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Treatment of auditory hallucinations by combining high-frequency repetitive transcranial magnetic stimulation and functional magnetic resonance imaging
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Schizophrenia Research 102 (2008) 348 – 351 www.elsevier.com/locate/schres
Letter to the Editors Treatment of auditory hallucinations by combining high-frequency repetitive transcranial magnetic stimulation and functional magnetic resonance imaging
Dear Editors, 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 al., 2007). However, the results are controversial (McIntosh et al., 2004; Fitzgerald et al., 2005; Lee et al., 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 of 20 Hz, guided by functional magnetic resonance imaging (fMRI) in a 56-year-old woman who presented persistent AVHs. The AVHs started in 1985 following her divorce but stopped after one year. In 1989, the voices returned after her husband died and lasted four years. Since 1998, the 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 absurd. She also presents bilateral tinnitus and has hypochondriac hallucinations 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 al., 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 antidepressant drug (citalopram; 10 mg/day) was added 0920-9964/$ - see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.schres.2008.04.012
15 days before the second rTMS. In February 2007, she received low-frequency (1 Hz) rTMS 20 min/day on 10 successive weekdays for a total of 12,000 pulses. The intensity was 90% rest motor threshold (MT) clinically assessed. A conventional site was used in the left temporoparietal cortex between T3 and P3, according to the 10–20 EEG electrodes position system. With no observed effect on the AVHs, 6 months later we attempted a new high-frequency therapy guided by anatomical and functional MRI. An anatomical T1-MRI with a 3D IR-FFE sequence (matrix size= 256 × 256 × 180; slice thickness = 1 mm, field of view= 256 mm), a 2D/T2weighted MRI with 70 axial slices (slice thickness =2 mm), and functional images (EPI-BOLD sequence; TR = 2 s, TE = 35 ms, FA = 80°, matrix size = 64 × 64 × 31, 138 volumes, slices 3.75 mm thick) were acquired using a Philips 3 Tesla. The stimulus, known to induce strong left activation in the left semantic network (Dollfus et al., 2005) lasted 5 min and consisted of listening to a factual story in French alternated 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 locally developed and encapsulated in an automatic processing pipeline. Data were analyzed using SPM5, generating a BOLD 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 al., 2007; Zhang et al., 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 over two days. Each rTMS train consisted of 200 pulses at 20 Hz for a total of 10,400 pulses. Intensity was 80% rest motor threshold (MT) assessed before each session with EMG. No side effects evaluated with UKU side effect rating scale were reported. From the second through the eighth days, progressive improvement of AVH was observed, as assessed using the Auditory Hallucination Rating Scale
Letter to the Editors
349
Fig. 1. Localization of the stimulation site based on fMRI using a frameless stereotactic system. Red crosses on axial coronal and sagittal slices indicate the target used during high-frequency therapy. In the 3D view, the red dot indicates the functional site used during high-frequency therapy, and the green dot indicates the conventional P3T3 site used during low-frequency therapy; the two sites are 2.5 cm apart.
