Original Article| Volume 36, ISSUE 8, P527-537, October 2013

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Alterations in Cortical and Cerebellar Motor Processing in Subclinical Neck Pain Patients Following Spinal Manipulation

Published:September 16, 2013DOI:



      The purpose of this study was investigate whether there are alterations in cerebellar output in a subclinical neck pain (SCNP) group and whether spinal manipulation before motor sequence learning might restore the baseline functional relationship between the cerebellum and motor cortex.


      Ten volunteers were tested with SCNP using transcranial magnetic stimulation before and after a combined intervention of spinal manipulation and motor sequence learning. In a separate experiment, we tested 10 healthy controls using the same measures before and after motor sequence learning. Our transcranial magnetic stimulation measurements included short-interval intracortical inhibition, long-interval intracortical inhibition, and cerebellar inhibition (CBI).


      The SCNP group showed a significant improvement in task performance as indicated by a 19% decrease in mean reaction time (P < .0001), which occurred concurrently with a decrease in CBI following the combined spinal manipulation and motor sequence learning intervention (F1,6 = 7.92, P < .05). The control group also showed an improvement in task performance as indicated by a 25% increase in reaction time (P < .001) with no changes to CBI.


      Subclinical neck pain patients have altered CBI when compared with healthy controls, and spinal manipulation before a motor sequence learning task changes the CBI pattern to one similar to healthy controls.

