The relationship between brain oscillatory activity and therapeutic effectiveness of transcranial magnetic stimulation in the treatment of major depressive disorder

Andrew F Leuchter, Ian A Cook, Yi Jin, Bill Phillips, Andrew F Leuchter, Ian A Cook, Yi Jin, Bill Phillips

Abstract

Major depressive disorder (MDD) is marked by disturbances in brain functional connectivity. This connectivity is modulated by rhythmic oscillations of brain electrical activity, which enable coordinated functions across brain regions. Oscillatory activity plays a central role in regulating thinking and memory, mood, cerebral blood flow, and neurotransmitter levels, and restoration of normal oscillatory patterns is associated with effective treatment of MDD. Repetitive transcranial magnetic stimulation (rTMS) is a robust treatment for MDD, but the mechanism of action (MOA) of its benefits for mood disorders remains incompletely understood. Benefits of rTMS have been tied to enhanced neuroplasticity in specific brain pathways. We summarize here the evidence that rTMS entrains and resets thalamocortical oscillators, normalizes regulation and facilitates reemergence of intrinsic cerebral rhythms, and through this mechanism restores normal brain function. This entrainment and resetting may be a critical step in engendering neuroplastic changes and the antidepressant effects of rTMS. It may be possible to modify the method of rTMS administration to enhance this MOA and achieve better antidepressant effectiveness. We propose that rTMS can be administered: (1) synchronized to a patient's individual alpha frequency (IAF), or synchronized rTMS (sTMS); (2) as a low magnetic field strength sinusoidal waveform; and, (3) broadly to multiple brain areas simultaneously. We present here the theory and evidence indicating that these modifications could enhance the therapeutic effectiveness of rTMS for the treatment of MDD.

Keywords: individual alpha frequency; major depressive disorder; mechanism of action of TMS; rTMS; sTMS.

Figures

Figure 1
Figure 1
Effects of rTMS stimulation on brain function. On average, patients with MDD exhibit a broad pattern of highly synchronous theta and alpha activity over most brain regions (A). rTMS administered as a train of high amplitude pulses at a frequency of 10 Hz entrains brain oscillatory activity to the frequency of stimulation, for the duration of the stimulation period (B). Multiple treatments over time may have the effect of resetting cortical oscillators. Once oscillators are reset, regionally-specific endogenous rhythms of the brain may reemerge. These consist of beta and gamma activity in the frontal cortex, beta in the parietal cortex, and alpha in the occipital cortex (C).
Figure 2
Figure 2
Effects of sTMS stimulation on brain function. On average, patients with MDD exhibit a pattern of highly synchronous theta and alpha activity seen broadly over most brain regions (A). The low-amplitude sinusoidal stimulation provided by the neodymium magnets rotating at the IAF entrains brain oscillatory activity to the frequency of stimulation for the duration of the stimulation period (B). Like the high amplitude pulses of rTMS, multiple treatments of subthreshold sinusoidal stimulation may have the effect of resetting cortical oscillators. Once oscillators are reset, regionally-specific endogenous rhythms of the brain may reemerge. These consist of beta and gamma activity in the frontal cortex, beta in the parietal cortex, and alpha in the occipital cortex (C).

References

    1. Anastassiou C. A., Perin R., Markram H., Koch C. (2011). Ephaptic coupling of cortical neurons. Nat. Neurosci. 14, 217–223 10.1038/nn.2727
    1. Antal A., Boros K., Poreisz C., Chaieb L., Terney D., Paulus W. (2008). Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans. Brain Stimul. 1, 97–105 10.1016/j.brs.2007.10.001
    1. Arai N., Okabe S., Furubayashi T., Terao Y., Yuasa K., Ugawa Y. (2005). Comparison between short train, monophasic and biphasic repetitive transcranial magnetic stimulation (rTMS) of the human motor cortex. Clin. Neurophysiol. 116, 605–613 10.1016/j.clinph.2004.09.020
    1. Arns M., Spronk D., Fitzgerald P. B. (2010). Potential differential effects of 9 Hz rTMS and 10 Hz rTMS in the treatment of depression. Brain Stimul. 3, 124–126 10.1016/j.brs.2009.07.005
    1. Awata S., Ito H., Konno M., Ono S., Kawashima R., Fukuda H., et al. (1988). Regional cerebral blood flow abnormalities in late-life depression: relation to refractoriness and chronification. Psychiatry Clin. Neurosci. 52, 97–105 10.1111/j.1440-1819.1998.tb00980.x
    1. Baeken C., De Raedt R., Bossuyt A., Van Hove C., Mertens J., Dobbeleir A., et al. (2011). The impact of HF-rTMS treatment on serotonin(2A) receptors in unipolar melancholic depression. Brain Stimul. 4, 104–111 10.1016/j.brs.2010.09.002