(Hoffman et al., 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 citalopram was increased (to 40 mg/day) because of the persistent depressive syndrome, although the AVHs had ceased. After 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 herself decreased the doses of risperidone to 4 mg/day 5 months after 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 results. The use of fMRI can improve the localization of the stimulation site, as suggested recently (Hoffman et al., 2007). As shown by individual electrical cortical stimulation studies, language area localization, especially in the temporal lobe, varies considerably from one
person to another (Ojemann et al., 1989) and cannot be accurately predicted by the 10–20 EEG system. In our case, the question is whether the 2.5-cm separation between the two selected sites (Fig. 1) can explain the difference in treatment efficacy. In our opinion, this distance between sites seems too small to explain it because the electric field was larger in the first session than in the second. Indeed, MT assessed clinically in the first session is usually at least 10% greater than MT assessed with EMG and consequently could compensate for the inaccuracy of the site location in the first session. Moreover, the superiority of fMRI-guided compared to non-guided TMS has not yet been proven. Indeed, the use of fMRI scans of hallucinatory activation to guide 1 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 (Sommer et al., 2007). The second factor, high frequency, has to be strongly considered. Based on sensory motor cortex research,
350
Letter to the Editors
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 overactivation of the language network is supported by several neuroimaging studies that have associated occurrences of AVHs with activation in diverse brain regions involved in speech generation and speech perception (Hoffman et al., 2007). Otherwise, it has been shown that rTMS increases cortical inhibition, particularly with high frequency and in individuals with reduced baseline inhibition (Daskalakis et al., 2006). Because γ-aminobutyric acid (GABA) is involved in cortical inhibition, high-frequency rTMS may affect AVHs through GABAergic inhibitory neurotransmission (Daskalakis et al., 2007). This idea finds support in the hypothesis of a deficient inhibitory neurotransmission of GABA in schizophrenia (Busatto et al., 1997). This hypothesis does not, however, exclude the possibility that an excess of dopamine underlies positive symptoms because DA and GABA neurons are interconnected. In our case, high-frequency therapy was much more efficient than low-frequency therapy in halting AVHs. Moreover, high-frequency TMS was less time consuming (2 days) compared to low-frequency (2 weeks) and well tolerated. Because rTMS was applied according to present rTMS guidelines (Wassermann, 1998), we observed no side effects, in particular no seizures or impairments in concentration or memory. Moreover, a recent review of rTMS applied to non-motor cortical areas including the temporal area showed that seizure occurred only with supra-motor threshold intensity, which was not the case in our study (Machii et al., 2006). This case description demonstrates the efficiency of high-frequency, short-duration rTMS therapy in patient with auditory hallucinations and the interest of identifying the site of stimulation using fMRI. However, clinical trials are warranted to further establish the clinical significance of this novel treatment. References Aleman, A., Sommer, I.E., Kahn, R.S., 2007. Efficacy of slow repetitive transcranial magnetic stimulation in the treatment of resistant auditory hallucinations in schizophrenia: A metaAnalysis. J. Clin. Psychiatry 68, 416–421. Busatto, G.F., Pilowsky, L.S., Costa, D.C., Ell, P.J., David, A.S., Lucey, J.V., Kerwin, R.W., 1997. Correlation between reduced in
