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REVIEW: MANAGEMENT UPDATES (REVIEWS ON ADVANCES IN TREATMENT)
Year : 2011  |  Volume : 14  |  Issue : 4  |  Page : 245-251
 

Repetitive transcranial magnetic stimulation in psychiatry


1 Department of Psychiatry, M.K.C.G. Medical College, Berhampur, Orissa, India
2 Department of Psychiatry, Mahatma Gandhi Medical College and Research Institute, Pudduchery, India
3 Department of Psychiatry, Kasturba Medical College, Manipal, Karnataka, India
4 Department of Psychiatry, Central Institute of Psychiatry, Kanke, Ranchi, Jharkhand, India

Date of Submission25-Mar-2011
Date of Decision25-Mar-2011
Date of Acceptance14-Oct-2011
Date of Web Publication17-Jan-2012

Correspondence Address:
Samir Kumar Praharaj
Department of Psychiatry, Kasturba Medical College, Manipal, Karnataka - 576 104
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-2327.91935

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   Abstract 

Repetitive transcranial magnetic stimulation (rTMS) is a non-invasive and relatively painless tool that has been used to study various cognitive functions as well as to understand the brain-behavior relationship in normal individuals as well as in those with various neuropsychiatric disorders. It has also been used as a therapeutic tool in various neuropsychiatric disorders because of its ability to specifically modulate distinct brain areas. Studies have shown that repeated stimulation at low frequency produces long-lasting inhibition, which is called as long-term depression, whereas repeated high-frequency stimulation can produce excitation through long-term potentiation. This paper reviews the current status of rTMS as an investigative and therapeutic modality in various neuropsychiatric disorders. It has been used to study the cortical and subcortical functions, neural plasticity and brain mapping in normal individuals and in various neuropsychiatric disorders. rTMS has been most promising in the treatment of depression, with an overall milder adverse effect profile compared with electroconvulsive therapy. In other neuropsychiatric disorders such as schizophrenia, mania, epilepsy and substance abuse, it has been found to be useful, although further studies are required to establish therapeutic efficacy. It appears to be ineffective in the treatment of obsessive compulsive disorder. There is a paucity of studies of efficacy and safety of rTMS in pediatric and geriatric population. Although it appears safe, further research is required to optimize its efficacy and reduce the side-effects. Magnetic seizure therapy, which involves producing seizures akin to electroconvulsive therapy, appears to be of comparable efficacy in the treatment of depression with less cognitive adverse effects.


Keywords: Long-term potentiation, long-term depression, neuropsychiatry, repetitive transcranial magnetic stimulation


How to cite this article:
Mishra BR, Sarkar S, Praharaj SK, Mehta VS, Diwedi S, Nizamie S H. Repetitive transcranial magnetic stimulation in psychiatry. Ann Indian Acad Neurol 2011;14:245-51

How to cite this URL:
Mishra BR, Sarkar S, Praharaj SK, Mehta VS, Diwedi S, Nizamie S H. Repetitive transcranial magnetic stimulation in psychiatry. Ann Indian Acad Neurol [serial online] 2011 [cited 2019 Nov 14];14:245-51. Available from: http://www.annalsofian.org/text.asp?2011/14/4/245/91935



   Introduction Top


The past century has witnessed huge strides in the understanding of normal functioning of the human brain as well as its different pathophysiological states mainly through the development of more efficient structural and functional neuroimaging tools and electrophysiological measures. Although we have come a long way, it seems that the complexities of the human brain demand as many novel ways to unravel these. The induction of finger and foot movements through a magnetic coil placed on the motor cortex by Barker et al. [1] opened up the possibility of a novel research tool in neurosciences. Transcranial magnetic stimulation (TMS) is a non-invasive and relatively painless tool that is used in the investigation of cortical functions and also has important therapeutic applications in various psychiatric disorders.


   Basic Principles of Transcranial Magnetic Stimulation Top


TMS works on the principle of "electromagnetic induction," involving a bank of capacitors that discharge very large current (peak current: Approximately 5000 amps), which rapidly flows through a simple circuit and then through a copper-wire coil. This subsequently results in the induction of a brief and pulsed magnetic field (rise time ~0.1 ms, field strength ~2 Tesla), which is perpendicular to the electric current. When the copper coil is held to the head of the subject, this induced magnetic field generates an electrical current, which is parallel to the plane of the coil and of adequate intensity to cause localized depolarization of superficial cortical and subcortical neurons, generating a propagating action potential that is then used to study the various neuronal functions. [2] The application of TMS can produce immediate (within seconds) effects such as quick jerky movements and perception of flashes of light, etc. Different frequencies of TMS have been found to result in divergent intermediate-term (seconds to several minutes) biologic effects. Studies have revealed that repeated stimulation of a single neuron at low frequency produces long-lasting inhibition of cell-cell communications, which is called as long-term depression (LTD); conversely, repeated high-frequency stimulation can improve cell-cell communication by long-term potentiation (LTP). [3],[4] Long term (days to weeks) effects have also been observed with TMS administration reflected as sustained changes in neurotransmitter release, signaling pathways and gene expression. [5]


