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Transcranial magnetic stimulation in brain injury§ Les stimulations magne´tiques transcraˆniennes chez les ce´re´brole´se´s E. Castel-Lacanal a,*,b, M. Tarri b, I. Loubinoux b, D. Gasq a,b, X. de Boissezon a,b, P. Marque a,b, M. Simonetta-Moreau b,c a

Service de me´decine physique et re´adaptation, CHU Rangueil, 1, avenue Jean-Poulhe`s, TSA 50032, 31059 Toulouse cedex 9, France Inserm U 825, CHU Purpan, pavillon Baudot, place du Dr-Baylac, 31024 Toulouse cedex 3, France c Service de neurologie, CHU Purpan, pavillon Riser, place du Dr-Baylac, 31024 Toulouse cedex 3, France b

A R T I C L E I N F O

A B S T R A C T

Keywords: Stroke Traumatic brain injury Transcranial magnetic stimulation

Objectives. – Transcranial magnetic stimulations (TMS) have been used for many years as a diagnostic tool to explore changes in cortical excitability, and more recently as a tool for therapeutic neuromodulation. We are interested in their applications following brain injury: stroke, traumatic and anoxic brain injury. Data synthesis. – Following brain injury, there is decreased cortical excitability and changes in interhemispheric interactions depending on the type, the severity, and the time-lapse between the injury and the treatment implemented. rTMS (repetitive TMS) is a therapeutic neuromodulation tool which restores the interhemispheric interactions following stroke by inhibiting the healthy cortex with frequencies  1 Hz, or by exciting the lesioned cortex with frequencies between 3 and 50 Hz. Results in motor recovery are promising and those in improving aphasia or visuospatial neglect are also encouraging. Finally, the use of TMS is mainly limited by the risk of seizure, and is therefore contraindicated for many patients. Conclusion. – TMS is a useful non-invasive brain stimulation tool to diagnose the effects of brain injury, to study the mechanisms of recovery and a non-invasive neuromodulation promising tool to influence the post-lesional recovery. ß 2013 Published by Elsevier Masson SAS on behalf of the Socie´te´ franc¸aise d’anesthe´sie et de re´animation (Sfar). R E´ S U M E´

Mots cle´s : AVC Traumatisme craˆnien Stimulations magne´tiques transcraˆniennes

Objectifs. – Les stimulations magne´tiques transcraˆniennes (transcranial magnetic stimulation ou TMS) sont utilise´es depuis de nombreuses anne´es comme outil diagnostique des modifications de l’excitabilite´ corticale, et plus re´cemment comme outil de neuromodulation a` vise´e the´rapeutique. Nous sous sommes inte´resse´s a` leurs applications apre`s une le´sion ce´re´brale : accident vasculaire ce´re´bral (AVC) ou traumatisme craˆnien (TC), ou anoxie ce´re´brale. Synthe`se des donne´es. – Apre`s une le´sion ce´re´brale, il existe une diminution de l’excitabilite´ corticale, une modification des interactions transcallosales, variables selon le type de le´sion, la se´ve´rite´ de l’atteinte, le de´lai apre`s la le´sion et les traitements mis en œuvre. La rTMS (stimulations magne´tiques transcraˆniennes re´pe´titives) est un outil de neuromodulation the´rapeutique qui apre`s un AVC, a pour but de re´tablir l’e´quilibre de la balance interhe´misphe´rique, en inhibant l’he´misphe`re sain a` des fre´quences  1 Hz, ou en stimulant l’he´misphe`re le´se´ a` des fre´quences comprises entre 3 et 50 Hz. Les re´sultats dans la re´cupe´ration motrice sont prometteurs, ceux dans la prise en charge des aphasies ou de l’he´mine´gligence sont encourageants. Enfin, la principale limite de l’utilisation de la TMS est le risque convulsif qui la contre-indique donc chez un certain nombre de patients. Conclusion. – La TMS est un outil de stimulation ce´re´brale non invasive utile pour diagnostiquer les conse´quences de la le´sion ce´re´brale, e´tudier les me´canismes de re´cupe´ration et un outil non invasif de neuromodulation prometteur pour agir sur la re´cupe´ration post-le´sionnelle. ß 2013 Publie´ par Elsevier Masson SAS pour la Socie´te´ franc¸aise d’anesthe´sie et de re´animation (Sfar).

