Advertisement
Original Report| Volume 11, ISSUE 11, P1083-1094, November 2010

Temporomandibular Disorder Modifies Cortical Response to Tactile Stimulation

      Abstract

      Individuals with temporomandibular disorder (TMD) suffer from persistent facial pain and exhibit abnormal sensitivity to tactile stimulation. To better understand the pathophysiological mechanisms underlying TMD, we investigated cortical correlates of this abnormal sensitivity to touch. Using functional magnetic resonance imaging (fMRI), we recorded cortical responses evoked by low-frequency vibration of the index finger in subjects with TMD and in healthy controls (HC). Distinct subregions of contralateral primary somatosensory cortex (SI), secondary somatosensory cortex (SII), and insular cortex responded maximally for each group. Although the stimulus was inaudible, primary auditory cortex was activated in TMDs. TMDs also showed greater activation bilaterally in anterior cingulate cortex and contralaterally in the amygdala. Differences between TMDs and HCs in responses evoked by innocuous vibrotactile stimulation within SI, SII, and the insula paralleled previously reported differences in responses evoked by noxious and innocuous stimulation, respectively, in healthy individuals. This unexpected result may reflect a disruption of the normal balance between central resources dedicated to processing innocuous and noxious input, manifesting itself as increased readiness of the pain matrix for activation by even innocuous input. Activation of the amygdala in our TMD group could reflect the establishment of aversive associations with tactile stimulation due to the persistence of pain.

      Perspective

      This article presents evidence that central processing of innocuous tactile stimulation is abnormal in TMD. Understanding the complexity of sensory disruption in chronic pain could lead to improved methods for assessing cerebral cortical function in these patients.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to The Journal of Pain
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Aaron L.A.
        • Burke M.M.
        • Buchwald D.
        Overlapping conditions among patients with chronic fatigue syndrome, fibromyalgia, and temporomandibular disorder.
        Arch Intern Med. 2000; 160: 221-227
        • Albanese M.C.
        • Duerden E.G.
        • Bohotin V.
        • Rainville P.
        • Duncan G.H.
        Differential effects of cognitive demand on human cortical activation associated with vibrotactile stimulation.
        J Neurophysiol. 2009; 102: 1623-1631
        • Apkarian A.V.
        Pain perception in relation to emotional learning.
        Curr Opin Neurobiol. 2008; 18: 464-468
        • Beckmann C.F.
        • Jenkinson M.
        • Smith S.M.
        General multilevel linear modeling for group analysis in fMRI.
        Neuroimage. 2003; 20: 1052-1063
        • Birbaumer N.
        • Lutzenberger W.
        • Montoya P.
        • Larbig W.
        • Unertl K.
        • Topfner S.
        • Grodd W.
        • Taub E.
        • Flor H.
        Effects of regional anesthesia on phantom limb pain are mirrored in changes in cortical reorganization.
        J Neurosci. 1997; 17: 5503-5508
        • Blatow M.
        • Nennig E.
        • Sarpaczki E.
        • Reinhardt J.
        • Schlieter M.
        • Herweh C.
        • Rasche D.
        • Tronnier V.M.
        • Sartor K.
        • Stippich C.
        Altered somatosensory processing in trigeminal neuralgia.
        Hum Brain Mapp. 2009; 30: 3495-3508
        • Budinger E.
        • Scheich H.
        Anatomical connections suitable for the direct processing of neuronal information of different modalities via the rodent primary auditory cortex.
        Hear Res. 2009; 258: 16-27
        • Bush F.M.
        • Harkins S.W.
        • Harrington W.G.
        • Price D.D.
        Analysis of gender effects on pain perception and symptom presentation in temporomandibular pain.
        Pain. 1993; 53: 73-80
        • Caetano G.
        • Jousmaki V.
        Evidence of vibrotactile input to human auditory cortex.
        Neuroimage. 2006; 29: 15-28
        • Cappe C.
        • Barone P.
        Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey.
        Eur J Neurosci. 2005; 22: 2886-2902
        • Coghill R.C.
        • Sang C.N.
        • Maisog J.M.
        • Iadarola M.J.
        Pain intensity processing within the human brain: A bilateral, distributed mechanism.
        J Neurophysiol. 1999; 82: 1934-1943
        • Coghill R.C.
