Advertisement

Journal of Neural Transmission

, Volume 126, Issue 12, pp 1667–1677 | Cite as

Theta burst stimulation for the treatment of obsessive–compulsive disorder: a pilot study

  • Antonino Naro
  • Luana Billeri
  • Antonino Cannavò
  • Rosaria De Luca
  • Simona Portaro
  • Placido Bramanti
  • Rocco Salvatore CalabròEmail author
Psychiatry and Preclinical Psychiatric Studies - Original Article
  • 65 Downloads

Abstract

A non-negligible part of patients with obsessive–compulsive disorder (OCD) experiences inadequate response to pharmacological and cognitive therapies. Therefore, new approaches are required to overcome this problem. The present pilot study estimates the capacity of theta burst stimulation (TBS) in reducing OCD symptoms, also focusing on the neurophysiological basis of TBS aftereffects. Ten patients with OCD who were unsatisfactorily responsive to the pharmacological and neuropsychological treatment, participated to the present randomized crossover pilot study, in which they were subjected to a real or sham intermittent TBS (iTBS) paradigm over the left dorsolateral prefrontal cortex (L-DLPFC) as add-on treatment. They were randomly assigned to a real or sham iTBS in a 1:1 allocation ratio. Patients received the TBS treatment every morning, 5 days a week for 1 month, and were clinically and electrophysiologically evaluated (EEG phase synchronization and coherence) before, immediately after (T0), and one (T1), three (T3) and six (T6) months after the end of the TBS treatment. Then, each patient was subjected to the alternative treatment (that was not practiced before), and followed up to 6 months. We found that all the patients improved in OCD symptomatology up to T1, while four among them improved up to T3. These patients were those showing a more extensive reshape of frontal areas phase synchronization and frontoparietal coherence compared to the other participants. Our pilot study suggests that iTBS over L-DLPFC may represent a feasible approach to improve OCD symptoms. The efficacy of iTBS seems to depend on the extent of frontal and frontoparietal connectivity modulation.

Keywords

Obsessive–compulsive disorder Theta burst stimulation Coherence Connectivity Dorsolateral-prefrontal cortex Cortico-striato-thalamo-cortical network 

Notes

Funding

No funding to be reported.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Data availability

