Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1981;313:121–140. doi: 10.1113/jphysiol.1981.sp013654

Direct observations on the contacts made between Ia afferent fibres and alpha-motoneurones in the cat's lumbosacral spinal cord.

A G Brown, R E Fyffe
PMCID: PMC1274440  PMID: 7277213

Abstract

1. The enzyme horseradish peroxidase was injected into identified lumbosacral alpha-motoneurones and Group Ia afferent fibres in cats anaesthetized with chloralose and paralysed with gallamine triethiodide. Subsequent histological examination allowed the determination of (a) the extent of the motoneuronal dendritic trees, (b) the number and location of Ia synapses upon the motoneurones. 2. alpha-motoneurones had seven to eighteen primary dendrites and each produced daughter branches up to the fourth to the sixth order. At dendritic bifurcations Rall's 3/2 Power Law was obeyed. There was little or no dendritic tapering up to about 800 micrometers from the soma. Beyond this distance, however, there was considerable tapering. 3. Horseradish peroxidase injections revealed that motoneuronal dendrites are much longer than previously thought. Individual dendrites could be traced for up to 1600 micrometers from the soma and dendritic trees were usually 2-3 mm from tip to tip. Nearly all the motoneurones had dendrites that entered the white matter of the cord. Dendrites could also reach as far dorsally as laminae V and VI. 4. Ia synapses upon motoneuronal somata were examined in cords counterstained with cresyl violet or methylene green. About 10% of Ia boutons in lamina IX were on somata and each Ia collateral terminated on 3.66 motoneuronal somata or the most proximal (30 micrometer) dendrites, with on average about two contacts per motoneurone. 5. Ten Ia afferent fibre-motoneurone pairs were injected with horseradish peroxidase. The following conclusions were drawn: (i) only one collateral of any given Ia axon makes contact with a motoneurone even though other collaterals from the same axon might pass through the dendritic tree, (ii) usually all contacts made between a Ia fibre and a motoneurone are at about the same geometrical distance from the soma, even when on different dendrites, (iii) between two and five contacts are made upon the dendritic tree (average 3.4) at distances of between 20 and 820 micrometers from the soma. 6. The results are discussed in relation to previous anatomical and electrophysiological work.

Full text

PDF
121

Images in this article

140-2Plate 2
on p.140-2
140-3Plate 3
on p.140-3
140-4Plate 4
on p.140-4
140-1Plate 1
on p.140-1