        • Talbot J.D.
        • Evans A.C.
        • Meyer E.
        • Gjedde A.
        • Bushnell M.C.
        • Duncan G.H.
        Distributed processing of pain and vibration by the human brain.
        J Neurosci. 1994; 14: 4095-4108
        • Dworkin S.F.
        • Huggins K.H.
        • LeResche L.
        • Von Korff M.
        • Howard J.
        • Truelove E.
        • Sommers E.
        Epidemiology of signs and symptoms in temporomandibular disorders: Clinical signs in cases and controls.
        J Am Dent Assoc. 1990; 120: 273-281
        • Dworkin S.F.
        • LeResche L.
        Research diagnostic criteria for temporomandibular disorders: Review, criteria, examinations and specifications, critique.
        J Craniomandib Disord. 1992; 6: 301-355
        • Eickhoff S.B.
        • Amunts K.
        • Mohlberg H.
        • Zilles K.
        The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results.
        Cereb Cortex. 2006; 16: 268-279
        • Eickhoff S.B.
        • Paus T.
        • Caspers S.
        • Grosbras M.H.
        • Evans A.C.
        • Zilles K.
        • Amunts K.
        Assignment of functional activations to probabilistic cytoarchitectonic areas revisited.
        Neuroimage. 2007; 36: 511-521
        • Eickhoff S.B.
        • Schleicher A.
        • Zilles K.
        • Amunts K.
        The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions.
        Cereb Cortex. 2006; 16: 254-267
        • Eickhoff S.B.
        • Stephan K.E.
        • Mohlberg H.
        • Grefkes C.
        • Fink G.R.
        • Amunts K.
        • Zilles K.
        A new spm toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data.
        Neuroimage. 2005; 25: 1325-1335
        • Ferretti A.
        • Babiloni C.
        • Gratta C.D.
        • Caulo M.
        • Tartaro A.
        • Bonomo L.
        • Rossini P.M.
        • Romani G.L.
        Functional topography of the secondary somatosensory cortex for nonpainful and painful stimuli: An fMRI study.
        Neuroimage. 2003; 20: 1625-1638
        • Flor H.
        • Elbert T.
        • Knecht S.
        • Wienbruch C.
        • Pantev C.
        • Birbaumer N.
        • Larbig W.
        • Taub E.
        Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation.
        Nature. 1995; 375: 482-484
        • Foxe J.J.
        • Wylie G.R.
        • Martinez A.
        • Schroeder C.E.
        • Javitt D.C.
        • Guilfoyle D.
        • Ritter W.
        • Murray M.M.
        Auditory-somatosensory multisensory processing in auditory association cortex: An fMRI study.
        J Neurophysiol. 2002; 88: 540-543
        • Francis S.T.
        • Kelly E.F.
        • Bowtell R.
        • Dunseath W.J.
        • Folger S.E.
        • McGlone F.
        fMRI of the responses to vibratory stimulation of digit tips.
        Neuroimage. 2000; 11: 188-202
        • Frostig R.D.
        • Xiong Y.
        • Chen-Bee C.H.
        • Kvasnak E.
        • Stehberg J.
        Large-scale organization of rat sensorimotor cortex based on a motif of large activation spreads.
        J Neurosci. 2008; 28: 13274-13284
        • Fu K.M.
        • Johnston T.A.
        • Shah A.S.
        • Arnold L.
        • Smiley J.
        • Hackett T.A.
        • Garraghty P.E.
        • Schroeder C.E.
        Auditory cortical neurons respond to somatosensory stimulation.
        J Neurosci. 2003; 23: 7510-7515
        • Gelb H.
        • Gelb M.L.
        • Wagner M.L.
        The relationship of tinnitus to craniocervical mandibular disorders.
        Cranio. 1997; 15: 136-143
        • Geyer S.
        • Schleicher A.
        • Zilles K.
        Areas 3a, 3b, and 1 of human primary somatosensory cortex. 1. Microstructural organization and interindividual variability.
        Neuroimage. 1999; 10: 63-83
        • Geyer S.
        • Schormann T.
        • Mohlberg H.
        • Zilles K.
        Areas 3a, 3b, and 1 of human primary somatosensory cortex. Part 2. Spatial normalization to standard anatomical space.
        Neuroimage. 2000; 11: 684-696
        • Guest S.