   Types of Transcranial Magnetic Stimulation Top


Various types of TMS have been devised depending on the frequency and type of magnetic pulse delivered. Single-pulse TMS discharges a single magnetic pulse at a given time, whereas repetitive pulse TMS (rTMS) delivers repeated single magnetic pulse of the same intensity to a discrete brain area. [6] In paired pulse TMS (ppTMS), a subthreshold stimulus is paired with a suprathreshold stimulus, with an interstimulus interval of 1-4 ms. When the interstimulus interval is 1-4 ms, there is intracortical inhibition (ICI) mediated by GABA and dopamine interneurons, whereas when the interstimulus interval is 5-30 ms, there is intracortical facilitation (ICF) mediated by excitatory NMDA interneuron. [7] Repeated paired pulse TMS (rppTMS) delivers paired pulse at a very low frequency (2 Hz). When the interval between the pairs of pulse is 3 ms, it has been found to reduce cortical excitability, and when the interval is 1.5 ms, it has been found to increase cortical excitability. [8] Theta Burst Stimulation (TBS) is a novel paradigm consisting of short bursts at 50-100 Hz stimulation frequency that are repeated at 5 Hz ("theta frequency"). It is based on theta burst protocols applied in experimental neurophysiology for inducing LTP, which were developed to resemble normal patterns of neural firing occurring in the hippocampus of rats during exploratory behavior. [9]

The frequency of stimulation of rTMS can range from ≤1 to 20 or more per second. In low-frequency rTMS (or slow rTMS), stimulation of <1 Hz is applied for a longer duration (10-15 min), resulting in LTD of cortical neuronal, whereas high-frequency rTMS (or fast rTMS) involves >1 Hz frequency stimulation for a shorter duration, manifested as neuronal LTP. [6],[10]


   Neuronal Functional Measurements Top


Various parameters have been devised using TMS to measure the cortical and subcortical neuronal functions:

Motor threshold

A single magnetic pulse applied to the motor cortex generates a twitch in the corresponding muscle known as the motor-evoked potential (MEP). The intensity of the stimulus required to produce the response is the Motor Threshold (MT), which has been defined as the lowest stimulus intensity required producing MEPs of >50 μV peak to peak amplitude in at least 50% of successive trials in a resting or activated muscle. [11] TMS application to the occipital cortex can produce experience of flashes of light known as phosphenes, and the threshold of stimuli to elicit this response is called phosphenes threshold (PT), which is more variable than MT measures. [12]

Cortical silent period

The application of a suprathreshold stimulus can cause suppression of the background EMG activity after the production of MEP in a contracting muscle. This period of suppression from MEP to the return of voluntary muscle activity is known as the Cortical Silent Period (CSP). The first 50-60 ms of the CSP is partly due to Renshaw cell inhibition while the rest is contributed by the reduced cortical excitability. [13]

Transcallosal inhibition

TMS stimulation of the motor cortex can suppress the voluntary contraction of the muscle on the ipsilateral side beginning 10-15 ms after the minimum corticospinal conduction time to the recorded muscle. This inhibition is mediated through corpus callosal fibers and can be used to study the connectivity between different cortical regions. [14]

Central motor conduction time

The latency of motor response evoked by a single motor pulse gives an idea about the neuronal conduction velocity. The difference in conduction latency of MEP evoked with cortical and spinal TMS indicates the central motor conduction time. [15]

rTMS Studies in Normal Individuals

TMS has been used in normal individuals to map brain functions, measure cortical excitability and modulate functional neuronal networks and to study their interrelations.

Cortical and subcortical functions

Various brain properties and cortical and subcortical functions have been studied using TMS, including motor and sensory function, memory, language, visual information processing and saccades. [15]

Neural plasticity

Neural plasticity is defined as a functional reorganization of synaptic connections in response to environmental contingencies or due to disease. Compensatory plasticity is studied by creating virtual lesions with rTMS on one side of the cerebral cortex and observing the dynamic compensatory process in the opposite cerebral hemisphere. In deafferentation experiments, rTMS has been used to study cortical plasticity and the underlying mechanisms. [16]

Brain mapping

This is a method to establish a causal relationship between neuronal activity in a discrete brain region and a particular cognitive, behavioral or neurophysiological phenomenon. This relationship is studied by generating virtual lesions in specific cortical areas, and studying the deterioration in the performance of the corresponding event, as well as the exact timing of the same (known as causal chronometry). In the process of creating virtual lesions, functional neuroimaging tools such as functional magnetic resonance imaging (fMRI), positron emission tomography (PET) and single photon emission computed tomography (SPECT) are used to locate the probable cortical area implicated in a cognitive task thus facilitating the exact TMS coil positioning; this method is called imaging-guided TMS neuronavigation. [17]

Neuroendocrinal effects of TMS

The effect of rTMS on the plasma levels of a variety of hormones, including cortisol, prolactin and thyroid stimulating hormone, has been documented in several studies. Although results of these studies were not conclusive, they indicate that TMS might affect neuroendocrine function. [18],[19]

Therapeutic Uses of rTMS in Psychiatric Disorders

The pathophysiology of psychiatric disorders is conceptualized in terms of dysfunction of neuronal circuits. Therefore, rTMS holds the potential of being able to selectively modulate activities in brain areas involved in various psychiatric disorders.

