Soleus H-reflex and its relation to static postural control

Gait and Posture

Volumn 33, Issue 2, 2011, Pages 169-178

  Chen, Yung Sheng ^a   Zhou, Shi ^a  

^a SOUTHERN CROSS UNIVERSITY   (Australia)

Author keywords

Balance training; H reflex; Spinal mechanisms; Static postural control; Supraspinal mechanisms

Indexed keywords

ACTION POTENTIAL; BASAL GANGLION; BODY EQUILIBRIUM; BODY POSITION; BODY POSTURE; BRAIN CELL; CEREBELLUM; ELECTRODE; ELECTROMYOGRAM; ELECTROSTIMULATION; GAIT; GALVANIC VESTIBULAR TEST; H WAVE; HOFFMANN REFLEX; HUMAN; INTERNEURON; JOINT STABILITY; LOCOMOTION; M WAVE; MOTOR COORDINATION; MOVEMENT PERCEPTION; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE FORCE; MUSCLE FUNCTION; MUSCLE INNERVATION; MUSCLE SPINDLE AFFERENT NERVE; MUSCLE TONE; NERVE CELL EXCITABILITY; NERVE CONDUCTION; NERVE STIMULATION; NEUROMODULATION; PASSIVE MOVEMENT; PRESYNAPTIC INHIBITION; PRIMARY AFFERENT DEPOLARIZATION; PRIORITY JOURNAL; PROPRIOCEPTIVE FEEDBACK; RECURRENT INHIBITION; RENSHAW CELL; RESISTANCE TRAINING; REVIEW; SKIN SENSATION; SOLEUS MUSCLE; SOMATOSENSORY STIMULATION; SPATIAL ORIENTATION; SPINE MOBILITY; STANDING; SYNAPTIC INHIBITION; TRAINING; TRICEPS SURAE MUSCLE; VESTIBULAR STIMULATION; VISUAL FEEDBACK; VOLUNTARY MOVEMENT;

ELECTRODES; H-REFLEX; HUMANS; MUSCLE, SKELETAL; POSTURE; SPINE;

EID: 79951552711     PISSN: 09666362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gaitpost.2010.12.008     Document Type: Review

References (121)