French NeuroAnesthesia and Intensive Care society Meeting, Paris, November 2013, 21st and 22nd: ‘‘The acutely brain-injured patient: consciousness and neuroethic’’. * Corresponding author. E-mail address: [email protected] (E. Castel-Lacanal).

§

0750-7658/$ – see front matter ß 2013 Published by Elsevier Masson SAS on behalf of the Socie´te´ franc¸aise d’anesthe´sie et de re´animation (Sfar). http://dx.doi.org/10.1016/j.annfar.2013.11.006

Please cite this article in press as: Castel-Lacanal E, et al. Transcranial magnetic stimulation in brain injury. Ann Fr Anesth Reanim (2013), http://dx.doi.org/10.1016/j.annfar.2013.11.006

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1. Introduction Transcranial magnetic stimulation (TMS) in humans after brain injury (BI) for diagnostic purposes for more than 20 years and more recent therapeutic applications of these neuromodulation tools are booming. In this article, we will explain the general principles of the TMS, its diagnostic and prognostic interests, and its applications as a therapeutic neuromodulation tool after brain injury following stroke, traumatic brain injury (TBI) and axonal injury (AI). 2. Terms of data acquisition In order to carry out the literature search we used the PubMed research database and entered the keywords ‘‘stroke’’, ‘‘traumatic brain injury’’, ‘‘diffuse axonal injury’’, ‘‘transcranial magnetic stimulation’’, and ‘‘cerebral plasticity’’. Articles were selected based on their abstracts, focusing on the last 5 years and selection was completed by a manual search. 3. Transcranial magnetic stimulation

cortex: low frequency ( 1 Hz) rTMS decreases it [6,7], while high frequency (> 5 Hz) rTMS enhances it [8–10]. A subtype of rTMS, the theta burst stimulation (TBS) consists in delivering short bursts of 3 pulses at 50 Hz, repeated every 200 ms [11]. Intermittent TBS (iTBS), in which TBS is delivered in 2-s trains separated by 10 s, has excitatory modulatory effects on the cortex, whereas continuous TBS (cTBS) causes cortical inhibition. The rTMS and TBS after-effects are considered to be the consequence of modulation of long-term depression (LTD) and long-term potentiation (LTP), involving of synaptic plasticity mechanisms [12]. 3.4. TMS: a cortical excitability evaluation tool in brain injury Changes in cortical excitability studied by TMS reflect the direct effects of brain injury, and brain plasticity, defined as the mechanisms, which allows the brain to adapt to a new situation. Changes in cortical excitability therefore depend on the injury, its severity, time-lapse following injury, the rehabilitation care provided, but also on individual factors. These are explored in order to describe and understand the injury mechanisms, the mechanisms and factors involved in recovery, the prognosis and to define more clearly the impact of treatment.

3.1. Principles 3.5. Changes in cortical excitability and stroke TMS is a safe and painless method based on the application, to the scalp, of magnetic waves via a coil in single-, paired- or repeated-pulses mode (single- or paired-pulse TMS, repetitive TMS [rTMS]) [1,2]. It is based on Faraday’s principles of electromagnetic induction. The magnetic stimulator comprises a capacitor capable of generating a high voltage (2–3 kV) and very short (0.3 to 1 ms) electric current in a coil containing a spiral of copper wire [3]. This variation of current in the coil creates a very short (1 s) but very intense (1.5 to 2 Tesla) magnetic field, with a peak at 100 microseconds. This magnetic stimulation induces an electric current in the brain, parallel to the surface of the brain and in the opposite direction to that of the current through the coil. When stimulation is applied to the upper limb area of the motor cortex, the induced current preferentially activates interneurons which themselves activate, via transsynaptic ways, neurons in the corticospinal tract. The peripheral muscular response to this stimulation is registered by electromyography as a motor evoked potential (MEP). 3.2. TMS: a cortical excitability evaluation tool Single-pulse TMS can be used to evaluate corticospinal tract conduction in clinical practice, and the motor cortical excitability: area of the MEP, rest motor threshold (RMT), active motor threshold (AMT), cortical mapping, silent period, intensity curve [2]. Paired-pulse TMS can be used to evaluate intra-cortical inhibitory/excitatory circuits (intra-cortical inhibition [ICI], intra-cortical facilitation [ICF]) when applied to a single hemisphere [4] and cortico-cortical connectivity (transcallosal inhibition) when applied to two hemispheres [5].

