Skip to main content
SpringerLink
Log in

Phase-dependent reversal of the crossed conditioning effect on the soleus Hoffmann reflex from cutaneous afferents during walking in humans

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We previously demonstrated that non-noxious electrical stimulation of the cutaneous nerve innervating the contralateral foot modified the excitability of the Hoffmann (H-) reflex in the soleus muscle (SOL) in a task-dependent manner during standing and walking in humans. To date, however, it remains unclear how the crossed conditioning effect on the SOL H-reflex from the contralateral foot is modified during the various phases of walking. We sought to answer this question in the present study. The SOL H-reflex was evoked in healthy volunteers by an electrical test stimulation (TS) of the right (ipsilateral) posterior tibial nerve at five different phases during treadmill walking (4 km/h). A non-noxious electrical stimulation was delivered to the superficial peroneal nerve of the left (contralateral) ankle ~100 ms before the TS as a conditioning stimulation (CS). This CS significantly suppressed the H-reflex amplitude during the early stance phase, whereas the same CS significantly facilitated the H-reflex amplitude during the late stance phase. The CS alone did not produce detectable changes in the full-wave rectified electromyogram of the SOL. This result indicates that presynaptic mechanisms driven by the activation of low-threshold cutaneous afferents in the contralateral foot play a role in regulating the transmission between the Ia terminal and motoneurons in a phase-dependent manner. The modulation pattern of the crossed conditioning effect on the SOL H-reflex may be functionally relevant for the left–right coordination of leg movements during bipedal walking.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Burke RE (1999) The use of state-dependent modulation of spinal reflexes as a tool to investigate the organization of spinal interneurons. Exp Brain Res 128:263–277

    Article  PubMed  CAS  Google Scholar 

  • Bussel B, Roby-Brami A, Azouvi P, Biraben A, Yakovleff A, Held JP (1988) Myoclonus in a patient with spinal cord transection. Possible involvement of the spinal stepping generator. Brain 111(5):1235–1245

    Article  PubMed  Google Scholar 

  • Capaday C, Stein RB (1986) Amplitude modulation of the soleus H-reflex in the human during walking and standing. J Neurosci 6:1308–1313

    PubMed  CAS  Google Scholar 

  • Capaday C, Lavoie BA, Comeau F (1995) Differential effects of a flexor nerve input on the human soleus H-reflex during standing versus walking. Can J Physiol Pharmacol 73:436–449

    Article  PubMed  CAS  Google Scholar 

  • Christensen LO, Morita H, Petersen N, Nielsen J (1999) Evidence suggesting that a transcortical reflex pathway contributes to cutaneous reflexes in the tibialis anterior muscle during walking in man. Exp Brain Res 124:59–68

    Article  PubMed  CAS  Google Scholar 

  • 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 81:35–45

    Article  PubMed  CAS  Google Scholar 

  • De Serres SJ, Yang JF, Patrick SK (1995) Mechanism for reflex reversal during walking in human tibialis anterior muscle revealed by single motor unit recording. J Physiol 488(Pt 1):249–258

    Article  PubMed  PubMed Central  Google Scholar 

  • Delwaide PJ, Crenna P, Fleron MH (1981) Cutaneous nerve stimulation and motoneuronal excitability: I, soleus and tibialis anterior excitability after ipsilateral and contralateral sural nerve stimulation. J Neurol Neurosurg Psychiatry 44:699–707

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Duysens J, Trippel M, Horstmann GA, Dietz V (1990) Gating and reversal of reflexes in ankle muscles during human walking. Exp Brain Res 82:351–358

    Article  PubMed  CAS  Google Scholar 

  • Duysens J, Tax AA, van der Doelen B, Trippel M, Dietz V (1991) Selective activation of human soleus or gastrocnemius in reflex responses during walking and running. Exp Brain Res 87:193–204

    Article  PubMed  CAS  Google Scholar 

  • Eng JJ, Winter DA, Patla AE (1994) Strategies for recovery from a trip in early and late swing during human walking. Exp Brain Res 102:339–349

    Article  PubMed  CAS  Google Scholar 

  • Faist M, Dietz V, Pierrot-Deseilligny E (1996) Modulation, probably presynaptic in origin, of monosynaptic Ia excitation during human gait. Exp Brain Res 109:441–449

    Article  PubMed  CAS  Google Scholar 

  • Forssberg H (1979) Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion. J Neurophysiol 42:936–953

    PubMed  CAS  Google Scholar 

  • Frigon A, Collins DF, Zehr EP (2004) Effect of rhythmic arm movement on reflexes in the legs: modulation of soleus H-reflexes and somatosensory conditioning. J Neurophysiol 91:1516–1523. doi:10.1152/jn.00695.2003

    Article  PubMed  Google Scholar 

  • Fukushima Y, Yamashita N, Shimada Y (1982) Facilitation of H-reflex by homonymous Ia-afferent fibers in man. J Neurophysiol 48:1079–1088