1. Hoffmann P. Beitrag zur Kenntnis der menschlichen Reflexe mit besonderer Berucksichtigung der elektrischen Erscheinungen. Arch Anat Physiol 1910, 1:223-246.
2. Magladery J.W., Porter W.E., Park A.M., Teasdall R.D. Electrophysiological studies on nerve and reflex activity in normal man. IV. Two-neurone reflex and identification of certain action potentials from spinal roots and cord. Bull Johns Hopkin's Hosp 1951, 88:499-519.
3. Hultborn H. Spinal reflexes, mechanisms and concepts: from Eccles to Lundberg and beyond. Prog Neurobiol 2006, 78:215-232.
4. Zehr P. Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 2002, 86(6):455-468.
5. Taube W., Leukel C., Gollhofer A. Influence of enhanced visual feedback on postural control and spinal reflex modulation during stance. Exp Brain Res 2008, 188:353-361.
6. Tokuno C.D., Carpenter M.G., Thorstensson A., Garland S.J., Cresswell A.G. Control of the triceps surae during the postural sway of quiet standing. Acta Physiol (Oxf) 2007, 191:229-236.
7. Tokuno C.D., Garland S.J., Carpenter M.G., Thorstensson A., Cresswell A.G. Sway-dependent modulation of the triceps surae H-reflex during standing. J Appl Physiol 2008, 104:1359-1365.
8. Earles D.R., Koceja D.M., Shively C.W. Environmental changes in soleus H-reflex excitability in young and elderly subjects. Int J Neurosci 2000, 105:1-13.
9. Mynark R.G., Koceja D.M. Down training of the elderly soleus H reflex with the use of a spinally induced balance perturbation. J Appl Physiol 2002, 93:127-133.
10. Taube W., Gruber M., Gollhofer A. Spinal and supraspinal adaptations associated with balance training and their functional relevance. Acta Physiol (Oxf) 2008, 193:101-116.
11. Aagaard P., Simonsen E.B., Andersen J.L., Magnusson P., Dyhre-Poulsen P. Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 2002, 92:2309-2318.
12. Tucker K.J., Tuncer M., Turker K.S. A review of the H-reflex and M-wave in the human triceps surae. Hum Mov Sci 2005, 24:667-688.
13. Frigon A., Carroll T.J., Jones K.E., Zehr E.P., Collins D.F. Ankle position and voluntary contraction alter maximal M waves in soleus and tibialis anterior. Muscle Nerve 2007, 35:756-766.
14. Misiaszek J.E. The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function. Muscle Nerve 2003, 28:144-160.
15. Panizza M., Nilsson J., Roth B.J., Grill S.E., Demirci M., Hallett M. Differences between the time constant of sensory and motor peripheral nerve fibers: further studies and considerations. Muscle Nerve 1998, 21:48-54.
16. Pierrot-Deseilligny E., Mazevet D. The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits. Neurophysiol Clin 2000, 30:67-80.
17. Ali A., Sabbahi M.A. Test-retest reliability of the soleus H-reflex in three different positions. Electromyogr Cin Neurophysiol 2001, 41:209-214.
18. Hopkins J.T., Ingersoll C.D., Cordova M.L., Edwards J.E. Intrasession and intersession reliability of the soleus H-reflex in supine and standing positions. Electromyogr Clin Neurophysiol 2000, 40:89-94.
19. Mynark R.G. Reliability of the soleus H-reflex from supine to standing in young and elderly. Clin Neurophysiol 2005, 116:1400-1404.
20. Earles D.R., Morris H.H., Peng C.Y., Koceja D.M. Assessment of motoneuron excitability using recurrent inhibition and paired reflex depression protocols: a test of reliability. Electromyogr Clin Neurophysiol 2002, 42:159-166.
21. Jaberzadeh S., Scutter S., Warden-Flood A., Nazeran H. Between-days reliability of H-reflexes in human flexor carpi radialis. Arch Phys Med Rehabil 2004, 85:1168-1173.
22. Stowe A.M., Hughes-Zahner L., Stylianou A.P., Schindler-Ivens S., Quaney B.M. Between-day reliability of upper extremity H-reflexes. J Neurosci Methods 2008, 170:317-323.
23. Palmieri R.M., Hoffman M.A., Ingersoll C.D. Intersession reliability for H-reflex measurements arising from the soleus, peroneal, and tibialis anterior musculature. Int J Neurosci 2002, 112:841-850.