TMS was used to study the time course of changes in cortical excitability following stroke [13]. For example, Traversa et al. [13,14] showed a decrease in cortical excitability (increased RMT, decreased MEP amplitude and area of cortical mapping) of the hemiplegic side compared to the unaffected side and controls. Following a reeducation of 2 months, they showed an increase of the area of cortical mapping, and MEP amplitude. Moreover, they initially found a cortical hyperexcitability in the healthy side, which normalized over time. These results were correlated with the functional progress, reflecting the brain plasticity induced by spontaneous recovery and rehabilitation. In a longitudinal study, Swayne et al. [15] showed that a decrease in cortical excitability in the lesioned side (motor threshold and intensity curve), correlated to motor performance in the first three months post-stroke, and a decrease of the intracortical inhibition and facilitation in the two hemispheres correlated to motor performance beyond 3 months post-stroke. Furthermore, TMS can explore interhemispheric transcallosal interactions which are numerous and principally inhibitory [16– 18]. Following stroke, the interhemispheric balance is modified: in the controlesioned hemisphere there is a hyperaxcitability and a decreased ICI, while in the lesioned hemisphere, there is a hypoexcitability and a decrease of the inhibition to the controlesioned hemisphere [19,20]. The increase of the inhibition from the healthy hemisphere to the lesioned should be conversely correlated to the level of motor recovery: the more interhemispheric inhibition is altered, the poorer the motor recovery will be [21,22]. This concept of altered interhemispheric balance is the basis for the development of non-invasive brain modulation tools.

3.3. rTMS: a neuromodulation tool 3.6. TMS: prognosis marker following stroke rTMS consists in applying a series of same-intensity magnetic stimulations for a given frequency, ranging from 1 to 50 stimuli per second to a targeted cortical area. It modulates the cortical excitbality by suppressing or facilitating cortical process for a variable period after the end of stimulation (after-effects), depending upon the stimulation parameters. rTMS induces longterm and reversible changes in the excitability of the underlying

The presence of a MEP, particularly within 7 days after stroke is a prognostic factor in post-stroke motor recovery [23]. For example, the presence or absence of a MEP is in the prediction algorithm of the recovery of the upper limb proposed by Stinear, which also depends on the level of motor impairments and fMRI data [24].

Please cite this article in press as: Castel-Lacanal E, et al. Transcranial magnetic stimulation in brain injury. Ann Fr Anesth Reanim (2013), http://dx.doi.org/10.1016/j.annfar.2013.11.006