    1. Barker A. T., Jalinous R., Freeston I. L. (1985). Non-invasive magnetic stimulation of the human motor cortex. Lancet 1, 1106–1107
    1. Benedek M., Bergner S., Könen T., Fink A., Neubauer A. C. (2011). EEG alpha synchronization is related to top-down processing in convergent and divergent thinking. Neuropsychologia 49, 3505–3511 10.1016/j.neuropsychologia.2011.09.004
    1. Ben-Shachar D., Gazawi H., Riboyad-Levin J., Klein E. (1999). Chronic repetitive transcranial magnetic stimulation alters beta-adrenergic and 5-HT2 receptor characteristics in rat brain. Brain Res. 816, 78–83 10.1016/S0006-8993(98)01119-6
    1. Bish J. P., Martin T., Houck J., Ilmoniemi R. J., Tesche C. (2004). Phase shift detection in thalamocortical oscillations using magnetoencephalography in humans. Neurosci. Lett. 362, 48–52 10.1016/j.neulet.2004.02.032
    1. Bluhm R., Williamson P., Lanius R., Théberge J., Densmore M., Bartha R. (2009). Resting state default-mode network connectivity in early depression using a seed region-of-interest analysis: decreased connectivity with caudate nucleus. Psychiatry Clin. Neurosci. 63, 754–761 10.1111/j.1440-1819.2009.02030.x
    1. Bocchio-Chiavetto L., Miniussi C., Zanardini R., Gazzoli A., Bignotti S., Specchia C., et al. (2008). 5-HTTLPR and BDNF Val66Met polymorphisms and response to rTMS treatment in drug resistant depression. Neurosci. Lett. 437, 130–134 10.1016/j.neulet.2008.04.005
    1. Boggio P. S., Valasek C. A., Campanha C., Giglio A. C., Baptista N. I., Lapenta O. M., et al. (2011). Non-invasive brain stimulation to assess and modulate neuroplasticity in Alzheimer's disease. Neuropsychol. Rehabil. 21, 703–716 10.1080/09602011.2011.617943
    1. Boynton R. M., Olson C. X. (1990). Salience of chromatic basic color terms confirmed by three measures. Vision Res. 30, 1311–1317 10.1016/0042-6989(90)90005-6
    1. Brignani D., Manganotti P., Rossini P. M., Miniussi C. (2008). Modulation of cortical oscillatory activity during transcranial magnetic stimulation. Hum. Brain Mapp. 29, 603–612 10.1002/hbm.20423
    1. Britz J., Van De Ville D., Michel C. M. (2010). BOLD correlates of EEG topography reveal rapid resting-state network dynamics. Neuroimage 52, 1162–1170 10.1016/j.neuroimage.2010.02.052
    1. Bruder G. E., Fong R., Tenke C. E., Leite P., Towey J. P., Stewart J. E., et al. (1997). Regional brain asymmetries in major depression with or without an anxiety disorder: a quantitative electroencephalographic study. Biol. Psychiatry 41, 939–948 10.1016/S0006-3223(96)00260-0
    1. Buzsáki G., Draguhn A. (2004). Neuronal oscillations in cortical networks. Science 304, 1926–1929 10.1126/science.1099745
    1. Carlezon W. A., Jr., Rohan M. L., Mague S. D., Meloni E. G., Parsegian A., Cayetano K., et al. (2005). Antidepressant-like effects of cranial stimulation within a low-energy magnetic field in rats. Biol. Psychiatry 57, 571–576 10.1016/j.biopsych.2004.12.011
    1. Carpenter L. L., Janicak P. G., Aaronson S. T., Boyadjis T., Brock D. G., Cook I. A., et al. (2012). Transcranial magnetic stimulation (TMS) for major depression: a multisite, naturalistic, observational study of acute treatment outcomes in clinical practice. Depress. Anxiety 29, 587–596 10.1002/da.21969
    1. Cheeran B., Tallelli P., Mori F., Koch G., Suppa A., Edwards M., et al. (2008). A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J. Physiol. 586, 5717–5725 10.1113/jphysiol.2008.159905
    1. Cho S. S., Strafella A. P. (2009). rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS ONE 4:e6725 10.1371/journal.pone.0006725
    1. Cintia A. E. (2005). Relationship between regional cerebral blood flow and separate symptom clusters of major depression: a single photon emission computed comography study using statistical parametric mapping. Neurosci. Lett. 384, 265–270 10.1016/j.neulet.2005.04.088
    1. Coan J. A., Allen J. J. (2004). Frontal EEG asymmetry as a moderator and mediator of emotion. Biol. Psychol. 67, 7–49 10.1016/j.biopsycho.2004.03.002
    1. Cohrs S., Tergau F., Korn J., Becker W., Hajak G. (2001). Suprathreshold repetitive transcranial magnetic stimulation elevates thyroid-stimulating hormone in healthy male subjects. J. Nerv. Ment. Dis. 189, 393–397
    1. Cook C. M., Saucier D. M., Thomas A. W., Prato F. S. (2009). Changes in human EEG alpha activity following exposure to two different pulsed magnetic field sequences. Bioelectromagnetics 30, 9–20 10.1002/bem.20434
    1. Cook C. M., Thomas A. W., Keenliside L., Prato F. S. (2005). Resting EEG effects during exposure to a pulsed ELF magnetic field. Bioelectromagnetics 26, 367–376 10.1002/bem.20113
    1. Cullen K. R., Gee D. G., Klimes-Dougan B., Gabbay V., Hulvershorn L., Mueller B. A., et al. (2009). A preliminary study of functional connectivity in comorbid adolescent depression. Neurosci. Lett. 460, 227–231 10.1016/j.neulet.2009.05.022
