]
  19. Kernell D. Functional properties of spinal motoneurons and gradation of muscle force. Adv Neurol. 1983;39:213–226. [PubMed] [Google Scholar]
  20. Kernell D., Monster A. W. Motoneurone properties and motor fatigue. An intracellular study of gastrocnemius motoneurones of the cat. Exp Brain Res. 1982;46(2):197–204. doi: 10.1007/BF00237177. [DOI] [PubMed] [Google Scholar]
  21. Kernell D., Monster A. W. Threshold current for repetitive impulse firing in motoneurones innervating muscle fibres of different fatigue sensitivity in the cat. Brain Res. 1981 Dec 14;229(1):193–196. doi: 10.1016/0006-8993(81)90756-3. [DOI] [PubMed] [Google Scholar]
  22. Kernell D. Organization and properties of spinal motoneurones and motor units. Prog Brain Res. 1986;64:21–30. [PubMed] [Google Scholar]
  23. Kernell D. Rhythmic properties of motoneurones innervating muscle fibres of different speed in m. gastrocnemius medialis of the cat. Brain Res. 1979 Jan 5;160(1):159–162. doi: 10.1016/0006-8993(79)90612-7. [DOI] [PubMed] [Google Scholar]
  24. Kernell D. The repetitive impulse discharge of a simple neurone model compared to that of spinal motoneurones. Brain Res. 1968 Dec;11(3):685–687. doi: 10.1016/0006-8993(68)90157-1. [DOI] [PubMed] [Google Scholar]
  25. Kernell D., Zwaagstra B. Dendrites of cat's spinal motoneurones: relationship between stem diameter and predicted input conductance. J Physiol. 1989 Jun;413:255–269. doi: 10.1113/jphysiol.1989.sp017652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kernell D., Zwaagstra B. Input conductance axonal conduction velocity and cell size among hindlimb motoneurones of the cat. Brain Res. 1981 Jan 12;204(2):311–326. doi: 10.1016/0006-8993(81)90591-6. [DOI] [PubMed] [Google Scholar]
  27. McDonagh J. C., Binder M. D., Reinking R. M., Stuart D. G. Tetrapartite classification of motor units of cat tibialis posterior. J Neurophysiol. 1980 Oct;44(4):696–712. doi: 10.1152/jn.1980.44.4.696. [DOI] [PubMed] [Google Scholar]
  28. Moore J., Appenteng K. The membrane properties and firing characteristics of rat jaw-elevator motoneurones. J Physiol. 1990 Apr;423:137–153. doi: 10.1113/jphysiol.1990.sp018015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pinter M. J., Curtis R. L., Hosko M. J. Voltage threshold and excitability among variously sized cat hindlimb motoneurons. J Neurophysiol. 1983 Sep;50(3):644–657. doi: 10.1152/jn.1983.50.3.644. [DOI] [PubMed] [Google Scholar]
  30. Tötösy de Zepetnek J. E., Zung H. V., Erdebil S., Gordon T. Motor-unit categorization based on contractile and histochemical properties: a glycogen depletion analysis of normal and reinnervated rat tibialis anterior muscle. J Neurophysiol. 1992 May;67(5):1404–1415. doi: 10.1152/jn.1992.67.5.1404. [DOI] [PubMed] [Google Scholar]
  31. Zengel J. E., Reid S. A., Sypert G. W., Munson J. B. Membrane electrical properties and prediction of motor-unit type of medial gastrocnemius motoneurons in the cat. J Neurophysiol. 1985 May;53(5):1323–1344. doi: 10.1152/jn.1985.53.5.1323. [DOI] [PubMed] [Google Scholar]

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