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Influence of high-frequency repetitive transcranial magnetic stimulation over the dorsolateral prefrontal cortex on the inhibition of emotional information in healthy volunteers

Published online by Cambridge University Press:  06 October 2008

L. Leyman ,
R. De Raedt ,
M.-A. Vanderhasselt  and
C. Baeken
L. Leyman*
Affiliation:
Department of Psychology, Ghent University, Belgium
R. De Raedt
Affiliation:
Department of Psychology, Ghent University, Belgium
M.-A. Vanderhasselt
Affiliation:
Department of Psychology, Ghent University, Belgium
C. Baeken
Affiliation:
Department of Psychiatry, Academic Hospital (UZ), Free University of Brussels, Belgium
*
*Address for correspondence: Drs. L. Leyman, Ghent University, Department of Psychology, Henri Dunantlaan 2, B-9000 Ghent, Belgium. (Email: lemke.leyman@UGent.be)
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Abstract

Background

Evidence suggests that repetitive transcranial magnetic stimulation (rTMS) over the left dorsolateral prefrontal cortex (DLPFC) might be a promising new treatment procedure for depression. However, underlying working mechanisms of this technique are yet unclear. Multiple sessions of rTMS may – apart from the reported antidepressant effects – cause primary improvements in attentional control over emotional information, modulated by changes in cortical brain excitability within stimulated prefrontal regions.

Method

In two experiments, we examined the temporary effects of high-frequency (HF) rTMS (10 Hz) applied over the left and right DLPFC on the attentional processing of emotional information and self-reported mood within samples of healthy volunteers.

Results

The present study showed that one session of HF-rTMS over the right DLPFC produces instant impairments in the ability to inhibit negative information, in line with a characteristic cognitive vulnerability found in depressive pathology, whereas HF-rTMS of the left DLPFC did not lead to significant changes in attentional control. These effects could not be attributed to mood changes.

Conclusions

The findings of the present study may suggest a specific involvement of the right DLPFC in the attentional processing of emotional information.

Keywords

DepressionDLPFCinhibitionrTMS
Type
Original Articles
Information
Psychological Medicine , Volume 39 , Issue 6 , June 2009 , pp. 1019 - 1028
Copyright
Copyright © Cambridge University Press 2008