    PubMed  CAS  Google Scholar 

  • Fung J, Barbeau H (1994) Effects of conditioning cutaneomuscular stimulation on the soleus H-reflex in normal and spastic paretic subjects during walking and standing. J Neurophysiol 72:2090–2104

    PubMed  CAS  Google Scholar 

  • Haridas C, Zehr EP (2003) Coordinated interlimb compensatory responses to electrical stimulation of cutaneous nerves in the hand and foot during walking. J Neurophysiol 90:2850–2861. doi:10.1152/jn.00531.2003

    Article  PubMed  Google Scholar 

  • Haridas C, Zehr EP, Misiaszek JE (2005) Postural uncertainty leads to dynamic control of cutaneous reflexes from the foot during human walking. Brain Res 1062:48–62. doi:10.1016/j.brainres.2005.09.003

    Article  PubMed  CAS  Google Scholar 

  • Hayes HB, Chang YH, Hochman S (2012) Stance-phase force on the opposite limb dictates swing-phase afferent presynaptic inhibition during locomotion. J Neurophysiol 107:3168–3180. doi:10.1152/jn.01134.2011

    Article  PubMed  PubMed Central  Google Scholar 

  • Holmqvist B (1961) Crossed spinal reflex actions evoked by volleys in somatic afferents. Acta Physiol Scand Suppl 52:1–66

    Article  PubMed  CAS  Google Scholar 

  • Iles JF (1996) Evidence for cutaneous and corticospinal modulation of presynaptic inhibition of Ia afferents from the human lower limb. J Physiol 491(Pt 1):197–207

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Knikou M (2010) Plantar cutaneous afferents normalize the reflex modulation patterns during stepping in chronic human spinal cord injury. J Neurophysiol 103:1304–1314. doi:10.1152/jn.00880.2009

    Article  PubMed  Google Scholar 

  • Komiyama T, Zehr EP, Stein RB (2000) Absence of nerve specificity in human cutaneous reflexes during standing. Exp Brain Res 133:267–272

    Article  PubMed  CAS  Google Scholar 

  • Mummidisetty CK, Smith AC, Knikou M (2013) Modulation of reciprocal and presynaptic inhibition during robotic-assisted stepping in humans. Clin Neurophysiol 124:557–564. doi:10.1016/j.clinph.2012.09.007

    Article  PubMed  Google Scholar 

  • Nakajima T, Kamibayashi K, Takahashi M, Komiyama T, Akai M, Nakazawa K (2008) Load-related modulation of cutaneous reflexes in the tibialis anterior muscle during passive walking in humans. Eur J Neurosci 27:1566–1576. doi:10.1111/j.1460-9568.2008.06120.x

    Article  PubMed  Google Scholar 

  • Nakajima T, Mezzarane RA, Klarner T, Barss TS, Hundza SR, Komiyama T, Zehr EP (2013) Neural mechanisms influencing interlimb coordination during locomotion in humans: presynaptic modulation of forearm H-reflexes during leg cycling. PLoS ONE 8:e76313. doi:10.1371/journal.pone.0076313

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Petersen N, Morita H, Nielsen J (1999) Modulation of reciprocal inhibition between ankle extensors and flexors during walking in man. J Physiol 520(Pt 2):605–619

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pierrot-Deseilligny E, Bussel B, Sideri G, Cathala HP, Castaigne P (1973) Effect of voluntary contraction on H reflex changes induced by cutaneous stimulation in normal man. Electroencephalogr Clin Neurophysiol 34:185–192

    Article  PubMed  CAS  Google Scholar 

  • Pierrot-Desseilligny E, Burke DC (2005) The circuitry of the human spinal cord: its role in motor control and movement disorders. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rietdyk S, Patla AE (1998) Context-dependent reflex control: some insights into the role of balance. Exp Brain Res 119:251–259

    Article  PubMed  CAS  Google Scholar 

  • Roby-Brami A, Bussel B (1990) Effects of flexor reflex afferent stimulation on the soleus H reflex in patients with a complete spinal cord lesion: evidence for presynaptic inhibition of Ia transmission. Exp Brain Res 81:593–601

    Article  PubMed  CAS  Google Scholar 

  • Rossignol S, Gauthier L (1980) An analysis of mechanisms controlling the reversal of crossed spinal reflexes. Brain Res 182:31–45

    Article  PubMed  CAS  Google Scholar 

  • Rudomin P, Schmidt RF (1999) Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129:1–37

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto M, Endoh T, Nakajima T, Tazoe T, Shiozawa S, Komiyama T (2006) Modulations of interlimb and intralimb cutaneous reflexes during simultaneous arm and leg cycling in humans. Clin Neurophysiol 117:1301–1311. doi:10.1016/j.clinph.2006.03.005

    Article  PubMed  Google Scholar 

  • Stanislaus V, Mummidisetty CK, Knikou M (2010) Soleus H-reflex graded depression by contralateral hip afferent feedback in humans. Brain Res 1310:77–86. doi:10.1016/j.brainres.2009.11.013

