Cognitive effects of high-frequency repetitive transcranial magnetic stimulation: a systematic review

Journal of Neural Transmission - Tập 117 - Trang 105-122 - 2009
Birgit Guse1, Peter Falkai1, Thomas Wobrock1
1Department of Psychiatry and Psychotherapy, Georg-August-University Göttingen, Gottingen, Germany

Tóm tắt

Transcranial magnetic stimulation (TMS) was introduced as a non-invasive tool for the investigation of the motor cortex. The repetitive application (rTMS), causing longer lasting effects, was used to study the influence on a variety of cerebral functions. High-frequency (>1 Hz) rTMS is known to depolarize neurons under the stimulating coil and to indirectly affect areas being connected and related to emotion and behavior. Researchers found selective cognitive improvement after high-frequency (HF) stimulation specifically over the left dorsolateral prefrontal cortex (DLPFC). This article provides a systematic review of HF-rTMS studies (1999–2009) stimulating over the prefrontal cortex of patients suffering from psychiatric/neurological diseases or healthy volunteers, where the effects on cognitive functions were measured. The cognitive effect was analyzed with regard to the impact of clinical status (patients/healthy volunteers) and stimulation type (verum/sham). RTMS at 10, 15 or 20 Hz, applied over the left DLPFC, within a range of 10–15 successive sessions and an individual motor threshold of 80–110%, is most likely to cause significant cognitive improvement. In comparison, patients tend to reach a greater improvement than healthy participants. Limitations concern the absence of healthy groups in clinical studies and partly the absence of sham groups. Thus, future investigations are needed to assess cognitive rTMS effects in different psychiatric disorders versus healthy subjects using an extended standardized neuropsychological test battery. Since the pathophysiological and neurobiological basis of cognitive improvement with rTMS remains unclear, additional studies including genetics, experimental neurophysiology and functional brain imaging are necessary to explore stimulation-related functional changes in the brain.

Tài liệu tham khảo

Avery DH, Hotzheimer PE, Fawaz W, Russo J, Neumaier J, Dunner DL, Haynor DR, Claypoole KH, Wajdik C, Roy-Byrne P (2006) A controlled study of repetitive transcranial magnetic stimulation in medication-resistant major depression. Biol Psychiatry 59:187–194 Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex (letter). Lancet 1:1106–1107 Ben-Shachar D, Belmaker RH, Grisaru N, Klein E (1997) Transcranial magnetic stimulation induces alternations in brain monoamines. J Neural Transm 104:191–197 Boggio PS, Fregni F, Bermpohl F, Mansur CG, Rosa M, Rumi DO, Barbosa ER, Rosa MO, Pascual-Leone A, Rigonatti SP, Marcolin MA, Silva MTA (2005) Effect of repetitive TMS and fluoxetine on cognitive function in patients with Parkinson’s disease and concurrent depression. Brief reports. Mov Disord 20(9):1178–1219 Burt T, Lisanby SH, Sackheim HA (2002) Neuropsychiatric applications of transcranial magnetic stimulation: a meta analysis. Int J Neuropsychopharmacol 5:73–103 Carpenter PA, Just MA, Shell P (1990) What one intelligence test measures: a theoretical account of the processing in the Raven Progressive Matrices Test. Psychol Rev 97:404–431 Chao LL, Knight RT (1995) Human prefrontal lesions increase distractibility to irrelevant sensory inputs. Neuroreport 21:1605–1610 Conca A, Koppi S, Konig P, Swoboda E, Krecke N (1996) Transcranial magnetic stimulation: a novel antidepressive strategy? Neuropsychobiology 34:204–207 Conca A, Peschina W, Konig P, Fritzsche H, Hausmann A (2002) Effect of chronic repetitive transcranial magnetic stimulation on regional cerebral blood flow and regional glucose uptake in drug treatment-resistant depressives: a brief report. Neuropsychobiology 45:27–31 Cordes J, Mobascher A, Arends M, Agelink MW, Klimke A (2005) A new method for the treatment of depression: Transcranial magnetic stimulation. Dtsch Med Wochenschr 130:889–892 Davies DR, Jones DM, Taylor A (1984) Selective and sustained-attention tasks: Individual and group differences. In: Parasuraman R, Davies DR (eds) Varieties of Attention. Academic, Orlando Dolan