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Local control of information flow in segmental and ascending collaterals of single afferents

Nature volume 395, pages 600–604 (1998)Cite this article

Abstract

In the vertebrate spinal cord, the activation of GABA(γ-aminobutyric acid)-releasing interneurons that synapse with intraspinal terminals of sensory fibres leading into the central nervous system (afferent fibres) produces primary afferent depolarization and presynaptic inhibition1,2,3. It is not known to what extent these presynaptic mechanisms allow a selective control of information transmitted through specific sets of intraspinal branches of individual afferents4,5,6,7. Here we study the local nature of the presynaptic control by measuring primary afferent depolarization simultaneously in two intraspinal collaterals of the same muscle spindle afferent. One of these collaterals ends at the L6–L7 segmental level in the intermediate nucleus, and the other ascends to segment L3 within Clarke's column, the site of origin of spinocerebellar neurons8. Our results indicate that there are central mechanisms that are able to affect independently the synaptic effectiveness of segmental and ascending collaterals of individual muscle spindle afferents. Focal control of presynaptic inhibition thus allows the intraspinal branches of afferent fibres to function as a dynamic assembly that can be fractionated to convey information to selected neuronal targets. This may be a mechanism by which different spinal postsynaptic targets that are coupled by sensory input from a common source could be uncoupled.

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Figure 1: The procedure.
Figure 2: Selective inhibition of PAD in pairs of collaterals of single afferents.
Figure 3: Spinalization reverses inhibition of PAD by cutaneous afferents in the L3 and L6 collaterals of same muscle spindle.
Figure 4: Neuronal connections explaining the local character of inhibition of PAD in the L3 and L6 collaterals of individual muscle spindle afferen.

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References

  1. Rudomin, P. in The Segmental Motor System (eds Binder, M.S. & Mendell, L. M.) 349–380 (Oxford Univ. Press, New York, 1990).

    Google Scholar 

  2. Nusbaum, M. P., El-Manira, A., Gossard, J. P. & Rossignol, S. in Neurons, Networks and Motor Behaviour (eds Stein, P. S. G., Grillner, S., Selverston, A. I. & Stuart, D. G.). 237–253 (MIT Press, Cambridge, Massachusetts, 1997).

    Google Scholar 

  3. Gossard, J. P. Control of transmission in muscle Ia afferents during fictive locomotion in cat. J. Neurophysiol. 76, 4104–4112 (1996).

    Article  CAS  Google Scholar 

  4. Quevedo, J., Eguibar, J. R., Lomelí, J. & Rudomin, P. Patterns of connectivity of spinal interneurons with single muscle afferents. Exp. Brain Res. 115, 387–402 (1997).

    Article  CAS  Google Scholar 

  5. Eguibar, J. R., Quevedo, J. & Rudomin, P. Selective cortical and segmental control of primary afferent depolarization of single muscle afferents in the cat spinal cord. Exp. Brain Res. 113, 411–430 (1997).

    Article  CAS  Google Scholar 

  6. Luscher, H. R. in Presynaptic Inhibition and Neural Control (eds Rudomin, P., Romo, R. & Mendell, L.M.) 126–137 (Oxford Univ. Press, Oxford, 1998).

    Google Scholar 

  7. Wall, P. D. Do nerve impulses penetrate terminal aborizations? Trends Neurosci. 18, 99–103 (1995).

    Article  CAS  Google Scholar 

  8. Mann, M. D. Clarke's column and the dorsal spinocerebellar tract. Brain Behav. Evol. 7, 34–83 (1973).

    Article  CAS  Google Scholar 

  9. Rudomin, P., Engberg, I. & Jiménez, I. Mechanisms involved in presynaptic depolarization of group I and rubrospinal fibers in cat spinal cord. J. Neurophysiol. 72, 532–548 (1981).

    Article  Google Scholar 

  10. Madrid, J., Alvarado, J., Dutton, H. & Rudomin, P. Amethod for the dynamic continuous estimation of excitability changes of single fiber terminals in the central nervous system. Neurosci. Lett. 11, 253–258 (1979).

    Article  CAS  Google Scholar 

  11. Enríquez, M., Jiménez, I. & Rudomin, P. Segmental and supraspinal control of synaptic effectiveness of functionally identified muscle afferents in the cat. Exp. Brain Res. 107, 391–404 (1996).

    PubMed  Google Scholar 

  12. Riddell, J. S., Jankowska, A. & Eide, E. Depolarization of group II muscle afferents by stimuli applied in the locus coeruleus and raphe nuclei of the cat. J. Physiol. (Lond) 461, 723–741 (1993).

    Article  CAS  Google Scholar 

  13. Rudomin, P., Núñez, R., Madrid, J. & Burke, R. E. Primary afferent hyperpolarization and presynaptic facilitation of Ia afferent terminals induced by large cutaneous fibres. J. Neurophysiol. 37, 413–429 (1979).

