Reduced neuronal activity in language-related regions after transcranial magnetic stimulation therapy for auditory verbal hallucinations
Open accessAbstract
Background Transcranial magnetic stimulation (TMS) is a novel therapeutic approach, used in patients with pharmacoresistant auditory verbal hallucinations (AVH). To investigate the neurobiological effects of TMS on AVH, we measured cerebral blood flow with pseudo-continuous magnetic resonance-arterial spin labeling 20 ± 6 hours before and after TMS treatment.Methods Thirty patients with schizophrenia or schizoaffective disorder were investigated. Fifteen patients received a 10-day TMS treatment to the left temporoparietal cortex, and 15 received the standard treatment. The stimulation location was chosen according to an individually determined language region determined by a functional magnetic resonance imaging language paradigm, which identified the sensorimotor language area, area Spt (sylvian parietotemporal), as the target region.Results TMS-treated patients showed positive clinical effects, which were indicated by a reduction in AVH scores (p ≤ .001). Cerebral blood flow was significantly decreased in the primary auditory cortex (p ≤ .001), left Broca's area (p ≤ .001), and cingulate gyrus (p ≤ .001). In control subjects, neither positive clinical effects nor cerebral blood flow decreases were detected. The decrease in cerebral blood flow in the primary auditory cortex correlated with the decrease in AVH scores (p ≤ .001).Conclusions TMS reverses hyperactivity of language regions involved in the emergence of AVH. Area Spt acts as a gateway to the hallucination-generating cerebral network. Successful therapy corresponded to decreased cerebral blood flow in the primary auditory cortex, supporting its crucial role in triggering AVH and contributing to the physical quality of the false perceptions.
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rTMS treatment is usually targeted at the left temporoparietal junction, an area adjacent to and with high connectivity to primary and secondary auditory cortex.
“rTMS treatment is usually targeted at the left temporoparietal junction (TPJ), an area adjacent to, and with high levels of connectivity to, primary and secondary auditory cortex (Kindler et al., 2013).”
From Auditory verbal hallucinations as atypical inner speech monitoring, and the potential of neurostimulation as a treatment option (2013) · cites this paper as Kindler et al., 2013
Measurement of cerebral blood flow post-TMS treatment showed reductions in activation in primary auditory cortex (part of the STG), Broca's area and the cingulate gyrus after 10 days of rTMS treatment.
“In a separate study, measurement of cerebral blood flow post-TMS treatment, relative to pre-treatment, showed reductions in activation in primary auditory cortex (part of the STG), Broca's area and the cingulate gyrus after 10 days of rTMS treatment”
From Auditory verbal hallucinations as atypical inner speech monitoring, and the potential of neurostimulation as a treatment option (2013) · cites this paper as Kindler et al., 2013
Only reduced activation in the STG correlated with a reduction in AVHs.
“Importantly, only reduced activation in the STG correlated with a reduction in AVHs”
From Auditory verbal hallucinations as atypical inner speech monitoring, and the potential of neurostimulation as a treatment option (2013) · cites this paper as Kindler et al., 2013
Cites
The cortical organization of speech processing
Hickok, G., & Poeppel, D. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2113 · Cited by 5,495 · see citing works
Rossi, S., Hallett, M., Rossini, P. M., & Pascual-Leone, A. (2009) · Clinical Neurophysiology · doi:10.1016/j.clinph.2009.08.016 · Cited by 5,367 · see citing works
HADDOCK, G., McCARRON, J., TARRIER, N., & FARAGHER, E. B. (1999) · Psychological Medicine · doi:10.1017/s0033291799008661 · Cited by 1,461 · see citing works
Cortical midline structures and the self
Northoff, G., & Bermpohl, F. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.01.004 · Cited by 1,446 · see citing works
Reliability and validity of the positive and negative syndrome scale for schizophrenics
Kay, S. R., Opler, L. A., & Lindenmayer, J.-P. (1988) · Psychiatry Research · doi:10.1016/0165-1781(88)90038-8 · Cited by 1,007 · see citing works
Dai, W., Garcia, D., de BAZELAIRE, C., & Alsop, D. C. (2008) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21790 · Cited by 986 · see citing works
Activation of Heschl’s Gyrus during Auditory Hallucinations
Dierks, T., Linden, D. E. J., Jandl, M., Formisano, E., Goebel, R., Lanfermann, H., & Singer, W. (1999) · Neuron · doi:10.1016/s0896-6273(00)80715-1 · Cited by 752 · see citing works
Self-citationIs there a future for therapeutic use of transcranial magnetic stimulation?