RJ, Bench CJ, Liddle PF (1993) Dorsolateral prefrontal cortex dysfunction in the major psychoses: symptoms or disease specificity? J Neurosurg Psychiatr 56:1290–1294 Esser SK, Huber R, Massimini M, Peterson MJ, Ferrarelli F, Tononi G (2006) A direct demonstration of cortical LTP in humans: A combined TMS/EEG study. J Brain Res Bull 69(1):86–94 Fabre I, Galinowski A, Oppenheim C, Gallarda T, Meder JF, de Montigny C, Olié JP, Poirier MF (2004) Antidepressant efficacy and cognitive effects of repetitive transcranial magnetic stimulation in vascular depression: an open trial. Int J Geriatr Psychiatry 19:833–842 Fitzgerald PB, Benitez J, Daskalakis JZ, Brown TL, Marston N, de Castella A, Kulkarni J (2005) A double-blind sham-controlled trial of repetitive transcranial magnetic stimulation in the treatment of refractory auditory hallucinations. J Clin Psychopharmacol 25(4):358–362 Fox P, Ingham R, George MS, Mayberg H, Ingham J, Roby J, Martin C, Jerabek P (1997) Imaging human intra-cerebral connectivity ba PET during rTMS. Neuroreport 8:2787–2791 Fregni F, Otachi P, do Valle A, Boggio PS, Thut G, Rigonatti S, Pascual-Leone A, Valente KD (2006) A randomized clinical trial of repetitive transcranial magnetic stimulation in patients with refractory epilepsy. Ann Neurol 60:447–455 Fuster JM (1987) The prefrontal cortex: anatomy, physiology, and neuropsychology of the frontal lobe. Lippincott-Raven, New York George MS, Belmaker RH (2000) Transcranial magnetic stimulation in neuropsychiatry. American Psychiatric Association, Washington Gershon AA, Dannon PN, Grunhaus L (2003) Transcranial magnetic stimulation in the treatment of depression. Am J Psychiatry 160:835–845 Goldmann-Rakic PS (1997) Circuitry of primate prefrontal cortex and regulation of behaviour by representational memory. In: Plum F (ed) Handbook of physiology. Nervous system, vol 5. Higher functions of the brain. American Physiological Society, Bethesda, pp 373–417 Hajak G, Marienhagen J, Langguth B, Werner S, Binder H, Eichhammer P (2004) High frequency transcranial magnetic stimulation in schizophrenia: a combined treatment and neuroimaging study. Psychol Med 34:1157–1163 Haraldsson HM, Ferrarelli F, Kalin NH, Tononi G (2004) Transcranial magnetic stimulation in the investigation and treatment of schizophrenia: a review. Schizophr Res 71:1–16 Hausmann A, Pascual-Leone A, Kemmler G, Rupp CI, Lechner-Schoner T, Kramer-Reinstadler K, Walpoth M, Mechtcheriakov S, Conca A, Weiss EM (2004) No deterioration of cognitive performance in an aggressive unilateral and bilateral antidepressant rTMS add-on trial. J Clin Psychiatry 65(6):772–782 Herwig U, Padberg F, Unger J, Spitzer M, Schönfeldt-Lecuona C (2001) Transcranial magnetic stimulation in therapy studies: examination of the reliability of “standard” coil positioning by neuronavigation. Biol Psychiatry 50(1):58–61 Hoffmann RE, Gueorguieva R, Hawkins KA, Varanko M, Boutros NN, Wu YT, Caroll K, Krystal JH (2005) Temporoparietal transcranial magnetic stimulation for auditory hallucinations: safety, efficacy and moderators in a fifty patients sample. Biol Psychiatry 58:97–104 Höppner J, Schulz M, Mau R, Schläfke D, Richter J (2003) Antidepressant efficacy of two different rTMS procedures. Eur Arch Psychiatry Clin Neurosci 253:103–109 Huang CC, Su TP, Shan IK, Wei IH (2004) Effect of 5 Hz repetitive transcranial magnetic stimulation on cognition during a Go/NoGo task. J Psychiatr Res 38:513–520 Huber TJ, Schneider U, Rollnik J (2003) Gender differences in the effect of repetitive transcranial magnetic stimulation in schizophrenia. Psychiatry Res 120(1):103–105 Jandl M, Bittner R, Sack A, Weber B, Günther T, Maurer K, Kaschka WP (2004) Effects of rTMS on negative symptoms and EEG-topography in schizophrenic patients. Eur Psychiatry 19(Suppl 1):164 Jandl M, Bittner R, Sack A, Weber B, Günther T, Pieschl D, Kaschka WP, Maurer K (2005) Changes in negative symptoms and EEG in schizophrenic patients after repetitive transcranial magnetic stimulation (rTMS): an open-label pilot study. J Neural Transm 112:955–967 Januel D, Dumortier G, Verdon CM, Stamatiadis L, Saba G, Cabaret W, Benadhira R, Rocamora JF, Braha S, Kalalou K, Vicaut PE, Fermanian J (2006) A double-blind sham controlled study of