The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Abramovitch A, Cooperman A (2015) The cognitive neuropsychology of obsessive-compulsive disorder: a critical review. J Obsess Compuls Relat Disord 5:24–36CrossRefGoogle Scholar
  2. Alexander G (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9(1):357–381CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alvarez JA, Emory E (2006) Executive function and the frontal lobes: a meta-analytic review. Neuropsychol Rev 16(1):17–42CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bandelow B, Zohar J, Hollander E, Kasper S, Möller H, WFSBP Task Force On Treatment Guide (2008) World federation of societies of biological psychiatry (WFSBP) guidelines for the pharmacological treatment of anxiety, obsessive-compulsive and post-traumatic stress disorders—first revision. World J Biol Psychiatry 9(4):248–312CrossRefGoogle Scholar
  5. Bation R, Poulet E, Haesebaert F, Saoud M, Brunelin J (2016) Transcranial direct current stimulation in treatment-resistant obsessive-compulsive disorder: an open-label pilot study. Prog Neuropsychopharmacol Biol Psychiatry 65:153–157CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chung SW, Sullivan CM, Rogasch NC, Hoy KE, Bailey NW, Cash RFH, Fitzgerald PB (2019) The effects of individualised intermittent theta burst stimulation in the prefrontal cortex: a TMS-EEG study. Hum Brain Mapp 40(2):608–627CrossRefGoogle Scholar
  7. Di Lazzaro V, Pilato F, Dileone M, Profice P, Oliviero A, Mazzone P, Rothwell JC (2008) The physiological basis of the effects of intermittent theta burst stimulation of the human motor cortex. J Physiol 586(16):3871–3879CrossRefPubMedPubMedCentralGoogle Scholar
  8. D’Urso G, Brunoni AR, Anastasia A, Micillo M, de Bartolomeis A, Mantovani A (2016) Polarity-dependent effects of transcranial direct current stimulation in obsessive-compulsive disorder. Neurocase 22:60–64CrossRefGoogle Scholar
  9. Fitzgerald KD, Stern ER, Angstadt M, Nicholson-Muth KC, Maynor MR, Welsh RC et al (2010) Altered function and connectivity of the medial frontal cortex in pediatric obsessive–compulsive disorder. Biol Psychiatry 68:1039–1047CrossRefPubMedPubMedCentralGoogle Scholar
  10. Goodman WK, Price LH, Rasmussen SA, Mazure C, Fleischmann RL, Hill CL et al (1989) The yale-brown obsessive-compulsive scale. I. Development, use, and reliability. Arch Gen Psychiatry 46:1006–1011CrossRefGoogle Scholar
  11. Greenberg BD, George MS, Martin JD, Benjamin J, Schlaepfer TE, Altemus M, Wassermann EM, Post RM, Murphy DL (1997) Effect of prefrontal repetitive transcranial magnetic stimulation in obsessive-compulsive disorder: a preliminary study. Am J Psychiatry 154(6):867–869CrossRefGoogle Scholar
  12. Haber SN (2003) The primate basal ganglia: Parallel and integrative networks. J Chem Neuroanat 26(4):317–330CrossRefGoogle Scholar
  13. Harrison BJ, Soriano-Mas C, Pujol J, Ortiz H, López-Solà M, Hernández-Ribas R et al (2009) Altered corticostriatal functional connectivity in obsessive-compulsive disorder. Arch Gen Psychiatry 66:1189–1200CrossRefGoogle Scholar
  14. Horwath E, Weissman MM (2000) The epidemiology and cross-national presentation of obsessive-compulsive disorder Psychiatr. Clin North Am 23:493–507CrossRefGoogle Scholar
  15. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45(2):201–206CrossRefGoogle Scholar
  16. Huang YZ, Rothwell JC, Edwards MJ, Chen RS (2008) Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb Cortex 18(3):563–570CrossRefGoogle Scholar
  17. Jahangard L, Haghighi M, Shyayganfard M, Ahmadpanah M, Bahmani DS, Bajoghli H, Brand S (2016) Repetitive transcranial magnetic stimulation improved symptoms of obsessive-compulsive disorder, but also cognitive performance: results from a randomized clinical trial with a cross-over design and sham condition. Neuropsychobiology 73(4):224–232CrossRefGoogle Scholar
  18. Klimke A, Nitsche MA, Maurer K, Voss U (2016) Case report: successful treatment of therapy-resistant OCD with application of transcranial alternating current stimulation (tACS). Brain Stimul 9:463–465CrossRefGoogle Scholar