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References

Anand, S, Hotson, J (2002). Transcranial magnetic stimulation: neurophysiological applications and safety. Brain and Cognition 50, 366–386.Google Scholar
Avery, DH, Holtzheimer, PE 3rd, 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. Biological Psychiatry 59, 187–194.CrossRefGoogle ScholarPubMed
Baeken, C, Leyman, L, De Raedt, R, Vanderhasselt, MA, D'Haenen, H (2006). Lack of impact of repetitive high frequency transcranial magnetic stimulation on mood in healthy female subjects. Journal of Affective Disorders 90, 63–66.Google Scholar
Baeken, C, Leyman, L, De Raedt, R, Vanderhasselt, MA, D'Haenen, H (2008). Left and right high frequency repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex does not affect mood in female volunteers. Clinical Neurophysiology 119, 568–575.Google Scholar
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erlbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561–565.CrossRefGoogle ScholarPubMed
Boggio, PS, Bermpohl, F, Vergara, AO, Muniz, ALCR, Nahas, FH, Leme, PB, Rigonatti, SP, Fregni, F (2007). Go-no-go task performance improvement after anodal transcranial DC stimulation of the left dorsolateral prefrontal cortex in major depression. Journal of Affective Disorders 101, 91–98.Google Scholar
Bortolomasi, M, Minelli, A, Fuggetta, G, Perini, M, Comencini, S, Fiaschi, A, Manganotti, P (2007). Long-lasting effects of high frequency repetitive transcranial magnetic stimulation in major depressed patients. Psychiatry Research 150, 181–186.CrossRefGoogle ScholarPubMed
d'Alfonso, AAL, van Honk, J, Hermans, E, Postma, A, de Haan, EHF (2000). Laterality effects in selective attention to threat after repetitive transcranial magnetic stimulation at the prefrontal cortex in female subjects. Neuroscience Letters 280, 195–198.CrossRefGoogle ScholarPubMed
Davidson, RJ, Pizzagalli, D, Nitschke, JB, Putman, K (2002). Depression: perspectives from affective neuroscience. Annual Review of Psychology 53, 545–574.CrossRefGoogle ScholarPubMed
Drevets, WC (2000). Neuroimaging studies of mood disorders. Biological Psychiatry 48, 813–829.CrossRefGoogle ScholarPubMed
Eranti, S, Mogg, A, Pluck, G, Landau, S, Purvis, R, Brown, RG, Howard, R, Knapp, M, Philpot, M, Rabe-Hesketh, S, Romeo, R, Rothwell, J, Edwards, D, McLoughlin, DM (2007). A randomized, controlled trial with 6-month follow-up of repetitive transcranial magnetic stimulation and electroconvulsive therapy for severe depression. American Journal of Psyhiatry 164, 73–81.Google ScholarPubMed
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. International Journal of Geriatric Psychiatry 19, 833–842.CrossRefGoogle ScholarPubMed
Fitzgerald, PB, Benitez, J, de Castella, A, Daskalakis, ZJ, Brown, TL, Kulkarni, J (2006). A randomized, controlled trial of sequential bilateral repetitive transcranial magnetic stimulation for treatment-resistant depression. American Journal of Psychiatry 163, 88–94.CrossRefGoogle ScholarPubMed
Gershon, AA, Dannon, PN, Grunhaus, L (2003). Transcranial magnetic stimulation in the treatment of depression. American Journal of Psychiatry 160, 835–845.Google Scholar
Goeleven, E, De Raedt, R, Baert, S, Koster, EHW (2006). Deficient inhibition of emotional information in depression. Journal of Affective Disorders 93, 149–157.CrossRefGoogle ScholarPubMed
Goeleven, E, De Raedt, R, Leyman, L, Verschuere, B (2008). The Karolinska Directed Emotional Faces: a validation study. Cognition and Emotion 22, 1094–1118.CrossRefGoogle Scholar
Gotlib, IH, Yue, DN, Joormann, J (2005). Selective attention in dysphoric individuals: the role of affective interference and inhibition. Cognitive Therapy and Research 29, 417–432.Google Scholar
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. Journal of Clinical Psychiatry 65, 772–782.CrossRefGoogle Scholar
Heller, W, Nitschke, JB (1997). Regional brain activity in emotion: a framework for understanding cognition in depression. Cognition and Emotion 11, 638–661.Google Scholar
Henriques, JB, Davidson, RJ (1991). Left frontal hypoactivation in depression. Journal of Abnormal Psychology 100, 535–545.CrossRefGoogle ScholarPubMed
