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ARTIGO SOBRE TMS E ALUCINAÇÕES AUDITIVAS Revista Schizofrenia Research, janeiro de 2008 Este descrição do caso demonstra a eficiência do TMS de alta freqüência, de curta- duração na terapia de paciente com alucinação auditivas e o interesse de identificar o local de estimulação usando ressonância magnética funcional Entretanto, as experimentações clinicas são garantias de que o futuramente será estabelecida a This case dcscription demonstrates the efficiency of high-frequency, short-duration rTMS therapy in patient with auditory hallucinations and the interest of identifying the site ofstimulation using fMRI. However, clinicaI trials are warranted to further establish the clinicaI Schizophrenia Research 102 (2008) 348 - 351 Treatment of auditory hallucinations by combining high-frequcncy rcpctitivc transcranial magnetic stimulation and functional magnetic resonancc Several studies showed an efficacy of low repetitive transcranial magnetic stimulation (rTMS); at a frequency of 1 Hz, in reducing the severity of auditory verbal hallucinations (AVHs) in schizophrenia (Aleman et aI., 2007). However, the results are controversial (McIntosh et aI., 2004; Fitzgerald et aI., 2005; Lee et aI., 2005). Two major factors, the site and the frequency of the stimulation, could explain this discrepancy. Here is reported a remarkable effect of rTMS, at a high-frequency of20 Hz, guided by functional magnetic resonance imaging (fMRI) in a 56-year-old woman who presented persistent AVHs. The AVHs started in 1985 fol1owing her divorce but stopped after one year. In 1989, the voices retumed after her husband died and lasted four years. Since 1998, th~ voices have been continuous as she became suspicious and unfriendly toward her co-workers. She feels that her neighbours are watching and spying on her. The voices are loud, constant, threatening, and insulting; they also speak to her in the third person. She perceives the voices as real even while criticising them and considering them absurdo She also presents bilateral tinnitus and has hypochondriac hal1ucinations like electric shocks. Both schizophrenic disorder (DSM-IV) and 'chronic hallucinatory psychosis' can be suggested with the acknowledgement that overlap between these diagnostic entities has been described (Dollfus et aI., 1992). She has received several antipsychotics, including haloperidol, loxapine, amisulpride, sulpiride, penfluridol, and finally risperidone (6 mg/day) prescribed several months before rTMS. Because she felt depressed as a result of distressing voices'; lorazepam (7.5 mg/day) also was started several months before.the first rTMS. An antidepressanf drug (citalopram; 10 mg,/day) was added 0920-9964/$ - see front matter 2008 Elsevier B.V. Ali rights reserved. 15 days before the second rTMS. In February 2007, she received low-frequency (I Hz) rTMS 20 min!day on lO successive weekdays for a total of 12,000 pulses. lhe intensity was 90% rest motor threshold (Ml) clinical1y assessed. A conventional site was used in the lefi temporoparietal cortex between T3 and P3, according to . the 10-20 EEG electrodes position system. With no observed effcct on the AVHs, 6 months latcr we attempted a new high-frequency therapy guided by anatomical and functional MRI. An anatomical Tl-MRI with a3D IR-FFE sequence (matrix size=256x256x 180; slice thickness= 1 mm, field ofview=256 mm), a 2Dn'2weighted MRI with 70 axial slices (slice thickness=2 mm), and functional imagcs (EPI-BOLD sequence; TR=2 s, TE=35 mS,FA=80°, matrix size=64 x 64 x 31, 138 volumes, siices 3.75 mm thick) were acquired using a Philips 3 Tesla. The stimulus, known to induce strong leU activation in the left semantic network (Dol1fus et aI., 2005) lasted 5 min and consisted oflistcning to a factual story in French altemated with the same story in Tamil. The patient was instructed to attentively listen to the story with eyes closed. The pre-processing was built on the basis of SPM5 subroutines 10cal1y developed and encapsulated in an automatic processing pipeline. Data were analyzed using SPM5, generating a BOLO signal contrast (French versus Tamil) map for the patient. With the presumption that AVHs depend on the same brain regions as those associated with language processing (Hoffman et aI., 2007; Zhang et aI., 2007), we targeted the stimulation site with a frameless stereotactic system based on fMRI. The target was chosen as the highest activation spot located in the left superior temporal sulcus on SPM(t) maps (Fig. 1, red cross). rTMS consisted of trains once per minute for 13 min!session for a total of four sessions ovcr two days. Each rTMS train consisted of200 pulses at 20 Hz for a total of I0,400 pulses. Intensity was 80% rest motor threshold (MT) No side effects evaluated with UKU side effect rating scale were reported. From the second through the eighth days, progressive improvement ofAVH was observed, as assessed using the Auditory Hal1ucination Rating Scale Fig. . Loealization 01' lhe stimulation silc baseei on tMRI using a frameless stereolactic system. Recl erosses on axial carona! and sagittal slices inclicate the target useel c1uring high-frequeney therapy. In the 3D view, lhe reei dot inelicates thc functional site useel c1uring high-frequency therapy, and the green dot indicates lhe conventional P3T3 site uscd during low-frequency therapy; the two sites are 2.5 cm apart. (Hoffman ct aI., 2007). From the ninth day through a 6month follow-up, the voices have ceased entirely. However, the persecutory delirious ideation, tinnitus, and hypochondriac hallucinations persist. After 3 months of follow-up, the dose of cilalopram was increased (to 40 mg/day) because of the persistent depressive syndrome, although the AVHs had ceased. Afier 5 months of follow-up, citalopram was changed to venlafaxine (150 