Experimental Brain Research

, Volume 161, Issue 4, pp 486–501

Group II excitations from plantar foot muscles to human leg and thigh motoneurones

  • P. Marque
  • G. Nicolas
  • M. Simonetta-Moreau
  • E. Pierrot-Deseilligny
  • V. Marchand-Pauvert
Research Article

Abstract

Projections of group II afferents from intrinsic foot muscles to lower limb motoneurones were investigated in humans after electrical stimuli were applied to the tibial nerve (TN) at ankle level, using modulation of the quadriceps H reflex, on-going EMG of the quadriceps and peroneus brevis, and PSTHs of single quadriceps, biceps, semitendinosus, tibialis anterior, and peroneus brevis motor units. TN stimulation evoked late and high-threshold excitation in all leg and thigh muscles investigated. The mean latency of the late excitation was 13.5±0.4 ms longer than that of the heteronymous monosynaptic Ia excitation, and the more caudal the motor nucleus the longer the central delay of the late effect, suggesting mediation through interneurones located rostral to motoneurones. The electrical threshold and conduction velocity of the largest diameter fibres evoking the late excitation were estimated to be ~2 and 0.67 times, respectively, those of the fastest Ia afferents, i.e. consistent with a mediation by group II afferents. Stimulation of the skin areas innervated by TN did not evoke late excitations. Further support for mediation through group II afferents was provided by the findings that:
  1. 1.

    the latency of the TN-induced late and high-threshold excitation in Per brev units was more delayed by cooling the nerve than that of the excitation evoked by group I afferents, and

     
  2. 2.

    tizanidine intake (known to depress selectively transmission of group II effects) suppressed the TN-induced late and high-threshold excitation whereas the group I facilitation was not modified.

     

