Training-induced adaptive plasticity in human somatosensory reflex pathways

Journal of Applied Physiology

Volumn 101, Issue 6, 2006, Pages 1783-1794

  Zehr, E Paul ^a,b  

^a UNIVERSITY OF VICTORIA   (Canada)

^b Human Discovery Science   (Canada)

Author keywords

Electrical stimulation; Movement; Neural function; Neuroscience; Rehabilitation

Indexed keywords

BODY POSTURE; ELECTROSTIMULATION; HUMAN; LOCOMOTION; MEDICAL RESEARCH; NERVE FUNCTION; NERVOUS SYSTEM; PLASTICITY; PRIORITY JOURNAL; REFLEX; REVIEW; SOMATOSENSORY SYSTEM; TRAINING;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; AFFERENT PATHWAYS; ANIMALS; EXERCISE; HUMANS; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE, SKELETAL; NEURONAL PLASTICITY; PHYSICAL FITNESS; REFLEX; SOMATOSENSORY CORTEX;

EID: 33845430412     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00540.2006     Document Type: Review

References (99)

1. Aagaard P. Training-induced changes in neural function. Exerc Sport Sci Rev 31: 61-67, 2003.
2. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, and Dyhre-Poulsen P. Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 92: 2309-2318, 2002.
3. Aimonetti JM, Schmied A, Vedel JP, and Pagni S. Ia presynaptic inhibition in human wrist extensor muscles: effects of motor task and cutaneous afferent activity. J Physiol Paris 93: 395-401, 1999.
4. Aimonetti JM, Vedel JP, Schmied A, and Pagni S. Distribution of presynaptic inhibition on type-identified motoneurones in the extensor carpi radialis pool in man. J Physiol 522: 125-135, 2000.
5. Aimonetti JM, Vedel JP, Schmied A, and Pagni S. Task dependence of Ia presynaptic inhibition in human wrist extensor muscles: a single motor unit study. Clin Neurophysiol 111: 1165-1174, 2000.
6. Angulo-Kinzler RM, Mynark RG, and Koceja DM. Soleus H-reflex gain in elderly and young adults: modulation due to body position. J Gerontol A Biol Sci Med Sci 53: M120-M125, 1998.
7. Balter JE and Zehr EP. Neural coupling between the arms and legs during locomotion: evidence from cutaneous reflex modulation in a leg muscle. Proc Can Phys Soc Winter Meeting 2006, Lake Louise, Alberta.
8. Barbeau H, Ladouceur M, Mirbagheri MM, and Kearney RE. The effect of locomotor training combined with functional electrical stimulation in chronic spinal cord injured subjects: walking and reflex studies. Brain Res Rev 40: 274-291, 2002.
9. Behrman AL and Harkema SJ. Locomotor training after human spinal cord injury: a series of case studies. Phys Ther 80: 688-700, 2000.
10. Brooke JD, Cheng J, Collins DF, McIlroy WE, Misiaszek JE, and Staines WR. Sensori-sensory afferent conditioning with leg movement: gain control in spinal reflex and ascending paths. Prog Neurobiol 51: 393-421, 1997.
11. Brooke JD and Zehr EP. Limits to fast-conducting somatosensory feedback in movement control. Exerc Sport Sci Rev 34: 22-28, 2006.
12. Burke RE. 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, 1999.
13. Capaday C and Stein RB. Amplitude modulation of the soleus H-reflex in the human during walking and standing. J Neurosci 6: 1308-1313, 1986.
14. Carp JS and Wolpaw JR. Motoneuron plasticity underlying operantly conditioned decrease in primate H-reflex. J Neurophysiol 72: 431-442, 1994.
15. Carp JS and Wolpaw JR. Motoneuron properties after operantly conditioned increase in primate H-reflex. J Neurophysiol 73: 1365-1373, 1995.