    1. Czeh B., Welt T., Fischer A. K., Erhardt A., Schmitt W., Muller M. B., et al. (2002). Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol. Psychiatry 52, 1057–1065
    1. Dannon P. N., Grunhaus L. (2001). Effect of electroconvulsive therapy in repetitive transcranial magnetic stimulation non-responder MDD patients: a preliminary study. Int. J. Neuropsychopharmacol. 4, 265–268 10.1017/S1461145701002498
    1. Davidson R. J., Mednick D., Moss E., Saron C., Schaffer C. E. (1987). Ratings of emotion in faces are influenced by the visual field to which stimuli are presented. Brain Cogn. 6, 403–411
    1. Debener S., Beauducel A., Nessler D., Brocke B., Heilemann H., Kayser J. (2000). Is resting anterior EEG alpha asymmetry a trait marker for depression? Findings for healthy adults and clinically depressed patients. Neuropsychobiology 41, 31–37 10.1159/000026630
    1. Deng Z. D., Lisanby S. H., Peterchev A. V. (2013). Electric field depth-focality tradeoff in transcranial magnetic stimulation: simulation comparison of 50 coil designs. Brain Stimul. 6, 1–13 10.1016/j.brs.2012.02.005
    1. Di Lazzaro V., Dileone M., Pilato F., Capone F., Musumeci G., Ranieri F., et al. (2011). Modulation of motor cortex neuronal networks by rTMS: comparison of local and remote effects of six different protocols of stimulation. J. Neurophysiol. 105, 2150–2156 10.1152/jn.00781.2010
    1. Dolan R. J., Bench C. J., Brown R. G., Scott L. C., Frackowiak R. S. (1994). Neuropsychological dysfunction in depression: the relationship to regional cerebral blood flow. Psychol. Med. 24, 849–857
    1. Dzirasa K., Phillips H., Sotnikova T., Salahpour A., Kumar S., Gainetdinov R. R., et al. (2010). Noradrenergic control of cortico-striato-thalamic and mesolimbic crossstructural synchrony. J. Neurosci. 30, 6387–6397 10.1523/JNEUROSCI.0764-10.2010
    1. Epstein J., Perez D., Ervin K., Pan H., Kocsis J., Butler T., et al. (2011). Failure to segregate emotional processing from cognitive and sensorimotor processing in major depression. Psychiatry Res. 193, 144–150 10.1016/j.pscychresns.2011.01.012
    1. Evers S., Böckermann I., Nyhuis P. W. (2001). The impact of transcranial magnetic stimulation on cognitive processing: an event-related potential study. Neuroreport 12, 2915–2918
    1. Fecteau S., Pascual-Leone A., Theoret H. (2006). Paradoxical facilitation of attention in healthy humans. Behav. Neurol. 17, 159–162
    1. Feige B., Scheffler K., Esposito F., Di Salle F., Hennig J. (2005). Cortical and subcortical correlates of electroencephalographic alpha rhythm modulation. J. Neurophysiol. 93, 2864–2872 10.1152/jn.00721.2004
    1. Fingelkurts A. A., Fingelkurts A. A., Rytsälä H., Suominen K., Isomestsa E., Kahkonen S. (2006). Composition of brain oscillations in ongoing EEG during major depression disorder. Neurosci. Res. 56, 133–144 10.1016/j.neures.2006.06.006
    1. Fingelkurts A. A., Fingelkurts A. A., Rytsälä H., Suominen K., Isometsa E., Kahkonen S. (2007). Impaired functional connectivity at EEG alpha and theta frequency bands in major depression. Hum. Brain Mapp. 28, 247–261 10.1002/hbm.20275
    1. Fitzgerald P. B., Fountain S., Daskalakis Z. J. (2006). A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin. Neurophysiol. 117, 2584–2585 10.1016/j.clinph.2006.06.712
    1. Francis J. T., Gluckman B. J., Schiff S. J. (2003). Sensitivity of neurons to weak electric fields. J. Neurosci. 23, 7255–7261
    1. Freitas C., Mondragón-Llorca H., Pascual-Leone A. (2011). Noninvasive brain stimulation in Alzheimer's disease: systematic review and perspectives for the future. Exp. Gerontol. 46, 611–627 10.1016/j.exger.2011.04.001
    1. Freitas C., Perez J., Knobel M., Tormos J. M., Oberman L., Eldaief M., et al. (2011). Changes in cortical plasticity across the lifespan. Front. Aging Neurosci. 3:5 10.3389/fnagi.2011.00005
    1. Fröhlich F., McCormick D. A. (2010). Endogenous electric fields may guide neocortical network activity. Neuron 67, 129–143 10.1016/j.neuron.2010.06.005
    1. Fuggetta G., Fiaschi A., Manganotti P. (2005). Modulation of cortical oscillatory activities induced by varying single-pulse transcranial magnetic stimulation intensity over the left primary motor area: a combined EEG and TMS study. Neuroimage 27, 896–908 10.1016/j.neuroimage.2005.05.013
    1. Fuggetta G., Noh N. A. (2012). A neurophysiological insight into the potential link between transcranial magnetic stimulation, thalamocortical dysrhythmia and neuropsychiatric disorders. Exp. Neurol. pii: S0014-4886(12)00393-7. [Epub ahead of print]. 10.1016/j.expneurol.2012.10.010
    1. Fuggetta G., Pavone E. F., Fiaschi A., Manganotti P. (2008). Acute modulation of cortical oscillatory activities during short trains of high-frequency repetitive transcranial magnetic stimulation of the human motor cortex: a combined EEG and TMS study. Hum. Brain Mapp. 29, 1–13 10.1002/hbm.20371