rTMS in depression

The therapeutic effects of rTMS have been robust in the field of depression. The efficacy studies of rTMS in depression, including open trials, sham-controlled studies and comparison studies, have involved different methodological designs using various stimulation parameters (frequency, intensity, stimulation site, number of stimuli, duration of treatment, etc.) and heterogeneous sample characteristics (age, unipolar vs. bipolar depression, level of treatment resistance). Two major categories of rTMS have been used in most of the studies: High frequency to the left prefrontal cortex (PFC) and low frequency to the right PFC. Both strategies are found to have similar antidepressant effect, while low-frequency rTMS of right PFC is better tolerated with lower risk of seizure. [20] Several randomized sham-controlled trials [21],[22],[23] have reported the antidepressant effect of left prefrontal high frequency rTMS over sham, but some results were negative. [24] In a sham-controlled study involving 40 patients with unipolar or bipolar depression, significant improvement was noted in depression and psychosis rating scores following high-frequency rTMS of left PFC. [25] Metaanalysis of the studies [20],[26] further support the antidepressant effects of left prefrontal high-frequency rTMS with small to medium effect size. In contrast, few studies have found superior antidepressant properties of right prefrontal low-frequency rTMS as compared with high-frequency or sham group. [27],[28] A 5-week, randomized, double-blind, placebo-controlled trial involving 10 daily applications of high-frequency rTMS to the left PFC in 54 drug-resistant depressed patients revealed rTMS to be an effective and safe adjunctive treatment for drug-resistant major depression. [29] Positive predictors of antidepressant response include patients who are younger, non-psychotic, with shorter duration of depressive episode, low level of treatment resistance and history of previous response to electroconvulsive therapy (ECT) and/or rTMS. Patients with significantly higher level of psychomotor retardation and lower level of agitation at baseline, along with a high level of sleep disturbances, have also shown good response to rTMS. Subjects with depressed mood and feeling of guilt are less likely to benefit from rTMS. Elderly subjects, with psychotic depression, having more treatment resistance and longer duration of depressive episode, respond poorly to rTMS. [30]

rTMS in mania

Studies on the therapeutic efficacy of rTMS in the manic phase of bipolar disorder are few. In the initial therapeutic study of rTMS in mania, comparative effect of high-frequency rTMS of right versus left PFC, as an adjunct to mood stabilizers and neuroleptics, was studied in 18 bipolar mania patients; significantly more improvement was observed with right prefrontal rTMS as compared with left side, and a worsening of mania was noted with left prefrontal rTMS, suggesting that the therapeutic effect of rTMS in mania may show a laterality effect opposite to that in depression. [31] An open-label, prospective study reported therapeutic efficacy of right prefrontal rapid rTMS in nine patients with either bipolar mania or mixed episodes. [32] In another open-label study, add-on 10-Hz rTMS of right PFC demonstrated significant improvement in manic symptoms in bipolar patients. [33] A sham-controlled study involving 41 bipolar manic patients has revealed significant improvement in manic symptoms following high-frequency rTMS application to the right PFC. [34]

rTMS in schizophrenia

In schizophrenia, hypoactivity of prefrontal cortex plays a role in the pathophysiology of negative symptoms, [35] for which high-frequency rTMS of prefrontal cortex has been used; whereas for positive symptoms such as hallucinations, which are associated with hyperactivity of temporoparietal areas, [36] low-frequency rTMS has been studied.

Left prefrontal rTMS for negative symptoms: The effects of rapid TMS of the prefrontal cortex on negative symptoms were studied initially by Cohen et al. [37] in an open trial of 20-Hz left prefrontal rTMS for 2 weeks on six schizophrenic patients with chronic negative symptoms. They found a significant reduction in negative symptoms. Subsequently, several open-label, randomized sham-controlled studies and crossover designs have demonstrated the efficacy of high-frequency rTMS of the left PFC in reducing negative symptoms of schizophrenia and producing functional improvement. [38],[39],[40] A review of the studies on the effect of rTMS on the negative symptoms of schizophrenia support a selective effect of high-frequency rTMS over PFC on negative symptoms, with more consistent results demonstrated by the open studies as compared with controlled trials. [41]

Left temporoparietal rTMS for auditory hallucinations (AH): Hoffman et al. [42],[43] conducted preliminary studies on patients with schizophrenia who had frequent AH, with 1-Hz TMS at 80% of MT to the left temporoparietal cortex using a figure-of-eight coil. In a double-blind crossover design, 12 medicated patients underwent active and sham TMS each for 4 days and the stimulation duration was gradually increased from 4 to 16 min/day. Eight of the patients reported a significant improvement in AH with TMS, and the improvement reached significance following the third and fourth days of stimulation. Low-frequency rTMS (1 Hz, 90% motor threshold) application to the left temporoparietal cortex for 10 days has been reported to produce significant improvement in auditory hallucinations. [44] A review of the studies on the effect of rTMS on AH concluded rTMS to be overall active enough in reducing AH in schizophrenic patients. [41] The two aspects of AH that showed significant improvement with active rTMS compared with sham stimulation were frequency and attentional salience, whereas other AH parameters such as number of voices, loudness, duration of voices and levels of distress were not affected by any condition. [41] Few case reports have also demonstrated the efficacy of rTMS in reducing refractory AH. [45],[46] There are case reports suggesting reduction in catatonic symptoms with application of rTMS in schizophrenic patients, [47] although randomized studies are lacking.