vivo benzodiazepine receptor binding and severity of psychotic symptoms in schizophrenia. Am. J. Psychiatry 154, 56–63. Daskalakis, J.Z., Fitzgerald, P.B., Christensen, B.K., 2007. The role of cortical inhibition in the pathopsysiology and treatment of schizophrenia. Brain Res. Rev. 56, 427–442. Daskalakis, Z.J., Moller, B., Christensen, B.K., Fitzgerald, P.B., Gunraj, C., Chen, R., 2006. The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects. Exp. Brain Res. 174, 403–412. Dollfus, S., Petit, M., Ménard, J.F., 1992. The relationship between “chronic hallucinatory psychosis” (CHP) and Schizophrenia. Eur. Psychiatry 7, 271–276. Dollfus, S., Razafimandimby, A., Delamillieure, P., Brazo, P., Joliot, M., Mazoyer, B., Tzourio-Mazoyer, N., 2005. Atypical hemispheric specialization for language in right-handed schizophrenic patients. Biol. Psychiatry 57, 1020–1028. Fitzgerald, P.B., Benitez, J., Daskalakis, J.Z., Brown, T.L., Marston, N.A., de Castella, A., Kulkarni, J., 2005. A double-blind sham-controlled trial of repetitive transcranial magnetic stimulation in the treatment of refractory auditory hallucinations. J. Clin. Psychopharmacol. 25, 358–362. Fregni, F., Marcondes, R., Boggio, P.S., Rigonatti, S.P., Sanchez, T.G., Nitsche, M.A., Pascual-Leone, A., 2006. Transient tinnitus suppression induced by repetitive transcranial magnetic stimulation and transcranial direct current stimulation. Eur. J. Neurol. 13, 996–1001. Hoffman, R.E., Hampson, M., Wu, K., Anderson, A.W., Gore, J.C., Buchanan, R.J., Constable, R.T., Hawkins, K.A., Sahay, N., Krystal, J.H., 2007. Probing the pathophysiology of auditory/ verbal hallucinations by combining functinal magnetic resonance imaging and transcranial magnetic stimulation. Cereb. Cortex 17, 2733–2743. Khedr, E.M., Rothwell, J.C., Ahmed, M.A., El-Atar, A., 2008. Effect of daily repetitive transcranial magnetic stimulation for treatment of tinnitus: comparison of different stimulus frequencies. J. Neurol. Neurosurg. Psychiatry 79, 212–215. Lee, S.H., Won, L., Young-cho, C., Kyung-Hee, J., Won-Myong, B., Tae-Yun, J., Kwang-Soo, K., Mark, S.G., Jeong-Ho, C., 2005. A double blind study showing that two weeks of daily repetitive TMS over the left or right temporoparietal cortex reduces symptoms in patients with schizophrenia who are having treatment-refractory auditory hallucinations. Neurosci. Lett. 376, 177–181. Machii, K., Cohen, D., Ramos-Estebanez, C., Pascual-Leone, A., 2006. Safety of rTMS to non-motor cortical areas in healthy participants and patients. Clin. Neurophysiol. 117, 455–471. McIntosh, A.M., Semple, D., Tasker, K., Harrison, L.K., Owens, D.G.C., Johnstone, E.C., Ebmeier, K.P., 2004. Transcranial magnetic stimulation for auditory hallucinations in schizophrenia. Psychiatry Res. 127, 9–17. Ojemann, G., Ojemann, J., Lettich, E., Berger, M., 1989. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J. Neurosurg. 71, 316–326. Pascual-Leone, A., Gates, J.R., Dhuna, A., 1991. Induction of speech arrest and counting errors with rapid-rate transcranial magnetic stimulation. Neurology 41, 697–702. Sommer, I.E.C., de Weijer, A.D., Daalman, K., Neggers, S.F., Somers, M., Kahn, R.S., Slotema, C.W., Blom, J.D., Hoek, H.W., Aleman, A., 2007. Can fMRI-guidance improve the efficacy of rTMS treatment for auditory verbal hallucinations? Schizophr. Res. 93, 406–408.
Letter to the Editors Wassermann, E.M., 1998. Risk and safety of repetitive transcranial magnetic stimulation : report and suggested guidelines from the international workshop on the safety of repetitive transcranial magnetic stimulation, June 5–7, 1996. Electroencephalogr. Clin. Neurophysiol. 108, 1–16. Zhang, Z., Shi, J., Yuan, Y., Hao, G., Yao, Z., Chen, N., 2007. Relationship of auditory verbal hallucinations with cerebral asymmetry in patients with schizophrenia: An event-related fMRI study. J. Psychiatr. Res. 42 (6), 477–486.