    1. Galynker I. E., Galynker I. I., Cai J., Onseng F., Finestone H., Dutta E., et al. (1998). Hypofrontality and negative symptoms in major depressive disorder. J. Nucl. Med. 39, 608–612
    1. Gentner R., Wankerl K., Reinsberger C., Zeller D., Classen J. (2008). Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb. Cortex 18, 2046–2053 10.1093/cercor/bhm239
    1. George M. S., Lisanby S. H., Avery D., McDonald W. M., Durkalski V., Pavlicova M., et al. (2010). Daily left prefrontal transcranial magnetic stimulation therapy for major depressive disorder: a sham-controlled randomized trial. Arch. Gen. Psychiatry 67, 507–516 10.1001/archgenpsychiatry.2010.46
    1. George M. S., Nahas Z., Molloy M., Speer A. M., Oliver N. C., Li X., et al. (2000). A controlled trial of daily left prefrontal cortex TMS for treating depression. Biol. Psychiatry 48, 962–970
    1. George M. S., Wassermann E. M. (1994). Rapid-rate transcranial magnetic stimulation and ECT. Convuls. Ther. 10, 251–254
    1. George M. S., Wassermann E. M., Williams W. A., Callahan A., Ketter T. A., Basser P., et al. (1995). Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression. Neuroreport 6, 1853–1856
    1. Gotlib I. H. (1998). EEG alpha asymmetry, depression, and cognitive functioning. Cogn. Emotion 12, 449–478
    1. Greicius M. D., Flores B. H., Menon V., Glover G. H., Solvason H. B., Kenna H., et al. (2007). Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol. Psychiatry 62, 429–437 10.1016/j.biopsych.2006.09.020
    1. Grimm S., Boesiger P., Beck J., Schuepbach D., Bermpohl F., Walter M., et al. (2009). Altered negative BOLD responses in the default-mode network during emotion processing in depressed subjects. Neuropsychopharmacology 34, 932–943 10.1038/npp.2008.81
    1. Gross M., Nakamura L., Pascual-Leone A., Fregni F. (2007). Has repetitive transcranial magnetic stimulation (rTMS) treatment for depression improved? A systematic review and meta-analysis comparing the recent vs. the earlier rTMS studies. Acta Psychiatr. Scand. 116, 165–173 10.1111/j.1600-0447.2007.01049.x
    1. Grunhaus L., Dolberg O. T., Polak D., Dannon P. N. (2002). Monitoring the response to rTMS in depression with visual analog scales. Hum. Psychopharmacol. 17, 349–352 10.1002/hup.418
    1. Grunhaus L., Schreiber S., Dolberg O. T., Polak D., Dannon P. N. (2003). A randomized controlled comparison of electroconvulsive therapy and repetitive transcranial magnetic stimulation in severe and resistant nonpsychotic major depression. Biol. Psychiatry 53, 324–331 10.1016/S0006-3223(02)01499-3
    1. Hamidi M., Slagter H. A., Tononi G., Postle B. R. (2009). Repetitive transcranial magnetic stimulation affects behavior by biasing endogenous cortical oscillations. Front. Integr. Neurosci. 3:14 10.3389/neuro.07.014.2009
    1. Hamilton J. P., Chen G., Thomason M. E., Schwartz M. E., Gotlib I. H. (2011). Investigating neural primacy in Major Depressive Disorder: multivariate Granger causality analysis of resting-state fMRI time-series data. Mol. Psychiatry 16, 763–772 10.1038/mp.2010.46
    1. Hamilton R. H., Pascual-Leone A. (1998). Cortical plasticity associated with Braille learning. Trends Cogn. Sci. 2, 168–174 10.1016/S1364-6613(98)01172-3
    1. Hedges D. W., Massari C., Salyer D. L., Lund T. D., Hellewell J. L., Johnson A. C., et al. (2003). Duration of transcranial magnetic stimulation effects on the neuroendocrine stress response and coping behavior of adult male rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 27, 633–638 10.1016/S0278-5846(03)00052-6
    1. Henriques J. B., Davidson R. J. (1991). Left frontal hypoactivation in depression. J. Abnorm. Psychol. 100, 535–545
    1. Henriques J. B., Davidson R. J. (1997). Brain electrical asymmetries during cognitive task performance in depressed and nondepressed subjects. Biol. Psychiatry 42, 1039–1050 10.1016/S0006-3223(97)00156-X
    1. Higgins E. S., George M. S. (2009). Brain Stimulation Therapies for Clinicians. Washington, DC: American Psychiatric Publishing, Inc
    1. Hoogendam J. M., Ramakers G. M., Di Lazzaro V. (2010). Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul. 3, 95–118 10.1016/j.brs.2009.10.005
    1. Hughes S. W., Crunelli V. (2005). Thalamic mechanisms of EEG alpha rhythms and their pathological implications. Neuroscientist 11, 357–372 10.1177/1073858405277450
    1. Iezzi E., Suppa A., Conte A., Li Voti P., Bologna M., Berardelli A. (2011). Short-term and long-term plasticity interaction in human primary motor cortex. Eur. J. Neurosci. 33, 1908–1915 10.1111/j.1460-9568.2011.07674.x
    1. Jäncke L., Lutz K., Koeneke S. (2006). Converging evidence of ERD/ERS and BOLD responses in motor control research. Prog. Brain Res. 159, 261–271 10.1016/S0079-6123(06)59018-1
