fMRI study of brain activity elicited by oral parafunctional movements.

Parafunctional masticatory activity, such as the tooth clenching and grinding that is associated with bruxism, is encountered by clinicians in many disciplines, including dentistry, neurology and psychiatry. Despite this, little is known about the neurological basis for these activities. To identify the brain network engaged in such complex oromotor activity, functional magnetic resonance imaging (fMRI) was used to elucidate the brain activation patterns of 20 individuals (10 males and 10 females, mean s.d. age of 26.3+/-4.1 years) with (parafunctional, PFx group, 5M/5F) and without (normal functional, NFx group, 5 M/5F) self-reported parafunctional grinding and clenching habits during clenching and grinding tasks. Subject group classification was based on: (i) self-reported history, (ii) clinical examination, (iii) evaluation of dental casts and (iv) positive responses to the temporomandibular disorder (TMD) History Questionnaire [Dworkinand LeResche, Journal of Craniomandibular Disorders, (1992) 6:301]. While subjects performed these oromotor tasks, each wore a custom-designed oral appliance minimizing head motion during imaging. Mean per cent signal changes showed significant between group differences in motor cortical (supplementary motor area, sensorimotor cortex and rolandic operculum) and subcortical (caudate) regions. Supplementary motor area data suggest that motor planning and initiation, particularly during the act of clenching, are less prominent in individuals with oromotor parafunctional behaviours. The overall extent of activated areas was reduced in subjects with self-reported parafunctional masticatory activity compared with the controls. This study's methodology and findings provide an initial step in understanding the neurological basis of parafunctional masticatory activities that are relevant for therapeutic research applications of temporomandibular joint and muscle disorders and associated comorbidities.

[1]  B. Vogt,et al.  Structural and functional dichotomy of human midcingulate cortex , 2003, The European journal of neuroscience.

[2]  R. Omar,et al.  Identification and management of tooth wear. , 1994, The International journal of prosthodontics.

[3]  M. Jeannerod,et al.  Mental motor imagery: a window into the representational stages of action , 1995, Current Opinion in Neurobiology.

[4]  C. Büchel,et al.  Dissociable Neural Responses Related to Pain Intensity, Stimulus Intensity, and Stimulus Awareness within the Anterior Cingulate Cortex: A Parametric Single-Trial Laser Functional Magnetic Resonance Imaging Study , 2002, The Journal of Neuroscience.

[5]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[6]  Krish D. Singh,et al.  fMRI of Thermal Pain: Effects of Stimulus Laterality and Attention , 2002, NeuroImage.

[7]  S. Ogawa Brain magnetic resonance imaging with contrast-dependent oxygenation , 1990 .

[8]  M. Jeannerod Mental imagery in the motor context , 1995, Neuropsychologia.

[9]  Andreas Hennenlotter,et al.  The functional neuroanatomy of coordinated orofacial movements: Sparse sampling fMRI of whistling , 2005, NeuroImage.

[10]  T. Haraldson,et al.  A system for assessing the severity and progression of occlusal tooth wear. , 1993, Journal of oral rehabilitation.

[11]  E Honda,et al.  Chewing-side Preference is Involved in Differential Cortical Activation Patterns during Tongue Movements after Bilateral Gum-chewing: a Functional Magnetic Resonance Imaging Study , 2004, Journal of dental research.

[12]  F. Lobbezoo,et al.  No association between incisal tooth wear and temporomandibular disorders. , 2002, The Journal of prosthetic dentistry.

[13]  P. Matthews,et al.  Exacerbation of Pain by Anxiety Is Associated with Activity in a Hippocampal Network , 2001, The Journal of Neuroscience.

[14]  M. Onozuka,et al.  Mapping Brain Region Activity during Chewing: A Functional Magnetic Resonance Imaging Study , 2002, Journal of dental research.

[15]  David Borsook,et al.  Functional imaging of the human trigeminal system: opportunities for new insights into pain processing in health and disease. , 2004, Journal of neurobiology.

[16]  J. Maisog,et al.  Pain intensity processing within the human brain: a bilateral, distributed mechanism. , 1999, Journal of neurophysiology.

[17]  F. Lobbezoo Taking up Challenges at the Interface of Wear and Tear , 2007, Journal of dental research.

[18]  M. Hallett,et al.  Functional properties of brain areas associated with motor execution and imagery. , 2003, Journal of neurophysiology.

[19]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[20]  T. Kawasaki,et al.  Functional magnetic resonance imaging of human jaw movements. , 2003, Journal of oral rehabilitation.

[21]  G. Lavigne,et al.  Neurobiological mechanisms involved in sleep bruxism. , 2003, Critical reviews in oral biology and medicine : an official publication of the American Association of Oral Biologists.

[22]  M. Onozuka,et al.  Age-related Changes in Brain Regional Activity during Chewing: A Functional Magnetic Resonance Imaging Study , 2003, Journal of dental research.

[23]  T. Rudy,et al.  The association between wear facets, bruxism, and severity of facial pain in patients with temporomandibular disorders. , 2003, The Journal of prosthetic dentistry.

[24]  R. de Leeuw,et al.  The contribution of neuroimaging techniques to the understanding of supraspinal pain circuits: implications for orofacial pain. , 2005, Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics.

[25]  J. Tanji,et al.  The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. , 1993, Brain : a journal of neurology.

[26]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[27]  V D Calhoun,et al.  Spatial and temporal independent component analysis of functional MRI data containing a pair of task‐related waveforms , 2001, Human brain mapping.

[28]  E Kruse,et al.  Foix-Chavany-Marie (anterior operculum) syndrome in childhood: a reappraisal of Worster-Drought syndrome. , 2000 .

[29]  S. Lehéricy,et al.  Foot, hand, face and eye representation in the human striatum. , 2003, Cerebral cortex.

[30]  C. Elias,et al.  Alternative pathways for catecholamine action in oral motor control , 2005, Neuroscience Letters.

[31]  P. Rompré,et al.  Identification of a Sleep Bruxism Subgroup with a Higher Risk of Pain , 2007, Journal of dental research.

[32]  A. Dale,et al.  Tonotopic organization in human auditory cortex revealed by progressions of frequency sensitivity. , 2004, Journal of neurophysiology.

[33]  J. R. Baker,et al.  Imaging subcortical auditory activity in humans , 1998, Human brain mapping.

[34]  W. Schady,et al.  The influence of external timing cues upon the rhythm of voluntary movements in Parkinson's disease. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[35]  Gang Chen,et al.  Contextual Fear Conditioning in Humans: Cortical-Hippocampal and Amygdala Contributions , 2008, The Journal of Neuroscience.

[36]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[37]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[38]  Arlette Kolta,et al.  Brainstem circuits that control mastication: do they have anything to say during speech? , 2006, Journal of communication disorders.

[39]  Changes in regional cerebral blood flow during mastication in young and old normal subjects measured with positron emission tomography , 1992 .

[40]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[41]  Y Sasaki,et al.  Effect of mastication on regional cerebral blood flow in humans examined by positron-emission tomography with ¹⁵O-labelled water and magnetic resonance imaging. , 1997, Archives of oral biology.

[42]  Hans-Otto Karnath,et al.  Awareness of the Functioning of One's Own Limbs Mediated by the Insular Cortex? , 2005, The Journal of Neuroscience.

[43]  M. Kryger,et al.  Principles and Practice of Sleep Medicine , 1989 .

[44]  G. Menexes,et al.  Association between self-reported bruxism activity and occurrence of dental attrition, abfraction, and occlusal pits on natural teeth. , 2008, The Journal of prosthetic dentistry.

[45]  G. Pagnoni,et al.  Does Anticipation of Pain Affect Cortical Nociceptive Systems? , 2002, The Journal of Neuroscience.

[46]  S. Grillner,et al.  Mechanisms for selection of basic motor programs – roles for the striatum and pallidum , 2005, Trends in Neurosciences.

[47]  J. Valls-Solé,et al.  Chewing pattern in patients with Meige's syndrome , 2005, Movement disorders : official journal of the Movement Disorder Society.

[48]  C Büchel,et al.  Painful stimuli evoke different stimulus-response functions in the amygdala, prefrontal, insula and somatosensory cortex: a single-trial fMRI study. , 2002, Brain : a journal of neurology.

[49]  M. Glickstein,et al.  What does the cerebellum really do? , 2007, Current Biology.

[50]  A. Glaros,et al.  Incidence of diurnal and nocturnal bruxism. , 1981, The Journal of prosthetic dentistry.

[51]  D. Crammond Motor imagery: never in your wildest dream , 1997, Trends in Neurosciences.

[52]  J. Bremner,et al.  Functional neuroimaging studies in posttraumatic stress disorder: review of current methods and findings , 2007, Depression and anxiety.

[53]  S. Dworkin,et al.  Research diagnostic criteria for temporomandibular disorders: review, criteria, examinations and specifications, critique. , 1992, Journal of craniomandibular disorders : facial & oral pain.

[54]  Sabrina M. Tom,et al.  The Neural Correlates of Motor Skill Automaticity , 2005, The Journal of Neuroscience.

[55]  J. Konczak,et al.  The effect of damage to the cerebellum on sensorimotor and cognitive function in children and adolescents , 2007, Neuroscience & Biobehavioral Reviews.

[56]  F Lobbezoo,et al.  Bruxism is mainly regulated centrally, not peripherally. , 2001, Journal of oral rehabilitation.

[57]  Takao Kawasaki,et al.  Analysis of brain activity during clenching by fMRI. , 2002, Journal of oral rehabilitation.

[58]  Bruce R. Rosen,et al.  Motion detection and correction in functional MR imaging , 1995 .

[59]  David Borsook,et al.  Somatotopic Activation in the Human Trigeminal Pain Pathway , 2002, The Journal of Neuroscience.

[60]  L. Lynd,et al.  Selective Serotonin-Reuptake Inhibitor–Induced Movement Disorders , 1998, The Annals of pharmacotherapy.

[61]  H. Kirshner,et al.  The opercular-subopercular syndrome: four cases with review of the literature. , 1998, Behavioural neurology.

[62]  K. Koyano,et al.  Assessment of bruxism in the clinic. , 2008, Journal of oral rehabilitation.

[63]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[64]  G. M. Murray,et al.  Neuronal activity patterns in primate primary motor cortex related to trained or semiautomatic jaw and tongue movements. , 2002, Journal of neurophysiology.

[65]  C. L. Kwan,et al.  Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold, and tactile stimuli. , 1998, Journal of neurophysiology.

[66]  M. Lowe,et al.  Neural network for encoding immediate memory in phonological processing , 2004, Neuroreport.

[67]  J. Decety The neurophysiological basis of motor imagery , 1996, Behavioural Brain Research.

[68]  E. Chudler,et al.  Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanesthetized monkeys. , 1994, Journal of neurophysiology.

[69]  I. McGregor,et al.  The distribution of 3,4-methylenedioxymethamphetamine “Ecstasy”-induced c-fos expression in rat brain , 1999, Neuroscience.

[70]  James S. Hyde,et al.  Strategies for block-design fMRI experiments during task-related motion of structures of the oral cavity , 2006, NeuroImage.

[71]  Bruce Pike,et al.  Differentiating noxious- and innocuous-related activation of human somatosensory cortices using temporal analysis of fMRI. , 2002, Journal of neurophysiology.

[72]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[73]  K. Raphael,et al.  Bruxism physiology and pathology: an overview for clinicians. , 2008, Journal of oral rehabilitation.