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3.7. Changes in cortical excitability following a TBI or AI Studies on the changes in cortical excitability following TBI or AI are less than after stroke [25]. Chistyakov’s work showed a decrease in cortical excitability (decrease of MEP amplitude, increase of the rest motor threshold) in the initial phase of a mild or moderate TBI, and a return to normal within 3 months following the TBI [26,27]. However, the results are different in other studies, highlighting the heterogeneity of brain lesions and clinical presentations. For example, Tallus et al. reported an increase of the motor threshold after a mild TBI with or without sequelae [28]. However these changes in cortical excitability would be greater in patients with a motor deficit or diffuse AI [29,30]. This data is strengthened by Moosavi’s work, in which the motor cortical excitability was not altered in chronic patients with severely impaired consciousness and without motor impairment [31]. After mild TBI, any change in ICI or ICF was reported [32,33]. Takeuchi et al. reported a change in the interhemispheric balance after AI, with a decreased interhemispheric inhibition correlated to the clinical severity measured by the Glasgow Coma Score [34]. 3.8. TMS: marker of severity of TBI An increase of ICI and a decrease of ICF have been reported in patients in vegetative state (VS) or in a minimally conscious state (MCS) [35] while ICI and ICF are not modified after mild TBI [32]. The level of ICI and ICF could be used to evaluate the severity of a TBI, however, there is still a lack of data. TMS combined with high-density ElectroEncephaloGraphy (EEG) can be used to explore the cortical effective connectivity in vegetative patients. Rosanova et al. reported that TMS triggered only a simple and local response in patients in a VS but complex activations in MCS patients, reflecting an effective connectivity [36]. This association of TMS and EEG could be used at the bedside to detect recovery of consciousness following BI. 4. TMS: neuromodulation tool following BI 4.1. Motor recovery The cerebral reorganization over time after stroke has been described in some functional imaging studies. In the early poststroke phase, a compensatory network develops away from the lesion and in the healthy hemisphere. In the sub-acute phase, a hyperactivation of the affected hemisphere appears and finally the motor network is near normal when the motor recovery is quasicomplete [37–40]. These data, coupled with data on changes in transacallosal inhibition, allowed the development of neuromodulation tools to restore the interhemispheric balance. Many studies have explored the interests of repetitive stimulation in motor recovery in which the objectives were to reduce the inhibition of the healthy hemisphere on the lesioned hemisphere by stimulating the lesioned hemisphere, or by inhibiting the healthy hemisphere. There are various non-invasive neuromodulation tools: rTMS, galvanic currents (transcranial direct current stimulation [tDCS], paired associative stimulation [PAS]) [12,41,42]. The stimulation pattern is highly variable in the studies: single or repetitive sessions, stroke in the acute or chronic phase, cortical or sub-cortical stroke, inhibition of the healthy hemisphere or stimulation of the lesioned hemisphere. The tools used to assess effectiveness are too varied.

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Studies used 1 Hz rTMS to inhibit the healthy hemisphere, and 3–20 Hz to stimulate the lesioned hemisphere. These programs were well tolerated, with no serious adverse effects, and notably without seizure [12,41,42]. The results were encouraging with a 10–30% improvement in motor tests albeit in small cohorts (< 50 patients). In a metaanalysis, Hsu et al. confirmed the positive effects of rTMS on motor recovery, particularly after sub-cortical stroke; inhibitory rTMS on healthy hemisphere and iTBS on the lesioned hemisphere would be the most effective [43]. However the use of rTMS in motor recovery is still in the preclinical stage, many questions remain unanswered: which patients? Which non-invasive brain stimulation tool? Which stimulation pattern? How long after stroke? Should it be coupled with other rehabilitation techniques and in what way? To our knowledge, there is no data on TBI patients. Data on rTMS and the recovery of walking is more rare. For example, Wang et al. applied inhibitory rTMS on healthy lower limb motor cortex, repeated the application over 10 days and, coupled with rehabilitative care, improved the walk of hemiplegic patients [44]. 4.2. Aphasia and hemineglect According to the same principle applied to motor recovery, neuromodulation is proposed to improve cognitive symptoms by stimulating the lesioned cortical areas or inhibiting healthy cortical areas. Thus 1 Hz rTMS inhibition of right BA 45 area [45–48], and iTBS stimulation of Broca area [49] would have a beneficial effect in non-fluent aphasia. In addition, 1 Hz rTMS or cTBS inhibition of the healthy parietal cortex decrease hemineglect [50–52]. 4.3. Neuropathic pain High Frequency rTMS ( 5 Hz) applied to the motor cortex (hemisphere contralateral to the pain) reduces neuropathic pain. This treatment has been proven and can be recommended in clinical practice in cases of usual analgesic failure [53–55]. 5. TMS risks TMS has been used for over 25 years and complications are rare. The side effects most frequently reported were transient headache and minor concentration disorders [56,57]. The most feared complication is the occurrence of seizure. In 2009, international recommendations regarding the intensity and frequency of magnetic stimulation parameters were updated in order to minimize this risk in healthy subjects, as well as in those with BI [57]. TMS is non-indicated in patients with a history of seizure, which is relatively common in those with brain-damage and this therefore limits its use. 6. Conclusion TMS is a tool for assessing the consequences and severity of BI and the cerebral plasticity secondary to spontaneous recovery mechanisms and specific care (drug therapy, rehabilitation). It is also a neuromodulation tool to facilitate post-BI recovery. The results on motor recovery are encouraging, but there is insufficient data for it to be proposed in clinical practice. Studies on aphasia and neglect are still few and far between. Finally, the main limitation for the use of TMS is the risk of seizure, resulting in a contre-indication for many patients.