    1. Jann K., Dierks T., Boesch C., Kottlow M., Strik W., Koenig T. (2009). BOLD correlates of EEG alpha phase-locking and the fMRI default mode network. Neuroimage 45, 903–916
    1. Jann K., Koenig T., Dierks T., Boesch C., Federspiel A. (2010). Association of individual resting state EEG alpha frequency and cerebral blood flow. Neuroimage 51, 365–372 10.1016/j.neuroimage.2010.02.024
    1. Jeanmonod D., Schulman J., Ramirez R., Cancro R., Lanz M., Morel A., et al. (2003). Neuropsychiatric thalamocortical dysrhythmia: surgical implications. Thalamus Relat. Syst. 2, 103–113
    1. Jin Y., Kemp A. S., Huang Y., Thai T. M., Liu Z., Xu W., et al. (2012). Alpha EEG guided TMS in schizophrenia. Brain Stimul. 5, 560–568 10.1016/j.brs.2011.09.005
    1. Jin Y., Potkin S. G., Kemp A. S., Huerta S. T., Alva G., Thai T. M., et al. (2006). Therapeutic effects of individualized alpha frequency transcranial magnetic stimulation (alphaTMS) on the negative symptoms of schizophrenia. Schizophr. Bull. 32, 556–561 10.1093/schbul/sbj020
    1. Jin Y., Potkin S. G., Patterson J. V., Sandman C. A., Hetrick W. P., Bunney W. E. (1997). Effects of P50 temporal variability on sensory gating in schizophrenia. Psychiatry Res. 70, 71–81
    1. Johnson J. S., Hamidi M., Postle B. R. (2010). Using EEG to explore how rTMS produces its effects on behavior. Brain Topogr. 22, 281–293 10.1007/s10548-009-0118-1
    1. Keck M. E., Welt T., Post A., Muller M. B., Toschi N., Wigger A., et al. (2001). Neuroendocrine and behavioral effects of repetitive transcranial magnetic stimulation in a psychopathological animal model are suggestive of antidepressant-like effects. Neuropsychopharmacology 24, 337–349 10.1016/S0893-133X(00)00191-3
    1. Kito S., Fujita K., Koga Y. (2008). Changes in regional cerebral blood flow after repetitive transcranial magnetic stimulation of the left dorsolateral prefrontal cortex in treatment-resistant depression. J. Neuropsychiatry Clin. Neurosci. 20, 74–80 10.1176/appi.neuropsych.20.1.74
    1. Kito S., Hasegawa T., Fujita K., Koga Y. (2010). Changes in hypothalamic-pituitary-thyroid axis following successful treatment with low-frequency right prefrontal transcranial magnetic stimulation in treatment-resistant depression. Psychiatry Res. 175, 74–77 10.1016/j.psychres.2008.10.002
    1. Klimesch W., Sauseng P., Gerloff C. (2003). Enhancing cognitive performance with repetitive transcranial magnetic stimulation at human individual alpha frequency. Eur. J. Neurosci. 17, 1129–1133
    1. Klimesch W., Sauseng P., Hanslmayr S. (2007). EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res. Rev. 53, 63–88 10.1016/j.brainresrev.2006.06.003
    1. Knott V., Mahoney C., Kennedy S., Evans K. (2001). EEG power, frequency, asymmetry and coherence in male depression. Psychiatry Res. 106, 123–140
    1. Kudina T., Sudnitsyn V., Kutyreva E., Kichigina V. (2004). The serotonin reuptake inhibitor fluoxetine suppresses theta oscillations in the electroencephalogram of the rabbit hippocampus. Neurosci. Behav. Physiol. 34, 929–933
    1. Lefaucheur J. P. (2009). Methods of therapeutic cortical stimulation. Clin. Neurophys. 39, 1–14 10.1016/j.neucli.2008.11.001
    1. Leuchter A. F., Cook I. A., Hunter A. M., Cai C., Horvath S. (2012). Resting-state quantitative electroencephalography reveals increased neurophysiologic connectivity in depression. PLoS ONE 7:e32508 10.1371/journal.pone.0032508
    1. Lisanby S. H., Belmaker R. H. (2000). Animal models of the mechanisms of action of repetitive transcranial magnetic stimulation (RTMS): comparisons with electroconvulsive shock (ECS). Depress. Anxiety 12, 178–187 10.1002/1520-6394(2000)12:3<178::AID-DA10>;2-N
    1. Llinás R. R., Ribary U., Jeanmonod D., Kronberg E., Mitra P. P. (1999). Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc. Natl. Acad. Sci. U.S.A. 96, 15222–15227 10.1073/pnas.96.26.15222
    1. Llinás R. R., Steriade M. (2006). Bursting of thalamic neurons and states of vigilance. J. Neurophysiol. 95, 3297–3308 10.1152/jn.00166.2006
    1. Loo C. K., Sachdev P. S., Haindl W., Wen W., Mitchell P. B., Croker V. M., et al. (2003). High (15 Hz) and low (1 Hz) frequency transcranial magnetic stimulation have different acute effects on regional cerebral blood flow in depressed patients. Psychol. Med. 33, 997–1006
    1. Malaguti A., Rossini D., Lucca A., Magri L., Lorenzi C., Pirovano A., et al. (2011). Role of COMT, 5-HT(1A), and SERT genetic polymorphisms on antidepressant response to Transcranial Magnetic Stimulation. Depress. Anxiety 28, 568–573 10.1002/da.20815
    1. Manna C. B., Tenke C. E., Gates N. A., Kayser J., Borod J. C., Stewart J. W., et al. (2010). EEG hemispheric asymmetries during cognitive tasks in depressed patients with high versus low trait anxiety. Clin. EEG Neurosci. 41, 196–202 10.1177/155005941004100406