Ridding, M. C., & Rothwell, J. C. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2169 · Cited by 687 · see citing works
Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging
Shergill, S. S., Brammer, M. J., Williams, S. C. R., Murray, R. M., & McGuire, P. K. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.11.1033 · Cited by 666 · see citing works
Allen, P., Larøi, F., McGuire, P. K., & Aleman, A. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.07.012 · Cited by 579 · see citing works
Hoffman, R. E., Hawkins, K. A., Gueorguieva, R. V., Boutros, N. N., Rachid, F., Carroll, K. M., & Krystal, J. H. (2003) · Archives of General Psychiatry · doi:10.1001/archpsyc.60.1.49 · Cited by 517 · see citing works
Wu, W.-C., Fernández-Seara, M., Detre, J., Wehrli, F. W., & Wang, J.-J. (2007) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21403 · Cited by 507 · see citing works
Hubl, D., Koenig, T. W., Strik, W. K., Federspiel, A., Kreis, R., Boesch, C., Maier, S. E., Schroth, G., Lövblad, K., & Dierks, T. (2004) · Archives of General Psychiatry · doi:10.1001/archpsyc.61.7.658 · Cited by 466 · see citing works
Self-citationOptimizing Functional Accuracy of TMS in Cognitive Studies: A Comparison of Methods
Sack, A., Kadosh, R. C., Schuhmann, T., Moerel, M., Walsh, V., & Goebel, R. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21126 · Cited by 434 · see citing works
Abnormal monitoring of inner speech: a physiological basis for auditory hallucinations
McGuire, P. K., David, A. S., Murray, R. M., Frackowiak, R. S. J., Frith, C. D., Wright, I., & Silbersweig, D. A. (1995) · The Lancet · doi:10.1016/s0140-6736(95)91435-8 · Cited by 349 · see citing works
Auditory hallucinations: a review of psychological treatments
Shergill, S. S., Murray, R. M., & McGuire, P. K. (1998) · Schizophrenia Research · doi:10.1016/s0920-9964(98)00052-8 · Cited by 313 · see citing works
Transcranial magnetic stimulation and auditory hallucinations in schizophrenia
Hoffman, R. E., Boutros, N. N., Hu, S., Berman, R., Krystal, J. H., & Charney, D. S. (2000) · The Lancet · doi:10.1016/s0140-6736(00)02043-2 · Cited by 303 · see citing works
Auditory verbal hallucinations predominantly activate the right inferior frontal area
Sommer, I. E. C., Diederen, K. M. J., Blom, J.-D., Willems, A., Kushan, L., Slotema, K., Boks, M. P. M., Daalman, K., Hoek, H. W., Neggers, S. F. W., et al. (2008) · Brain · doi:10.1093/brain/awn251 · Cited by 297 · see citing works
Thielscher, A., & Kammer, T. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.02.019 · Cited by 295 · see citing works
Hoffman, R. E., & Çavuş, I. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.7.1093 · Cited by 286 · see citing works
Xu, G., Rowley, H. A., Wu, G., Alsop, D. C., Shankaranarayanan, A., Dowling, N. M., Christian, B. T., Oakes, T. R., & Johnson, S. C. (2009) · NMR in Biomedicine · doi:10.1002/nbm.1462 · Cited by 280 · see citing works
Kompus, K., Westerhausen, R., & Hugdahl, K. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.08.010 · Cited by 274 · see citing works
Aleman, A., Sommer, I. E., & Kahn, R. S. (2007) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v68n0310 · Cited by 246 · see citing works