Please cite this article in press as: Castel-Lacanal E, et al. Transcranial magnetic stimulation in brain injury. Ann Fr Anesth Reanim (2013), http://dx.doi.org/10.1016/j.annfar.2013.11.006

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Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.

[30]

[31]

References [32] [1] Hallett M. Transcranial magnetic stimulation: a primer. Neuron 2007;55:187– 99. [2] Siebner HR, Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 2003;148:1–16. [3] Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet 1985;1:1106–7. [4] Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol 1993;471:501–19. [5] 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. [6] Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 1997;48:1398–403. [7] Fitzgerald PB, Brown TL, Daskalakis ZJ, Chen R, Kulkarni J. Intensity-dependent effects of 1 Hz rTMS on human corticospinal excitability. Clin Neurophysiol 2002;113:1136–41. [8] Berardelli A, Inghilleri M, Cruccu G, Manfredi M. Descending volley after electrical and magnetic transcranial stimulation in man. Neurosci Lett 1990;112:54–8. [9] Modugno N, Nakamura Y, MacKinnon CD, Filipovic SR, Bestmann S, Berardelli A, et al. Motor cortex excitability following short trains of repetitive magnetic stimuli. Exp Brain Res 2001;140:453–9. [10] Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M. Responses to rapidrate transcranial magnetic stimulation of the human motor cortex. Brain 1994;117(Pt 4):847–58. [11] Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron 2005;45:201–6. [12] Edwardson MA, Lucas TH, Carey JR, Fetz EE. New modalities of brain stimulation for stroke rehabilitation. Exp Brain Res 2012;224:335–58. [13] Traversa R, Cicinelli P, Oliveri M, Giuseppina Palmieri M, Filippi MM, Pasqualetti P, et al. Neurophysiological follow-up of motor cortical output in stroke patients. Clin Neurophysiol 2000;111:1695–703. [14] Traversa R, Cicinelli P, Pasqualetti P, Filippi M, Rossini PM. Follow-up of interhemispheric differences of motor evoked potentials from the ‘affected’ and ‘unaffected’ hemispheres in human stroke. Brain Res 1998;803:1–8. [15] Swayne OB, Rothwell JC, Ward NS, Greenwood RJ. Stages of motor output reorganization after hemispheric stroke suggested by longitudinal studies of cortical physiology. Cereb Cortex 2008;18:1909–22. [16] Baumer T, Bock F, Koch G, Lange R, Rothwell JC, Siebner HR, et al. Magnetic stimulation of human premotor or motor cortex produces interhemispheric facilitation through distinct pathways. J Physiol 2006;572:857–68. [17] Hanajima R, Ugawa Y, Machii K, Mochizuki H, Terao Y, Enomoto H, et al. Interhemispheric facilitation of the hand motor area in humans. J Physiol 2001;531:849–59. [18] Meyer BU, Roricht S, Grafin von Einsiedel H, Kruggel F, Weindl A. Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain 1995;118(Pt 2):429–40. [19] Liepert J, Hamzei F, Weiller C. Motor cortex disinhibition of the unaffected hemisphere after acute stroke. Muscle Nerve 2000;23:1761–3. [20] Shimizu T, Hosaki A, Hino T, Sato M, Komori T, Hirai S, et al. Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain 2002;125:1896–907. [21] Duque J, Hummel F, Celnik P, Murase N, Mazzocchio R, Cohen LG. Transcallosal inhibition in chronic subcortical stroke. Neuroimage 2005;28:940–6. [22] Murase N, Duque J, Mazzocchio R, Cohen LG. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 2004;55:400–9. [23] Bembenek JP, Kurczych K, Karli Nski M, Czlonkowska A. The prognostic value of motor-evoked potentials in motor recovery and functional outcome after stroke: a systematic review of the literature. Funct Neurol 2012;27:79–84. [24] Stinear CM, Barber PA, Petoe M, Anwar S, Byblow WD. The PREP algorithm predicts potential for upper limb recovery after stroke. Brain 2012;135:2527– 35. [25] Demirtas-Tatlidede A, Vahabzadeh-Hagh AM, Bernabeu M, Tormos JM, Pascual-Leone A. Noninvasive brain stimulation in traumatic brain injury. J Head Trauma Rehabil 2012;27:274–92. [26] Chistyakov AV, Soustiel JF, Hafner H, Elron M, Feinsod M. Altered excitability of the motor cortex after minor head injury revealed by transcranial magnetic stimulation. Acta Neurochir (Wien) 1998;140:467–72. [27] Chistyakov AV, Hafner H, Soustiel JF, Trubnik M, Levy G, Feinsod M. Dissociation of somatosensory and motor evoked potentials in non-comatose patients after head injury. Clin Neurophysiol 1999;110:1080–9. [28] Tallus J, Lioumis P, Hamalainen H, Kahkonen S, Tenovuo O. Long-lasting TMS motor threshold elevation in mild traumatic brain injury. Acta Neurol Scand 2012;126:178–82. [29] Barba C, Formisano R, Sabatini U, Cicinelli P, Elisabeth Hagberg G, Marconi B, et al. Dysfunction of a structurally normal motor pathway in a brain injury