    1. Marshall L., Helgadóttir H., Mölle M., Born J. (2006). Boosting slow oscillations during sleep potentiates memory. Nature 444, 610–613 10.1038/nature05278
    1. Martiny K., Lunde M., Bech P. (2010). Transcranial low voltage pulsed electromagnetic fields in patients with treatment-resistant depression. Biol. Psychiatry 68, 163–169 10.1016/j.biopsych.2010.02.017
    1. Mayberg H. (1994). Functional imaging studies in secondary depression. Psychiatr. Ann. 24, 643–647
    1. Mu Y., Han S. (2010). Neural oscillations involved in self-referential processing. Neuroimage 53, 757–768 10.1016/j.neuroimage.2010.07.008
    1. Musso F., Brinkmeyer J., Mobascher A., Warbrick T., Winterer G. (2010). Spontaneous brain activity and EEG microstates. A novel EEG/fMRI analysis approach to explore resting-state networks. Neuroimage 52, 1149–1161 10.1016/j.neuroimage.2010.01.093
    1. Nardone R., Bergmann J., Christova M., Caleri F., Tezzon F., Ladurner G., et al. (2012). Effect of transcranial brain stimulation for the treatment of Alzheimer disease: a review. Int. J. Alzheimers Dis. 2012:687909 10.1155/2012/687909
    1. Nieber D., Schlegel S. (1992). Relationships between psychomotor retardation and EEG power spectrum in major depression. Neuropsychobiology 25, 20–23
    1. Oberman L., Ifert-Miller F., Najib U., Bashir S., Woollacott I., Gonzalez-Heydrich J., et al. (2010). Transcranial magnetic stimulation provides means to assess cortical plasticity and excitability in humans with Fragile X syndrome and autism spectrum disorder. Front. Synaptic Neurosci. 2:26 10.3389/fnsyn.2010.00026
    1. O'Reardon J. P., Cristancho P., Pilania P., Bapatla K. B., Chul S., Peshek A. D. (2007). Patients with a major depressive episode responding to treatment with repetitive transcranial magnetic stimulation (rTMS) are resistant to the effects of rapid tryptophan depletion. Depress. Anxiety 24, 537–544 10.1002/da.20261
    1. O'Reardon J. P., Solvason H. B., Janicak P. G., Sampson S., Isenberg K. E., Nahas Z., et al. (2007). Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multisite randomized controlled trial. Biol. Psychiatry 62, 1208–1216 10.1016/j.biopsych.2007.01.018
    1. Ottowitz W. E., Dougherty D. D., Savage C. R. (2002). The neural network basis for abnormalities of attention and executive function in major depressive disorder: implications for application of the medical disease model to psychiatric disorders. Harv. Rev. Psychiatry 10, 86–99
    1. Ozen S., Sirota A., Belluscio M. A., Anastassiou C. A., Stark E., Koch C., et al. (2010). Transcranial electric stimulation entrains cortical neuronal populations in rats. J. Neurosci. 30, 11476–11485 10.1523/JNEUROSCI.5252-09.2010
    1. Park J. H., Lee S. B., Lee T. J., Lee D. Y., Jhoo J. H., Youn J. C., et al. (2007). Depression in vascular dementia is quantitatively and qualitatively different from depression in Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 23, 67–73 10.1159/000097039
    1. Pascual-Leone A., Freitas C., Oberman L., Horvath J. C., Halko M., Eldaief M., et al. (2011). Characterizing brain cortical plasticity and network dynamics across the age-span in health and disease with TMS-EEG and TMS-fMRI. Brain Topogr. 24, 302–315 10.1007/s10548-011-0196-8
    1. Pascual-Leone A., Rubio B., Pallardó F., Catalá M. D. (1996). Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. Lancet 348, 233–237
    1. Pascual-Leone A., Walsh V., Rothwell J. (2000). Transcranial magnetic stimulation in cognitive neuroscience-virtual lesion, chronometry, and functional connectivity. Curr. Opin. Neurobiol. 10, 232–237 10.1016/S0959-4388(00)00081-7
    1. Paulus W. (2011). Transcranial static magnetic field stimulation in man: making things as simple as possible? J. Physiol. 589, 5917–5918 10.1113/jphysiol.2011.221655
    1. Paus T., Barrett J. (2004). Transcranial magnetic stimulation (TMS) of the human frontal cortex: implications for repetitive TMS treatment of depression. J. Psychiatry Neurosci. 29, 268–279
    1. Paus T., Sipila P. K., Strafella A. P. (2001). Synchronization of neuronal activity in the human primary motor cortex by transcranial magnetic stimulation: an EEG study. J. Neurophysiol. 86, 1983–1990
    1. Peinemann A., Reimer B., Loer C., Quartarone A., Munchau A., Conrad B., et al. (2004). Long-lasting increase in corticospinal excitability after 1800 pulses of subthreshold 5 Hz repetitive TMS to the primary motor cortex. Clin. Neurophysiol. 115, 1519–1526 10.1016/j.clinph.2004.02.005
    1. Perez-Reyes E., Lory P. (2006). Molecular biology of T-type calcium channels. CNS Neurol. Disord. Drug Targets 5, 605–609 10.2174/187152706779025508
    1. Phillips B., Jin Y. (2012). EEG synchronized TMS for individualized therapy in Major Depressive Disorder, in Poster at the International Society for Affective Disorders Congress, April 18–20. (London, England: ).