16. 15a. Carroll TJ, Herbert RD, Munn J, Lee M, and Gandevia SC. Contralateral effects of unilateral strength training: evidence and possible mechanisms. J Appl Physiol 101: 1514-1522, 2006.
17. Casabona A, Polizzi MC, and Perciavalle V. Differences in H-reflex between athletes trained for explosive contractions and non-trained subjects. Eur J Appl Physiol 61: 26-32, 1990.
18. Chen XY, Carp JS, Chen L, and Wolpaw JR. Sensorimotor cortex ablation prevents H-reflex up-conditioning and causes a paradoxical response to down-conditioning in rats. J Neurophysiol 96: 119-127, 2006.
19. Chen XY, Chen L, and Wolpaw JR. Conditioned H-reflex increase persists after transection of the main corticospinal tract in rats. J Neurophysiol 90: 3572-3578, 2003.
20. Chen Y, Chen XY, Jakeman LB, Schalk G, Stokes BT, and Wolpaw JR. The interaction of a new motor skill and an old one: H-reflex conditioning and locomotion in rats. J Neurosci 25: 6898-6906, 2005.
21. Cooper SJ. Donald O. Hebb's synapse and learning rule: a history and commentary. Neurosci Biobehav Rev 28: 851-874, 2005.
22. Cote MP and Gossard JP. Step training-dependent plasticity in spinal cutaneous pathways. J Neurosci 24: 11317-11327, 2004.
23. Crenna P and Frigo C. Excitability of the soleus H-reflex arc during walking and stepping in man. Exp Brain Res 66: 49-60, 1987.
24. Dewald JP, Given JD, and Rymer WZ. Long-lasting reductions of spasticity induced by skin electrical stimulation. IEEE Trans Rehabil Eng 4: 231-242, 1996.
25. Dimitrijevic MM, Stokic DS, Wawro AW, and Wun CC. Modification of motor control of wrist extension by mesh-glove electrical afferent stimulation in stroke patients. Arch Phys Med Rehabil 77: 252-258, 1996.
26. Dimitrijevic MR and Nathan PW. Studies of spasticity in man. 4. Changes in flexion reflex with repetitive cutaneous stimulation in spinal man. Brain 93: 743-768, 1970.
27. Dobkin BH, Apple D, Barbeau H, Basso M, Behrman A, Deforge D, Ditunno J, Dudley G, Elashoff R, Fugate L, Harkema S, Saulino M, and Scott M. Methods for a randomized trial of weight-supported treadmill training versus conventional training for walking during inpatient rehabilitation after incomplete traumatic spinal cord injury. Neurorehabil Neural Repair 17: 153-167, 2003.
28. Duysens J, Baken BCM, Burgers L, Plat FM, den Otter AR, and Kremer HPH. Cutaneous reflexes from the foot during gait in hereditary spastic paraparesis. Clin Neurophysiol 115: 1057-1062, 2004.
29. Duysens J, Bastiaanse CM, Smits-Engelsman BC, and Dietz V. Gait acts as a gate for reflexes from the foot. Can J Physiol Pharmacol 82: 715-722, 2004.
30. Duysens J and Tax T. Interlimb reflexes during gait in cat and human. In: Interlimb Coordination: Neural, Dynamical, and Cognitive Constraints, edited by Swinnen SP, Heuer H, Massion J, and Casaer P. San Diego, CA: Academic, 1994, p. 97-126.
31. Earles DR, Dierking JT, Robertson CT, and Koceja DM. Pre- and post-synaptic control of motoneuron excitability in athletes. Med Sci Sports Exerc 34: 1766-1772, 2002.
32. Enoka RM. Neuromechanics of Human Movement. Champaign, IL: Human Kinetics, 2002.
33. Evatt ML, Wolf SL, and Segal RL. Modification of human spinal stretch reflexes: preliminary studies. Neurosci Lett 105: 350-355, 1989.
34. Feng-Chen KC and Wolpaw JR. Operant conditioning of H-reflex changes synaptic terminals on primate motoneurons. Proc Natl Acad Sci USA 93: 9206-9211, 1996.
35. Fung J and Barbeau H. 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, 1994.