S. Dollfus* A. Larmurier-Montagne Département Universitaire de Psychiatrie, Centre Esquirol, Centre Hospitalier Universitaire de Caen, avenue côte de nacre, Caen, 14000, France ⁎Corresponding author. Département Universitaire de Psychiatrie, Centre Esquirol, Centre Hospitalier Universitaire de Caen, avenue côte de nacre, Caen, 14 000, France. E-mail address: [email protected] (S. Dollfus). A. Razafimandimby N. Delcroix S. Dollfus* A. Larmurier-Montagne Centre d'Imagerie-Neurosciences et Appliquation aux PathologieS, UMR 6232 CNRS CEA Universités de Caen et René Descartes, centre Cyceron, bl H. Becquerel, Caen, 14000, France
351
G. Allio J.M. Membrey Centre Hospitalier du Rouvray, 4 rue Paul Eluard, Sotteville les Rouen, 76301, France O. Etard Service d'explorations fonctionnelles du système nerveux, Centre Hospitalier Universitaire de Caen, avenue côte de nacre, Caen, 14000, France 11 January 2008
Schizophrenia Research 102 (2008) 348 – 351 www.elsevier.com/locate/schres
Letter to the Editors Treatment of auditory hallucinations by combining high-frequency repetitive transcranial magnetic stimulation and functional magnetic resonance imaging
Dear Editors, 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 al., 2007). However, the results are controversial (McIntosh et al., 2004; Fitzgerald et al., 2005; Lee et al., 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 of 20 Hz, guided by functional magnetic resonance imaging (fMRI) in a 56-year-old woman who presented persistent AVHs. The AVHs started in 1985 following her divorce but stopped after one year. In 1989, the voices returned after her husband died and lasted four years. Since 1998, the 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 absurd. She also presents bilateral tinnitus and has hypochondriac hallucinations 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 al., 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 antidepressant drug (citalopram; 10 mg/day) was added 0920-9964/$ - see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.schres.2008.04.012
15 days before the second rTMS. In February 2007, she received low-frequency (1 Hz) rTMS 20 min/day on 10 successive weekdays for a total of 12,000 pulses. The intensity was 90% rest motor threshold (MT) clinically assessed. A conventional site was used in the left temporoparietal cortex between T3 and P3, according to the 10–20 EEG electrodes position system. With no observed effect on the AVHs, 6 months later we attempted a new high-frequency therapy guided by anatomical and functional MRI. An anatomical T1-MRI with a 3D IR-FFE sequence (matrix size= 256 × 256 × 180; slice thickness = 1 mm, field of view= 256 mm), a 2D/T2weighted MRI with 70 axial slices (slice thickness =2 mm), and functional images (EPI-BOLD sequence; TR = 2 s, TE = 35 ms, FA = 80°, matrix size = 64 × 64 × 31, 138 volumes, slices 3.75 mm thick) were acquired using a Philips 3 Tesla. The stimulus, known to induce strong left activation in the left semantic network (Dollfus et al., 2005) lasted 5 min and consisted of listening to a factual story in French alternated 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 locally developed and encapsulated in an automatic processing pipeline. Data were analyzed using SPM5, generating a BOLD 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 al., 2007; Zhang et al., 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 over two days. Each rTMS train consisted of 200 pulses at 20 Hz for a total of 10,400 pulses. Intensity was 80% rest motor threshold (MT) assessed before each session with EMG. No side effects evaluated with UKU side effect rating scale were reported. From the second through the eighth days, progressive improvement of AVH was observed, as assessed using the Auditory Hallucination Rating Scale
Letter to the Editors
349
Fig. 1. Localization of the stimulation site based on fMRI using a frameless stereotactic system. Red crosses on axial coronal and sagittal slices indicate the target used during high-frequency therapy. In the 3D view, the red dot indicates the functional site used during high-frequency therapy, and the green dot indicates the conventional P3T3 site used during low-frequency therapy; the two sites are 2.5 cm apart.