[33]

[34]

[35]

[36]

[37]

[38]

[39]

[40]

[41]

[42] [43]

[44]

[45]

[46]

[47]

[48]

[49]

[50]

[51]

[52]

[53]

[54] [55] [56]

[57]

patient as revealed by multimodal integrated techniques. Neurocase 2006;12:232–5. Bernabeu M, Demirtas-Tatlidede A, Opisso E, Lopez R, Tormos JM, PascualLeone A. Abnormal corticospinal excitability in traumatic diffuse axonal brain injury. J Neurotrauma 2009;26:2185–93. Moosavi SH, Ellaway PH, Catley M, Stokes MJ, Haque N. Corticospinal function in severe brain injury assessed using magnetic stimulation of the motor cortex in man. J Neurol Sci 1999;164:179–86. Centonze D, Palmieri MG, Boffa L, Pierantozzi M, Stanzione P, Brusa L, et al. Cortical hyperexcitability in post-traumatic stress disorder secondary to minor accidental head trauma: a neurophysiologic study. J Psychiatry Neurosci 2005;30:127–32. Fujiki M, Hikawa T, Abe T, Ishii K, Kobayashi H. Reduced short latency afferent inhibition in diffuse axonal injury patients with memory impairment. Neurosci Lett 2006;405:226–30. Takeuchi N, Ikoma K, Chuma T, Matsuo Y. Measurement of transcallosal inhibition in traumatic brain injury by transcranial magnetic stimulation. Brain Inj 2006;20:991–6. Bagnato S, Boccagni C, Sant’Angelo A, Prestandrea C, Rizzo S, Galardi G. Patients in a vegetative state following traumatic brain injury display a reduced intracortical modulation. Clin Neurophysiol 2012;123:1937–41. Rosanova M, Gosseries O, Casarotto S, Boly M, Casali AG, Bruno MA, et al. Recovery of cortical effective connectivity and recovery of consciousness in vegetative patients. Brain 2012;135:1308–20. Chollet F, DiPiero V, Wise RJ, Brooks DJ, Dolan RJ, Frackowiak RS. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol 1991;29:63–71. Loubinoux I, Carel C, Pariente J, Dechaumont S, Albucher JF, Marque P, et al. Correlation between cerebral reorganization and motor recovery after subcortical infarcts. Neuroimage 2003;20:2166–80. Tombari D, Loubinoux I, Pariente J, Gerdelat A, Albucher JF, Tardy J, et al. A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients. Neuroimage 2004;23:827–39. Weiller C, Chollet F, Friston KJ, Wise RJ, Frackowiak RS. Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol 1992;31:463–72. Adeyemo BO, Simis M, Macea DD, Fregni F. Systematic review of parameters of stimulation, clinical trial design characteristics, and motor outcomes in noninvasive brain stimulation in stroke. Front Psychiatry 2012;3:88. Schulz R, Gerloff C, Hummel FC. Non-invasive brain stimulation in neurological diseases. Neuropharmacology 2013;64:579–87. Hsu WY, Cheng CH, Liao KK, Lee IH, Lin YY. Effects of repetitive transcranial magnetic stimulation on motor functions in patients with stroke: a metaanalysis. Stroke 2012;43:1849–57. Wang RY, Tseng HY, Liao KK, Wang CJ, Lai KL, Yang YR. rTMS combined with task-oriented training to improve symmetry of interhemispheric corticomotor excitability and gait performance after stroke: a