  19. Lapidus KA, Stern ER, Berlin HA, Goodman WK (2014) Neuromodulation for obsessive-compulsive disorder. Neurotherapeutics 11:485–495CrossRefPubMedPubMedCentralGoogle Scholar
  20. Lara GA, Alekseichuk I, Turi Z, Lehr A, Antal A, Paulus W (2018) Perturbation of theta-gamma coupling at the temporal lobe hinders verbal declarative memory. Brain Stimul 11:509–517CrossRefGoogle Scholar
  21. Lisanby SH, Gutman D, Luber B, Schroeder C, Sackeim HA (2001) Sham TMS: intracerebral measurement of the induced electrical field and the induction of motor-evoked potentials. Biol Psychiatry 49(5):460–463CrossRefGoogle Scholar
  22. Lisman JE, Jensen O (2013) The theta-gamma neural code. Neuron 77:1002–1016CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lusicic A, Schruers KR, Pallanti S, Castle DJ (2018) Transcranial magnetic stimulation in the treatment of obsessive-compulsive disorder: current perspectives. Neuropsychiatr Dis Treat 14:1721–1736CrossRefPubMedPubMedCentralGoogle Scholar
  24. Ma X, Huang Y, Liao L, Jin Y (2014) A randomized double-blinded sham-controlled trial of electroencephalogram-guided transcranial magneticStimulationfor obsessive–compulsive disorder. Chin Med J 127:601–606PubMedGoogle Scholar
  25. Macdonald AW, Cohen JD, Stenger VA, Carter CS (2000) Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288(5472):1835–1838CrossRefGoogle Scholar
  26. Mantovani A, Rossi S, Bassi BD, Simpson HB, Fallon BA, Lisanby SH (2013) Modulation of motor cortex excitability in obsessive-compulsive disorder: an exploratory study on the relations of neurophysiology measures with clinical outcome. Psychiatry Res 210(3):1026–1032CrossRefGoogle Scholar
  27. Mataix-Cols D, Heuvel OA (2006) Common and distinct neural correlates of obsessive-compulsive and related disorders. Psychiatr Clin North Am 29(2):391–410CrossRefPubMedPubMedCentralGoogle Scholar
  28. Menzies L, Chamberlain SR, Laird AR, Thelen SM, Sahakian BJ, Bullmore ET (2008) Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: the orbitofronto-striatal model revisited. Neurosci Biobehav Rev 32(3):525–549CrossRefGoogle Scholar
  29. Milad MR, Rauch SL (2012) Obsessive-compulsive disorder: beyond segregated cortico-striatal pathways. Trends Cogn Sci 16(1):43–51CrossRefGoogle Scholar
  30. Miyaguchi S, Otsuru N, Kojima S, Saito K, Inukai Y, Masaki M, Onishi H (2018) Transcranial alternating current stimulation with gamma oscillations over the primary motor cortex and cerebellar hemisphere improved visuomotor performance. Front Behav Neurosci 12:132CrossRefPubMedPubMedCentralGoogle Scholar
  31. Mondino M, Haesebaert F, Poulet E, Suaud-Chagny MF, Brunelin J (2015) Efficacy of cathodal transcranial direct current stimulation over the left orbitofrontal cortex in a patient with treatment-resistant obsessive-compulsive disorder. J ECT 31:271–272CrossRefGoogle Scholar
  32. Nakao T, Okada K, Kanba S (2014) Neurobiological model of obsessive-compulsive disorder: evidence from recent neuropsychological and neuroimaging findings. Psychiatry Clin Neurosci 68:587–605CrossRefGoogle Scholar
  33. Narayanaswamy JC, Jose D, Chhabra H, Agarwal SM, Shrinivasa B, Hegde A, Bose A, Kalmady SV, Venkatasubramanian G, Reddy YCJ (2015) Successful application of add-on transcranial direct current stimulation (tDCS) for treatment of SSRI resistant OCD. Brain Stimul 8:655–657CrossRefGoogle Scholar
  34. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25CrossRefGoogle Scholar
  35. Nordmann G, Azorina V, Langguth B, Schecklmann M (2015) A systematic review of non-motor rTMS induced motor cortex plasticity. Front Hum Neurosci 9:416CrossRefPubMedPubMedCentralGoogle Scholar
  36. Olbrich S, Olbrich H, Adamaszek M, Jahn I, Hegerl U, Stengler K (2013) Altered EEG lagged coherence during rest in obsessive–compulsive disorder. Clin Neurophysiol 124:2421–2430CrossRefGoogle Scholar
  37. Pallanti S, Quercioli L (2006) Treatment-refractory obsessive-compulsive disorder: methodological issues, operational definitions and therapeutic lines. Prog Neuropsychopharmacol Biol Psychiatry 30:400–412CrossRefGoogle Scholar