(Hoffman et al., 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 citalopram was increased (to 40 mg/day) because of the persistent depressive syndrome, although the AVHs had ceased. After 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 herself decreased the doses of risperidone to 4 mg/day 5 months after 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 results. The use of fMRI can improve the localization of the stimulation site, as suggested recently (Hoffman et al., 2007). As shown by individual electrical cortical stimulation studies, language area localization, especially in the temporal lobe, varies considerably from one
person to another (Ojemann et al., 1989) and cannot be accurately predicted by the 10–20 EEG system. In our case, the question is whether the 2.5-cm separation between the two selected sites (Fig. 1) can explain the difference in treatment efficacy. In our opinion, this distance between sites seems too small to explain it because the electric field was larger in the first session than in the second. Indeed, MT assessed clinically in the first session is usually at least 10% greater than MT assessed with EMG and consequently could compensate for the inaccuracy of the site location in the first session. Moreover, the superiority of fMRI-guided compared to non-guided TMS has not yet been proven. Indeed, the use of fMRI scans of hallucinatory activation to guide 1 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 (Sommer et al., 2007). The second factor, high frequency, has to be strongly considered. Based on sensory motor cortex research,
350
Letter to the Editors
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 overactivation of the language network is supported by several neuroimaging studies that have associated occurrences of AVHs with activation in diverse brain regions involved in speech generation and speech perception (Hoffman et al., 2007). Otherwise, it has been shown that rTMS increases cortical inhibition, particularly with high frequency and in individuals with reduced baseline inhibition (Daskalakis et al., 2006). Because γ-aminobutyric acid (GABA) is involved in cortical inhibition, high-frequency rTMS may affect AVHs through GABAergic inhibitory neurotransmission (Daskalakis et al., 2007). This idea finds support in the hypothesis of a deficient inhibitory neurotransmission of GABA in schizophrenia (Busatto et al., 1997). This hypothesis does not, however, exclude the possibility that an excess of dopamine underlies positive symptoms because DA and GABA neurons are interconnected. In our case, high-frequency therapy was much more efficient than low-frequency therapy in halting AVHs. Moreover, high-frequency TMS was less time consuming (2 days) compared to low-frequency (2 weeks) and well tolerated. Because rTMS was applied according to present rTMS guidelines (Wassermann, 1998), we observed no side effects, in particular no seizures or impairments in concentration or memory. Moreover, a recent review of rTMS applied to non-motor cortical areas including the temporal area showed that seizure occurred only with supra-motor threshold intensity, which was not the case in our study (Machii et al., 2006). This case description demonstrates the efficiency of high-frequency, short-duration rTMS therapy in patient with auditory hallucinations and the interest of identifying the site of stimulation using fMRI. However, clinical trials are warranted to further establish the clinical significance of this novel treatment. References Aleman, A., Sommer, I.E., Kahn, R.S., 2007. Efficacy of slow repetitive transcranial magnetic stimulation in the treatment of resistant auditory hallucinations in schizophrenia: A metaAnalysis. J. Clin. Psychiatry 68, 416–421. Busatto, G.F., Pilowsky, L.S., Costa, D.C., Ell, P.J., David, A.S., Lucey, J.V., Kerwin, R.W., 1997. Correlation between reduced in