mg/day), leading to an improvement in the mood disorder. At the same time, she herselfdecreased the doses of risperidone to 4 mg/day 5 months afier rTMS. This case is the first demonstration of the spectacular efficacy of high-frequency therapy following failure of low-frequency therapy. At least two factors, the site and the frequency of stimulation, can account for our resulls. The use of fMRI can improve the 10calization of the stimulation sitc, as suggested recently (Hoffrnan et 2007). As shown by individual electrical cortical stimulalion studies, language area localization, especially in the temporallobe, varies considerably from one person to anolher (Ojernann et aI., 1989) and cannot be accurately predicted by the 10-20 EEG system. In our case, the question is whether the 2.S-cm separation between the two selected silcs (Fig. ) can explain the difference in treatrnent efficacy. In our opinion, this distance between sites scems toa small to explain it because the electric field was larger in the first session than in the second. lndecd, MT assessed clinically in lhe first session is usually at least 10% greater than MT assessed with EMG and eonsequently could compensate for lhe inaccuracy ofthe site location in the first session. Moreover, the superiority of :fI\!IRI-guided compared to non-guided TMS has not yet been proven. Indeed, the use of fMRl scans of hallucinatory activation to guide I Hz-TMS treatment has shown a trend to a decreasing severity of general psychosis but failed to demonstrate any advantage in decreasing the severity of AVHs The second faclor, high frequency, has to be strongly considered. Based on sensory molor cortex research, low frequency is usually considered to be inhibitory. However, studies have found that high frequency can also suspend high cognitive functions or pathological processes like speech production (Pascual-Leone et aL, 1991) or tinnitus (Fregni et aL, 2006; Khedr et aL, 2008). Consequently, rTMS focused on the language areas as in our study could interrupt an overactivated circuit involved in the language network. This ovcractivation several neuroimaging studies that have associated occurrcnces of AVHs with activation in diversc brain regions involved in speech generation and speech Otherwise, it has been shown that rTMS increases cortical inhibition, particularly with high frequcncy and in individuaIs with reduced baseline inhibition (Daskalakis et aL, 2006). Because -y-aminobutyric acid (GABA) is involved in cortical inhibition, high-frequency rTMS may afTect AVHs through GABAergic inhibitory neurotransmission (Daskalakis et aL, 2007). This idea finds support in the hypothesis ofa deficient inhibitory neurotransmission of GABA in schizophrenia (Busatto et aL, 1997). This hypothcsis does not, however, exclude the possibility that an excess ofdopamine undcrlics positive symptoms because DA and GABA neurons are interconnected. In our case, high-frequency therapy was much more efficient than low-frequcncy therapy in halting AVHs. Morcovcr, high-freqllency TMS was less time consuming (2 days) compared to low-frequency (2 weeks) and well tolerated. Because rTMS was applied according to present rTMS guidclines (Wassermaim, 1998), we observed no side efTects, in particular no seizures or impairments in concentration or memory. Moreover, a reccnt review of rTMS applicd to non-motor cortical areas including the temporal area showed that scizure occurred only with supra-motor threshold intensity, which was not the case in our study (Machii et aL, Aleman, A., Sommer, I.E., Kahn, R.S., :2007. 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Probing the pathophysioIogy of auditory! verbal hallucinations by combining functinal magnetic resonance imaging and transcranial magnetic stimulation. Cereb. Cortex 17, Khedr, E.M., Rothwell, 1.C., Ahmed, M.A., EI-Atar, A, 2008. Effect of daily repetitive transcranial magnetic slimulation for treatment oftinnitus: comparison ofdifferent stimuIus frequencies. 1. Ncurol. Lee, S.H., Won, L., Young-cho, C., Kyung-Hee, 1., Won-Myong, B., Tae-Yun, 1., Kwang-Soo, K., Mark, S.G., leong-Ho, C., 2005. A double blind study showing that two weeks of daily repetitive TMS over the left ar right temporoparietal cortex reduces symptoms in patients with schizophrenia who are having treatment-refractory auditory hallucinalions. Neurosci. Lett. 376, Machii, K., Cohen, D., Ramos-Estcbanez, C., Pascual-Leone, A, 2006. Safety of rTMS to non-molor cortical areas in healthy participants and patients. Clin. Neurophysiol. 117,455-471. 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Risk and safety of repetitive transcranial magnetic stimulation : report and suggested guidelines from the intemational workshop on lhe safety of rcpetitive transcranial magnetic stimulation, June 5-7, 1996. Electroencephalogr. Clin. Zhang, Z., Shi, J., Yuan, Y., Hao, a., Yao, Z., Chen, N., 2007. Relationship of audilory verbal hallucinations wilh cerebral asymmetry in patients wilh schizophrenia: An event-related fMRI study. J. Psychiatr. Res. 42 (6), 477-486. Départemellt Ulliversitaire de Psychiatrie, Celltre Esqllim/, Celltre Hospitalier Ulliversitaire de Caell, avelllle côte de llacre, Caell, 14000, Frallce *Corresponding author. Département Universitaire de Psychiatrie, Centre Esquirol, Centre Hospitalier Universitaire de Caen, avenue côte de nacre, Caen, 14 000, France.
Centre d'Imagerie-Nellrosciellces et Appliqllation all:'( PatlzologieS, UMR 6232 CNRS CEA Ulliversités de Caell et Rellé Descartes, centre Cyceroll, bl H. Centre Hospitalier dll ROln'I'G}j 4 rue Palll Elllard, Sotteville les ROllen, 76301, Frallce Sen'ice d'exploratiolls jonctionllel/es dll syste,ne llen:ezn:, Centre Hospitalier Ulliversitaire de Caen, avelllle côte de llacre, Caell, 14000, Frallce 11 January 2008

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