Journal of Manipulative and Physiological Therapeutics
Volume 31, Issue 2 , Pages 115-126 , February 2008

Altered Sensorimotor Integration With Cervical Spine Manipulation

  • Heidi Haavik Taylor, BSc(Chiro), PhD

      Affiliations

    • Director of Research, New Zealand College of Chiropractic, Auckland, New Zealand
    • Corresponding Author InformationSubmit requests for reprints to: Heidi Haavik Taylor, BSc(Chiro), PhD, Director of Research, Department of Sport and Exercise Science, Human Neurophysiology and Rehabilitation Laboratory, Tamaki Campus, University of Auckland, Auckland, New Zealand.
    • Department/Institution work should be attributed to Human Neurophysiology and Rehabilitation Laboratory, Department of Sport and Exercise Science, University of Auckland.
  • ,
  • Bernadette Murphy, DC, PhD

      Affiliations

    • Postgraduate and MSc-Exercise Rehabilitation Coordinator and Director, Department of Sport and Exercise Science, Human Neurophysiology and Rehabilitation Laboratory, University of Auckland, Auckland, New Zealand
    • Department/Institution work should be attributed to Human Neurophysiology and Rehabilitation Laboratory, Department of Sport and Exercise Science, University of Auckland.

Received 6 October 2007 ,Revised 29 October 2007

References 

  1. Hurwitz EL, Aker PD, Adams AH, Meeker WC, Shekelle PG. Manipulation and mobilization of the cervical spine. A systematic review of the literature. Spine. 1996;21:1746–1760
  2. Vernon LF. Spinal manipulation as a valid treatment for low back pain. Del Med J. 1996;68:175–178
  3. Haavik-Taylor H, Murphy B. Transient modulation of intracortical inhibition following spinal manipulation. Chiropr J Aust. 2007;37:106–116
  4. Brasil-Neto JP, Valls-Sole J, Pascual-Leone A, Cammarota A, Amassian VE, Cracco R, et al. Rapid modulation of human cortical motor outputs following ischaemic nerve block. Brain. 1993;116(Pt 3):511–525
  5. Byl NN, Merzenich MM, Cheung S, Bedenbaugh P, Nagarajan SS, Jenkins WM. A primate model for studying focal dystonia and repetitive strain injury: effects on the primary somatosensory cortex. Phys Ther. 1997;77:269–284
  6. Hallett M, Chen R, Ziemann U, Cohen LG. Reorganization in motor cortex in amputees and in normal volunteers after ischemic limb deafferentation. Electroencephalogr Clin Neurophysiol Suppl. 1999;51:183–187
  7. Pascual-Leone A, Torres F. Plasticity of the sensorimotor cortex representation of the reading finger in braille readers. Brain. 1993;116(Pt 1):39–52
  8. Tinazzi M, Zanette G, Polo A, Volpato D, Manganotti P, Bonato C, et al. Transient deafferentation in humans induces rapid modulation of primary sensory cortex not associated with subcortical changes: a somatosensory evoked potential study. Neurosci Lett. 1997;223:21–24
  9. Tinazzi M, Zanette G, Volpato D, Testoni R, Bonato C, Manganotti P, et al. Neurophysiological evidence of neuroplasticity at multiple levels of the somatosensory system in patients with carpal tunnel syndrome. Brain. 1998;121(Pt 9):1785–1794
  10. Ziemann U, Hallett M, Cohen LG. Mechanisms of deafferentation-induced plasticity in human motor cortex. J Neurosci. 1998;18:7000–7007
  11. Liepert J, Classen J, Cohen LG, Hallett M. Task-dependent changes of intracortical inhibition. Exp Brain Res. 1998;118:421–426
  12. Liepert J, Weiss T, Meissner W, Steinrucke K, Weiller C. Exercise-induced changes of motor excitability with and without sensory block. Brain Res. 2004;1003:68–76
  13. Murphy BA, Haavik Taylor H, Wilson SA, Oliphant G,, Mathers KM. Rapid reversible changes to multiple levels of the human somatosensory system following the cessation of repetitive contractions: a somatosensory evoked potential study. Clin Neurophysiol. 2003;114:1531–1537
  14. Wall JT, Xu J, Wang X. Human brain plasticity: an emerging view of the multiple substrates and mechanisms that cause cortical changes and related sensory dysfunctions after injuries of sensory inputs from the body. Brain Res Rev. 2002;39:181–215
  15. Bolton PS, Holland CT. Afferent signaling of vertebral displacement in the neck of the cat. Soc Neurosci Abstr. 1996;22:1802
  16. Bolton PS, Holland CT. An in vivo method for studying afferent fibre activity from cervical paravertebral tissue during vertebral motion in anaesthetised cats. J Neurosci Methods. 1998;85:211–218