36. 34a. Gardiner P, Dai Y, and Heckman CJ. Effects of exercise training on alpha-motoneurones. J Appl Physiol 101: 1228-1236, 2006.
37. Gondin J, Duclay J, and Martin A. Soleus and gastrocnemii evoked V-wave responses increase following neuromuscular electrical stimulation training. J Neurophysiol 95: 3328-3335, 2006.
38. Goulart F, Valls-Sole J, and Alvarez R. Posture-related changes of soleus H-reflex excitability. Muscle Nerve 23: 925-932, 2000.
39. Hebb DO. The Organization of Behaviour. New York: Wiley, 1949.
40. Jensen JL, Marstrand PCD, and Nielsen JB. Motor skill training and strength training are associated with different plastic changes in the central nervous system. J Appl Physiol 99: 1558-1568, 2005.
41. Jones CA and Yang JF. Reflex behavior during walking in incomplete spinal-cord-injured subjects. Exp Neurol 128: 239-248, 1994.
42. Kandel ER, Schwartz JH, and Jessel TM. Principles of Neural Science. New York: McGraw-Hill, 2000.
43. Kiser TS, Reese NB, Maresh T, Hearn S, Yates C, Skinner RD, Pait TG, and Garcia-Rill E. Use of a motorized bicycle exercise trainer to normalize frequency-dependent habituation of the H-reflex in spinal cord injury. J Spinal Cord Med 28: 241-245, 2005.
44. Koceja DM, Burke JR, and Kamen G. Organization of segmental reflexes in trained dancers. Int J Sports Med 12: 285-189, 1991.
45. Koceja DM, Davison E, and Robertson CT. Neuromuscular characteristics of endurance- and power-trained athletes. Res Q Exerc Sport 75: 23-30, 2004.
46. Koceja DM, Markus CA, and Trimble MH. Postural modulation of the soleus H reflex in young and old subjects. Electroencephalogr Clin Neurophysiol 97: 387-393, 1995.
47. Koceja DM, Trimble MH, and Earles DR. Inhibition of the soleus H-reflex in standing man. Brain Res 629: 155-158, 1993.
48. Lagerquist O, Zehr EP, and Docherty D. Increased spinal reflex excitability is not associated with neural plasticity underlying the cross-education effect. J Appl Physiol 100: 83-90, 2006.
49. Levin M and Chapman CE. Inhibitory and facilitatory effects from the peroneal nerve onto the soleus H-reflex in normal and spinal man. Electroencephalogr Clin Neurophysiol 67: 468-478, 1987.
50. max ratio in power-and endurance-trained athletes. J Appl Physiol 90: 3-9, 2001.
51. Maffiuletti N, Pensini M, Scaglioni G, Ferri A, Ballay Y, and Martin A. Effect of electromyostimulation training on soleus and gastrocnemii H-and T-reflex properties. Eur J Appl Physiol 90: 601-607, 2003.
52. Mirbagheri MM, Ladouceur M, Barbeau H, and Kearney RE. The effects of long-term FES-assisted walking on intrinsic and reflex dynamic stiffness in spastic spinal-cord-injured subjects. IEEE Trans Neural Syst Rehabil Eng 10: 280-289, 2002.
53. Misiaszek JE. The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function. Muscle Nerve 28: 144-160, 2003.
54. Muir GD and Steeves JD. Phasic cutaneous input facilitates locomotor recovery after incomplete spinal injury in the chick. J Neurophysiol 74: 358-368, 1995.
55. Muir GD and Steeves JD. Sensorimotor stimulation to improve locomotor recovery after spinal cord injury. Trends Neurosci 20: 72-77, 1997.
56. Mynark RG and Koceja DM. Comparison of soleus H-reflex gain from prone to standing in dancers and controls. Electroencephalogr Clin Neurophysiol 105: 135-140, 1997.
57. Mynark RG and Koceja DM. Down training of the elderly soleus H reflex with the use of a spinally induced balance perturbation. J Appl Physiol 93: 127-133, 2002.