rTMS in obsessive compulsive disorder

Studies evaluating the therapeutic efficacy of rTMS in OCD are limited, and the results have been rather inconsistent. Greenberg et al. [48] administered 2 Hz rTMS at 80% of MT to left prefrontal, right prefrontal and midline occipital cortex in 12 patients with OCD; compulsive urges were reduced by right prefrontal stimulation up to 8 h after single stimulation, whereas left prefrontal stimulation and occipital stimulation did not produce these improvements. In another sham-controlled study, involving 42 patients of OCD, 10 adjunctive rTMS sessions (10 Hz, at 110% of MT, 20 trains for 5 s) were applied to the right PFC; there was no significant difference in improvement of obsessive-compulsive symptoms between the two groups; nevertheless, there was significant reduction in secondary depression in those receiving active rTMS. [49]

rTMS for craving in substance dependence

Studies have also revealed the potential anticraving effects of rTMS in substance dependence. In a randomized sham-controlled study, 11 nicotine-dependent subjects were randomly assigned to a course of active- and sham-rTMS on consecutive days; craving was significantly decreased after active-stimulation compared with sham-stimulation intraindividually. [50] Similarly, in a study involving 14 smokers, a single session of active high-frequency (20 Hz) rTMS application to the left PFC was found to produce reduction in craving, but was not significant. [51] In a recent outpatient randomized, double-blind, sham-controlled study, 48 chronic smokers were randomly allotted to real and sham rTMS stimulation (10 Hz over the left PFC, at 100% of MT, 20 trains/day, 50 pulses/train, intertrain interval 15 s for 10 days), each group again being randomly presented with either smoking-related or neutral pictures just before TMS intervention. There was significant reduction in cigarette consumption, as evaluated objectively by measuring nicotine levels in urine samples and subjectively by participants' self-reports; furthermore, the treatment blocked the craving induced by presentation of smoking cues. [52] In another randomized cross-over study involving six right-handed patients with cocaine dependence, two sessions of 10-Hz rTMS at 90% of MT was applied on the left or right PFC. The right, but not left, PFC rTMS was found to transiently reduce craving by 19% from baseline, which disappeared after 4 h. [53] Mishra et al. [54] in a prospective, single-blind, sham-controlled study, involving 45 patients with alcohol dependence, compared active and sham rTMS with the right PFC (10 Hz, 4.9 seconds/train, intertrain interval of 30 s, 20 trains per session, total 10 sessions). Right PFC high-frequency rTMS was found to have significant anticraving effects in alcohol dependence, with high effect size. [54]

rTMS in other anxiety disorders

Use of rTMS in panic disorder was based on the observation that panic and anxiety increased after fast rTMS over the left or right PFC. [55] In an open case series, three patients with treatment-resistant panic disorder showed modest improvement with 10 rTMS sessions (1 Hz, 110% of MT, 30 trains of 60 s duration) to the right PFC. [56] Alternating low-frequency rTMS to the right PFC with 20-Hz rTMS to the left PFC failed to produce further benefits. Grisaru et al. [57] were the first to administer rTMS in post-traumatic stress disorder (PTSD); 10 patients received 0.3 Hz rTMS to both left and right motor cortex at maximum power of the stimulator, 15 pulses to each side; transient improvement in avoidance behavior and overall clinical state was noted. In a placebo-controlled, cross-over design of imaginal exposure therapy with rTMS (1 Hz) versus sham in nine subjects with chronic, treatment-refractory PTSD, active rTMS resulted in significant improvement in hyperarousal symptoms, with an increase in 24-h urinary norepinephrine, serum T 4 and decreased serum prolactin levels. [58]

rTMS in neuropsychiatric disorders

Various studies have demonstrated the efficacy of low-frequency rTMS (0.33-1 Hz) in treating epilepsy and other manifestations of cortical hyperirritability. [59],[60],[61] Bae et al. [62] reviewed 30 studies of rTMS application in epilepsy, including open-label and controlled trials; significant reduction in seizure frequencies was seen in a majority of the studies with low-frequency rTMS; however, few studies did not demonstrate any seizure reduction. Low-frequency rTMS has been reported to reduce epileptic cortical myoclonus; [63] rTMS delivered in high-frequency (20-100 Hz) bursts or as prolonged low-frequency (1 Hz) trains, over the seizure focus, has been found to produce brief (20-30 min) pause in epilepsia partialis continua. [63] The therapeutic effect of rTMS has been suggested in Parkinson's disease and in other movement disorders. Studies reveal that rTMS application over the primary motor cortex and PFC, with a frequency range from 0.2 Hz to 5 Hz and varying intensity of stimulus (20-120% of MT), frequency of sessions (once a week for 8 weeks to twice a day for 10 days), produced improvement in motor functions, cumulative improvement of gait and bradykinesia by repeating the rTMS sessions. [64]


   rTMS In Special Populations Top


Children and adolescents

There are no controlled trials conducted on the efficacy of rTMS for treatment of any disorder in children and adolescents. However, there are case reports of improvement with rTMS in bipolar disorder, unipolar depression, schizophrenia and seizure disorders such as epilepsia partialis continua, action myoclonus and progressive myoclonic epilepsy. [65] In attention deficit/hyperactivity disorder (ADHD), there is a dysfunction in dopamine neuronal circuitry and rTMS has been suggested as a treatment modality that requires further investigation. [66] There is a need to initially evaluate the safety of rTMS in the child and adolescent population before studying it for therapeutic applications.