  17. Murphy BA, Dawson NJ, Slack JR. Sacroiliac joint manipulation decreases the h-reflex. Electroencephalogr Clin Neurophysiol. 1995;35:87–94
  18. Zhu Y, Haldeman S, Starr A, Seffinger MA, Su SH. Paraspinal muscle evoked cerebral potentials in patients with unilateral low back pain. Spine. 1993;18:1096–1102
  19. Zhu Y, Haldeman S, Hsieh CY, Wu P, Starr A. Do cerebral potentials to magnetic stimulation of paraspinal muscles reflect changes in palpable muscle spasm, low back pain, and activity scores?. J Manipulative Physiol Ther. 2000;23:458–464
  20. Haavik-Taylor H, Murphy B. Cervical spine manipulation alters sensorimotor integration: a somatosensory evoked potential study. Clin Neurophysiol. 2007;118:391–402
  21. Rossi S, della Volpe R, Ginanneschi F, Ulivelli M, Bartalini S, Spidalieri R, et al. Early somatosensory processing during tonic muscle pain in humans: relation to loss of proprioception and motor 'defensive' strategies. Clin Neurophysiol. 2003;114:1351–1358
  22. Kanovský P, Bare M, Rektor I. The selective gating of the n30 cortical component of the somatosensory evoked potentials of median nerve is different in the mesial and dorsolateral frontal cortex: evidence from intracerebral recordings. Clin Neurophysiol. 2003;114:981–991
  23. Mauguiere F, Desmedt JE, Courjon J. Astereognosis and dissociated loss of frontal or parietal components of somatosensory evoked potentials in hemispheric lesions. Detailed correlations with clinical signs and computerized tomographic scanning. Brain. 1983;106:271–311
  24. Rossini PM, Gigli GL, Marciani MG, Zarola F, Caramia M. Non-invasive evaluation of input-output characteristics of sensorimotor cerebral areas in healthy humans. Electroencephalogr Clin Neurophysiol. 1987;68:88–100
  25. Rossini PM, Babiloni F, Bernardi G, Cecchi L, Johnson PB, Malentacca A, et al. Abnormalities of short-latency somatosensory evoked potentials in parkinsonian patients. Electroencephalogr Clin Neurophysiol. 1989;74:277–289
  26. Waberski TD, Buchner H, Perkuhn M, Gobbele R, Wagner M, Kucker W, et al. N30 and the effect of explorative finger movements: a model of the contribution of the motor cortex to early somatosensory potentials. Clin Neurophysiol. 1999;110:1589–1600
  27. Haavik Taylor H, Murphy B. Transient modulation of intracortical inhibition following spinal manipulation. Chiropr J Aust. 2007;37:106–116
  28. Chen R, Corwell B, Hallett M. Modulation of motor cortex excitability by median nerve and digit stimulation. Exp Brain Res. 1999;129:77–86
  29. Inghilleri M, Berardelli A, Cruccu G, Manfredi M. Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol (Lond). 1993;466:521–534
  30. Cantello R, Gianelli M, Civardi C, Mutani R. Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology. 1992;42:1951–1959
  31. Kukowski B, Haug B. Quantitative evaluation of the silent period, evoked by transcranial magnetic stimulation during sustained muscle contraction, in normal man and in patients with stroke. Electroencephalogr Clin Neurophysiol. 1992;32:373–378
  32. Roick H, von Giesen HJ, Benecke R. On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects. Exp Brain Res. 1993;94:489–498
  33. Brasil-Neto JP, Cammarota A, Valls-Sole J, Pascual-Leone A, Hallett M, Cohen LG. Role of intracortical mechanisms in the late part of the silent period to transcranial stimulation of the human motor cortex. Acta Neurol Scand. 1995;92:383–386
  34. Herzog W, Scheele D, Conway PJ. Electromyographic responses of back and limb muscles associated with spinal manipulative therapy. Spine. 1999;24:146–153
  35. Symons BP, Herzog W, Leonard T, Nguyen H. Reflex responses associated with activator treatment. J Manipulative Physiol Ther. 2000;23:155–159
  36. Fisher MA. H reflexes and F waves: physiology and clinical indications. Muscle Nerve. 1992;15:1223–1233
  37. Panayiotopoulos CP, Chroni E. F-waves in clinical neurophysiology: a review, methodological issues and overall value in peripheral neuropathies. Electroencephalogr Clin Neurophysiol. 1996;101:365–374
  38. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol (Lond). 1993;471:501–519
  39. Ziemann U, Tergau F, Wassermann EM, Wischer S, Hildebrandt J, Paulus W. Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J Physiol (Lond). 1998;511(Pt 1):181–190