        • Catmur C.
        • Lloyd D.
        • Spence C.
        Audiotactile interactions in roughness perception.
        Exp Brain Res. 2002; 146: 161-171
        • Guilbaud G.
        • Peschanski M.
        • Briand A.
        • Gautron M.
        The organization of spinal pathways to ventrobasal thalamus in an experimental model of pain (the arthritic rat). An electrophysiological study.
        Pain. 1986; 26: 301-312
        • Hagberg C.
        General musculoskeletal complaints in a group of patients with craniomandibular disorders (CMD). A case control study.
        Swed Dent J. 1991; 15: 179-185
        • Han J.S.
        • Neugebauer V.
        mGluR1 and mGluR5 antagonists in the amygdala inhibit different components of audible and ultrasonic vocalizations in a model of arthritic pain.
        Pain. 2005; 113: 211-222
        • Hollins M.
        • Harper D.
        • Gallagher S.
        • Owings E.W.
        • Lim P.F.
        • Miller V.
        • Siddiqi M.Q.
        • Maixner W.
        Perceived intensity and unpleasantness of cutaneous and auditory stimuli: An evaluation of the generalized hypervigilance hypothesis.
        Pain. 2009; 141: 215-221
        • Hollins M.
        • Sigurdsson A.
        Vibrotactile amplitude and frequency discrimination in temporomandibular disorders.
        Pain. 1998; 75: 59-67
        • Hollins M.
        • Sigurdsson A.
        • Fillingim L.
        • Goble A.K.
        Vibrotactile threshold is elevated in temporomandibular disorders.
        Pain. 1996; 67: 89-96
        • Jasmin L.
        • Rabkin S.D.
        • Granato A.
        • Boudah A.
        • Ohara P.T.
        Analgesia and hyperalgesia from gaba-mediated modulation of the cerebral cortex.
        Nature. 2003; 424: 316-320
        • Jenkinson M.
        • Bannister P.
        • Brady M.
        • Smith S.
        Improved optimization for the robust and accurate linear registration and motion correction of brain images.
        Neuroimage. 2002; 17: 825-841
        • Jenkinson M.
        • Smith S.
        A global optimisation method for robust affine registration of brain images.
        Med Image Anal. 2001; 5: 143-156
        • Jensen R.
        • Hystad T.
        • Kvale A.
        • Baerheim A.
        Quantitative sensory testing of patients with long lasting patellofemoral pain syndrome.
        Eur J Pain. 2007; 11: 665-676
        • Jousmaki V.
        • Hari R.
        Parchment-skin illusion: Sound-biased touch.
        Curr Biol. 1998; 8: R190
        • Kurth R.
        • Villringer K.
        • Mackert B.M.
        • Schwiemann J.
        • Braun J.
        • Curio G.
        • Villringer A.
        • Wolf K.J.
        fMRI assessment of somatotopy in human brodmann area 3b by electrical finger stimulation.
        Neuroreport. 1998; 9: 207-212
        • LaBar K.S.
        • Gatenby J.C.
        • Gore J.C.
        • LeDoux J.E.
        • Phelps E.A.
        Human amygdala activation during conditioned fear acquisition and extinction: A mixed-trial fMRI study.
        Neuron. 1998; 20: 937-945
        • LaMotte R.H.
        • Mountcastle V.B.
        Disorders in somesthesis following lesions of parietal lobe.
        J Neurophysiol. 1979; 42: 400-419
        • Lamour Y.
        • Guilbaud G.
        • Willer J.C.
        Altered properties and laminar distribution of neuronal responses to peripheral stimulation in the SmI cortex of the arthritic rat.
        Brain Res. 1983; 273: 183-187
        • Leffler A.S.
        • Kosek E.
        • Hansson P.
        The influence of pain intensity on somatosensory perception in patients suffering from subacute/chronic lateral epicondylalgia.
        Eur J Pain. 2000; 4: 57-71
        • Mao J.
        • Mayer D.J.
        • Price D.D.
        Patterns of increased brain activity indicative of pain in a rat model of peripheral mononeuropathy.
        J Neurosci. 1993; 13: 2689-2702
        • McGlone F.
        • Kelly E.F.
        • Trulsson M.
        • Francis S.T.
        • Westling G.
        • Bowtell R.