rTMS in the geriatric population

The application of rTMS has been little studied in the geriatric population. High-frequency stimulation to the left and right dorsolateral prefrontal cortex (DLPFC) has been found to improve accuracy in action naming in Alzheimer's disease. [67] It has also been found to be useful in late-onset depression, post-stroke depression and depression in Parkinson's disease. [68]


   Side-effects of rTMS Top


Transient headache is the most common adverse effect of rTMS, which resolves spontaneously or requires mild analgesics. Severe adverse effects have been reported rarely. High-frequency rTMS has been reported to induce seizures, [62] induce manic switch and delusions in patients with depression. [69] There is a report of transient increase in auditory threshold upon exposure to single-pulse TMS. [70] In studies of speech arrest involving stimulation of the motor speech area, unexplained crying and laughter has also been observed. [6],[68] Local pain and scalp burns from surface EEG electrodes during rTMS sessions have also been documented. [6] Histotoxicity due to rTMS results from mass hyperexcitation of cortical neurons as well as ohmic heating of poorly perfused cortical tissues. Single-pulse TMS has been found to produce distinct immunological effects by producing changes in the CD8+ lymphocyte subset. [6]


   Magnetic Seizure Therapy Top


The latest version of rTMS is Magnetic Seizure Therapy (MST), in which intense level of rTMS is applied for induction of seizures. In an FDA-approved trial, MST was administered to 21 depressed individuals, and all the patients showed response to therapy and had a milder side-effect profile as compared with ECT. Keeping in view these advantages over ECT, it could be thought of replacing the same in the near future. [71]


   Conclusion Top


It is evident that rTMS is a unique tool in the history of psychiatry, which has got a wide range of research and therapeutic uses. We need to know more about the patients who benefit from rTMS, the optimal form of treatment delivery, the magnitude of therapeutic effects and risks of treatment. It seems that a new era has begun with the advent of rTMS, in which we have novel options of physical treatment and non-invasive brain modulations.

 
   References Top

1.Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of the human motor cortex. Lancet 1985;1:1106-7.  Back to cited text no. 1
    
2.George MS, Nahas Z, Kozel FA, Li X, Denslow S, Yamanaka K, et al. Mechanisms and state of the art of transcranial magnetic stimulation. J ECT 2002;18:170-81.  Back to cited text no. 2
    
3.Bear MF. Homosynaptic long-term depression: A mechanism for memory? Proc Natl Acad Sci U S A 1999;96:9457-8.  Back to cited text no. 3
    
4.Malenka RC, Nicoll RA. Long-term potentiation-a decade of progress? Science 1999;285:1870-4.  Back to cited text no. 4
    
5.Post A, Keck ME. Transcranial magnetic stimulation as a therapeutic tool in psychiatry: What do we know about neurobiologic mechanisms? J Psychiatr Res 2001;35:193-215.  Back to cited text no. 5
    
6.Wassermann EM, Grafman J, Berry C, Hollnagel C, Wild K, Clark K, et al. Use and safety of a new repetitive transcranial magnetic stimulator. Electroencephalogr Clin Neurophysiol 1996;101:412-7.  Back to cited text no. 6
    
7.Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: A transcranial magnetic stimulation study. Ann Neurol 1996;40:367-78.  Back to cited text no. 7
    
8.Fitzgerald PB, Benitez J, de Castella A, Daskalakis ZJ, Brown TL, Kulkarni J. A randomized controlled trial of sequential bilateral repetitive transcranial magnetic stimulation for treatment-resistant depression. Am J Psychiatry 2006;163:88-94.  Back to cited text no. 8
    
9.Grossheinrich N, Rau A, Pogarell O, Hennig-Fast K, Reinl M, Karch S, et al. Theta burst stimulation of the prefrontal cortex: Safety and impact on cognition, mood, and resting electroencephalogram. Biol Psychiatry 2009;65:778-84.  Back to cited text no. 9
    
10.Pascual-Leone A, Houser CM, Reese K, Shotland LI, Grafman J, Sato S, et al. Safety of rapid-rate transcranial magnetic stimulation in normal volunteers. Electroencephalogr Clin Neurophysiol 1993;89:120-30.  Back to cited text no. 10
    
11.Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: Basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 1994;91:79-92.  Back to cited text no. 11
    
12.Marg E, Rudiak D. Phosphenes induced by magnetic stimulation over the occipital brain description and probable site of stimulation. Optom Vis Sci 1994;71:301-11.  Back to cited text no. 12
    
13.Cantello R, Gianelli M, Civardi C, Mutani R. Magnetic brain stimulation: The silent period after the motor evoked potential. Neurology 1992;42:1951-9.  Back to cited text no. 13
    
14.Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD. Interhemispheric inhibition of the human motor cortex. J Physiol 1992;453:525-46.  Back to cited text no. 14
    
15.George MS, Lisanby SH, Sackeim HA. Transcranial magnetic stimulation: Applications in neuropsychiatry. Arch Gen Psychiatry 1999;56:300-11.  Back to cited text no. 15
    