    1. Pizzagalli D. A., Sherwood R. J., Henriques J. B., Davidson R. J. (2005). Frontal brain asymmetry and reward responsiveness: a source-localization study. Psychol. Sci. 16, 805–813 10.1111/j.1467-9280.2005.01618.x
    1. Pogarell O., Koch W., Pöpperl G., Tatsch K., Jakob F., Zwanzger P., et al. (2006). Striatal dopamine release after prefrontal repetitive transcranial magnetic stimulation in major depression: preliminary results of a dynamic [123I] IBZM SPECT study. J. Psychiatr. Res. 40, 307–314 10.1016/j.jpsychires.2005.09.001
    1. Pridmore S. (1999). Rapid transcranial magnetic stimulation and normalization of the dexamethasone suppression test. Psychiatry Clin. Neurosci. 53, 33–37 10.1046/j.1440-1819.1999.00467.x
    1. Prudic J., Olfson M., Marcus S. C., Fuller R. B., Sackeim H. A. (2004). Effectiveness of electroconvulsive therapy in community settings. Biol. Psychiatry 55, 301–312 10.1016/j.biopsych.2003.09.015
    1. Reato D., Rahman A., Bikson M., Parra L. C. (2010). Low-intensity electrical stimulation affects network dynamics by modulating population rate and spike timing. J. Neurosci. 30, 15067–15079 10.1523/JNEUROSCI.2059-10.2010
    1. Rohan M., Parow A., Stoll A. L., Demopulos C., Friedman S., Dager S., et al. (2004). Low-field magnetic stimulation in bipolar depression using an MRI-based stimulator. Am. J. Psychiatry 161, 93–98 10.1176/appi.ajp.161.1.93
    1. Rokni-Yazdi H., Sotoudeh S., Akhondzadeh E., Sotoudeh H., Asadi H., Shakiba M. (2007). Antidepressant-like effect of magnetic resonance imaging-based stimulation in mice. Prog. Neuro-psychopharmacol. Biol. Psychiatry 31, 503–509 10.1016/j.pnpbp.2006.11.021
    1. Rosanova M., Casali A., Bellina V., Resta F., Mariotti M., Massimini M. (2009). Natural frequencies of human corticothalamic circuits. J. Neurosci. 29, 7679–7685 10.1523/JNEUROSCI.0445-09.2009
    1. Rossi S., Hallett M., Rossini P. M., Pascual-Leone A. (2009). Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 120, 2008–2039 10.1016/j.clinph.2009.08.016
    1. Rossini D., Lucca A., Magri L., Malaguti A., Smeraldi E., Colombo C., et al. (2010). A symptom-specific analysis of the effect of high-frequency left or low-frequency right transcranial magnetic stimulation over the dorsolateral prefrontal cortex in major depression. Neuropsychobiology 62, 91–97 10.1159/000315439
    1. Sadaghiani S., Scheeringa R., Lehongre K., Morillon B., Giraud A. L., Kleinschmidt A. (2010). Intrinsic connectivity networks, alpha oscillations, and tonic alertness: a simultaneous electroencephalography/functional magnetic resonance imaging study. J. Neurosci. 30, 10243–10250 10.1523/JNEUROSCI.1004-10.2010
    1. Sauseng P., Klimesch W., Gruber W. R., Birbaumer N. (2008). Cross-frequency phase synchronization: a brain mechanism of memory matching and attention. Neuroimage 40, 308–317 10.1016/j.neuroimage.2007.11.032
    1. Savitz J. B., Drevets W. C. (2009). Imaging phenotypes of major depressive disorder: genetic correlates. Neuroscience 164, 300–330 10.1016/j.neuroscience.2009.03.082
    1. Schulman J. J., Cancro R., Lowe S., Lu F., Walton K. D., Llinás R. R. (2011). Imaging of thalamocortical dysrhythmia in neuropsychiatry. Front. Hum. Neurosci. 5:69 10.3389/fnhum.2011.00069
    1. Seagrave R. A., Thomson R. H., Cooper N. R., Croft R. J., Sheppard D. M., Fitzgerald P. B. (2010). Upper alpha activity during working memory processing reflects abnormal inhibition in major depression. J. Affect. Disord. 127, 191–198 10.1016/j.jad.2010.05.022
    1. Sela T., Kilim A., Lavidor M. (2012). Transcranial alternating current stimulation increases risk-taking behavior in the balloon analog risk task. Front. Neurosci. 6:22 10.3389/fnins.2012.00022
    1. Shafi M. M., Westover M. B., Fox M. D., Pascual-Leone A. (2012). Exploration and modulation of brain network interactions with noninvasive brain stimulation in combination with neuroimaging. Eur. J. Neurosci. 35, 805–825 10.1111/j.1460-9568.2012.08035.x
    1. Sheline Y. I., Price J. L., Yan Z., Mintun M. A. (2010). Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proc. Natl. Acad. Sci. U.S.A. 107, 11020–11025 10.1073/pnas.1000446107
    1. Shutter D. J. (2009). Antidepressant efficacy of high-frequency transcranial magnetic stimulation over the left dorsolateral prefrontal cortex in double-blind sham-controlled designs: a meta-analysis. Psychol. Med. 39, 65–75 10.1017/S0033291708003462
    1. Sibon I., Strafella A. P., Gravel P., Ko J. H., Booij L., Soucy J. P., et al. (2007). Acute prefrontal cortex TMS in healthy volunteers: effects on brain 11C-alphaMtrp trapping. Neuroimage 34, 1658–1664 10.1016/j.neuroimage.2006.08.059
    1. Siebner H. R., Rothwell J. (2003). Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp. Brain Res. 148, 1–16 10.1007/s00221-002-1234-2
    1. Slotema C. W., Blom J. D., Hoek H. W., Sommer I. E. (2010). Should we expand the toolbox of psychiatric treatment methods to include repetitive transcranial magnetic stimulation (rTMS)? A meta-analysis of the efficacy of rTMS in psychiatric disorders. J. Clin. Psychiatry 71, 873–884 10.4088/JCP.08m04872gre