58. Mynark RG, Koceja DM, and Lewis CA. Heteronymous monosynaptic Ia facilitation from supine to standing and its relationship to the soleus H-reflex. Int J Neurosci 92: 171-186, 1997.
59. Neilson PD and McCaughey J. Self-regulation of spasm and spasticity in cerebral palsy. J Neurol Neurosurg Psychiatry 45: 320-330, 1982.
60. Nielsen J, Crone C, and Hultborn H. H-reflexes are smaller in dancers from The Royal Danish Ballet than in well-trained athletes. Eur J Appl Physiol 66: 116-121, 1993.
61. Peurala SH, Pitkanen K, Sivenius J, and Tarkka IM. Cutaneous electrical stimulation may enhance sensorimotor recovery in chronic stroke. Clin Rehabil 16: 709-716, 2002.
62. Pierrot-Deseilligny E and Burke D. The Circuitry of the Human Spinal Cord: Its Role in Motor Control and Movement Disorders. Cambridge, UK: Cambridge University Press, 2005.
63. Potisk KP, Gregoric M, and Vodovnik L. Effects of transcutaneous electrical nerve stimulation (TENS) on spasticity in patients with hemiplegia. Scand J Rehabil Med 27: 169-174, 1995.
64. Rochcongar P, Dassonville J, and Le Bars R. Modifications du reflexe de Hoffmann en fonktion de l'entrainement chez le sportif. Eur J Appl Physiol 40: 165-170, 1979.
65. Rossi-Durand C, Jones KE, Adams S, and Bawa P. Comparison of the depression of H-reflexes following previous activation in upper and lower limb muscles in human subjects. Exp Brain Res 126: 117-127, 1999.
66. Schieppati M. The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 28: 345-376, 1987.
67. Schneider C and Capaday C. Progressive adaptation of the soleus H-reflex with daily training at walking backward. J Neurophysiol 89: 648-656, 2003.
68. Segal RL and Wolf SL. Operant conditioning of spinal stretch reflexes in patients with spinal cord injuries. Exp Neurol 130: 202-213, 1994.
69. Segal RL, Wolf SL, Catlin PA, Gilliand RL, Taffs JK, Bass HC, and Vickers EF. Uncoupling of human short and long latency stretch reflex responses with operant conditioning. Restor Neurol Neurosci 17: 17-22, 2000.
70. Seib TP, Price R, Reyes MR, and Lehmann JF. The quantitative measurement of spasticity: effect of cutaneous electrical stimulation. Arch Phys Med Rehabil 75: 746-750, 1994.
71. Sonde L, Gip C, Fernaeus SE, Nilsson CG, and Viitanen M. Stimulation with low frequency (1.7 Hz) transcutaneous electric nerve stimulation (low-tens) increases motor function of the post-stroke paretic arm. Scand J Rehabil Med 30: 95-99, 1998.
72. Sonde L, Kalimo H, Fernaeus SE, and Viitanen M. Low TENS treatment on post-stroke paretic arm: a three-year follow-up. Clin Rehabil 14: 14-19, 2000.
73. Stein RB. Presynaptic inhibition in humans. Prog Neurobiol 47: 533-544, 1995.
74. Stein RB and Capaday C. The modulation of human reflexes during functional motor tasks. Trends Neurosci 11: 328-332, 1988.
75. Trimble MH, Behrman AL, Flynn SM, Thigpen MT, and Thompson FJ. Acute effects of locomotor training on overground walking speed and H-reflex modulation in individuals with incomplete spinal cord injury. J Spinal Cord Med 24: 74-80, 2001.
76. Trimble MH and Koceja DM. Modulation of the triceps surae H-reflex with training. Int J Neurosci 76: 293-303, 1994.
77. Trimble MH and Koceja DM. Effect of a reduced base of support in standing and balance training on the soleus H-reflex. Int J Neurosci 106: 1-20, 2001.