16.Ziemann U, Hallett M, Cohen LG. Mechanisms of deafferentation-induced plasticity in human motor cortex. J Neurosci 1998;18:7000-7.  Back to cited text no. 16
    
17.Sack AT, Kohler A, Linden DE, Goebel R, Muckli L. The temporal characteristics of motion processing in hMT/V5+: Combining fMRI and neuronavigated TMS. Neuroimage 2006;29:1326-35.  Back to cited text no. 17
    
18.Szuba MP, O'Reardon JP, Rai AS, Snyder-Kastenberg J, Amsterdam JD, Gettes DR, et al. Acute mood and thyroid stimulating hormone effects of transcranial magnetic stimulation in major depression. Biol Psychiatry 2001;50:22-7.  Back to cited text no. 18
    
19.Zwanzger P, Minov C, Ella R, Schüle C, Baghai T, Möller HJ, et al. Transcranial magnetic stimulation for panic. Am J Psychiatry 2002;159:315-6.  Back to cited text no. 19
    
20.Rachid F, Bertschy G. Safety and efficacy of repetitive transcranial magnetic stimulation in the treatment of depression: A critical appraisal of the last 10 years. Neurophysiol Clin 2006;36:157-83.  Back to cited text no. 20
    
21.Schüle C, Zwanzger P, Baghai T, Mikhaiel P, Thoma H, Möller HJ, et al. Effects of antidepressant pharmacotherapy after repetitive transcranial magnetic stimulation in major depression: An open follow-up study. J Psychiatr Res 2003;37:145-53.  Back to cited text no. 21
    
22.Rumi DO, Gattaz WF, Rigonatti SP, Rosa MA, Fregni F, Rosa MO, et al. Transcranial magnetic stimulation accelerates the antidepressant effect of amitryptiline in severe depression: A double-blind placebo-controlled study. Biol Psychiatry 2005;57:162-6.  Back to cited text no. 22
    
23.Bortolomasi M, Minelli A, Fuggetta G, Perini M, Comencini S, Fiaschi A, et al. Long-lasting effects of high frequency repetitive transcranial magnetic stimulation in major depressed patients. Psychiatry Res 2007;150:181-6.  Back to cited text no. 23
    
24.Poulet E, Brunelin J, Boeuve C, Lerond J, D'Amato T, Dalery J, et al. Repetitive transcranial magnetic stimulation does not potentiate antidepressant treatment. Eur Psychiatry 2004;19:382-3.  Back to cited text no. 24
    
25.Ray S, Nizamie SH, Akhtar S, Praharaj SK, Mishra BR, Zia-ul-Haq M. Efficacy of adjunctive high frequency repetitive transcranial magnetic stimulation of left prefrontal cortex in depression: A randomized sham controlled study. J Affect Disord 2011;128:153-9.  Back to cited text no. 25
    
26.Aarre TF, Dahl AA, Johansen JB, Kjønniksen I, Neckelmann D. Efficacy of repetitive transcranial magnetic stimulation in depression: A review of evidence. Nord J Psychiatry 2003;57:227-32.  Back to cited text no. 26
    
27.Klein E, Kreinin I, Chistyakov A, Koren D, Mecz L, Marmur S, et al. Therapeutic efficacy of right prefrontal slow repetitive transcranial magnetic stimulation in major depression: A double blind controlled study. Arch Gen Psychiatry 1999;56:315-20.  Back to cited text no. 27
    
28.Padberg F, Zwanzger P, Thoma H, Kathmann N, Haag C, Greenberg BD, et al. Repetitive transcranial magnetic stimulation (rTMS) in pharmacotherapy refractory major depression: Comparative study of fast, slow and sham rTMS. Psychiatry Res 1999;88:163-71.  Back to cited text no. 28
    
29.Rossini D, Lucca A, Zanardi R, Magri L, Smeraldi E. Transcranial magnetic stimulation in treatment-resistant depressed patients: A double-blind, placebo-controlled trial. Psychiatry Res 2005;137:1-10.  Back to cited text no. 29
    
30.Brakemeier EL, Wilbertz G, Rodax S, Danker-Hopfe H, Zinka B, Zwanzger P, et al. Patterns of response to repetitive transcranial magnetic stimulation (rTMS) in major depression: Replication study in drug-free patients. J Affect Disord 2008;108:59-70.  Back to cited text no. 30
    
31.Grisaru N, Chudakov B, Yaroslavsky Y, Belmaker RH. Transcranial magnetic stimulation in mania: A controlled study. Am J Psychiatry 1998;155:1608-10.  Back to cited text no. 31
    
32.Michael N, Erfurth A. Treatment of bipolar mania with right prefrontal rapid transcranial magnetic stimulation. J Affect Disord 2004;78:253-7.  Back to cited text no. 32
    
33.Saba G, Rocamora JF, Kalalou K, Benadhira R, Plaze M, Lipski H, et al. Repetitive transcranial magnetic stimulation as an add-on therapy in the treatment of mania: A case series of eight patients. Psychiatry Res 2004;128:199-202.  Back to cited text no. 33
    
34.Praharaj SK, Ram D, Arora M. Efficacy of high frequency (rapid) suprathreshold repetitive transcranial magnetic stimulation of right prefrontal cortex in bipolar mania: A randomized sham controlled study. J Affect Disord 2009;117:146-50.  Back to cited text no. 34
    