Keywords

Muscle group II afferents Spinal pathways Human 

References

  1. Abbruzzese M, Rubino V, Schieppati M (1996) Task-dependent effects evoked by foot muscle afferents on leg muscle activity in humans. Electroencephalogr Clin Neurophysiol 101:339–348CrossRefPubMedGoogle Scholar
  2. Araki T, Eccles JC, Ito M (1960) Correlation of the inhibitory post-synaptic potential of motoneurones with the latency and time course of inhibition of monosynaptic reflexes. J Physiol 154:354–377PubMedGoogle Scholar
  3. Berger W, Dietz V, Quintern J (1984) Corrective reactions to stumbling in man: neuronal co-ordination of bilateral leg muscle activity during gait. J Physiol 357:109–125PubMedGoogle Scholar
  4. Bras H, Cavallari P, Jankowska E, McCrea D (1989) Comparison of effects of monoamines on transmission in spinal pathways from group I and II muscle afferents in the cat. Exp Brain Res 76:27–37CrossRefPubMedGoogle Scholar
  5. Burke D, Gandevia SC, McKeon B (1984) Monosynaptic and oligosynaptic contributions to human ankle jerk and H-reflex. J Neurophysiol 52:435–448PubMedGoogle Scholar
  6. Burke D, Hagbarth KE, Lofstedt L (1978) Muscle spindle activity in man during shortening and lengthening contractions. J Physiol 277:131–142PubMedGoogle Scholar
  7. Bussel B, Pierrot-Deseilligny E (1977) Inhibition of human motoneurones, probably of Renshaw origin, elicited by an orthodromic motor discharge. J Physiol 269:319–339PubMedGoogle Scholar
  8. Chaix Y, Marque P, Meunier S, Pierrot-Deseilligny E, Simonetta-Moreau M (1997) Further evidence for non-monosynaptic group I excitation of motoneurones in the human lower limb. Exp Brain Res 115:35–46PubMedGoogle Scholar
  9. Corna S, Grasso M, Nardone A, Schieppati M (1995) Selective depression of medium-latency leg and foot muscle responses to stretch by an alpha 2-agonist in humans. J Physiol 484:803–809PubMedGoogle Scholar
  10. Crone C, Hultborn H, Mazieres L, Morin C, Nielsen J, Pierrot-Deseilligny E (1990) Sensitivity of monosynaptic test reflexes to facilitation and inhibition as a function of the test reflex size: a study in man and the cat. Exp Brain Res 81:35–45PubMedGoogle Scholar
  11. Davies J, Johnston SE, Hill DR, Quilliam JE (1984) Tizanidine (Ds 103–282), a centrally acting muscle relaxant, selectively depresses excitation of feline dorsal horn neurons to noxious peripheral stimuli by an action of at α2-adrenoreceptors. Neurosci Lett 48:197–202CrossRefPubMedGoogle Scholar
  12. Edgley SA, Jankowska E (1987) An interneuronal relay for group I and II muscle afferents in the midlumbar segments of the cat spinal cord. J Physiol 389:647–674PubMedGoogle Scholar
  13. Fournier E, Meunier S, Pierrot-Deseilligny E, Shindo M (1986) Evidence for interneuronally mediated Ia excitatory effects to human quadriceps motoneurones. J Physiol 377:143–169PubMedGoogle Scholar
  14. Franz DN, Iggo A (1968) Conduction failure in myelinated and non-myelinated axons at low temperatures. J Physiol 199:319–345PubMedGoogle Scholar
  15. Gracies JM, Pierrot-Deseilligny E, Robain G (1994) Evidence for further recruitment of group I fibres with high stimulus intensities when using surface electrodes in man. EEG Clin Neurophysiol 93:353–357CrossRefGoogle Scholar
  16. Grey MJ, Ladouceur M, Andersen JB, Nielsen JB, Sinkjaer T (2001) Group II muscle afferents probably contribute to the medium latency soleus stretch reflex during walking in humans. J Physiol 534:925–933PubMedGoogle Scholar
  17. Gustafsson B, McCrea D (1984) Influence of stretch-evoked synaptic potentials on firing probability of cat spinal motoneurones. J Physiol 347:431–451PubMedGoogle Scholar
  18. Hongo T, Lundberg A, Phillips CG, Thompson RF (1984) The pattern of monosynaptic Ia-connections to hindlimb motor nuclei in the baboon: a comparison with the cat. Proc R Soc Lond B Biol Sci 221:261–289PubMedGoogle Scholar
  19. Hunt CC, Kuffler SW (1951) Stretch receptor discharges during muscle contraction. J Physiol 113:298–315PubMedGoogle Scholar
  20. Jankowska E (1992) Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38:335–378CrossRefPubMedGoogle Scholar
  21. Kendall HO, Kendall FP, Wadsworth GE (1971) Muscle testing and function. Williams and Wilkins, Baltimore, MD, USA, pp 42–43Google Scholar
  22. Kernell D, Hultborn H (1990) Synaptic effects on recruitment gain: a mechanism of importance for the input-output relations of motoneurone pools? Brain Res 507:176–179CrossRefPubMedGoogle Scholar