        Functional neuroimaging studies of human somatosensory cortex.
        Behav Brain Res. 2002; 135: 147-158
        • Melzack R.
        The short-form McGill pain questionnaire.
        Pain. 1987; 30: 191-197
        • Morosan P.
        • Rademacher J.
        • Schleicher A.
        • Amunts K.
        • Schormann T.
        • Zilles K.
        Human primary auditory cortex: Cytoarchitectonic subdivisions and mapping into a spatial reference system.
        Neuroimage. 2001; 13: 684-701
        • Moulton E.A.
        • Keaser M.L.
        • Gullapalli R.P.
        • Greenspan J.D.
        Regional intensive and temporal patterns of functional MRI activation distinguishing noxious and innocuous contact heat.
        J Neurophysiol. 2005; 93: 2183-2193
        • Nathan P.W.
        Improvement in cutaneous sensibility associated with relief of pain.
        J Neurol Neurosurg Psychiatry. 1960; 23: 202-206
        • Neugebauer V.
        • Li W.
        Differential sensitization of amygdala neurons to afferent inputs in a model of arthritic pain.
        J Neurophysiol. 2003; 89: 716-727
        • Ohara S.
        • Crone N.E.
        • Weiss N.
        • Treede R.D.
        • Lenz F.A.
        Cutaneous painful laser stimuli evoke responses recorded directly from primary somatosensory cortex in awake humans.
        J Neurophysiol. 2004; 91: 2734-2746
        • Ozcan M.
        • Baumgartner U.
        • Vucurevic G.
        • Stoeter P.
        • Treede R.D.
        Spatial resolution of fMRI in the human parasylvian cortex: Comparison of somatosensory and auditory activation.
        Neuroimage. 2005; 25: 877-887
        • Pinchoff R.J.
        • Burkard R.F.
        • Salvi R.J.
        • Coad M.L.
        • Lockwood A.H.
        Modulation of tinnitus by voluntary jaw movements.
        Am J Otol. 1998; 19: 785-789
        • Pleger B.
        • Ragert P.
        • Schwenkreis P.
        • Forster A.F.
        • Wilimzig C.
        • Dinse H.
        • Nicolas V.
        • Maier C.
        • Tegenthoff M.
        Patterns of cortical reorganization parallel impaired tactile discrimination and pain intensity in complex regional pain syndrome.
        Neuroimage. 2006; 32: 503-510
        • Plesh O.
        • Wolfe F.
        • Lane N.
        The relationship between fibromyalgia and temporomandibular disorders: Prevalence and symptom severity.
        J Rheumatol. 1996; 23: 1948-1952
        • Rollman G.B.
        • Gillespie J.M.
        Disturbances of pain perception in temporomandibular pain syndrome.
        in: Lautenbacher S. Fillingim R.B. Pathophysiology of Pain Perception. Plenum, New York, NY2004: 107-118
        • Sawamoto N.
        • Honda M.
        • Okada T.
        • Hanakawa T.
        • Kanda M.
        • Fukuyama H.
        • Konishi J.
        • Shibasaki H.
        Expectation of pain enhances responses to nonpainful somatosensory stimulation in the anterior cingulate cortex and parietal operculum/posterior insula: An event-related functional magnetic resonance imaging study.
        J Neurosci. 2000; 20: 7438-7445
        • Schurmann M.
        • Caetano G.
        • Hlushchuk Y.
        • Jousmaki V.
        • Hari R.
        Touch activates human auditory cortex.
        Neuroimage. 2006; 30: 1325-1331
        • Senapati A.K.
        • Lagraize S.C.
        • Huntington P.J.
        • Wilson H.D.
        • Fuchs P.N.
        • Peng Y.B.
        Electrical stimulation of the anterior cingulate cortex reduces responses of rat dorsal horn neurons to mechanical stimuli.
        J Neurophysiol. 2005; 94: 845-851
        • Simons S.B.
        • Tannan V.
        • Chiu J.
        • Favorov O.V.
        • Whitsel B.L.
        • Tommerdahl M.
        Amplitude-dependency of response of SI cortex to flutter stimulation.
        BMC Neurosci. 2005; 6: 43
        • Smith S.M.
        Fast robust automated brain extraction.
        Hum Brain Mapp. 2002; 17: 143-155
        • Smith S.M.
