Rhythmic arm cycling produces a non-specific signal that suppresses Soleus H-reflex amplitude in stationary legs

Abstract

Rhythmic arm cycling significantly suppresses Hoffmann (H-) reflex amplitude in Soleus muscles of stationary legs. The specific parameters of arm cycling contributing to this suppression, however, are unknown. Between the arms or legs, movement results in suppression of the H-reflex that is specifically related to the phase of movement and the locus of limb movement. We speculated that the effects of arm movement features on H-reflexes in the leg would be similar and hypothesized that the Soleus H-reflex suppression evoked by arm movement would therefore be specifically related to: (1) phase of the movement; (2) the locus of the movement (i.e., ipsilateral or contralateral arm); (3) range of arm motion; and (4) frequency of arm cycling. Participants performed bilateral arm cycling at 1 and 2 Hz with short and long-crank lengths. Ipsilateral and contralateral arm cycling was also performed at 1 Hz with a long-crank length. Soleus H-reflexes were evoked at four equidistant phases and comparisons were made while maintaining similar evoked motor waves and Soleus activation. Our results show that comparable suppressive effects were seen at all phases of the arm movement: there was no phase-dependence. Further, bilateral or unilateral (whether ipsi- or contralateral arm) cycling yielded equivalent suppression of the H-reflex amplitude. Cycling at 2 Hz resulted in a significantly larger suppression than with 1 Hz cycling. We conclude that a general, rather than a specific, signal related to the command to produce rhythmic arm muscle activity mediates the suppression of Soleus H-reflex during arm cycling.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Abbruzzese G, Berardelli A, Rothwell JC, Day BL, Marsden CD (1985) Cerebral potentials and electromyographic responses evoked by stretch of wrist muscles in man. Exp Brain Res 58:544–551

    PubMed  Article  CAS  Google Scholar 

  2. Bergmans J, Delwaide PJ, Gadea-Ciria M (1978) Short-latency effects of low-threshold muscular afferent fibers on different motoneuronal pools of the lower limb in man. Exp Neurol 60:380–385

    PubMed  Article  CAS  Google Scholar 

  3. Brooke JD, Cheng J, Collins DF, McIlroy WE, Misiaszek JE, Staines WR (1997) Sensori-sensory afferent conditioning with leg movement: gain control in spinal reflex and ascending paths. Prog Neurobiol 51:393–421

    PubMed  Article  CAS  Google Scholar 

  4. Capaday C, Stein RB (1987) Difference in the amplitude of the human soleus H reflex during walking and running. J Physiol (Lond) 392:513–522

    CAS  Google Scholar 

  5. Cheng J, Brooke JD, Misiaszek JE, Staines WR (1995a) The relationship between the kinematics of passive movement, the stretch of extensor muscles of the leg and the change induced in the gain of the soleus H reflex in humans. Brain Res 672:89–96

    Article  CAS  Google Scholar 

  6. Cheng J, Brooke JD, Misiaszek JE, Staines WR (1998) Crossed inhibition of the soleus H reflex during passive pedalling movement. Brain Res 779:280–284

    PubMed  Article  CAS  Google Scholar 

  7. Cheng J, Brooke JD, Staines WR, Misiaszek JE, Hoare J (1995b) Long-lasting conditioning of the human soleus H reflex following quadriceps tendon tap. Brain Res 681:197–200

    Article  Google Scholar 

  8. 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

    PubMed  Article  CAS  Google Scholar 

  9. Crone C, Nielsen J (1994) Central control of disynaptic reciprocal inhibition in humans. Acta Physiol Scand 152:351–363

    PubMed  CAS  Google Scholar 

  10. Delwaide PJ, Figiel C, Richelle C (1977) Effects of postural changes of the upper limb on reflex transmission in the lower limb. Cervicolumbar reflex interactions in man. J Neurol Neurosurg Psychiatr 40:616–621

    PubMed  CAS  Google Scholar 

  11. Dietz V (2002) Do human bipeds use quadrupedal coordination? Trends Neurosci 25:462–467

    PubMed  Article  Google Scholar 

  12. Dietz V, Fouad K, Bastiaanse CM (2001) Neuronal coordination of arm and leg movements during human locomotion. Eur J Neurosci 14:1906–1914