Herwig, U, Fallgatter, AJ, Höppner, J, Eschweiler, GW, Kron, M, Hajak, G, Padberg, F, Naderi-Heiden, A, Abler, B, Eichhammer, P, Grossheinrich, N, Hay, B, Kammer, T, Langguth, B, Laske, C, Plewnia, C, Richter, MM, Schulz, M, Unterecker, S, Zinke, A, Spitzer, M, Schönfeldt-Lecuona, C (2007). Antidepressant effects of augmentative transcranial magnetic stimulation: randomised multicentre trial. British Journal of Psychiatry 191, 441–448.CrossRefGoogle ScholarPubMed
Holtzheimer, PE, Russo, J, Avery, DH (2002). A meta-analysis of repetitive transcranial magnetic stimulation in the treatment of depression. Biological Psychiatry 51, 15s–15s.Google Scholar
Ingram, RE, Miranda, J, Zegal, ZV (1998). Cognitive Vulnerability to Depression. Guilford Press: New York.Google Scholar
Joormann, J (2004). Attentional bias in dysphoria: the role of inhibitory processes. Cognition and Emotion 18, 125–147.CrossRefGoogle Scholar
Klein, E, Kreinin, I, Chistyakov, A, Koren, D, Mecz, L, Marmur, S, Ben-Shachar, D, Feinsod, M (1999). Therapeutic efficacy of right prefrontal slow repetitive transcranial magnetic stimulation in major depression: a double-blind controlled study. Archives of General Psychiatry 56, 315–320.CrossRefGoogle ScholarPubMed
Kluger, BM, Triggs, WJ (2007). Use of transcranial magnetic stimulation to influence behavior. Current Neurology and Neuroscience Reports 7, 491–497.Google Scholar
Koster, EHW, De Raedt, R, Goeleven, E, Franck, E, Crombez, G (2005). Mood-congruent attentional bias in dysphoria: maintained attention to and impaired disengagement from negative information. Emotion 5, 446–455.CrossRefGoogle ScholarPubMed
Kozel, F, George, M (2002). Meta-analysis of left prefrontal repetitive transcranial magnetic stimulation (rTMS) to treat depression. Journal of Psychiatric Practice 8, 270–275.Google Scholar
Leppänen, JM (2006). Emotional information processing in mood disorder: a review of behavioural and neuroimaging findings. Current Opinion in Psychiatry 19, 34–39.Google Scholar
Leyman, L, De Raedt, R, Schacht, R, Koster, EHW (2007). Attentional biases for angry faces in unipolar depression. Psychological Medicine 37, 393–402.CrossRefGoogle ScholarPubMed
Liotti, M, Mayberg, HS (2001). The role of functional neuroimaging in the neuropsychology of depression. Journal of Clinical and Experimental Neuropsychology 23, 121–136.CrossRefGoogle ScholarPubMed
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 Neuropsychology and Behavioral Neurology 13, 119–124.Google ScholarPubMed
Levin, RL, Heller, W, Mohanty, A, Herrington, JD, Miller, GA (2007). Cognitive deficits in depression and functional specificity of regional brain activity. Cognitive Therapy and Research 31, 211–233.CrossRefGoogle Scholar
Loo, CK, Mitchell, PB (2005). A review of the efficacy of transcranial magnetic stimulation (TMS) treatment for depression, and current and future strategies to optimize efficacy. Journal of Affective Disorders 88, 255–267.CrossRefGoogle ScholarPubMed
Luborzewski, A, Schubert, F, Seifert, F, Danker-Hopfe, H, Brakemeier, EL, Schlattmann, P, Anghelescu, I, Colla, M, Bajbouj, M (2007). Metabolic alterations in the dorsolateral prefrontal cortex after treatment with high-frequency repetitive transcranial magnetic stimulation in patients with unipolar major depression. Journal of Psychiatric Research 41, 606–615.Google Scholar
MacDonald, III AW, Cohen, JD, Stenger, VA, Carter, CS (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288, 1835–1838.CrossRefGoogle ScholarPubMed
Martin, JLR, Barbanoj, MJ, Schlaepfer, TE, Thompson, E, Perez, V, Kulisevsky, J (2003). Repetitive transcranial magnetic stimulation for the treatment of depression – systematic review and meta-analysis. British Journal of Psychiatry 182, 480–491.CrossRefGoogle ScholarPubMed
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. Clinical Neurophysiology 114, 1125–1132.Google Scholar
Mayberg, HS (1997). Limbic-cortical dysregulation: a proposed model of depression. Journal of Neuropsychiatry and Clinical Neurosciences 9, 471–481.Google ScholarPubMed
Mayberg, HS (2007). Defining the neural circuitry of depression: toward a new nosology with therapeutic implications. Biological Psychiatry 61, 729–730.CrossRefGoogle Scholar
McCormack, HM, David, J, Horne, L, Sheater, S (1988). Clinical applications of visual analogue scales: a critical review. Psychological Medicine 18, 1007–1019.CrossRefGoogle ScholarPubMed