24. Palmieri R.M., Ingersoll C.D., Hoffman M.A. The Hoffmann reflex: methodologic considerations and applications for use in sports medicine and athletic training research. J Athl Train 2004, 39:268-277.
25. Capaday C. Neurophysiological methods for studies of the motor system in freely moving human subjects. J Neurosci Methods 1997, 74:201-218.
26. Hermens H.J., Freriks B., Disselhorst-Klug C., Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 2000, 10:361-374.
27. Brinkworth R.S., Tuncer M., Tucker K.J., Jaberzadeh S., Turker K.S. Standardization of H-reflex analyses. J Neurosci Methods 2007, 162:1-7.
28. Tucker K.J., Türker K.S. Muscle spindle feedback differs between the soleus and gastrocnemius in humans. Somatosens Mot Res 2004, 21:189-197.
29. Tucker K.J., Turker K.S. Triceps surae stretch and voluntary contraction alters maximal M-wave magnitude. J Electromyogr Kinesiol 2007, 17:203-211.
30. Stein R.B., Thompson A.K. Muscle reflexes in motion: how, what, and why?. Exerc Sport Sci Rev 2006, 34:145-153.
31. Kiernan M.C., Lin C.S., Burke D. Differences in activity-dependent hyperpolarization in human sensory and motor axons. J Physiol (Lond) 2004, 558:341-349.
32. Lin C.S., Chan J.H., Pierrot-Deseilligny E., Burke D. Excitability of human muscle afferents studied using threshold tracking of the H reflex. J Physiol (Lond) 2002, 545:661-669.
33. Lagerquist O., Collins D.F. Stimulus pulse-width influences H-reflex recruitment but not H(max)/M(max) ratio. Muscle Nerve 2008, 37:483-489.
34. Voigt M., Sinkjaer T. The H-reflex in the passive human soleus muscle is modulated faster than predicted from post-activation depression. Brain Res 1998, 783:332-346.
35. Hultborn H., Illert M., Nielsen J., Paul A., Ballegaard M., Wiese H. On the mechanism of the post-activation depression of the H-reflex in human subjects. Exp Brain Res 1996, 108:450-462.
36. Schieppati M., Nardone A., Siliotto R., Grasso M. Early and late stretch responses of human foot muscles induced by perturbation of stance. Exp Brain Res 1995, 105:411-422.
37. Stein R.B., Estabrooks K.L., McGie S., Roth M.J., Jones K.E. Quantifying the effects of voluntary contraction and inter-stimulus interval on the human soleus H-reflex. Exp Brain Res 2007, 182:309-319.
38. Beck T.W., Housh T.J., Johnson G.O., Weir J.P., Cramer J.T., Coburn J.W., et al. The effects of interelectrode distance on electromyographic amplitude and mean power frequency during isokinetic and isometric muscle actions of the biceps brachii. J Electromyogr Kinesiol 2005, 15:482-495.
39. Tucker K.J., Turker K.S. A new method to estimate signal cancellation in the human maximal M-wave. J Neurosci Methods 2005, 149:31-41.
40. Rainoldi A., Melchiorri G., Caruso I. A method for positioning electrodes during surface EMG recordings in lower limb muscles. J Neurosci Methods 2004, 134:37-43.
41. Mesin L., Merletti R., Rainoldi A. Surface EMG: the issue of electrode location. J Electromyogr Kinesiol 2009, 19:719-726.
42. Mario C., Vladimir M., Tonković S., Ostojić S. Surface EMG based muscle fatigue evaluation in biomechanics. Clin Biomech (Bristol, Avon) 2009, 24:327-340.
43. Cresswell A.G., Löscher W.N. Significance of peripheral afferent input to the α-motoneurone pool for enhancement of tremor during an isometric fatiguing contraction. Eur J Appl Physiol 2000, 82:129-136.
44. Rupp T., Girard O., Perrey S. Redetermination of the optimal stimulation intensity modifies resting H-reflex recovery after a sustained moderate-intensity muscle contraction. Muscle Nerve 2010, 41:642-650.
45. Walton D.M., Kuchinad R.A., Ivanova T.D., Garland S.J. Reflex inhibition during muscle fatigue in endurance-trained and sedentary individuals. Eur J Appl Physiol 2002, 87:462-468.
46. Sibley K.M., Carpenter M.G., Perry J.C., Frank J.S. Effects of postural anxiety on the soleus H-reflex. Hum Mov Sci 2007, 26:103-112.
47. Nozaki D., Nakazawa K., Yamamoto Y. Fractal correlation in human H-reflex. Exp Brain Res 1995, 105:402-410.