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        • Hogg-Johnson S
        • Van Der Velde G
        • Carroll LJ
        • et al.
        The burden and determinants of neck pain in the general population.
        Eur Spine J. 2008; 17: 39-51
        • Lee H
        • Nicholson LL
        • Adams RD
        Cervical range of motion associations with subclinical neck pain.
        Spine. 2004; 29: 33-40
        • Lee H
        • Nicholson LL
        • Adams RD
        • Bae S-S
        Proprioception and rotation range sensitization associated with subclinical neck pain.
        Spine. 2005; 30: E60-E67
        • Lee H-Y
        • Wang J-D
        • Yao G
        • Wang S-F
        Association between cervicocephalic kinesthetic sensibility and frequency of subclinical neck pain.
        Man Ther. 2008; 13: 419-425
        • Rossi S
        • della Volpe R
        • Ginanneschi F
        • 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
        • Strutton PH
        • Theodorou S
        • Catley M
        • McGregor AH
        • Davey NJ
        Corticospinal excitability in patients with chronic low back pain.
        J Spinal Disord Tech. 2005; 18: 420-424
        • Waberski T
        • Lamberty K
        • Dieckhöfer A
        • Buchner H
        • Gobbele R
        Short-term modulation of the ipsilateral primary sensory cortex by nociceptive interference revealed by SEPs.
        Neurosci Lett. 2008; 435: 137-141
        • Falla D
        Unravelling the complexity of muscle impairment in chronic neck pain.
        Man Ther. 2004; 9 (PubMed PMID: 15245706.): 125-133
        • van Vliet PM
        • Heneghan NR
        Motor control and the management of musculoskeletal dysfunction.
        Man Ther. 2006; 11: 208-213
        • Cowan SM
        • Bennell KL
        • Hodges PW
        • Crossley KM
        • McConnell J
        Simultaneous feedforward recruitment of the vasti in untrained postural tasks can be restored by physical therapy.
        J Orthop Res. 2003; 21 ([PubMed PMID: 12706031].): 553-558
        • Marshall P
        • Murphy B
        Delayed abdominal muscle onsets and self-report measures of pain and disability in chronic low back pain.
        J Electromyogr Kinesiol. 2010; 20: 833-839
        • Falla D
        • Bilenkij G
        • Jull G
        Patients with chronic neck pain demonstrate altered patterns of muscle activation during performance of a functional upper limb task.
        Spine. 2004; 29: 1436
        • Hodges P
        • Richardson C
        Altered trunk muscle recruitment in people with low back pain with upper limb movement at different speeds.
        Arch Phys Med Rehabil. 1999; 80: 1005-1012
        • Radebold A
        • Cholewicki J
        • Polzhofer GK
        • Greene HS
        Impaired postural control of the lumbar spine is associated with delayed muscle response times in patients with chronic idiopathic low back pain.
        Spine. 2001; 26: 724-730
        • van Dieen JH
        • Selen LP
        • Cholewicki J
        Trunk muscle activation in low-back pain patients, an analysis of the literature.
        J Electromyogr Kinesiol. 2003; 13: 333-351
        • Panjabi MM
        The stabilizing system of the spine. Part I. Function, dysfunction, adaptation and enhancement.
        J Spinal Disord. 1992; 5: 383-389
        • Jull G
        • Richardson C
        Motor control problems in patients with spinal pain: a new direction for therapeutic exercise.
        J Manipulative Physiol Ther. 2000; 23: 115-117
        • Sterling M
        • Jull G
        • Vicenzino B
        • Kenardy J
        • Darnell R
        Development of motor system dysfunction following whiplash injury.
        Pain. 2003; 103: 65-73
        • Jull G
        • Trott P
        • Potter H
        • et al.
        A randomized controlled trial of exercise and manipulative therapy for cervicogenic headache.
        Spine. 2002; 27: 1835-1843
        • Brumagne S
        • Cordo P
        • Lysens R
        • Verschueren S
        • Swinnen S
        The role of paraspinal muscle spindles in lumbosacral position sense in individuals with and without low back pain.
        Spine. 2000; 25: 989-994
        • 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
        • Fernández-Carnero J
        • Cleland JA
        • Arbizu RLT
        Examination of motor and hypoalgesic effects of cervical vs thoracic spine manipulation in patients with lateral epicondylalgia: a clinical trial.
        J Manipulative Physiol Ther. 2011; 34: 432-440
        • Fryer G
        • Pearce AJ
        The effect of lumbosacral manipulation on corticospinal and spinal reflex excitability on asymptomatic participants.
        J Manipulative Physiol Ther. 2012; 35: 86-93
        • Soon BT
        • Schmid AB
        • Fridriksson EJ
        • Gresslos E
        • Cheong P
        • Wright A
        A crossover study on the effect of cervical mobilization on motor function and pressure pain threshold in pain-free individuals.
        J Manipulative Physiol Ther. 2010; 33: 652-658
        • Haavik H
        • Murphy B
        Subclinical neck pain and the effects of cervical manipulation on elbow joint position sense.
        J Manipulative Physiol Ther. 2011; 34: 88-97
        • Herzog W
        • Scheele D
        • Conway PJ
        Electromyographic responses of back and limb muscles associated with spinal manipulative therapy.
        Spine. 1999; 24: 146
        • Murphy B
        • Dawson N
        • Slack J
        Sacroiliac joint manipulation decreases the H-reflex.
        Electromyogr Clin Neurophysiol. 1995; 35: 87-94
        • Haavik-Taylor H
        • Murphy B
        Transient modulation of intracortical inhibition following spinal manipulation.
        Chiropr J Aust. 2007; 37: 106
        • Haavik-Taylor H
        • Murphy B
        Cervical spine manipulation alters sensorimotor integration: a somatosensory evoked potential study.
        Clin Neurophysiol. 2007; 118: 391-402
        • Taylor HH
        • Murphy B
        The effects of spinal manipulation on central integration of dual somatosensory input observed after motor training: a crossover study.
        J Manipulative Physiol Ther. 2010; 33: 261-272
        • Manto M
        • Bastian A
        Cerebellum and the deciphering of motor coding.
        Cerebellum. 2007; 6: 3-6
        • Classen J
        • Liepert J
        • Wise S
        • Hallett M
        • Cohen L
        Rapid plasticity of human cortical movement representation induced by practice.
        J Neurophysiol. 1998; 79: 1117-1123
        • Doyon J
        • Penhune V
        • Ungerleider LG
        Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning.
        Neuropsychologia. 2003; 41: 252-262
        • Doyon J
        • Song AW
        • Karni A
        • Lalonde F
        • Adams MM
        • Ungerleider LG
        Experience-dependent changes in cerebellar contributions to motor sequence learning.
        Proc Natl Acad Sci U S A. 2002; 99: 1017-1022
        • Molinari M
        • Leggio MG
        • Thaut MH
        The cerebellum and neural networks for rhythmic sensorimotor synchronization in the human brain.
        Cerebellum. 2007; 6: 18-23
        • Manzoni D
        The cerebellum may implement the appropriate coupling of sensory inputs and motor responses: evidence from vestibular physiology.
        Cerebellum. 2005; 4: 178-188
        • Manzoni D
        The cerebellum and sensorimotor coupling: looking at the problem from the perspective of vestibular reflexes.
        Cerebellum. 2007; 6: 24-37
      1. Doyon J, Ungerleider LG. Functional anatomy of motor skill learning 2002. p. 225–38.