McNamara, B, Ray, JL, Arthurs, OJ, Boniface, S (2001). Transcranial magnetic stimulation for depression and other psychiatric disorders. Psychological Medicine 31, 1141–1146.CrossRefGoogle ScholarPubMed
Mosimann, UP, Rihs, TA, Engeler, J, Fisch, H, Schlaepfer, TE (2000). Mood effects of repetitive transcranial magnetic stimulation of the left prefrontal cortex in healthy volunteers. Psychiatry Research 94, 251–256.CrossRefGoogle ScholarPubMed
Miyake, A, Friedman, NP, Emerson, MJ, Witzki, AH, Howerter, A (2000). The unity and diversity of executive functions and their contributions to complex ‘Frontal Lobe’ tasks: a latent variable analysis. Cognitive Psychology 41, 49–100.CrossRefGoogle ScholarPubMed
O'Conner, MG, Jerskey, BA, Robertson, EM, Brenninkmeyer, C, Ozdemir, E, Leone, AP (2005). The effects of repetitive transcranial magnetic stimulation (rTMS) on procedural memory and dysphoric mood in patients with major depressive disorder. Cognitive and Behavioral Neurology 18, 223–227.CrossRefGoogle Scholar
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 Research 88, 163–171.CrossRefGoogle ScholarPubMed
Pascual-Leone, A, Catala, MD, Pascual-Leone, PA (1996). Lateralized effect of rapid-rate transcranial magnetic stimulation of the prefrontal cortex on mood. Neurology 46, 499–502.CrossRefGoogle ScholarPubMed
Pinninti, NR, Madison, H, Musser, E, Rissmiller, D (2003). MINI International Neuropsychiatric Schedule: clinical utility and patient acceptance. European Psychiatry 18, 361–364.Google Scholar
Posner, MI (1980). Orientation of attention. Quarterly Journal of Experimental Psychology 32, 3–25.Google Scholar
Post, A, Keck, ME (2001). Transcranial magnetic stimulation as a therapeutic tool in psychiatry: what do we know about the neurobiological mechanisms? Journal of Psychiatric Research 35, 193–215.CrossRefGoogle ScholarPubMed
Rachid, F, Bertschy, G (2006). Safety and efficacy of repetitive transcranial magnetic stimulation in the treatment of depression: a critical appraisal of the last 10 years. Clinical Neurophysiology 36, 157–183.Google Scholar
Rounis, E, Stephan, KE, Lee, L, Siebner, HR, Pesenti, A, Friston, KJ, Rothwell, JC, Frackowiak, RSJ (2006). Acute changes in frontoparietal activity after repetitive transcranial magnetic stimulation over the dorsolateral prefrontal cortex in a cued reaction time task. Journal of Neuroscience 26, 9629–2638.CrossRefGoogle Scholar
Schulze-Rauschenbach, SC, Harms, U, Schlaepfer, TE, Maier, W, Falkai, P, Wagner, M (2005). Distinctive neurocognitive effects of repetitive transcranial magnetic stimulation and electroconvulsive therapy in major depression. British Journal of Psychiatry 186, 410–416.Google Scholar
Siebner, HR, Lang, N, Rizzo, V, Nitsche, MA, Paulus, W, Lemon, RN, Rothwell, JC (2004). Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. Journal of Neuroscience 24, 3379–3385.CrossRefGoogle ScholarPubMed
Silvanto, J, Cattaneo, Z, Battelli, L, Pascual-Leone, A (2008). Baseline cortical excitability determines whether TMS disrupts or facilitates behaviour. Journal of Neurophysiology 99, 2725–2730.Google Scholar
Speer, AM, 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. Journal of ECT 17, 259–263.Google Scholar
Taylor, JG, Fragopanagos, NF (2005). The interaction of attention and emotion. Neural Networks 18, 353–369.Google Scholar
Tomarken, AJ, Keener, AD (1998). Frontal brain asymmetry and depression: a self-regulatory perspective. Cognition and Emotion 12, 387–420.Google Scholar
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. Experimental Brain Research 169, 279–282.Google Scholar
van Honk, J, Schutter, DJLG, d'Alfonso, AAL, Kessels, RPC, de Haan, EHF (2002). 1 Hz rTMS over the right prefrontal cortex reduces vigilant attention to unmasked but not to masked fearful faces. Biological Psychiatry 52, 312–317.CrossRefGoogle ScholarPubMed
Van Strien, JW (2001). Hand preference and language ascendency [in Dutch]. Neuropraxis 2, 10–15.Google Scholar
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. Electroencephalography and Clinical Neurophysiology 108, 1–16.CrossRefGoogle ScholarPubMed
Wentura, D (1999). Activation and inhibition of affective information. Evidence for negative priming in the evaluation task. Cognition and Emotion 13, 65–91.Google Scholar