48. Winter D.A., Patla A.E., Prince F., Ishac M., Gielo-Perczak K. Stiffness control of balance in quiet standing. J Neurophysiol 1998, 80:1211-1221.
49. Winter D.A., Patla A.E., Rietdyk S., Ishac M.G. Ankle muscle stiffness in the control of balance during quiet standing. J Neurophysiol 2001, 85:2630-2633.
50. Tsang W.W., Hui-Chan C.W. Effect of 4- and 8-wk intensive Tai Chi Training on balance control in the elderly. Med Sci Sports Exerc 2004, 36:648-657.
51. Slobounov S., Hallett M., Cao C., Newell K. Modulation of cortical activity as a result of voluntary postural sway direction: an EEG study. Neurosci Lett 2008, 442:309-313.
52. Taube W., Schubert M., Gruber M., Beck S., Faist M., Gollhofer A. Direct corticospinal pathways contribute to neuromuscular control of perturbed stance. J Appl Physiol 2006, 101:420-429.
53. Koceja D.M., Trimble M.H., Earles D.R. Inhibition of the soleus H-reflex in standing man. Brain Res 1993, 629:155-158.
54. Shaffer S.W., Harrison A.L. Aging of the somatosensory system: a translational perspective. Phys Ther 2007, 87:193-207.
55. Brooke J.D., Zehr E.P. Limits to fast-conducting somatosensory feedback in movement control. Exerc Sport Sci Rev 2006, 34:22-28.
56. Horak F.B., Earhart G.M., Dietz V. Postural responses to combinations of head and body displacements: vestibular-somatosensory interactions. Exp Brain Res 2001, 141:410-414.
57. Winter J.A., Allen T.J., Proske U. Muscle spindle signals combine with the sense of effort to indicate limb position. J Physiol (Lond) 2005, 568:1035-1046.
58. Iles J.F. Evidence for cutaneous and corticospinal modulation of presynaptic inhibition of Ia afferents from the human lower limb. J Physiol (Lond) 1996, 491(1):197-207.
59. McIlroy W.E., Bishop D.C., Staines W.R., Nelson A.J., Maki B.E., Brooke J.D. Modulation of afferent inflow during the control of balancing tasks using the lower limbs. Brain Res 2003, 961:73-80.
60. Sayenko D.G., Vette A.H., Obata H., Alekhina M.I., Akai M., Nakazawa K. Differential effects of plantar cutaneous afferent excitation on soleus stretch and H-reflex. Muscle Nerve 2009, 39:761-769.
61. Franklin D.W., So U., Burdet E., Kawato M. Visual feedback is not necessary for the learning of novel dynamics. PLoS One 2007, 19.2:e1336.
62. Duarte M., Zatsiorsky V.M. Effects of body lean and visual information on the equilibrium maintenance during stance. Exp Brain Res 2002, 146:60-69.
63. Wessberg J., Vallbo A.B. Human muscle spindle afferent activity in relation to visual control in precision finger movements. J Physiol (Lond) 1995, 482(1):225-233.
64. Hafström A., Fransson P.A., Karlberg M., Ledin T., Magnusson M. Visual influence on postural control, with and without visual motion feedback. Acta Otolaryngol 2002, 122:392-397.
65. Hue O., Simoneau M., Marcotte J., Berrigan F., Doré J., Marceau P., et al. Body weight is a strong predictor of postural stability. Gait Posture 2007, 26:32-38.
66. Van Deun S., Staes F.F., Stappaerts K.H., Janssens L., Levin O., Peers K.K. Relationship of chronic ankle instability to muscle activation patterns during the transition from double-leg to single-leg stance. Am J Sports Med 2007, 35:274-281.
67. Horak F.B., Shupert C.L., Dietz V., Horstmann G. Vestibular and somatosensory contributions to responses to head and body displacements in stance. Exp Brain Res 1994, 100:93-106.
68. Lowrey C.R., Bent L.R. Modulation of the soleus H-reflex following galvanic vestibular stimulation and cutaneous stimulation in prone human subjects. Muscle Nerve 2009, 40:213-220.
69. Keller A. Intrinsic synaptic organization of the motor cortex. Cereb Cortex 1993, 3:430-441.
70. Soto O., Valls-Sole J., Shanahan P., Rothwell J. Reduction of intracortical inhibition in soleus muscle during postural activity. J Neurophysiol 2006, 96:1711-1717.
71. Taube W., Gruber M., Beck S., Faist M., Gollhofer A., Schubert M. Cortical and spinal adaptations induced by balance training: correlation between stance stability and corticospinal activation. Acta Physiol (Oxf) 2007, 189:347-358.