  40. Chen R, Garg R. Facilitatory I wave interaction in proximal arm and lower limb muscle representations of the human motor cortex. J Neurophysiol. 2000;83:1426–1434
  41. Hanajima R, Ugawa Y, Terao Y, Enomoto H, Shiio Y, Mochizuki H, et al. Mechanisms of intracortical I-wave facilitation elicited with paired-pulse magnetic stimulation in humans. J Physiol (Lond). 2002;538(Pt 1):253–261
  42. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113
  43. Eisenberg E, Chistyakov AV, Yudashkin M, Kaplan B, Hafner H, Feinsod M. Evidence for cortical hyperexcitability of the affected limb representation area in CRPS: a psychophysical and transcranial magnetic stimulation study. Pain. 2005;113:99–105
  44. Cheong JY, Yoon TS, Lee SJ. Evaluations of inhibitory effect on the motor cortex by cutaneous pain via application of capsaicin. Electroencephalogr Clin Neurophysiol. 2003;43:203–210
  45. Kofler M, Fuhr P, Leis AA, Glocker FX, Kronenberg MF, Wissel J, et al. Modulation of upper extremity motor evoked potentials by cutaneous afferents in humans. Clin Neurophysiol. 2001;112:1053–1063
  46. Nakamura H, Kitagawa H, Kawaguchi Y, Tsuji H. Direct and indirect activation of human corticospinal neurons by transcranial magnetic and electrical stimulation. Neurosci Lett. 1996;210:45–48
  47. Boroojerdi B, Battaglia F, Muellbacher W, Cohen LG. Mechanisms influencing stimulus-response properties of the human corticospinal system. Clin Neurophysiol. 2001;112:931–937
  48. Fisher RJ, Nakaura Y, Bestmann S, Rothwell JC, Bostock H. Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking. Exp Brain Res. 2002;143:240–248
  49. Roshan L, Paradiso GO, Chen R. Two phases of short-interval intracortical inhibition. Exp Brain Res. 2003;151:330–337
  50. Tokimura H, Ridding MC, Tokimura Y, Amassian VE, Rothwell JC. Short latency facilitation between pairs of threshold magnetic stimuli applied to human motor cortex. Electroencephalogr Clin Neurophysiol. 1996;101:263–272
  51. Hestboek L, Leboeuf-Yde C. Are chiropractic tests for the lumbo-pelvic spine reliable and valid? A systematic critical literature review. J Manipulative Physiol Ther. 2000;23:258–275
  52. Fryer G, Morris T,, Gibbons P. Paraspinal muscles and intervertebral dysfunction: part one. J Manipulative Physiol Ther. 2004;27:267–274
  53. Hubka MJ, Phelan SP. Interexaminer reliability of palpation for cervical spine tenderness. J Manipulative Physiol Ther. 1994;17:591–595
  54. Jull G, Bogduk N, Marsland A. The accuracy of manual diagnosis for cervical zygapophysial joint pain syndromes. Med J Aust. 1988;148:233–236
  55. Rheault W, Albright B, Byers C, Franta M, Johnson A, Skowronek BS, et al. Intertester reliability of the cervical range of motion device. J Orthop Sports Phys Ther. 1992;15:147–150
  56. Youdas JW, Garrett TR, Suman VJ, Bogard CL, Hallman HO, Carey JR. Normal range of motion of the cervical spine: an initial goniometric study. Phys Ther. 1992;72:770–780
  57. Hessell BW, Herzog W, Conway PJ, McEwen MC. Experimental measurement of the force exerted during spinal manipulation using the Thompson technique. J Manipulative Physiol Ther. 1990;13:448–453
  58. Herzog W. Mechanical, physiologic, and neuromuscular considerations of chiropractic treatment. In:  Lawrence DJ,  Cassidy JD,  McGregor M,  Meeker WC,  Vernon HT editor. Advances in chiropractic. New York: Mosby-Year Book; 1996;p. 269–285
  59. Herzog W, Conway PJ, Zhang YT, Gail J, Guimaraes ACS. Reflex responses associated with manipulative treatments on the thoracic spine: a pilot study. J Manipulative Physiol Ther. 1995;18:233–234
  60. Pickar JG, Wheeler JD. Response of muscle proprioceptors to spinal manipulative-like loads in the anesthetized cat. J Manipulative Physiol Ther. 2001;24:2–11
  61. Arnold C, Bourassa R, Langer T,, Stoneham G. Doppler studies evaluating the effect of a physical therapy screening protocol on vertebral artery blood flow. Man Ther. 2004;9:13–21
  62. Allison GT. Trunk muscle onset detection technique for EMG signals with ECG artefact. J Electromyogr Kinesiology. 2003;13:209–216
  63. Tergau F, Wanschura V, Canelo M, et al. Complete suppression of voluntary motor drive during the silent period after transcranial magnetic stimulation. Exp Brain Res. 1999;124:447–454
  64. Siebner HR, Dressnandt J, Auer C, Conrad B. Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve. 1998;21:1209–1212