    Article  PubMed  CAS  Google Scholar 

  • Stevenson AJ, Geertsen SS, Andersen JB, Sinkjaer T, Nielsen JB, Mrachacz-Kersting N (2013) Interlimb communication to the knee flexors during walking in humans. J Physiol 591:4921–4935. doi:10.1113/jphysiol.2013.257949

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Stubbs PW, Nielsen JF, Sinkjaer T, Mrachacz-Kersting N (2011) Phase modulation of the short-latency crossed spinal response in the human soleus muscle. J Neurophysiol 105:503–511. doi:10.1152/jn.00786.2010

    Article  PubMed  Google Scholar 

  • Suzuki S, Nakajima T, Mezzarane RA, Ohtsuka H, Futatsubashi G, Komiyama T (2014) Differential regulation of crossed cutaneous effects on the soleus H-reflex during standing and walking in humans. Exp Brain Res 232:3069–3078. doi:10.1007/s00221-014-3953-6

    Article  PubMed  Google Scholar 

  • Szturm T, Ireland DJ, Jell RM (1987) Convergent effects from vestibulospinal tract and primary cutaneous afferent fibers on motoneurons to ankle extensor and flexor muscles in humans. Exp Neurol 97:529–541

    Article  PubMed  CAS  Google Scholar 

  • Tax AA, Van Wezel BM, Dietz V (1995) Bipedal reflex coordination to tactile stimulation of the sural nerve during human running. J Neurophysiol 73:1947–1964

    PubMed  CAS  Google Scholar 

  • Van Wezel BM, Ottenhoff FA, Duysens J (1997) Dynamic control of location-specific information in tactile cutaneous reflexes from the foot during human walking. J Neurosci 17:3804–3814

    PubMed  Google Scholar 

  • Yang JF, Stein RB (1990) Phase-dependent reflex reversal in human leg muscles during walking. J Neurophysiol 63:1109–1117

    PubMed  CAS  Google Scholar 

  • Yang JF, Stein RB, James KB (1991) Contribution of peripheral afferents to the activation of the soleus muscle during walking in humans. Exp Brain Res 87:679–687

    Article  PubMed  CAS  Google Scholar 

  • Zehr EP, Duysens J (2004) Regulation of arm and leg movement during human locomotion. Neuroscientist 10:347–361. doi:10.1177/1073858404264680

    Article  PubMed  Google Scholar 

  • Zehr EP, Collins DF, Chua R (2001) Human interlimb reflexes evoked by electrical stimulation of cutaneous nerves innervating the hand and foot. Exp Brain Res 140:495–504. doi:10.1007/s002210100857

    Article  PubMed  CAS  Google Scholar 

  • Zehr EP, Balter JE, Ferris DP, Hundza SR, Loadman PM, Stoloff RH (2007) Neural regulation of rhythmic arm and leg movement is conserved across human locomotor tasks. J Physiol 582:209–227. doi:10.1113/jphysiol.2007.133843

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by JSPS KAKENHI Grant Number 25350701 to T.K. R.A.M. was supported by the BEPE program (Proc. No. 2012/05304-5) from FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo).

Author information

Authors and Affiliations

  1. Division of Health and Sports Education, The United Graduate School of Education, Tokyo Gakugei University, Tokyo, Japan

    Shinya Suzuki, Genki Futatsubashi & Tomoyoshi Komiyama

  2. Department of Integrative Physiology, Kyorin University School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo, 181-8611, Japan

    Shinya Suzuki, Tsuyoshi Nakajima & Yukari Ohki

  3. Faculty of Business and Information Sciences, Jobu University, Gunma, Japan

    Genki Futatsubashi

  4. Laboratory of Signal Processing and Motor Control, College of Physical Education, University of Brasília, Brasília, Brazil

    Rinaldo A. Mezzarane

  5. Biomedical Engineering Laboratory, EPUSP, PTC, University of São Paulo, São Paulo, Brazil

    Rinaldo A. Mezzarane

  6. Division of Health and Sports Sciences, Faculty of Education, Chiba University, 1-33 Yayoicho, Inage-ku, Chiba, 263-8522, Japan

    Rinaldo A. Mezzarane & Tomoyoshi Komiyama

  7. Department of Physical Therapy, School of Rehabilitation Sciences, Health Sciences University of Hokkaido, Hokkaido, Japan

    Hiroyuki Ohtsuka

Authors
  1. Shinya Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tsuyoshi Nakajima
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Genki Futatsubashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rinaldo A. Mezzarane
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hiroyuki Ohtsuka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yukari Ohki
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tomoyoshi Komiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tomoyoshi Komiyama.

Ethics declarations

Conflict of interest

No conflict of interest exists.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suzuki, S., Nakajima, T., Futatsubashi, G. et al. Phase-dependent reversal of the crossed conditioning effect on the soleus Hoffmann reflex from cutaneous afferents during walking in humans. Exp Brain Res 234, 617–626 (2016). https://doi.org/10.1007/s00221-015-4463-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-015-4463-x

Keywords

Search

Navigation