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. AITKEN J. T., BRIDGER J. E. Neuron size and neuron population density in the lumbosacral region of the cat's spinal cord. J Anat. 1961 Jan;95:38–53. [PMC free article] [PubMed] [Google Scholar]
  2. Barrett J. N., Crill W. E. Specific membrane properties of cat motoneurones. J Physiol. 1974 Jun;239(2):301–324. doi: 10.1113/jphysiol.1974.sp010570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown A. G., Fyffe R. E. Synaptic contacts made by identified Ia afferent fibres upon motoneurones [proceedings]. J Physiol. 1978 Nov;284:43P–44P. [PubMed] [Google Scholar]
  4. Brown A. G., Fyffe R. E. The morphology of group Ia afferent fibre collaterals in the spinal cord of the cat. J Physiol. 1978 Jan;274:111–127. doi: 10.1113/jphysiol.1978.sp012137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown A. G., Fyffe R. E. The morphology of group Ib afferent fibre collaterals in the spinal cord of the cat. J Physiol. 1979 Nov;296:215–226. doi: 10.1113/jphysiol.1979.sp013001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown A. G., Rose P. K., Snow P. J. The morphology of hair follicle afferent fibre collaterals in the spinal cord of the cat. J Physiol. 1977 Nov;272(3):779–797. doi: 10.1113/jphysiol.1977.sp012073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Burke R. E. Composite nature of the monosynaptic excitatory postsynaptic potential. J Neurophysiol. 1967 Sep;30(5):1114–1137. doi: 10.1152/jn.1967.30.5.1114. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Burke R. E., Walmsley B., Hodgson J. A. HRP anatomy of group Ia afferent contacts on alpha motoneurones. Brain Res. 1979 Jan 12;160(2):347–352. doi: 10.1016/0006-8993(79)90430-x. [DOI] [PubMed] [Google Scholar]
  10. Conradi S., Ronnevi L. O. Spontaneous elimination of synapses on cat spinal motoneurons after birth: do half of the synapses on the cell bodies disappear? Brain Res. 1975 Jul 18;92(3):505–510. doi: 10.1016/0006-8993(75)90338-8. [DOI] [PubMed] [Google Scholar]
  11. Conradi S. Ultrastructure of dorsal root boutons on lumbosacral motoneurons of the adult cat, as revealed by dorsal root section. Acta Physiol Scand Suppl. 1969;332:85–115. [PubMed] [Google Scholar]
  12. Cullheim S., Kellerth J. O. A morphological study of the axons and recurrent axon collaterals of cat sciatic alpha-motoneurons after intracellular staining with horseradish peroxidase. J Comp Neurol. 1978 Apr 1;178(3):537–557. doi: 10.1002/cne.901780309. [DOI] [PubMed] [Google Scholar]
  13. Edwards F. R., Redman S. J., Walmsley B. Non-quantal fluctuations and transmission failures in charge transfer at Ia synapses on spinal motoneurones. J Physiol. 1976 Aug;259(3):689–704. doi: 10.1113/jphysiol.1976.sp011489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Edwards F. R., Redman S. J., Walmsley B. The effect of polarizing currents on unitary Ia excitatory post-synaptic potentials evoked in spinal motoneurones. J Physiol. 1976 Aug;259(3):705–723. doi: 10.1113/jphysiol.1976.sp011490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. FATT P. Sequence of events in synaptic activation of a motoneurone. J Neurophysiol. 1957 Jan;20(1):61–80. doi: 10.1152/jn.1957.20.1.61. [DOI] [PubMed] [Google Scholar]
  16. Fu T. C., Santini M., Schomburg E. D. Characteristics and distribution of spinal focal synaptic potentials generated by group II muscle afferents. Acta Physiol Scand. 1974 Jul;91(3):298–313. doi: 10.1111/j.1748-1716.1974.tb05686.x. [DOI] [PubMed] [Google Scholar]
  17. Fu T. C., Schomburg E. D. Electrophysiological investigation of the projection of secondary muscle spindle afferents in the cat spinal cord. Acta Physiol Scand. 1974 Jul;91(3):314–329. doi: 10.1111/j.1748-1716.1974.tb05687.x. [DOI] [PubMed] [Google Scholar]
  18. Fyffe R. E. The morphology of group II muscle afferent fibre collaterals [proceedings]. J Physiol. 1979 Nov;296:39P–40P. [PubMed] [Google Scholar]
  19. Gelfan S., Kao G., Ruchkin D. S. The dendritic tree of spinal neurons. J Comp Neurol. 1970 Aug;139(4):385–411. doi: 10.1002/cne.901390402. [DOI] [PubMed] [Google Scholar]
  20. Hanker J. S., Yates P. E., Metz C. B., Rustioni A. A new specific, sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Histochem J. 1977 Nov;9(6):789–792. doi: 10.1007/BF01003075. [DOI] [PubMed] [Google Scholar]