randomized trial. Neurorehabil Neural Repair 2012;26:222–30. Barwood CH, Murdoch BE, Whelan BM, Lloyd D, Riek S, O’Sullivan JD, et al. Improved language performance subsequent to low-frequency rTMS in patients with chronic non-fluent aphasia post-stroke. Eur J Neurol 2011;18:935–43. Barwood CH, Murdoch BE, Whelan BM, Lloyd D, Riek S, O’Sullivan J, et al. The effects of low frequency repetitive transcranial magnetic stimulation (rTMS) and sham condition rTMS on behavioural language in chronic non-fluent aphasia: short-term outcomes. NeuroRehabilitation 2011;28:113–28. Martin PI, Naeser MA, Theoret H, Tormos JM, Nicholas M, Kurland J, et al. Transcranial magnetic stimulation as a complementary treatment for aphasia. Semin Speech Lang 2004;25:181–91. Naeser MA, Martin PI, Nicholas M, Baker EH, Seekins H, Kobayashi M, et al. Improved picture naming in chronic aphasia after TMS to part of right Broca’s area: an open-protocol study. Brain Lang 2005;93:95–105. Szaflarski JP, Vannest J, Wu SW, DiFrancesco MW, Banks C, Gilbert DL. Excitatory repetitive transcranial magnetic stimulation induces improvements in chronic post-stroke aphasia. Med Sci Monit 2011;17:CR132–9. Lim JY, Kang EK, Paik NJ. Repetitive transcranial magnetic stimulation to hemispatial neglect in patients after stroke: an open-label pilot study. J Rehabil Med 2010;42:447–52. Nyffeler T, Cazzoli D, Hess CW, Muri RM. One session of repeated parietal theta burst stimulation trains induces long-lasting improvement of visual neglect. Stroke 2009;40:2791–6. Song W, Du B, Xu Q, Hu J, Wang M, Luo Y. Low-frequency transcranial magnetic stimulation for visual spatial neglect: a pilot study. J Rehabil Med 2009;41:162–5. Cruccu G, Aziz TZ, Garcia-Larrea L, Hansson P, Jensen TS, Lefaucheur JP, et al. EFNS guidelines on neurostimulation therapy for neuropathic pain. Eur J Neurol 2007;14:952–70. Leo RJ, Latif T. Repetitive transcranial magnetic stimulation (rTMS) in experimentally induced and chronic neuropathic pain: a review. J Pain 2007;8:453–9. Leung A, Donohue M, Xu R, Lee R, Lefaucheur JP, Khedr EM, et al. rTMS for suppressing neuropathic pain: a meta-analysis. J Pain 2009;10:1205–16. Lefaucheur JP, Andre-Obadia N, Poulet E, Devanne H, Haffen E, Londero A, et al. [French guidelines on the use of repetitive transcranial magnetic stimulation (rTMS): safety and therapeutic indications]. Neurophysiol Clin 2011;41:221–95. Rossi S, Hallett M, Rossini PM, Pascual-Leone A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009;120:2008–39.

Please cite this article in press as: Castel-Lacanal E, et al. Transcranial magnetic stimulation in brain injury. Ann Fr Anesth Reanim (2013), http://dx.doi.org/10.1016/j.annfar.2013.11.006

Transcranial magnetic stimulation in brain injury.

Transcranial magnetic stimulations (TMS) have been used for many years as a diagnostic tool to explore changes in cortical excitability, and more rece...
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