        • Apps R
        • Garwicz M
        Anatomical and physiological foundations of cerebellar information processing.
        Nat Rev Neurosci. 2005; 6: 297-311
        • Brighina F
        • Palermo A
        • Panetta ML
        • et al.
        Reduced cerebellar inhibition in migraine with aura: a TMS study.
        Cerebellum. 2009; 8: 260-266
        • Brighina F
        • Romano M
        • Giglia G
        • et al.
        Effects of cerebellar TMS on motor cortex of patients with focal dystonia: a preliminary report.
        Exp Brain Res. 2009; 192: 651-656
        • Bosco G
        • Rankin A
        • Poppele R
        Representation of passive hindlimb postures in cat spinocerebellar activity.
        J Neurophysiol. 1996; 76: 715-726
        • Giaquinta G
        • Casabona A
        • Valle MS
        • Bosco G
        • Perciavalle V
        On the relation of rat's external cuneate activity to global parameters of forelimb posture.
        Neuroreport. 1999; 10: 3075-3080
        • Haavik H
        • Murphy B
        The role of spinal manipulation in addressing disordered sensorimotor integration and altered motor control.
        J Electromyogr Kinesiol. 2012; 22: 768-776
        • Daskalakis ZJ
        • Paradiso GO
        • Christensen BK
        • Fitzgerald PB
        • Gunraj C
        • Chen R
        Exploring the connectivity between the cerebellum and motor cortex in humans.
        J Physiol (Lond). 2004; 557: 689-700
        • Vernon H
        The Neck Disability Index: state-of-the-art, 1991-2008.
        J Manipulative Physiol Ther. 2008; 31: 491-502
        • Fryer G
        • Morris T
        • Gibbons P
        Paraspinal muscles and intervertebral dysfunction: part one.
        J Manipulative Physiol Ther. 2004; 27: 267-274
        • Hubka MJ
        • Phelan SP
        Interexaminer reliability of palpation for cervical spine tenderness.
        J Manipulative Physiol Ther. 1994; 17: 591
        • Robinson R
        • Robinson HS
        • Bjørke G
        • Kvale A
        Reliability and validity of a palpation technique for identifying the spinous processes of C7 and L5.
        Man Ther. 2009; 14: 409-414
        • Shin S
        • Yoon D-M
        • Yoon KB
        Identification of the correct cervical level by palpation of spinous processes.
        Anesth Analg. 2011; 112: 1232-1235
        • Herzog W
        • Conway P
        • Zhang Y
        • Gal J
        • Guimaraes A
        Reflex responses associated with manipulative treatments on the thoracic spine: a pilot study.
        J Manipulative Physiol Ther. 1995; 18: 233
        • Kaneko K
        • Kawai S
        • Fuchigami Y
        • Morita H
        • Ofuji A
        The effect of current direction induced by transcranial magnetic stimulation on the corticospinal excitability in human brain.
        Electroencephalogr Clin Neurophysiol. 1996; 101: 478-482
        • Werhahn K
        • Fong J
        • Meyer B
        • et al.
        The effect of magnetic coil orientation on the latency of surface EMG and single motor unit responses in the first dorsal interosseous muscle.
        Electroencephalogr Clin Neurophysiol. 1994; 93: 138-146
        • Kujirai T
        • Caramia M
        • Rothwell J
        • et al.
        Corticocortical inhibition in human motor cortex.
        J Physiol (Lond). 1993; 471: 501
        • Nakamura H
        • Kitagawa H
        • Kawaguchi Y
        • Tsuji H
        Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans.
        J Physiol (Lond). 1997; 498: 817-823
        • Chen R
        • Lozano AM
        • Ashby P
        Mechanism of the silent period following transcranial magnetic stimulation evidence from epidural recordings.
        Exp Brain Res. 1999; 128: 539-542
        • Ugawa Y
        • Uesaka Y
        • Terao Y
        • Hanajima R
        • Kanazawa I
        Magnetic stimulation over the cerebellum in humans.
        Ann Neurol. 1995; 37: 703-713
        • Pascual-Leone A
        • Grafman J
        • Hallett M
        Modulation of cortical motor output maps during development of implicit and explicit knowledge.
        Science. 1994; 263: 1287-1289
        • Pascual-Leone A
        • Nguyet D
        • Cohen LG
        • Brasil-Neto JP
        • Cammarota A
        • Hallett M
        Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills.
        J Neurophysiol. 1995; 74: 1037-1045
        • Cirillo J
        • Rogasch NC
        • Semmler JG
        Hemispheric differences in use-dependent corticomotor plasticity in young and old adults.
        Exp Brain Res. 2010; 205: 57-68