  21. Iansek R., Redman S. J. The amplitude, time course and charge of unitary excitatory post-synaptic potentials evoked in spinal motoneurone dendrites. J Physiol. 1973 Nov;234(3):665–688. doi: 10.1113/jphysiol.1973.sp010366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Iles J. F. Central terminations of muscle afferents on motoneurones in the cat spinal cord. J Physiol. 1976 Oct;262(1):91–117. doi: 10.1113/jphysiol.1976.sp011587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ishizuka N., Mannen H., Hongo T., Sasaki S. Trajectory of group Ia afferent fibers stained with horseradish peroxidase in the lumbosacral spinal cord of the cat: three dimensional reconstructions from serial sections. J Comp Neurol. 1979 Jul 15;186(2):189–211. doi: 10.1002/cne.901860206. [DOI] [PubMed] [Google Scholar]
  24. Jack J. J., Miller S., Porter R., Redman S. J. The time course of minimal excitory post-synaptic potentials evoked in spinal motoneurones by group Ia afferent fibres. J Physiol. 1971 Jun;215(2):353–380. doi: 10.1113/jphysiol.1971.sp009474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. KUNO M. QUANTAL COMPONENTS OF EXCITATORY SYNAPTIC POTENTIALS IN SPINAL MOTONEURONES. J Physiol. 1964 Dec;175:81–99. doi: 10.1113/jphysiol.1964.sp007504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kirkwood P. A., Sears T. A. Monosynaptic excitation of motoneurones from secondary endings of muscle spindles. Nature. 1974 Nov 15;252(5480):243–244. doi: 10.1038/252243a0. [DOI] [PubMed] [Google Scholar]
  27. Kuno M., Miyahara J. T. Non-linear summation of unit synaptic potentials in spinal motoneurones of the cat. J Physiol. 1969 Apr;201(2):465–477. doi: 10.1113/jphysiol.1969.sp008767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mendell L. M., Weiner R. Analysis of pairs of individual Ia-E.P.S.P.S in single motoneurones. J Physiol. 1976 Feb;255(1):81–104. doi: 10.1113/jphysiol.1976.sp011271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nelson P. G., Lux H. D. Some electrical measurements of motoneuron parameters. Biophys J. 1970 Jan;10(1):55–73. doi: 10.1016/S0006-3495(70)86285-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. RALL W. Branching dendritic trees and motoneuron membrane resistivity. Exp Neurol. 1959 Nov;1:491–527. doi: 10.1016/0014-4886(59)90046-9. [DOI] [PubMed] [Google Scholar]
  31. ROMANES G. J. The motor cell columns of the lumbo-sacral spinal cord of the cat. J Comp Neurol. 1951 Apr;94(2):313–363. doi: 10.1002/cne.900940209. [DOI] [PubMed] [Google Scholar]
  32. Rall W., Burke R. E., Smith T. G., Nelson P. G., Frank K. Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. J Neurophysiol. 1967 Sep;30(5):1169–1193. doi: 10.1152/jn.1967.30.5.1169. [DOI] [PubMed] [Google Scholar]
  33. SPRAGUE J. M. The distribution of dorsal root fibres on motor cells in the lumbosacral spinal cord of the cat, and the site of excitatory and inhibitory terminals in monosynaptic pathways. Proc R Soc Lond B Biol Sci. 1958 Dec 24;149(937):534–556. doi: 10.1098/rspb.1958.0091. [DOI] [PubMed] [Google Scholar]
  34. Scheibel M. E., Scheibel A. B. Terminal patterns in cat spinal cord. 3. Primary afferent collaterals. Brain Res. 1969 May;13(3):417–443. doi: 10.1016/0006-8993(69)90258-3. [DOI] [PubMed] [Google Scholar]
  35. Scott J. G., Mendell L. M. Individual EPSPs produced by single triceps surae Ia afferent fibers in homonymous and heteronymous motoneurons. J Neurophysiol. 1976 Jul;39(4):679–692. doi: 10.1152/jn.1976.39.4.679. [DOI] [PubMed] [Google Scholar]
  36. Snow P. J., Rose P. K., Brown A. G. Tracing axons and axon collaterals of spinal neurons using intracellular injection of horseradish peroxidase. Science. 1976 Jan 23;191(4224):312–313. doi: 10.1126/science.54936. [DOI] [PubMed] [Google Scholar]
  37. Somogyi P., Smith A. D. Projection of neostriatal spiny neurons to the substantia nigra. Application of a combined Golgi-staining and horseradish peroxidase transport procedure at both light and electron microscopic levels. Brain Res. 1979 Dec 7;178(1):3–15. doi: 10.1016/0006-8993(79)90084-2. [DOI] [PubMed] [Google Scholar]
  38. Stauffer E. K., Watt D. G., Taylor A., Reinking R. M., Stuart D. G. Analysis of muscle receptor connections by spike-triggered averaging. 2. Spindle group II afferents. J Neurophysiol. 1976 Nov;39(6):1393–1402. doi: 10.1152/jn.1976.39.6.1393. [DOI] [PubMed] [Google Scholar]
  39. Zucker R. S. Changes in the statistics of transmitter release during facilitation. J Physiol. 1973 Mar;229(3):787–810. doi: 10.1113/jphysiol.1973.sp010167. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES