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01-01-2024 | Transcranial Magnetic Stimulation | Brief Report

Females with painful temporomandibular disorders present higher intracortical facilitation relative to pain-free controls

Authors: Alberto Herrero Babiloni, Marianne Jodoin, Catherine Provost, Camille Charlebois-Plante, Beatrice P. De Koninck, Amelie Apinis-Deshaies, Gilles J. Lavigne, Louis De Beaumont

Published in: Clinical Oral Investigations | Issue 1/2024

Abstract

Objectives

This study aimed to investigate cortical excitability differences in the primary motor cortex (M1) hand representation between individuals with temporomandibular disorders (TMD) and healthy controls. We assessed resting motor thresholds, motor-evoked potentials (MEPs), intracortical inhibition, and intracortical facilitation and explored potential associations with clinical and psychosocial characteristics in the TMD group.

Materials and methods

We recruited 36 female participants with TMD and 17 pain-free controls. Transcranial magnetic stimulation (TMS) was used to assess M1 cortical excitability. Correlations between clinical and psychosocial factors and cortical excitability measures were also evaluated.

Results

Patients with TMD showed significantly higher intracortical facilitation at 12 ms (z = 1.98, p = 0.048) and 15 ms (z = 2.65, p = 0.008) when compared to controls. Correlations revealed associations between intracortical facilitation and pain interference, sleep quality, depressive symptoms, and pain catastrophizing in the TMD group.

Conclusions

Females with TMD exhibit heightened motor cortex intracortical facilitation in the hand representation, potentially indicating altered cortical excitability beyond the motor face area. This suggests a role for cortical excitability in TMD pathophysiology, influenced by psychosocial factors.

Clinical relevance

Understanding cortical excitability in TMD may inform targeted interventions. Psychosocial variables may play a role in cortical excitability, emphasizing the multidimensional nature of TMD-related pain. Further research is needed to confirm and expand upon these findings, with potential implications for the management of TMD and related pain conditions.

Schiffman E, Ohrbach R, Truelove E, Look J, Anderson G, Goulet JP et al (2014) Diagnostic criteria for temporomandibular disorders (DC/TMD) for clinical and research applications: recommendations of the International RDC/TMD Consortium Network* and Orofacial Pain Special Interest Groupdagger. J Oral Facial Pain Headache 28(1):6–27PubMed

Kapos FP, Exposto FG, Oyarzo JF, Durham J (2020) Temporomandibular disorders: a review of current concepts in aetiology, diagnosis and management. Oral Surg 13(4):321–334PubMedPubMedCentral

Chang WJ, O’Connell NE, Beckenkamp PR, Alhassani G, Liston MB, Schabrun SM (2018) Altered primary motor cortex structure, organization, and function in chronic pain: a systematic review and meta-analysis. J Pain 19(4):341–359PubMed

Granovsky Y, Sprecher E, Sinai A (2019) Motor corticospinal excitability: a novel facet of pain modulation? Pain reports 4(2):e725PubMedPubMedCentral

Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol 108(1):1–16PubMed

Nakamura H, Kitagawa H, Kawaguchi Y, Tsuji H (1997) Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J Physiol 498(Pt 3):817–823

Parker RS, Lewis GN, Rice DA, McNair PJ (2016) Is motor cortical excitability altered in people with chronic pain? A systematic review and meta-analysis. Brain Stimul 9(4):488–500PubMed

Turk U, Rosler KM, Mathis J, Mullbacher W, Hess CW (1994) Assessment of motor pathways to masticatory muscles: an examination technique using electrical and magnetic stimulation. Muscle Nerve 17(11):1271–1277PubMed

Vucic S, Stanley Chen KH, Kiernan MC, Hallett M, Benninger DH, Di Lazzaro V et al (2023) Clinical diagnostic utility of transcranial magnetic stimulation in neurological disorders. Updated report of an IFCN committee. Clin Neurophysiol 150:131–175

10.

Galhardoni R, Ciampi de Andrade D, Puerta MY, Brunoni AR, Varotto BL, de Siqueira JT et al (2019) Altered cortical excitability in persistent idiopathic facial pain. Cephalalgia 39(2):219–228

11.

Ginatempo F, Loi N, Manca A, Rothwell JC, Deriu F (2022) Is it possible to compare inhibitory and excitatory intracortical circuits in face and hand primary motor cortex? J Physiol 600(15):3567–3583PubMed

12.

Mhalla A, de Andrade DC, Baudic S, Perrot S, Bouhassira D (2010) Alteration of cortical excitability in patients with fibromyalgia. Pain 149(3):495–500PubMed

13.

Siniatchkin M, Kroner-Herwig B, Kocabiyik E, Rothenberger A (2007) Intracortical inhibition and facilitation in migraine–a transcranial magnetic stimulation study. Headache 47(3):364–370PubMed

14.

Moana-Filho EJ, Herrero BA (2019) Endogenous pain modulation in chronic temporomandibular disorders: derivation of pain modulation profiles and assessment of its relationship with clinical characteristics. J Oral Rehabil 46(3):219–232PubMed

15.

Raphael KG, Janal MN, Sirois DA, Dubrovsky B, Klausner JJ, Krieger AC et al (2015) Validity of self-reported sleep bruxism among myofascial temporomandibular disorder patients and controls. J Oral Rehabil 42(10):751–758PubMedPubMedCentral

16.

Mun CJ, Weaver KR, Hunt CA, Owens MA, Phillips J, Lerman SF et al (2022) Pain expectancy and positive affect mediate the day-to-day association between objectively measured sleep and pain severity among women with temporomandibular disorder. J Pain 23(4):669–679PubMed

17.

Jodoin M, Rouleau DM, Bellemare A, Provost C, Larson-Dupuis C, Sandman E et al (2020) Moderate to severe acute pain disturbs motor cortex intracortical inhibition and facilitation in orthopedic trauma patients: a TMS study. PLoS ONE 15(3):e0226452PubMedPubMedCentral

18.

Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2011) Screening questionnaire before TMS: an update. Clin Neurophysiol 122(8):1686PubMed

19.

Keel JC, Smith MJ, Wassermann EM (2001) A safety screening questionnaire for transcranial magnetic stimulation. Clin Neurophysiol 112(4):720PubMed

20.

Von Korff M, DeBar LL, Krebs EE, Kerns RD, Deyo RA, Keefe FJ (2020) Graded chronic pain scale revised: mild, bothersome, and high-impact chronic pain. Pain 161(3):651–661

21.

Gracely RH, McGrath P, Dubner R (1978) Ratio scales of sensory and affective verbal pain descriptors. Pain 5(1):5–18PubMed

22.

Tan G, Jensen MP, Thornby JI, Shanti BF (2004) Validation of the Brief Pain Inventory for chronic nonmalignant pain. J Pain 5(2):133–137PubMed

23.

Hauser W, Jung E, Erbsloh-Moller B, Gesmann M, Kuhn-Becker H, Petermann F et al (2012) Validation of the Fibromyalgia Survey Questionnaire within a cross-sectional survey. PLoS ONE 7(5):e37504PubMedPubMedCentralADS

24.

Moana-Filho EJ, Herrero Babiloni A, Nisley A (2019) Endogenous pain modulation assessed with offset analgesia is not impaired in chronic temporomandibular disorder pain patients. J Oral Rehabil 46(11):1009–1022PubMed

25.

Miller VE, Poole C, Golightly Y, Barrett D, Chen DG, Ohrbach R et al (2019) Characteristics associated with high-impact pain in people with temporomandibular disorder: a cross-sectional study. J Pain 20(3):288–300PubMed

26.

Ohrbach R, Larsson P, List T (2008) The jaw functional limitation scale: development, reliability, and validity of 8-item and 20-item versions. J Orofac Pain 22(3):219–230PubMed

27.

Kroenke K, Spitzer RL, Williams JB (2001) The PHQ-9: validity of a brief depression severity measure. J Gen Intern Med 16(9):606–613PubMedPubMedCentral

28.

Spitzer RL, Kroenke K, Williams JB, Lowe B (2006) A brief measure for assessing generalized anxiety disorder: the GAD-7. Arch Intern Med 166(10):1092–1097PubMed

29.

Kroenke K, Spitzer RL, Williams JB (2002) The PHQ-15: validity of a new measure for evaluating the severity of somatic symptoms. Psychosom Med 64(2):258–266PubMed

30.

Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24(4):385–396PubMed

31.

Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 28(2):193–213PubMed

32.

Sullivan MJL, Bishop SR, Pivik J (1995) The Pain Catastrophizing Scale: development and validation. Psychol Assess 7(4):524–532

33.

Watson D, Clark LA, Tellegen A (1988) Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol 54(6):1063–1070PubMed

34.

Lefaucheur JP, Aleman A, Baeken C, Benninger DH, Brunelin J, Di Lazzaro V, Filipović SR, Grefkes C, Hasan A, Hummel FC, Jääskeläinen SK, Langguth B, Leocani L, Londero A, Nardone R, Nguyen JP, Nyffeler T, Oliveira-Maia AJ, Oliviero A, Padberg F, Palm U, Paulus W, Poulet E, Quartarone A, Rachid F, Rektorová I, Rossi S, Sahlsten H, Schecklmann M, Szekely D, Ziemann U (2020) Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): an update (2014–2018). Clin Neurophysiol 131(2):474–528. https://doi.org/10.1016/j.clinph.2019.11.002

35.

Rossini PM, Burke D, Chen R, Cohen LG, Daskalakis Z, Di Iorio R et al (2015) Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 126(6):1071–1107

36.

Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M et al (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48(5):1398–1403PubMed

37.

Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A et al (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519PubMedPubMedCentral

38.

Ziemann U, Rothwell JC, Ridding MC (1996) Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol 496(Pt 3):873–881PubMedPubMedCentral

39.

Ziemann U (2003) Pharmacology of TMS. Suppl Clin Neurophysiol 56:226–231PubMed

40.

Paulus W, Classen J, Cohen LG, Large CH, Di Lazzaro V, Nitsche M et al (2008) State of the art: pharmacologic effects on cortical excitability measures tested by transcranial magnetic stimulation. Brain Stimul 1(3):151–163PubMed

41.

Reis J, Swayne OB, Vandermeeren Y, Camus M, Dimyan MA, Harris-Love M et al (2008) Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control. J Physiol 586(2):325–351PubMed

42.

Wassermann EM, Greenberg BD, Nguyen MB, Murphy DL (2001) Motor cortex excitability correlates with an anxiety-related personality trait. Biol Psychiat 50(5):377–382PubMed

43.

Concerto C, Lanza G, Cantone M, Pennisi M, Giordano D, Spampinato C et al (2013) Different patterns of cortical excitability in major depression and vascular depression: a transcranial magnetic stimulation study. BMC Psychiatry 13:300PubMedPubMedCentral

44.

Volz MS, Medeiros LF, TarragoMda G, Vidor LP, Dall’Agnol L, Deitos A et al (2013) The relationship between cortical excitability and pain catastrophizing in myofascial pain. J Pain 14(10):1140–1147

45.

Larsen DB, Graven-Nielsen T, Boudreau SA (2019) Pain-induced reduction in corticomotor excitability is counteracted by combined action-observation and motor imagery. J Pain 20(11):1307–1316PubMed

46.

Civardi C, Boccagni C, Vicentini R, Bolamperti L, Tarletti R, Varrasi C et al (2001) Cortical excitability and sleep deprivation: a transcranial magnetic stimulation study. J Neurol Neurosurg Psychiatry 71(6):809–812PubMedPubMedCentral

47.

Mykland MS, Uglem M, Stovner LJ, Brenner E, Snoen MS, Gravdahl GB et al (2023) Insufficient sleep may alter cortical excitability near the migraine attack: a blinded TMS crossover study. Cephalalgia 43(3):3331024221148391PubMed

48.

Thibaut A, Zeng D, Caumo W, Liu J, Fregni F (2017) Corticospinal excitability as a biomarker of myofascial pain syndrome. Pain reports 2(3):e594PubMedPubMedCentral

49.

Castillo Saavedra L, Mendonca M, Fregni F (2014) Role of the primary motor cortex in the maintenance and treatment of pain in fibromyalgia. Med Hypotheses 83(3):332–336PubMed

50.

Henssen D, Giesen E, van der Heiden M, Kerperien M, Lange S, van Cappellen van Walsum AM et al (2020) A systematic review of the proposed mechanisms underpinning pain relief by primary motor cortex stimulation in animals. Neurosci Lett 719:134489

51.

DosSantos MF, Ferreira N, Toback RL, Carvalho AC, DaSilva AF (2016) Potential mechanisms supporting the value of motor cortex stimulation to treat chronic pain syndromes. Front Neurosci 10:18PubMedPubMedCentral

52.

Woolf CJ (2014) What to call the amplification of nociceptive signals in the central nervous system that contribute to widespread pain? Pain 155(10):1911–1912PubMed

53.

Woolf CJ (2011) Central sensitization: implications for the diagnosis and treatment of pain. Pain 152(3 Suppl):S2-15PubMed

54.

Radhu N, de Jesus DR, Ravindran LN, Zanjani A, Fitzgerald PB, Daskalakis ZJ (2013) A meta-analysis of cortical inhibition and excitability using transcranial magnetic stimulation in psychiatric disorders. Clin Neurophysiol 124(7):1309–1320PubMed

55.

Pacheco-Barrios K, Lima D, Pimenta D, Slawka E, Navarro-Flores A, Parente J et al (2022) Motor cortex inhibition as a fibromyalgia biomarker: a meta-analysis of transcranial magnetic stimulation studies. Brain Netw Modul 1(2):88–101PubMedPubMedCentral

56.

Maarrawi J, Peyron R, Mertens P, Costes N, Magnin M, Sindou M et al (2013) Brain opioid receptor density predicts motor cortex stimulation efficacy for chronic pain. Pain 154(11):2563–2568PubMed

57.

Pagano RL, Fonoff ET, Dale CS, Ballester G, Teixeira MJ, Britto LRG (2012) Motor cortex stimulation inhibits thalamic sensory neurons and enhances activity of PAG neurons: possible pathways for antinociception. Pain 153(12):2359–2369PubMed

58.

Hermans L, Levin O, Maes C, van Ruitenbeek P, Heise KF, Edden RAE et al (2018) GABA levels and measures of intracortical and interhemispheric excitability in healthy young and older adults: an MRS-TMS study. Neurobiol Aging 65:168–177PubMed

59.

Dyke K, Pepes SE, Chen C, Kim S, Sigurdsson HP, Draper A et al (2017) Comparing GABA-dependent physiological measures of inhibition with proton magnetic resonance spectroscopy measurement of GABA using ultra-high-field MRI. Neuroimage 152:360–370PubMed

60.

Dube JA, Mercier C (2011) Effect of pain and pain expectation on primary motor cortex excitability. Clin Neurophysiol 122(11):2318–2323PubMed

61.

Svensson P, Miles TS, McKay D, Ridding MC (2003) Suppression of motor evoked potentials in a hand muscle following prolonged painful stimulation. Eur J Pain 7(1):55–62PubMed

62.

Chowdhury NS, Chiang AKI, Millard SK, Skippen P, Chang WJ, Seminowicz DA, Schabrun SM (2023) Combined transcranial magnetic stimulation and electroencephalography reveals alterations in cortical excitability during pain. Elife 12:RP88567. https://doi.org/10.7554/eLife.88567

63.

De Martino E, Casali A, Casarotto S, Hassan G, Rosanova M, Graven-Nielsen T, Ciampi de Andrade D (2023) Acute pain drives different effects on local and global cortical excitability in motor and prefrontal areas: insights into interregional and interpersonal differences in pain processing. Cerebral Cortex 33(18):9986–9996. https://doi.org/10.1093/cercor/bhad259

64.

De Gennaro L, Bertini M, Ferrara M, Curcio G, Cristiani R, Romei V et al (2004) Intracortical inhibition and facilitation upon awakening from different sleep stages: a transcranial magnetic stimulation study. Eur J Neurosci 19(11):3099–3104PubMed

65.

Salas RE, Galea JM, Gamaldo AA, Gamaldo CE, Allen RP, Smith MT et al (2014) Increased use-dependent plasticity in chronic insomnia. Sleep 37(3):535–544PubMedPubMedCentral

66.

Kinjo M, Wada M, Nakajima S, Tsugawa S, Nakahara T, Blumberger DM et al (2021) Transcranial magnetic stimulation neurophysiology of patients with major depressive disorder: a systematic review and meta-analysis. Psychol Med 51(1):1–10PubMed

67.

Vidor LP, Torres IL, Medeiros LF, Dussan-Sarria JA, Dall’agnol L, Deitos A et al (2014) Association of anxiety with intracortical inhibition and descending pain modulation in chronic myofascial pain syndrome. BMC Neurosci 15:42

68.

Cueva AS, Galhardoni R, Cury RG, Parravano DC, Correa G, Araujo H et al (2016) Normative data of cortical excitability measurements obtained by transcranial magnetic stimulation in healthy subjects. Neurophysiol Clin = Clin Neurophysiol 46(1):43–51

69.

Herrero Babiloni A, Exposto FG, Peck CM, Lindgren BR, Martel MO, Lenglet C et al (2022) Temporomandibular disorders cases with high-impact pain are more likely to experience short-term pain fluctuations. Sci Rep 12(1):1657PubMedPubMedCentralADS

Title: Females with painful temporomandibular disorders present higher intracortical facilitation relative to pain-free controls
Authors: Alberto Herrero Babiloni
Marianne Jodoin
Catherine Provost
Camille Charlebois-Plante
Beatrice P. De Koninck
Amelie Apinis-Deshaies
Gilles J. Lavigne
Louis De Beaumont
Publication date: 01-01-2024
Publisher: Springer Berlin Heidelberg
Keywords: Transcranial Magnetic Stimulation
Transcranial Magnetic Stimulation
Motor Evoked Potential
Motor Evoked Potential
Published in: Clinical Oral Investigations / Issue 1/2024
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI: https://doi.org/10.1007/s00784-023-05412-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Females with painful temporomandibular disorders present higher intracortical facilitation relative to pain-free controls

Abstract

Objectives

Materials and methods

Results

Conclusions

Clinical relevance

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objectives

Materials and methods

Results

Conclusions

Clinical relevance

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