72. Ioffe M.E., Chernikova L.A., Ustinova K.I. Role of cerebellum in learning postural tasks. Cerebellum 2007, 6:87-94.
73. Morton S.M., Bastian A.J. Cerebellar control of balance and locomotion. Neuroscientist 2004, 10:247-259.
74. Tokuda T., Tako K., Hayashi R., Yanagisawa N. Disturbed modulation of the stretch reflex gain during standing in cerebellar ataxia. Electroencephalogr Clin Neurophysiol 1991, 81:421-426.
75. Mauritz K.H., Schmitt C., Dichgans J. Delayed and enhanced long latency reflexes as the possible cause of postural tremor in late cerebellar atrophy. Brain 1981, 104:97-116.
76. Middleton F.A., Strick P.L. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev 2000, 31:236-250.
77. Takakusaki K., Saitoh K., Harada H., Kashiwayanagi M. Role of basal ganglia-brainstem pathways in the control of motor behaviors. Neurosci Res 2004, 50:137-151.
78. Takakusaki K., Oohinata-Sugimoto J., Saitoh K., Habaguchi T. Role of basal ganglia-brainstem systems in the control of postural muscle tone and locomotion. Prog Brain Res 2004, 143:231-237.
79. Berardelli A., Rothwell J., Hallett M., Thompson P., Manfredi M., Marsden C. The pathophysiology of primary dystonia. Brain 1998, 121:1195-1212.
80. Berardelli A., Rothwell J.C., Thompson P.D., Hallett M. Pathophysiology of bradykinesia in Parkinson's disease. Brain 2001, 124:2131-2146.
81. Stein R.B. Presynaptic inhibition in humans. Prog Neurobiol 1995, 47:533-544.
82. Guissard N., Duchateau J. Neural aspects of muscle stretching. Exerc Sport Sci Rev 2006, 34:154-158.
83. Aggelopoulos N.C., Chakrabarty S., Edgley S.A. Presynaptic control of transmission through group II muscle afferents in the midlumbar and sacral segments of the spinal cord is independent of corticospinal control. Exp Brain Res 2008, 187:61-70.
84. Jankowska E. Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 1992, 38:335-378.
85. Knikou M. The H-reflex as a probe: pathways and pitfalls. J Neurosci Methods 2008, 171:1-12.
86. Rudomin P., Schmidt R.F. Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 1999, 129:1-37.
87. Widmaier E.P., Raff H., Strang K.T. Vander's human physiology: the mechanisms of body function 2008, McGraw-Hill, New York. 11th ed.
88. Pierrot-Deseilligny E. Assessing changes in presynaptic inhibition of Ia afferents during movement in humans. J Neurosci Methods 1997, 74:189-199.
89. Crone C., Hultborn H., Jespersen B., Nielsen J. Reciprocal Ia inhibition between ankle flexors and extensors in man. J Physiol (Lond) 1987, 389:163-185.
90. Leonard C.T., Sandholdt D.Y., McMillan J.A. Long-latency contributions to reciprocal inhibition during various levels of muscle contraction. Brain Res 1999, 817:1-12.
91. Nielsen J., Kagamihara Y. The regulation of disynaptic reciprocal Ia inhibition during co-contraction of antagonistic muscles in man. J Physiol (Lond) 1992, 456:373-391.
92. Hultborn H., Illert M., Santini M. Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. III. Effects from supraspinal pathways. Acta Physiol Scand 1976, 96:368-391.
93. Petersen N., Morita H., Nielsen J. Evaluation of reciprocal inhibition of the soleus H-reflex during tonic plantar flexion in man. J Neurosci Methods 1998, 84:1-8.
94. Crone C., Nielsen J. Spinal mechanisms in man contributing to reciprocal inhibition during voluntary dorsiflexion of the foot. J Physiol (Lond) 1989, 416:255-272.
95. Hultborn H., Illert M., Santini M. Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. II. Effects from segmental flexor reflex pathways. Acta Physiol Scand 1976, 96:351-367.
96. Baret M., Katz R., Lamy J.C., Penicaud A., Wargon I. Evidence for recurrent inhibition of reciprocal inhibition from soleus to tibialis anterior in man. Exp Brain Res 2003, 152:133-136.
97. Pierrot-Deseilligny E., Burke D. The circuitry of the human spinal cord 2005, Cambridge University Press, Cambridge, UK.