78. Trimble MH, Kukulka CG, and Behrman AL. The effect of treadmill gait training on low-frequency depression of the soleus H-reflex: comparison of a spinal cord injured man to normal subjects. Neurosci Lett 246: 186-188, 1998.
79. Tucker KJ, Tuncer M, and Turker KS. A review of the H-reflex and M-wave in the human triceps surae. Hum Mov Sci 24: 667-688, 2005.
80. Ung RV, Imbeault MA, Ethier C, Brizzi L, and Capaday C. On the potential role of the corticospinal tract in the control and progressive adaptation of the soleus H-reflex during backward walking. J Neurophysiol 94: 1133-1142, 2005.
81. Voigt M, Chelli F, and Frigo C. Changes in the excitability of soleus muscle short latency stretch reflexes during human hopping after 4 weeks of hopping training. Eur J Appl Physiol 78: 522-532, 1998.
82. Voormolen MM, Ladouceur M, Veltink PH, and Sinkjaer T. Soleus stretch reflex inhibition in the early swing phase of gait using deep peroneal nerve stimulation in spastic stroke participants. Neuromodulation 3: 107-117, 2000.
83. Wolf SL and Segal RL. Reducing human biceps brachii spinal stretch reflex magnitude. J Neurophysiol 75: 1637-1646, 1996.
84. Wolf SL, Segal RL, Heter ND, and Catlin PA. Contralateral and long latency effects of human biceps brachii stretch reflex conditioning. Exp Brain Res 107: 96-102, 1995.
85. Wolpaw JR. Adaptive plasticity in the primate spinal stretch reflex: reversal and re-development. Brain Res 278: 299-304, 1983.
86. Wolpaw JR. Operant conditioning of primate spinal reflexes: the H-reflex. J Neurophysiol 57: 443-459, 1987.
87. Wolpaw JR, Braitman DJ, and Seegal RF. Adaptive plasticity in primate spinal stretch reflex: initial development. J Neurophysiol 50: 1296-1311, 1983.
88. Wolpaw JR and Chen XY. The cerebellum in maintenance of a motor skill: a hierarchy of brain and spinal cord plasticity underlies H-reflex conditioning. Learn Mem 13: 208-215, 2006.
89. Wolpaw JR, Kieffer VA, Seegal RF, Braitman DJ, and Sanders MG. Adaptive plasticity in the spinal stretch reflex. Brain Res 267: 196-200, 1983.
90. Wolpaw JR and O'Keefe JA. Adaptive plasticity in the primate spinal stretch reflex: evidence for a two-phase process. J Neurosci 4: 2718-2724, 1984.
91. Wolpaw JR, Seegal RF, and O'Keefe JA. Adaptive plasticity in primate spinal stretch reflex: behavior of synergist and antagonist muscles. J Neurophysiol 50: 1312-1319, 1983.
92. Wolpaw JR and Tennisen AM. Activity-dependent spinal cord plasticity in health and disease. Annu Rev Neurosci 24: 807-843, 2001.
93. Zehr EP. Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86: 455-468, 2002.
94. Zehr EP. Neural control of rhythmic human movement: the common core hypothesis. Exerc Sport Sci Rev 33: 54-60, 2005.
95. Zehr EP, Carroll TJ, Chua R, Collins DF, Frigon A, Haridas C, Hundza SR, and Kido A. Possible contributions of spinal CPG activity to rhythmic human arm movement. Can J Physiol Pharmacol 82: 556-568, 2004.
96. Zehr EP and Chua R. Modulation of human cutaneous reflexes during rhythmic cyclical arm movement. Exp Brain Res 135: 241-250, 2000.
97. Zehr EP and Duysens J. Regulation of arm and leg movement during human locomotion. The Neuroscientist 10: 347-361, 2004.
98. Zehr EP, Fujita K, and Stein RB. Reflexes from the superficial peroneal nerve during walking in stroke subjects. J Neurophysiol 79: 848-858, 1998.
99. Zehr EP and Stein RB. What functions do reflexes serve during human locomotion? Prog Neurobiol 58: 185-205, 1999.