    PubMed  Article  CAS  Google Scholar 

  13. Donker SF, Beek PJ, Wagenaar RC, Mulder T (2001) Coordination between arm and leg movements during locomotion. J Mot Behav 33:86–102

    PubMed  CAS  Article  Google Scholar 

  14. Donker SF, Daffertshofer A, Beek PJ (2005) Effects of velocity and limb loading on the coordination between limb movements during walking. J Mot Behav 37:217–230

    PubMed  Article  CAS  Google Scholar 

  15. Eke-Okoro ST (1994) Evidence of interaction between human lumbosacral and cervical neural networks during gait. Electromyogr Clin Neurophysiol 34:345–349

    PubMed  CAS  Google Scholar 

  16. Fernandez-Ballesteros ML, Buchtal F, Rosenfalck P (1965) The pattern of muscular activity during the arm swing of natural walking. Acta Physiol Scand 63:296–310

    Google Scholar 

  17. Ferris DP, Huang HJ, Kao PC (2006) Moving the arms to activate the legs. Exerc Sport Sci Rev 34:113–120

    PubMed  Article  Google Scholar 

  18. Forssberg H, Grillner S, Rossignol S (1977) Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion. Brain Res 132:121–139

    PubMed  Article  CAS  Google Scholar 

  19. 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

    PubMed  Article  Google Scholar 

  20. Grillon C, Zarifian E (1985) Hoffmann reflex variations produced by task demand characteristics. Physiol Behav 34:213–216

    PubMed  Article  CAS  Google Scholar 

  21. 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

    PubMed  Article  Google Scholar 

  22. Hiraoka K (2001) Phase-dependent modulation of the soleus H-reflex during rhythmical arm swing in humans. Electromyogr Clin Neurophysiol 41:43–47

    PubMed  CAS  Google Scholar 

  23. Honore J, Demaire C, Coquery JM (1983) Effects of spatially oriented attention on the facilitation of the H reflex by a cutaneous stimulus. Electroencephalogr Clin Neurophysiol 55:156–161

    PubMed  Article  CAS  Google Scholar 

  24. Huang HJ, Ferris DP (2004) Neural coupling between upper and lower limbs during recumbent stepping. J Appl Physiol 97:1299–1308

    PubMed  Article  Google Scholar 

  25. Hultborn H, Meunier S, Morin C, Pierrot-Deseilligny E (1987) Assessing changes in presynaptic inhibition of Ia fibres: a study in man and cat. J Physiol 389:729–756

    PubMed  CAS  Google Scholar 

  26. Iles JF, Roberts RC (1986) Presynaptic inhibition of monosynaptic reflexes in the lower limbs of subjects with upper motoneuron disease. J Neurol Neurosurg Psychiatr 49:937–944

    PubMed  CAS  Article  Google Scholar 

  27. Iles JF, Roberts RC (1987) Inhibition of monosynaptic reflexes in the human lower limb. J Physiol (Lond) 385:69–87

    CAS  Google Scholar 

  28. Jackson KM, Joseph J, Wyard SJ (1983) The upper limbs during human walking. Part 2: function. Electromyogr Clin Neurophysiol 23:435–446

    PubMed  CAS  Google Scholar 

  29. Juvin L, Simmers J, Morin D (2005) Propriospinal circuitry underlying interlimb coordination in mammalian quadrupedal locomotion. J Neurosci 25:6025–6035

    PubMed  Article  CAS  Google Scholar 

  30. Kao PC, Ferris DP (2005) The effect of movement frequency on interlimb coupling during recumbent stepping. Motor Control 9:144–163

    PubMed  Google Scholar 

  31. Llewellyn M, Yang JF, Prochazka A (1990) Human H-reflexes are smaller in difficult beam walking than in normal treadmill walking. Exp Brain Res 83:22–28

    PubMed  Article  CAS  Google Scholar 

  32. McIlroy WE, Collins DF, Brooke JD (1992) Movement features and H-reflex modulation. II. Passive rotation, movement velocity and single leg movement. Brain Res 582:85–93

    PubMed  Article  CAS  Google Scholar 

  33. Meunier S, Pierrot-Deseilligny E, Simonetta M (1993) Pattern of monosynaptic heteronymous Ia connections in the human lower limb. Exp Brain Res 96:534–544