vivo benzodiazepine receptor binding and severity of psychotic symptoms in schizophrenia. Am. J. Psychiatry 154, 56–63. Daskalakis, J.Z., Fitzgerald, P.B., Christensen, B.K., 2007. The role of cortical inhibition in the pathopsysiology and treatment of schizophrenia. Brain Res. Rev. 56, 427–442. Daskalakis, Z.J., Moller, B., Christensen, B.K., Fitzgerald, P.B., Gunraj, C., Chen, R., 2006. The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects. Exp. Brain Res. 174, 403–412. Dollfus, S., Petit, M., Ménard, J.F., 1992. The relationship between “chronic hallucinatory psychosis” (CHP) and Schizophrenia. Eur. Psychiatry 7, 271–276. Dollfus, S., Razafimandimby, A., Delamillieure, P., Brazo, P., Joliot, M., Mazoyer, B., Tzourio-Mazoyer, N., 2005. Atypical hemispheric specialization for language in right-handed schizophrenic patients. Biol. Psychiatry 57, 1020–1028. Fitzgerald, P.B., Benitez, J., Daskalakis, J.Z., Brown, T.L., Marston, N.A., de Castella, A., Kulkarni, J., 2005. A double-blind sham-controlled trial of repetitive transcranial magnetic stimulation in the treatment of refractory auditory hallucinations. J. Clin. Psychopharmacol. 25, 358–362. Fregni, F., Marcondes, R., Boggio, P.S., Rigonatti, S.P., Sanchez, T.G., Nitsche, M.A., Pascual-Leone, A., 2006. Transient tinnitus suppression induced by repetitive transcranial magnetic stimulation and transcranial direct current stimulation. Eur. J. Neurol. 13, 996–1001. Hoffman, R.E., Hampson, M., Wu, K., Anderson, A.W., Gore, J.C., Buchanan, R.J., Constable, R.T., Hawkins, K.A., Sahay, N., Krystal, J.H., 2007. Probing the pathophysiology of auditory/ verbal hallucinations by combining functinal magnetic resonance imaging and transcranial magnetic stimulation. Cereb. Cortex 17, 2733–2743. Khedr, E.M., Rothwell, J.C., Ahmed, M.A., El-Atar, A., 2008. Effect of daily repetitive transcranial magnetic stimulation for treatment of tinnitus: comparison of different stimulus frequencies. J. Neurol. Neurosurg. Psychiatry 79, 212–215. Lee, S.H., Won, L., Young-cho, C., Kyung-Hee, J., Won-Myong, B., Tae-Yun, J., Kwang-Soo, K., Mark, S.G., Jeong-Ho, C., 2005. A double blind study showing that two weeks of daily repetitive TMS over the left or right temporoparietal cortex reduces symptoms in patients with schizophrenia who are having treatment-refractory auditory hallucinations. Neurosci. Lett. 376, 177–181. Machii, K., Cohen, D., Ramos-Estebanez, C., Pascual-Leone, A., 2006. Safety of rTMS to non-motor cortical areas in healthy participants and patients. Clin. Neurophysiol. 117, 455–471. McIntosh, A.M., Semple, D., Tasker, K., Harrison, L.K., Owens, D.G.C., Johnstone, E.C., Ebmeier, K.P., 2004. Transcranial magnetic stimulation for auditory hallucinations in schizophrenia. Psychiatry Res. 127, 9–17. Ojemann, G., Ojemann, J., Lettich, E., Berger, M., 1989. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J. Neurosurg. 71, 316–326. Pascual-Leone, A., Gates, J.R., Dhuna, A., 1991. Induction of speech arrest and counting errors with rapid-rate transcranial magnetic stimulation. Neurology 41, 697–702. Sommer, I.E.C., de Weijer, A.D., Daalman, K., Neggers, S.F., Somers, M., Kahn, R.S., Slotema, C.W., Blom, J.D., Hoek, H.W., Aleman, A., 2007. Can fMRI-guidance improve the efficacy of rTMS treatment for auditory verbal hallucinations? Schizophr. Res. 93, 406–408.
Letter to the Editors Wassermann, E.M., 1998. Risk and safety of repetitive transcranial magnetic stimulation : report and suggested guidelines from the international workshop on the safety of repetitive transcranial magnetic stimulation, June 5–7, 1996. Electroencephalogr. Clin. Neurophysiol. 108, 1–16. Zhang, Z., Shi, J., Yuan, Y., Hao, G., Yao, Z., Chen, N., 2007. Relationship of auditory verbal hallucinations with cerebral asymmetry in patients with schizophrenia: An event-related fMRI study. J. Psychiatr. Res. 42 (6), 477–486.
S. Dollfus* A. Larmurier-Montagne Département Universitaire de Psychiatrie, Centre Esquirol, Centre Hospitalier Universitaire de Caen, avenue côte de nacre, Caen, 14000, France ⁎Corresponding author. Département Universitaire de Psychiatrie, Centre Esquirol, Centre Hospitalier Universitaire de Caen, avenue côte de nacre, Caen, 14 000, France. E-mail address: [email protected] (S. Dollfus). A. Razafimandimby N. Delcroix S. Dollfus* A. Larmurier-Montagne Centre d'Imagerie-Neurosciences et Appliquation aux PathologieS, UMR 6232 CNRS CEA Universités de Caen et René Descartes, centre Cyceron, bl H. Becquerel, Caen, 14000, France
351
G. Allio J.M. Membrey Centre Hospitalier du Rouvray, 4 rue Paul Eluard, Sotteville les Rouen, 76301, France O. Etard Service d'explorations fonctionnelles du système nerveux, Centre Hospitalier Universitaire de Caen, avenue côte de nacre, Caen, 14000, France 11 January 2008