    1. Sommer M., Alfaro A., Rummel M., Speck S., Lang N., Tings T., et al. (2006). Half sine, monophasic and biphasic transcranial magnetic stimulation of the human motor cortex. Clin. Neurophysiol. 117, 838–844 10.1016/j.clinph.2005.10.029
    1. Song S., Sandrini M., Cohen L. G. (2011). Modifying somatosensory processing with non-invasive brain stimulation. Restor. Neurol. Neurosci. 29, 427–437 10.3233/RNN-2011-0614
    1. Sparing R., Mottaghy F. M., Hungs M., Brugmann M., Foltys H., Huber W., et al. (2001). Repetitive transcranial magnetic stimulation effects on language function depend on the stimulation parameters. J. Clin. Neurophysiol. 18, 326–330
    1. Speer A. M., Kimbrell T. A., Wassermann E. M., Repella D., Willis M. W., Herscovitch P., et al. (2000). Opposite effects of high and low frequency rTMS on regional brain activity in depressed patients. Biol. Psychiatry 48, 1133–1141
    1. Stagg C. J., O'Shea J., Johansen-Berg H. (2010). Imaging the effects of rTMS induced cortical plasticity. Restor. Neurol. Neurosci. 28, 425–436 10.3233/RNN-2010-0553
    1. Strafella A. P., 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, RC157
    1. Teneback C. C., Nahas Z., Speer A. M., Molloy M., Stallings L. E., Spicer K. M., et al. (1999). Changes in prefrontal cortex and paralimbic activity in depression following two weeks of daily left prefrontal TMS. J. Neuropsychiatry Clin. Neurosci. 11, 426–435
    1. Thut G., Miniussi C. (2009). New insights into rhythmic brain activity from TMS-EEG studies. Trends. Cogn. Sci. 13, 182–189 10.1016/j.tics.2009.01.004
    1. Thut G., Pascual-Leone A. (2010). A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience. Brain Topogr. 22, 219–232 10.1007/s10548-009-0115-4
    1. Thut G., Veniero D., Romei V., Miniussi C., Schyns P., Gross J. (2011). Rhythmic TMS causes local entrainment of natural oscillatory signatures. Curr. Biol. 21, 1176–1185 10.1016/j.cub.2011.05.049
    1. Tucker D. M., Stenslie C. E., Roth R. S., Shearer S. L. (1981). Right frontal lobe activation and right hemisphere performance. Decrement during a depressed mood. Arch. Gen. Psychiatry 38, 169–174 10.1001/archpsyc.1981.01780270055007
    1. van Wijk B., Beek P., Daffertshofer A. (2012). Neural synchrony within the motor system: what have we learned so far? Front. Hum. Neurosci. 6:252 10.3389/fnhum.2012.00252
    1. Veer I. M., Beckmann C. F., van Tol M. J., Ferrarini L., Milles J., Veltman D. J., et al. (2010). Whole brain resting-state analysis reveals decreased functional connectivity in major depression. Front. Syst. Neurosci. 4:41 10.3389/fnsys.2010.00041
    1. Veniero D., Brignani D., Thut G., Miniussi C. (2011). Alpha-generation as basic response-signature to transcranial magnetic stimulation (TMS) targeting the human resting motor cortex: a TMS/EEG co-registration study. Psychophysiology 48, 1381–1389 10.1111/j.1469-8986.2011.01218.x
    1. Videbech P. (2000). PET measurements of brain glucose metabolism and blood flow in major depressive disorder: a critical review. Acta Psychiatr. Scand. 101, 11–20
    1. Volkow N. D., Tomasi D., Wang G. J., Fowler J. S., Telang F., Wang R., et al. (2010). Effects of low-field magnetic stimulation on brain glucose metabolism. Neuroimage 51, 623–628 10.1016/j.neuroimage.2010.02.015
    1. Vorobyov V. V., Sosunov E. A., Kukushkin N. I., Lednev V. V. (1998). Weak combined magnetic field affects basic and morphine-induced rat's EEG. Brain Res. 781, 182–187 10.1016/S0006-8993(97)01228-6
    1. Walton K. D., Dubois M., Llinás R. R. (2010). Abnormal thalamocortical activity in patients with Complex Regional Pain Syndrome (CRPS) type I. Pain 150, 41–51 10.1016/j.pain.2010.02.023
    1. Wassermann E. M., Blaxton T. A., Hoffman E. A., Berry C. D., Oletesky H., Pascual-Leone A., et al. (1999). Repetitive transcranial magnetic stimulation of the dominant hemisphere can disrupt visual naming in temporal lobe epilepsy patients. Neuropsychologia 37, 537–544 10.1016/S0028-3932(98)00102-X
    1. Zaehle T., Rach S., Herrmann C. S. (2010). Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS ONE 5:e13766 10.1371/journal.pone.0013766
    1. Zanardi R., Magri L., Rossini D., Malaguti A., Giordani S., Lorenzi C., et al. (2007). Role of serotonergic gene polymorphisms on response to transcranial magnetic stimulation in depression. Eur. Neuropsychopharmacol. 17, 651–657 10.1016/j.euroneuro.2007.03.008
    1. Zarkowski P., Shin C. J., Dang T., Russo J., Avery D. (2006). EEG and the variance of motor evoked potential amplitude. Clin. EEG Neurosci. 37, 247–251 10.1177/155005940603700316
    1. Zhou Y., Yu C., Zheng H., Liu Y., Song M., Qin W., et al. (2010). Increased neural resources recruitment in the intrinsic organization in major depression. J. Affect. Disord. 121, 220–230 10.1016/j.jad.2009.05.029
    1. Zwanzger P., Baghai T. C., Padberg F., Ella R., Minov C., Mikhaiel P., et al. (2003). The combined dexamethasone-CRH test before and after repetitive transcranial magnetic stimulation (rTMS) in major depression. Psychoneuroendocrinology 28, 376–385 10.1016/S0306-4530(02)00029-X

Source: PubMed

Sponsorer og samarbejdspartnere

Medicinske tilstande

Narkotikainterventioner

3
Abonner