right prefrontal repetitive transcranial magnetic stimulation (rTMS): Therapeutic and cognitive effect in medication free unipolar depression during 4 weeks. Prog Neuropsychopharmacol Biol Psychiatry 30(1):126–130 Jin Y, Potkin SG, Kemp AS, Huerta ST, Alva G, Thai TM, Carreon D, Bunney WE Jr (2006) Therapeutic effects of individualized alpha frequency transcranial magnetic stimulation (alpha rTMS) on negative symptoms of schizophrenia. Schizophr Bull 32:556–561 Jorge RE, Robinson RG, Tateno A, Narushima K, Acion L, Moser L, Arndt S, Chemerinski E (2004) Repetitive transcranial magnetic stimulation as treatment of poststroke depression: a preliminary study. Biol Psychiatry 55:398–405 Kinchla RA (1992) Attention. Annu Rev Psychol 43:711–742 Kuroda Y, Motohashi N, Ito H, Ito S, Takano A, Nishikawa T, Suhara T (2006) Effects of repetitive transcranial magnetic stimulation on [11C] raclopride binding and cognitive function in patients with depression. J Affect Disord 95:35–42 Little JT, Kimbrell TA, Wassermann EM, Grafman J, Figueras S, Dunn RT, Danielson A, Repella J, Huggins T, George MS, Post RM (2000) Cognitive effects of 1- and 20-Hertz repetitive transcranial magnetic stimulation in depression: preliminary report. Neuropsychiatry Neuropsychol Behav Neurol 13(2):119–124 Loo C (2001) Effects of a 2- to 4-week course of repetitive transcranial magnetic stimulation (rTMS) on neuropsychologic functioning, electroencephalogram, and auditory threshold in depressed patients. Biol Psychiatry 49:615–623 Loo C, Mitchell PB, Croker VM, Malhi GS, Wen W, Gandevia SC, Sachdev PS (2003) Double-blind controlled investigation of bilateral prefrontal transcranial magnetic stimulation for the treatment of resistant major depression. Psychol Med 33:33–40 Martis B, Alam D, Dowd SM, Hill SK, Sharma RP, Rosen C, Pliskin N, Martin E, Carson V, Janicak PG (2003) Neurocognitive effects of repetitive transcranial magnetic stimulation in severe major depression. Clin Neurophysiol 114:1125–1132 May A, Hajak G, Gänsbauer S, Steffens T, Langguth B, Kleinjung T, Eichhammer P (2007) Structural brain alterations following 5 days of intervention: dynamic aspects of neuroplasticity. Cereb Cortex 17:205–210 Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. A Rev Neurosci 24:167–202 Mogg A, Pluck G, Eranti SV, Landau S, Purvis R, Brown RG, Curtis V, Howard R, Philpot M, McLoughlin DM (2008) A randomized controlled trial with 4-month follow-up of adjunctive repetitive transcranial magnetic stimulation of the left prefrontal cortex for depression. Psychol Med 38(3):323–333 Moser DJ, Jorge RE, Manes MD, Paradiso S, Benjamin BS, Robinson RG (2002) Improved executive functioning following repetitive transcranial magnetic stimulation. Neurology 58:1288–1290 Mosimann UP, Schmitt W, Greenberg BD, Kosel M, Müri RM, Berkhoff M, Hess CW, Fisch HU, Schlaepfer TE (2004) Repetitive transcranial magnetic stimulation: a putative add on treatment for major depression in elderly patients. Psychiatr Res 126:123–133 O’Connor M, Brenninkmeyer C, Morgan A, Bloomingdale K, Thall M, Vasile R, Pascual Leone A (2003) Magnetic stimulation and electroconvulsive therapy on mood and memory: a neurocognitive risk-benefit-analysis. Cogn Behav Neurol 6(2):118–127 Padberg F, Zwanzger P, Thoma H, Kathmann N, Haag C, Greenberg BD, Hampel H, Möller HJ (1999) Repetitive transcranial magnetic stimulation (rTMS) in pharmacotherapy-refractory major depression: comparative study of fast, slow and sham rTMS. Psychiatry Res 88(3):163–171 Posner MI (1975) The psychology of attention. In: Gazzaniga MS, Blakemore C (eds) Handbook of psychology. Academic, New York Posner MI, Boies SW (1971) Components of attention. Psychol Rev 78:391–408 Post A, Keck ME (2001) Transcranial magnetic stimulation as a therapeutic tool in psychiatry: what do we know about the neurobiological mechanism? J Psychiatr Res 35:193–215 Poulet E, Brunelin J, Bediou B, Forgeard L, Daleru J, D’Amato T, Saoud M (2005) Slow transcranial magnetic stimulation can rapidly reduce resistant auditory hallucinations in schizophrenia. Biol Psychiatry 57:188–191 Rektorova I, Megova S, Bares M, Rektor I (2005) Cognitive functioning after repetitive transcranial magnetic stimulation in patients with cerebrovascular