        • Jenkinson M.
        • Woolrich M.W.
        • Beckmann C.F.
        • Behrens T.E.
        • Johansen-Berg H.
        • Bannister P.R.
        • De Luca M.
        • Drobnjak I.
        • Flitney D.E.
        • Niazy R.K.
        • Saunders J.
        • Vickers J.
        • Zhang Y.
        • De Stefano N.
        • Brady J.M.
        • Matthews P.M.
        Advances in functional and structural MR image analysis and implementation as FSL.
        Neuroimage. 2004; 23: S208-219
        • Stammler T.
        • De Col R.
        • Seifert F.
        • Maihofner C.
        Functional imaging of sensory decline and gain induced by differential noxious stimulation.
        Neuroimage. 2008; 42: 1151-1163
        • Tommerdahl M.
        • Delemos K.A.
        • Favorov O.V.
        • Metz C.B.
        • Vierck Jr., C.J.
        • Whitsel B.L.
        Response of anterior parietal cortex to different modes of same-site skin stimulation.
        J Neurophysiol. 1998; 80: 3272-3283
        • Tommerdahl M.
        • Delemos K.A.
        • Vierck Jr., C.J.
        • Favorov O.V.
        • Whitsel B.L.
        Anterior parietal cortical response to tactile and skin-heating stimuli applied to the same skin site.
        J Neurophysiol. 1996; 75: 2662-2670
        • Tommerdahl M.
        • Whitsel B.L.
        • Vierck Jr., C.J.
        • Favorov O.
        • Juliano S.
        • Cooper B.
        • Metz C.
        • Nakhle B.
        Effects of spinal dorsal column transection on the response of monkey anterior parietal cortex to repetitive skin stimulation.
        Cereb Cortex. 1996; 6: 131-155
        • Vartiainen N.V.
        • Kirveskari E.
        • Forss N.
        Central processing of tactile and nociceptive stimuli in complex regional pain syndrome.
        Clin Neurophysiol. 2008; 119: 2380-2388
        • Voerman V.F.
        • van Egmond J.
        • Crul B.J.
        Elevated detection thresholds for mechanical stimuli in chronic pain patients: Support for a central mechanism.
        Arch Phys Med Rehabil. 2000; 81: 430-435
        • Weissman D.H.
        • Roberts K.C.
        • Visscher K.M.
        • Woldorff M.G.
        The neural bases of momentary lapses in attention.
        Nat Neurosci. 2006; 9: 971-978
        • Whitsel B.L.
        • Favorov O.V.
        • Li Y.
        • Quibrera M.
        • Tommerdahl M.
        Area 3a neuron response to skin nociceptor afferent drive.
        Cereb Cortex. 2009; 19: 349-366
        • Whitsel B.L.
        • Petrucelli L.M.
        • Werner G.
        Symmetry and connectivity in the map of the body surface in somatosensory area II of primates.
        J Neurophysiol. 1969; 32: 170-183
        • Woolrich M.W.
        • Jbabdi B.
        • Patenaude M.
        • Chappell S.
        • Makni T.
        • Behrens T.E.
        • Beckmann C.F.
        • Jenkinson M.
        • Smith S.
        Bayesian analysis of neuroimaging data in FSL.
        Neuroimage. 2009; 45: S173-186
        • Yap A.U.
        • Chua E.K.
        • Dworkin S.F.
        • Tan H.H.
        • Tan K.B.
        Multiple pains and psychosocial functioning/psychologic distress in TMD patients.
        Int J Prosthodont. 2002; 15: 461-466
        • Yau J.M.
        • Olenczak J.B.
        • Dammann J.F.
        • Bensmaia S.J.
        Temporal frequency channels are linked across audition and touch.
        Curr Biol. 2009; 19: 561-566
        • Zhang N.
        • Gore J.C.
        • Chen L.M.
        • Avison M.J.
        Dependence of bold signal change on tactile stimulus intensity in SI of primates.
        Magn Reson Imaging. 2007; 25: 784-794
        • Zolnoun D.A.
        • Rohl J.
        • Moore C.G.
        • Perinetti-Liebert C.
        • Lamvu G.M.
        • Maixner W.
        Overlap between orofacial pain and vulvar vestibulitis syndrome.
        Clin J Pain. 2008; 24: 187-191