    PubMed  Article  CAS  Google Scholar 

  34. Miller S, Ruit JB, van der Meche FG (1977) Reversal of sign of long spinal reflexes dependent on the phase of the step cycle in the high decerebrate cat. Brain Res 128:447–459

    PubMed  Article  CAS  Google Scholar 

  35. Miller S, van der Burg J, van der Meche FGA (1975) Coordination of movements of the hindlimbs and forelimbs in different forms of locomotion in normal and decerebrate cats. Brain Res 91:217–237

    PubMed  Article  CAS  Google Scholar 

  36. Petersen N, Morita H, Nielsen J (1998) Evaluation of reciprocal inhibition of the soleus H-reflex during tonic plantar flexion in man. J Neurosci Methods 84:1–8

    PubMed  Article  CAS  Google Scholar 

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

    Google Scholar 

  38. Pierrot-Deseilligny E, Mazevet D (2000) The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits. Neurophysiol Clin 30:67–80

    PubMed  Article  CAS  Google Scholar 

  39. Pierrot-Deseilligny E, Morin C, Katz R, Bussel B (1977) Influence of voluntary movement and posture on recurrent inhibition in human subjects. Brain Res 124:427–436

    PubMed  Article  CAS  Google Scholar 

  40. Schneider C, Lavoie BA, Capaday C (2000) On the origin of the soleus H-reflex modulation pattern during human walking and its task-dependent differences. J Neurophysiol 83:2881–2890

    PubMed  CAS  Google Scholar 

  41. Schomburg ED, Meinck HM, Haustein J, Roesler J (1978) Functional organization of the spinal reflex pathways from forelimb afferents to hindlimb motoneurones in the cat. Brain Res 139:21–33

    PubMed  Article  CAS  Google Scholar 

  42. Swett JE, Bourassa CM (1981) Electrical stimulation of peripheral nerve. In: Patterson MM, Kesner RP (eds) Electrical research stimulation techniques. Academic Press, New York, pp 243–295

    Google Scholar 

  43. Tanaka R (1974) Reciprocal Ia inhibition during voluntary movements in man. Exp Brain Res 21:529–540

    PubMed  Article  CAS  Google Scholar 

  44. Webb D, Tuttle RH, Baksh M (1994) Pendular activity of human upper limbs during slow and normal walking. Am J Phys Anthropol 93:477–489

    PubMed  Article  CAS  Google Scholar 

  45. Zehr EP (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468

    PubMed  Article  Google Scholar 

  46. Zehr EP (2005) Neural control of rhythmic human movement: the common core hypothesis. Exerc Sport Sci Rev 33:54–60

    PubMed  Google Scholar 

  47. Zehr EP, Carroll TJ, Chua R, Collins DF, Frigon A, Haridas C, Hundza SR, Kido A (2004a) Possible contributions of spinal CPG activity to rhythmic human arm movement. Can J Physiol Pharmacol 82:556–568

    Article  CAS  Google Scholar 

  48. Zehr EP, Collins DF, Frigon A, Hoogenboom N (2003) Neural control of rhythmic human arm movement: phase dependence and task modulation of Hoffmann reflexes in forearm muscles. J Neurophysiol 89:12–21

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  50. Zehr EP, Hoogenboom N, Frigon A, Collins DF (2004b) Facilitation of Soleus H-reflex amplitude evoked by cutaneous nerve stimulation at the wrist is not suppressed by rhythmic arm movement. Exp Brain Res 159:382–388

    Article  Google Scholar 

  51. Zehr EP, Stein RB (1999) What functions do reflexes serve during human locomotion? Prog Neurobiol 58:185–205

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants to EPZ from the Natural Sciences and Engineering Council of Canada (NSERC), the Heart and Stroke Foundation of Canada (BC & Yukon), and the Michael Smith Foundation for Health Research.

Author information

Affiliations

Authors

Corresponding author

Correspondence to E. Paul Zehr.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Loadman, P.M., Zehr, E.P. Rhythmic arm cycling produces a non-specific signal that suppresses Soleus H-reflex amplitude in stationary legs. Exp Brain Res 179, 199–208 (2007). https://doi.org/10.1007/s00221-006-0782-2

Download citation

Keywords

  • Tibialis Anterior
  • Vastus Lateralis
  • Flexor Carpus Radialis
  • Movement Trial
  • Recruitment Curve