disease without dementia: a pilot study of seven patients. J Neurol Sci 229–230:157–161 Ridding MC, Rothwell JC (2007) Is there a future for therapeutic use of transcranial magnetic stimulation? NatRevNeurosci 8(7):559–567 Rollnik JD, Huber TJ, Mogk H, Siggelkow S, Kropp S, Dengler R, Emrich HM, Schneider U (2000) High frequency repetitive transcranial magnetic stimulation (rTMS) of the dorsolateral prefrontal cortex in schizophrenic patients. NeuroReport 11:4013–4015 Rosa MA, Gattaz WF, Pascual-Leone A, Fregni F, Rosa MO, Rumi DO, Myczkowski M, Silva MF, Mansur C, Rigonatti SP, Teixeira MJ, Marcolin MA (2006) Comparison of repetitive transcranial magnetic stimulation and electroconvulsive therapy in unipolar non-psychotic depression: a randomized single-blind study. Int J Neuropsychopharmacol 9(6):667–676 Sachdev P, Loo C, Mitchell P, Malhi G (2005) Transcranial magnetic stimulation for the deficit syndrome of schizophrenia: A pilot investigation. Psychiatry Clin Neurosci 59(3):354–357 Sack AT, Linden DE (2003) Combining transcranial magnetic stimulation and functional imaging in cognitive brain research: possibilities and limitations. Brain Res Brain Res Rev 43(1):41–56 Sack AT, Cohen Kadosh R, Schumann T, Moerel M, Walsh V, Goebel R (2009) Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. J Cogn Neurosci 21(2):207–221 Sackeim HA, Portnoy S, Neeley P, Steif BL, Decina P, Malitz S (1986) Cognitive consequences of low-dosage electroconvulsive therapy. Ann NY Acad Sci 462:326–340 Schulze-Rauschenbach SC, Harms U, Schlaepfer TE, Maier W, Falkai F, Wagner M (2005) Distinctive neurocognitive effects of repetitive transcranial magnetic stimulation and electroconvulsive therapy in major depression. Br J Psychiatry 186:410–416 Shajahan PM, Glabus MF, Steele JD, Doris AB, Anderson K, Jenkins JA, Gooding PA, Ebmeier KP (2002) Left dorso-lateral repetitive transcranial magnetic stimulation affects cortical excitability and functional connectivity, but does not impair cognition in major depression. Prog Neuropsychopharmacol Biol Psychiatry 26(5):945–954 Solé-Padullés C, Bartrés-Faz D, Junqué C, Clemente IC, Molinuevo JL, Bargalló N, Sánchez-Aldeguer J, Bosch B, Falcón C, Valls-Solé J (2006) Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study. Cereb Cortex 16:1487–1493 Speer AM, Repella JD, Figueras S, Demian NK, Kimbrell TA, Wasserman EM, Post RM (2001) Lack of adverse cognitive effects of 1 Hz and 20 Hz repetitive transcranial magnetic stimulation at 100% of motor threshold over left prefrontal cortex in depression. J ECT 17(4):259–263 Squire LR (1982) Memory and electroconvulsive therapy (Letter). Am J Psychiatry 139:1221 Strafella A, Paus T, Barrett J, Dagher A (2001) Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci 21(157):1–4 Stuss DT, Benson DF (1986) The frontal lobes. Raven, New York Triggs WJ, McCoy KJM, Greer R, Rossi F, Bowers D, Kortenkamp S, Nadeau SE, Heilman KM, Goodman WK (1999) Effects of left frontal transcranial magnetic stimulation on depressed mood, cognition, and corticomotor threshold. Biol Psychiatry 45(11):1440–1446 Trojano L, Conson M, Maffei R, Grossi D (2006) Categorial and coordinate spatial processing in the imagery domain investigated by rTMS. Neuropsychologia 44(9):1569–1574 Vanderhasselt MA, De Raedt R, Baeken C, Leyman L, D’haenen H (2006) The influence of rTMS over the left dorsolateral prefrontal cortex on Stroop task performance. Exp Brain Res 169:279–282 Vanderhasselt MA, De Raedt R, Leyman L, Baeken C (2009) Acute effects of repetitive transcranial magnetic stimulation on attentional control are related to antidepressant outcomes. J Psychiatry Neurosci 34(2):119–126 Wagner W, Rihs TA, Mosimann UP, Fisch HU, Schlaepfer TE (2006) Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex affects divided attention immediately after cessation of stimulation. J Psychiatr Res 40:315–321 Weinberger DR, Berman KF, Chase TN (1988) Mesocortical dopaminergic function and human cognition. Ann NY Acad Sci 537:330–338 Weiner RD, Rogers HJ, Davidson JR, Squire LR (1986) Effects of stimulus parameters on cognitive side effects. Ann NY Acad Sci 462:315–325 Zimmermann P, Fimm B (1997) Test for Attentional Performance (TAP), version 1.5. Psytest Press, Freiburg