35.Andreasen NC, O'Leary DS, Flaum M, Nopoulos P, Watkins GL, Boles Ponto LL, et al. Hypofrontality in schizophrenia: Distributed dysfunctional circuits in neuroleptic-naïve patients. Lancet 1997;349:1730-4.  Back to cited text no. 35
    
36.Silbersweig DA, Stern E, Frith C, Cahill C, Holmes A, Grootoonk S, et al. A functional neuroanatomy of hallucinations in schizophrenia. Nature 1995;378:176-9.  Back to cited text no. 36
    
37.Cohen E, Bernardo M, Masana J, Arrufat FJ, Navarro V, Valls-Solé, et al. Repetitive transcranial magnetic stimulation in the treatment of chronic negative schizophrenia: A pilot study. J Neurol Neurosurg Psychiatry 1999;67:129-30.  Back to cited text no. 37
    
38.Sachdev P, Loo C, Mitchell P, Malhi G. Transcranial magnetic stimulation for deficit syndrome of schizophrenia: A pilot investigation. Psychiatry Clin Neurosci 2005;59:354-7.  Back to cited text no. 38
    
39.Prikryl R, Kasparek T, Skotakova S, Ustohal L, Kucerova H, Ceskova E. Treatment of negative symptoms of schizophrenia using repetitive transcranial magnetic stimulation in a double-blind, randomized controlled study. Schizophr Res 2007;95:151-7.  Back to cited text no. 39
    
40.Goyal N, Nizamie SH, Desarkar P. Efficacy of adjuvant high frequency repetitive transcranial magnetic stimulation on negative and positive symptoms of schizophrenia: Preliminary results of a double-blind sham-controlled study. J Neuropsychiatry Clin Neurosci 2007;19:464-7.  Back to cited text no. 40
    
41.Saba G, Schurhoff F, Leboyer M. Therapeutic and neurophysiologic aspects of transcranial magnetic stimulation in schizophrenia. Neurophysiol Clin 2006;36:185-94.  Back to cited text no. 41
    
42.Hoffman RE, Boutros NN, Berman RM, Roessler E, Belger A, Krystal JH, et al. Transcranial magnetic stimulation of left temporoparietal cortex in three patients reporting hallucinated "voices". Biol Psychiatry 1999;46:130-2.  Back to cited text no. 42
    
43.Hoffman RE, Boutros NN, Hu S, Berman RM, Krystal JH, Charney DS. Transcranial magnetic stimulation and auditory hallucinations in schizophrenia. Lancet 2000;355:1073-5.  Back to cited text no. 43
    
44.Bagati D, Nizamie SH, Prakash R. Effect of augmentatory repetitive transcranial magnetic stimulation on auditory hallucinations in schizophrenia: Randomized controlled study. Aust N Z J Psychiatry 2009;43:386-92.  Back to cited text no. 44
    
45.Franck N, Poulet E, Terra JL, Daléry J, d'Amato T. Left temporoparietal transcranial magnetic stimulation in treatment-resistant schizophrenia with verbal hallucinations. Psychiatry Res 2003;120:107-9.  Back to cited text no. 45
    
46.Fitzgerald PB, Sritharan A, Benitez J, Daskalakis ZJ, Jackson G, Kulkarni J, et al. A preliminary fMRI study of the effects on cortical activation of the treatment of refractory auditory hallucinations with rTMS. Psychiatry Res 2007;155:83-8.  Back to cited text no. 46
    
47.Grisaru N, Chudakov B, Yaroslavsky Y, Belmaker RH. Catatonia treated with transcranial magnetic stimulation. Am J Psychiatry 1998;155:1630.  Back to cited text no. 47
    
48.Greenberg BD, George MS, Martin JD, Benjamin J, Schlaepfer TE, Altemus M, et al. Effect of prefrontal repetitive transcranial magnetic stimulation in obsessive-compulsive disorder: A preliminary study. Am J Psychiatry 1997;154:867-9.  Back to cited text no. 48
    
49.Sarkhel S, Sinha VK, Praharaj SK. Adjunctive high frequency right prefrontal repetitive transcranial magnetic stimulation (rTMS) was not effective in obsessive-compulsive disorder but improved secondary depression. J Anxiety Disord 2010;24:535-9.  Back to cited text no. 49
    
50.Johann M, Wiegand R, Kharraz A, Bobbe G, Sommer G, Hajak G, et al. Repetitive transcranial magnetic stimulation in nicotine dependence. Psychiatr Prax 2003;30:129-31.  Back to cited text no. 50
    
51.Eichhammer P, Johann M, Kharraz A, Binder H, Pittrow D, Wodarz N, et al. High-frequency repetitive transcranial magnetic stimulation decreases cigarette smoking. J Clin Psychiatry 2003;64:951-3.  Back to cited text no. 51
    
52.Amiaz R, Levy D, Vainiger D, Grunhaus L, Zangen A. Repeated high-frequency transcranial magnetic stimulation over the dorsolateral prefrontal cortex reduces cigarette craving and consumption. Addiction 2009;104:653-60.  Back to cited text no. 52
    