  65. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol (Lond). 1999;517:591–597
  66. Ziemann U, Tergau F, Wischer S, Hildebrandt J, Paulus W. Pharmacological control of facilitatory I-wave interaction in the human motor cortex. A paired transcranial magnetic stimulation study. Electroencephalogr Clin Neurophysiol. 1998;109:321–330
  67. Wischer S, Paulus W, Sommer M, Tergau F. Piracetam affects facilitatory I-wave interaction in the human motor cortex. Clin Neurophysiol. 2001;112:275–279
  68. Alund M, Ledin T, Odkvist L, Larsson SE. Dynamic posturography among patients with common neck disorders. J Vestib Res. 1993;3:383–389
  69. Karlberg M, Persson L, Magnusson M. Reduced postural control in patients with chronic cervicobrachial pain syndrome. Gait Posture. 1995;3:241–249
  70. Persson L, Karlberg M, Magnusson M. Effects of different treatments on postural performance in patients with cervical root compression: a randomized prospective study assessing the importance of the neck in postural control. J Vestib Res. 1996;6:439–453
  71. Jull G, Kristjansson E, Dall'Alba P. Impairment in the cervical flexors: a comparison of whiplash and insidious onset neck pain patients. Manual Therapy. 2004;9:89–94
  72. Branstrom H, Malmgren-Olsson EB, Barnekow-Bergkvist M. Balance performance in patients with whiplash associated disorders and patients with prolonged musculoskeletal disorders. Adv Physiother. 2001;3:120–127
  73. Rubin AM, Woolley SM, Dailey VM, Goebel JA. Postural stability following mild head or whiplash injuries. Am J Otol. 1995;16:216–221
  74. Michaelson P, Michaelson M, Jaric S, Latash ML, Sjolander P, Djupsjobacka M. Vertical posture and head stability in patients with chronic neck pain. J Rehabil Med. 2003;35:229–235
  75. Sterling M, Jull G, Vicenzino B, Kenardy J, Darnell R. Development of motor system dysfunction following whiplash injury. Pain. 2003;103:65–73
  76. Jull G, Trott P, Potter H, Zito G, Niere K, Shirley D, et al. A randomized controlled trial of exercise and manipulative therapy for cervicogenic headache. Spine. 2002;27:1835–1843
  77. Yue GH, Liu JZ, Siemionow V, Ranganathan VK, Ng TC, Sahgal V. Brain activation during human finger extension and flexion movements. Brain Res. 2000;856:291–300
  78. Cheney PD, Fetz EE, Palmer SS. Patterns of facilitation and suppression of antagonist forelimb muscles from motor cortex sites in the awake monkey. J Neurophysiol. 1985;53:805–820
  79. Stapley PJ, Beretta MV, Toffola ED, Schieppati M. Neck muscle fatigue and postural control in patients with whiplash injury. Clin Neurophysiol. 2006;117:610–622
  80. Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol. 1996;40:367–378
  81. Ilic TV, Meintzschel F, Cleff U, Ruge D, Kessler KR, Ziemann U. Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol (Lond). 2002;545(Pt 1):153–167
  82. Butefisch CM, Davis BC, Wise SP, et al. Mechanisms of use-dependent plasticity in the human motor cortex. Proc Natl Acad Sci. 2000;97:3661–3665
  83. Floeter MK, Rothwell J. Releasing the brakes before pressing the gas pedal. Neurology. 1999;53:664–665
  84. Cote P, Cassidy JD,, Carroll L. The Saskatchewan health and back pain survey: the prevalence of neck pain and related disability in Saskatchewan adults. Spine. 1998;23:1689–1698
  85. Tinazzi M, Fiaschi A, Rosso T, Faccioli F, Grosslercher J, Aglioti SM. Neuroplastic changes related to pain occur at multiple levels of the human somatosensory system: a somatosensory-evoked potentials study in patients with cervical radicular pain. J. Neurosci. 2000;20:9277–9283
  86. Tinazzi M, Valeriani M, Moretto G, et al. Plastic interactions between hand and face cortical representations in patients with trigeminal neuralgia: a somatosensory-evoked potentials study. Neurosci. 2004;127:769–776
  87. Soros P, Knecht S, Bantel C, Imai T, Wusten R, Pantev C, et al. Functional reorganization of the human primary somatosensory cortex after acute pain demonstrated by magnetoencephalography. Neurosci Lett. 2001;298:195–198
  88. Flor H, Elbert T, Knecht S, et al. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature. 1995;375:482–484

PII: S0161-4754(07)00344-2

doi: 10.1016/j.jmpt.2007.12.011

Journal of Manipulative and Physiological Therapeutics
Volume 31, Issue 2 , Pages 115-126 , February 2008