  38. Pascual-Marqui RD (2007) Instantaneous and lagged measurements of linear and nonlinear dependence between groups of multivariate time series: frequency decomposition. ArXiv 0711.1455Google Scholar
  39. Pascual-Marqui RD, Esslen M, Kochi K, Lehmann D (2002) Functional imaging with low-resolution brain electromagnetic tomography (LORETA): a review. Methods Find Exp Clin Pharmacol 24(Suppl. C):91–95PubMedGoogle Scholar
  40. Pena-Garijo J, Ruipérez-Rodríguez MA, Barros-Loscertales A (2010) The neurobiology of obsessive-compulsive disorder: new findings from functional magnetic resonance imaging. Rev Neurol 50(8):477–485PubMedGoogle Scholar
  41. Rachid F (2017) Safety and efficacy of theta-burst stimulation in the treatment of psychiatric disorders: a review of the literature. J Nerv Ment Dis 205(11):823–839CrossRefGoogle Scholar
  42. Robertson E, Tormos J, Maeda F, Pascual-Leone A (2001) The role of the dorsolateral prefrontal cortex during sequence learning is specific for spatial information. Cereb Cortex 11(7):628–635CrossRefGoogle Scholar
  43. Rossi S, Bartalini S, Ulivelli M, Mantovani A, Muro AD, Goracci A, Passero S (2005) Hypofunctioning of sensory gating mechanisms in patients with obsessive-compulsive disorder. Biol Psychiat 57(1):16–20CrossRefGoogle Scholar
  44. Russo M, Naro A, Mastroeni C, Morgante F, Terranova C, Muscatello MR, Zoccali R, Calabrò RS, Quartarone A (2014) Obsessive-compulsive disorder: a “sensory-motor” problem? Int J Psychophysiol 92(2):74–78CrossRefGoogle Scholar
  45. Sachdev PS, Loo CK, Mitchell PB, McFarquhar TF, Malhi GS (2007) Repetitive transcranial magnetic stimulation for the treatment of obsessive compulsive disorder: a double-blind controlled investigation. Psychol Med 37(11):1645–1649CrossRefGoogle Scholar
  46. Schruers K, Koning K, Luermans J, Haack MJ, Griez E (2005) Obsessive–compulsive disorder: a critical review of therapeutic perspectives. Acta Psychiatr Scand 111(4):261–271CrossRefGoogle Scholar
  47. Storch EA, De Nadai AS, Conceição Do Rosário M, Shavitt RG, Torres AR, Ferrão YA, Fontenelle LF (2015) Defining clinical severity in adults with obsessive-compulsive disorder. Compr Psychiatry 63:30–35CrossRefPubMedPubMedCentralGoogle Scholar
  48. Suppa A, Huang Y, Funke K, Ridding M, Cheeran B, Lazzaro VD, Rothwell J (2016) Ten years of theta burst stimulation in humans: established knowledge, unknowns and prospects. Brain Stimul 9(3):323–335CrossRefGoogle Scholar
  49. Talelli P, Greenwood RJ, Rothwell JC (2007) Exploring theta burst stimulation as an intervention to improve motor recovery in chronic stroke. Clin Neurophysiol 118(2):333–342CrossRefGoogle Scholar
  50. Trevizol AP, Shiozawa P, Cook IA, Sato IA, Kaku CB, Guimaraes FB, Sachdev P, Sarkhel S, Cordeiro Q (2016) Transcranial magnetic stimulation for obsessive-compulsive disorder: an updated systematic review and meta-analysis. J ECT 32(4):262–266CrossRefGoogle Scholar
  51. Van den Heuvel OA, van Wingen G, Soriano-Mas C, Alonso P, Chamberlain SR, Nakannae T, Veltman DJ (2016) Brain circuitry of compulsivity. Eur Neuropsychopharmacol 26(5):810–827CrossRefGoogle Scholar
  52. Wassermann EM, Lisanby SH (2001) Therapeutic application of repetitive transcranial magnetic stimulation: a review. Clin Neurophysiol 112(8):1367–1377CrossRefGoogle Scholar
  53. Wu C, Tsai C, Lu M, Chen C, Shen W, Su K (2010) Theta-burst repetitive transcranial magnetic stimulation for treatment-resistant obsessive-compulsive disorder with concomitant depression. J Clin Psychiatry 71(04):504–506CrossRefGoogle Scholar
  54. Zhou D, Wang W, Wang G, Li D, Kuang L (2017) An updated meta-analysis: short-term therapeutic effects of repeated transcranial magnetic stimulation in treating obsessive-compulsive disorder. J Affect Disord 215:187–196CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Antonino Naro
    • 1
  • Luana Billeri
    • 1
  • Antonino Cannavò
    • 1
  • Rosaria De Luca
    • 1
  • Simona Portaro
    • 1
  • Placido Bramanti
    • 1
  • Rocco Salvatore Calabrò
    • 1
    Email author
  1. 1.IRCCS Centro Neurolesi Bonino PulejoMessinaItaly

Personalised recommendations