  23. Mann R, Inman VT (1964) Phasic activity of intrinsic muscles of the foot. J Bone Joint Surg Am 46:469–481PubMedGoogle Scholar
  24. Mao CC, Ashby P, Wang M, McCrea D (1984) Synaptic connections from large muscle afferents to the motoneurons of various leg muscles in man. Exp Brain Res 56:341–350PubMedGoogle Scholar
  25. Marchand-Pauvert V, Nicolas G, Burke D, Pierrot-Deseilligny E (2002) Suppression of the H reflex in humans by disynaptic autogenetic inhibitory pathways activated by the test volley. J Physiol 542:963–976CrossRefPubMedGoogle Scholar
  26. Marchand-Pauvert V, Nielsen JB (2002) Modulation of non-monosynaptic excitation from ankle dorsiflexor afferents to quadriceps motoneurones during human walking. J Physiol 538:647–657CrossRefPubMedGoogle Scholar
  27. Marchand-Pauvert V, Simonetta-Moreau M, Pierrot-Deseilligny E (1999) Cortical control of spinal pathways mediating group II excitation to human thigh motoneurones. J Physiol 517:301–313PubMedGoogle Scholar
  28. Marque P, Nicolas G, Marchand-Pauvert V, Gautier J, Simonetta-Moreau M, Pierrot-Deseilligny E (2001) Group I projections from intrinsic foot muscles to motoneurones of leg and thigh muscles in humans. J Physiol 536:313–327CrossRefPubMedGoogle Scholar
  29. Matthews PBC (1972) Mammalian muscle spindles and their central action. Arnold, London, pp 630Google Scholar
  30. Nardone A, Giordano A, Corra T, Schieppati M (1990) Responses of leg muscles in humans displaced while standing. Effects of types of perturbation and of postural set. Brain 113:65–84PubMedGoogle Scholar
  31. Nardone A, Schieppati M (1998) Medium-latency response to muscle stretch in human lower limb: estimation of conduction velocity of group II fibres and central delay. Neurosci Lett 249:29–32CrossRefPubMedGoogle Scholar
  32. Nardone A, Tarantola J, Miscio G, Pisano F, Schenone A, Schieppati M (2000) Loss of large-diameter spindle afferent fibres is not detrimental to the control of body sway during upright stance: evidence from neuropathy. Exp Brain Res 135:155–162CrossRefPubMedGoogle Scholar
  33. Nielsen J, Kagamihara Y (1993) Differential projection of the sural nerve to early and late recruited human tibialis anterior motor units: change of recruitment gain. Acta Physiol Scand 147:385–401PubMedGoogle Scholar
  34. Paintal AS (1965) Block of conduction in mammalian myelinated nerve fibres by low temperatures. J Physiol 180:1–19PubMedGoogle Scholar
  35. Pierrot-Deseilligny E (1999) Heteronymous group II pathways in the human lower limb: spinal organization, cortical control and possible functional role. J Physiol 518P:27SGoogle Scholar
  36. Rossi A, Mazzocchio R (1991) Presence of homonymous recurrent inhibition in motoneurones supplying different lower limb muscles in humans. Exp Brain Res 84:367–73CrossRefPubMedGoogle Scholar
  37. Schieppati M, Nardone A (1997) Medium-latency stretch reflexes of foot and leg muscles analysed by cooling the lower limb in standing humans. J Physiol 503:691-698CrossRefPubMedGoogle Scholar
  38. Schieppati M, Nardone A (1999) Group II spindle afferent fibers in humans: their possible role in the reflex control of stance. Prog Brain Res 123:461–472PubMedGoogle Scholar
  39. Schieppati M, Nardone A, Siliotto R, Grasso M (1995) Early and late stretch responses of human foot muscles induced by perturbation of stance. Exp Brain Res 105:411–422PubMedGoogle Scholar
  40. Simonetta-Moreau M, Marque P, Marchand-Pauvert V, Pierrot-Deseilligny E (1999) The pattern of excitation of human lower limb motoneurones by probable group II muscle afferents. J Physiol 517:287–300PubMedGoogle Scholar
  41. Sinkjaer T, Andersen JB, Ladouceur M, Christensen LOD, Nielsen, JB (2000) Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man. J Physiol 523:817–827PubMedGoogle Scholar
  42. Skoog B (1996) A comparison of the effects of two antispasic drugs, tizanidine and baclofen, on synaptic transmission from muscle spindle afferents to spinal interneurones in cats. Acta Physiol Scand 124:81–90CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • P. Marque
    • 1
  • G. Nicolas
    • 2
  • M. Simonetta-Moreau
    • 1
  • E. Pierrot-Deseilligny
    • 2
  • V. Marchand-Pauvert
    • 2
  1. 1.INSERM U455Pavillon RiserToulouseFrance
  2. 2.INSERM E349, Physiologie et Physiopathologie de la Motricité chez l’Homme, Sce de Médecine Physique et RéadaptationCHU Pitié-SalpêtrièreParis cedex 13France

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