98. Hwang I.S., Lin Y.C., Ho K.Y. Modulation of soleus H-reflex amplitude and variance during pretibial contraction-effects of joint position and effort level. Int J Neurosci 2002, 112:623-638.
99. Renshaw B. Central effects of centripetal impulses in axons of spinal ventral roots. J Neurophysiol 1946, 9:191-204.
100. Hultborn H., Pierrot-Deseilligny E. Changes in recurrent inhibition during voluntary soleus contractions in man studied by an H-reflex technique. J Physiol (Lond) 1979, 297:229-251.
101. Katz R., Pierrot-Deseilligny E. Recurrent inhibition in humans. Prog Neurobiol 1999, 57:325-355.
102. Hultborn H., Pierrot-Deseilligny E. Input-output relations in the pathway of recurrent inhibition to motoneurones in the cat. J Physiol (Lond) 1979, 297:267-287.
103. Barbeau H., Marchand-Pauvert V., Meunier S., Nicolas G., Pierrot-Deseilligny E. Posture-related changes in heteronymous recurrent inhibition from quadriceps to ankle muscles in humans. Exp Brain Res 2000, 130:345-361.
104. Faist M., Hoefer C., Hodapp M., Dietz V., Berger W., Duysens J. In humans Ib facilitation depends on locomotion while suppression of Ib inhibition requires loading. Brain Res 2006, 1076:87-92.
105. Stephens M.J., Yang J.F. Short latency, non-reciprocal group I inhibition is reduced during the stance phase of walking in humans. Brain Res 1996, 743:24-31.
106. Koceja D.M., Markus C.A., Trimble M.H. Postural modulation of the soleus H reflex in young and old subjects. Electroencephalogr Clin Neurophysiol 1995, 97:387-393.
107. Huang C.Y., Cherng R.J., Yang Z.R., Chen Y.T., Hwang I.S. Modulation of soleus H reflex due to stance pattern and haptic stabilization of posture. J Electromyogr Kinesiol 2009, 19:492-499.
108. Laudani L., Wood L., Casabona A., Giuffrida R., De Vito G. Effects of repeated ankle plantar-flexions on H-reflex and body sway during standing. J Electromyogr Kinesiol 2009, 19:85-92.
109. Hoffman M.A., Koceja D.M. The effects of vision and task complexity on Hoffmann reflex gain. Brain Res 1995, 700:303-307.
110. Chalmers G.R., Knutzen K.M. Soleus H-reflex gain in healthy elderly and young adults when lying, standing, and balancing. J Gerontol A: Biol Sci Med Sci 2002, 57:B321-B329.
111. Sefton J.M., Hicks-Little C.A., Koceja D.M., Cordova M.L. Modulation of soleus H-reflex by presynaptic spinal mechanisms during varying surface and ankle brace conditions. Neurophysiol Clin 2007, 37:15-21.
112. Knikou M., Rymer W.Z. Static and dynamic changes in body orientation modulate spinal reflex excitability in humans. Exp Brain Res 2003, 152:466-475.
113. Kennedy P.M., Cresswell A.G., Chua R., Inglis J.T. Vestibulospinal influences on lower limb motoneurons. Can J Physiol Pharmacol 2004, 82:675-681.
114. Chan C.W., Kearney R.E. Influence of static tilt on soleus motoneuron excitability in man. Neurosci Lett 1982, 33:333-338.
115. Trimble M.H. Postural modulation of the segmental reflex: effect of body tilt and postural sway. Int J Neurosci 1998, 95:85-100.
116. Wolpaw J.R. Spinal cord plasticity in acquisition and maintenance of motor skills. Acta Physiol (Oxf) 2007, 189:155-169.
117. Wolpaw J.R., Carp J.S. Plasticity from muscle to brain. Prog Neurobiol 2006, 78:233-263.
118. Trimble M.H., Koceja D.M. Modulation of the triceps surae H-reflex with training. Int J Neurosci 1994, 76:293-303.
119. Trimble M.H., Koceja D.M. Effect of a reduced base of support in standing and balance training on the soleus H-reflex. Int J Neurosci 2001, 106:1-20.
120. Schubert M., Beck S., Taube W., Amtage F., Faist M., Gruber M. Balance training and ballistic strength training are associated with task-specific corticospinal adaptations. Eur J Neurosci 2008, 27:2007-2018.
121. Taube W., Kullmann N., Leukel C., Kurz O., Amtage F., Gollhofer A. Differential reflex adaptations following sensorimotor and strength training in young elite athletes. Int J Sports Med 2007, 28:999-1005.