    Article  Google Scholar 

  14. Quevedo, J., Eguibar, J. R., Jiménez, I., Schmidt, R. F. & Rudomin, P. Primary afferent depolarization of muscle afferents elicited by stimulation of joint afferents in cats with intact neuraxis and during reversible spinalization. J. Neurophysiol. 70, 1–12 (1993).

    Article  Google Scholar 

  15. Chan, S. H. H. & Barnes, C. D. Apresynaptic mechanism evoked from brainstem reticular formation in the lumbar cord and its temporal significance. Brain Res. 45, 101–114 (1972).

    Article  CAS  Google Scholar 

  16. Curtis, D. R., Leah, J. D. & Peet, M. J. Effects of noradrenaline and 5-hydroxytriptamine on spinal Ia afferent terminations. Brain Res. 258, 328–332 (1983).

    Article  CAS  Google Scholar 

  17. Lundberg, A. in Physiology of Spinal Neruons (eds Eccles, J. C. & Schadé, J. P.) 197–221 (Elsevier, Amsterdam, 1964).

    Google Scholar 

  18. Jankowska, E. Interneuronal relay in pathways from proprioceptors. Prog. Neurobiol. 38, 335–378 (1992).

    Article  CAS  Google Scholar 

  19. Rudomin, P., Solodkin, M. & Jiménez, I. Synaptic potentials of primary afferent fibers and motoneurons evoked by single intermediate nucleus interneurons in the cat spinal cord. J. Neurophysiol. 57, 1288–1313 (1987).

    Article  CAS  Google Scholar 

  20. Geo, J. H. et al . Cerebellum implicated in sensory acquisition and discrimination rather than motor control. Science 272, 545–547 (1996).

    Article  ADS  Google Scholar 

  21. Raymond, J. L., Lisberger, S. G. & Mauk, M. D. The cerebellum: a neuronal learning machine? Science 272, 1126–1131 (1996).

    Article  ADS  CAS  Google Scholar 

  22. Jankowska, E. & Padel, Y. On the origin of presynaptic depolarization of group I muscle afferents in Clarke's column in the cat. Brain Res. 295, 195–201 (1984).

    Article  CAS  Google Scholar 

  23. Harrison, P. J. & Jankowska, E. Do interneurons in the lower lumbar segments contribute to presynaptic depolarization of group I muscle afferents in Clarke's column? Brain Res. 295, 203–210 (1984).

    Article  CAS  Google Scholar 

  24. Rudomin, P., Burke, R. E., Núñez, R., Madrid, J. & Dutton, H. Control by presynaptic correlation: a mechanism affecting information transmission from Ia fibers to motoneurons. J. Neurophysiol. 38, 267–284 (1975).

    Article  CAS  Google Scholar 

  25. Hultborn, H., Meunier, S., Morin, C., Pierrot-Deseilligny, E. & Shindo, E. Changes in presynaptic inhibition of Ia fibres at the onset of voluntary contraction of homonymous and synergistic muscles in man. J. Physiol. (Lond.) 389, 757–772 (1987).

    Article  CAS  Google Scholar 

  26. Iles, J. F. Evidence for cutaneous and corticospinal modulation of presynaptic inhibition of Ia afferents from the human lower limb. J. Physiol. (Lond.) 491, 197–207 (1996).

    Article  CAS  Google Scholar 

  27. Nelson, R. J. Interactions between motor commands and somatic perception in sensorimotor cortex. Curr. Opin. Neurobiol. 6, 801–810 (1996).

    Article  CAS  Google Scholar 

  28. Curtis, D. R., Wilson, W. J. & Malik, R. The effect of GABA on the terminations of vestibulospinal neurons in the cat spinal cord. Brain Res. 291, 372–375 (1984).

    Article  Google Scholar 

  29. Jankowska, E., McCrea, D., Rudomin, P. & Sykova, E. Observations on neuronal pathways subserving primary afferent depolarization. J. Neurophysiol. 46, 506–516 (1981).

    Article  CAS  Google Scholar 

  30. Rudomin, P., Jiménez, I., Solodkin, M. & Dueñas, S. Sites of action of segmental and descending control of transmission on pathways mediating PAD of Ia- and Ib-afferent fibers in cat spinal cord. J. Neurophysiol. 50, 743–769 (1983).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank C. León for help with the experiments and J. E. Velazquez, P. Reyes and L.Jiménez for computational support. This study was supported partly by grants from the NIH and CONACyT.

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Authors and Affiliations

  1. Department of Physiology, Biophysics and Neurosciences, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Apartado Postal 14-740, México D.F., 07000, México

    J. Lomelí, J. Quevedo, P. Linares & P. Rudomin

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  1. J. Lomelí
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  2. J. Quevedo
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  3. P. Linares
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  4. P. Rudomin
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Correspondence to P. Rudomin.

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Lomelí, J., Quevedo, J., Linares, P. et al. Local control of information flow in segmental and ascending collaterals of single afferents. Nature 395, 600–604 (1998). https://doi.org/10.1038/26975

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