53.Camprodon JA, Martínez-Raga J, Alonso-Alonso M, Shih MC, Pascual-Leone A. One session of high frequency repetitive transcranial magnetic stimulation (rTMS) to the right prefrontal cortex transiently reduces cocaine craving. Drug Alcohol Depend 2007;86:91-4.  Back to cited text no. 53
    
54.Mishra BR, Nizamie SH, Das B, Praharaj SK. Efficacy of repetitive transcranial magnetic stimulation in alcohol dependence: A sham-controlled study. Addiction 2010;105:49-55.  Back to cited text no. 54
    
55.Greenberg BD, McCann U, Benjamin J, Murphy DL. Repetitive TMS as a probe in anxiety disorders: Theoretical considerations and case reports. CNS Spectr 1997;2:47-52.  Back to cited text no. 55
    
56.García-Toro M, Salva Coll J, Crespí Font M, Andrés Tauler J, Aguirre Orue I, Bosch Calero C. Panic disorder and transcranial magnetic stimulation. Actas Esp Psiquiatr 2002;30:221-4.  Back to cited text no. 56
    
57.Grisaru N, Amir M, Cohen H, Kaplan Z. Effect of transcranial magnetic stimulation in posttraumatic stress disorder: A preliminary study. Biol Psychiatry 1998;44:52-5.  Back to cited text no. 57
    
58.Osuch EA, Benson BE, Luckenbaugh DA, Geraci M, Post RM, McCann U. Repetitive TMS combined with exposure therapy for PTSD: A preliminary study. J Anxiety Disord 2009;23:54-9.  Back to cited text no. 58
    
59.Theodore WH, Hunter K, Chen R, Vega-Bermudez F, Boroojerdi B, Reeves-Tyer P, et al. Transcranial magnetic stimulation for the treatment of seizures: A controlled study. Neurology 2002;59:560-2.  Back to cited text no. 59
    
60.Cantello R, Rossi S, Varrasi C, Ulivelli M, Civardi C, Bartalini S, et al. Slow repetitive TMS for drug-resistant epilepsy: Clinical and EEG findings of a placebo-controlled trial. Epilepsia 2007;48:366-74.  Back to cited text no. 60
    
61.Santiago-Rodríguez E, Cárdenas-Morales L, Harmony T, Fernández-Bouzas A, Porras-Kattz E, Hernández A. Repetitive transcranial magnetic stimulation decreases the number of seizures in patients with focal neocortical epilepsy. Seizure 2008;17:677-83.  Back to cited text no. 61
    
62.Bae EH, Schrader LM, Machii K, Alonso-Alonso M, Riviello JJ Jr, Pascual-Leone A, et al. Safety and tolerability of repetitive transcranial magnetic stimulation in patients with epilepsy: A review of the literature. Epilepsy Behav 2007;10:521-8.  Back to cited text no. 62
    
63.Wedegaertner F, Garvey M, Cohen LG, Hallett M, Wasserman EM. Low frequency repetitive transcranial magnetic stimulation can reduce action myoclonus. Neurology 1997;48:119-25.  Back to cited text no. 63
    
64.Helmich RC, Siebner HR, Bakker M, Münchau A, Bloem BR. Repetitive transcranial magnetic stimulation to improve mood and motor function in Parkinson's disease. J Neurol Sci 2006;248:84-96.  Back to cited text no. 64
    
65.Hirshberg LM, Chiu S, Frazier JA. Emerging brain-based interventions for children and adolescents: Overview and clinical perspective. Child Adolesc Psychiatr Clin N Am 2005;14:1-19.  Back to cited text no. 65
    
66.Acosta MT, Leon-Sarmiento FE. Repetitive transcranial magnetic stimulation (rTMS): New tool, new therapy and new hope for ADHD. Curr Med Res Opin 2003;19:125-30.  Back to cited text no. 66
    
67.Cotelli M, Manenti R, Cappa SF, Geroldi C, Zanetti O, Rossini PM, et al. Effect of transcranial magnetic stimulation on action naming in patients with Alzheimer disease. Arch Neurol 2006;63:1602-4.  Back to cited text no. 67
    
68.Epstein CM, Lah JJ, Meador K, Weissman JD, Gaitan LE, Dihenia B. Optimum stimulus parameters for lateralized suppression of speech with magnetic brain stimulation. Neurology 1996;47:1590-3.  Back to cited text no. 68
    
69.Sakkas P, Mihalopoulou P, Mourtzouhou P, Psarros C, Masdrakis V, Politis A, et al. Induction of mania by rTMS: Report of two cases. Eur Psychiatry 2003;18:196-8.  Back to cited text no. 69
    
70.Pascual-Leone A, Cohen LG, Shotland LI, Dang N, Pikus A, Wassermann EM, et al. No evidence of hearing loss in humans due to transcranial magnetic stimulation. Neurology 1992;42:647-51.  Back to cited text no. 70
    
71.Lisanby SH, Morales O, Payne N, Kwon E, Fitzsimons L, Luber B, et al. New developments in electroconvulsive therapy and magnetic seizure therapy. CNS Spectr 2003;8:529-36.  Back to cited text no. 71
    



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    Abstract
   Introduction
    Basic Principles...
    Types of Transcr...
    Neuronal Functio...
    rTMS In Special ...
   Side-effects of rTMS
    Magnetic Seizure...
   Conclusion
    References

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