Kuhn, S., & Gallinat, J. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq152 · Cited by 245 · see citing works
McGuire, P. K., Silbersweig, D., Wright, I. C., Murray, R. M., Frackowiak, R. S. J., & Frith, C. (1996) · The British Journal of Psychiatry · doi:10.1192/bjp.169.2.148 · Cited by 241 · see citing works
Area Spt in the Human Planum Temporale Supports Sensory-Motor Integration for Speech Processing
Hickok, G. S., Okada, K., & Serences, J. T. (2009) · Journal of Neurophysiology · doi:10.1152/jn.91099.2008 · Cited by 230 · see citing works
Agent-Specific Responses in the Cingulate Cortex During Economic Exchanges
Tomlin, D., Kayali, M., King-Casas, B., Anen, C., Camerer, C., Quartz, S., & Montague, P. (2006) · Science · doi:10.1126/science.1125596 · Cited by 222 · see citing works
Nyffeler, T., Cazzoli, D., Hess, C. W., & Müri, R. M. (2009) · Stroke · doi:10.1161/strokeaha.109.552323 · Cited by 188 · see citing works
Trippe, J., Mix, A., Aydın-Abidin, S., Funke, K., & Benali, A. (2009) · Experimental Brain Research · doi:10.1007/s00221-009-1961-8 · Cited by 176 · see citing works
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) · Cerebral Cortex · doi:10.1093/cercor/bhl183 · Cited by 169 · see citing works
Repetitive TMS over the human oculomotor cortex: Comparison of 1-Hz and theta burst stimulation
Nyffeler, T., Wurtz, P., Lüscher, H.-R., Hess, C. W., Senn, W., Pflugshaupt, T., von Wartburg, R., Lüthi, M., & Müri, R. M. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.09.011 · Cited by 151 · see citing works
Neural correlates of the misattribution of speech in schizophrenia
Allen, P., Amaro, E., Fu, C. H. Y., Williams, S. C. R., Brammer, M. J., Johns, L. C., & McGuire, P. K. (2007) · British Journal of Psychiatry · doi:10.1192/bjp.bp.106.025700 · Cited by 147 · see citing works
Neural activity in speech-sensitive auditory cortex during silence
Hunter, M. D., Eickhoff, S. B., Miller, T. W. R., Farrow, T. F. D., Wilkinson, I. D., & Woodruff, P. W. R. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506268103 · Cited by 132 · see citing works
Association of individual resting state EEG alpha frequency and cerebral blood flow
Jann, K., Koenig, T. W., Dierks, T., Boesch, C., & Federspiel, A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.02.024 · Cited by 128 · see citing works
Self-citationStructural and metabolic changes in language areas linked to formal thought disorder
Horn, H., Federspiel, A., Wirth, M., Müller, T., Wiest, R., Wang, J.-J., & Strik, W. K. (2009) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.107.045633 · Cited by 123 · see citing works
Self-citationHoráček, J., Brunovský, M., Novák, T., Skrdlantová, L., Klírová, M., Bubeníková‐Valešová, V., Krajča, V., Tislerova, B., Kopeček, M., Španiel, F., et al. (2007) · Neuropsychobiology · doi:10.1159/000106055 · Cited by 117 · see citing works
Competition for neuronal resources: how hallucinations make themselves heard
Hubl, D., Koenig, T. W., Strik, W. K., Garcia, L. M., & Dierks, T. (2006) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.106.022954 · Cited by 99 · see citing works
Self-citationScheef, L., Manka, C., Daamen, M., Kühn, K.-U., Maier, W., Schild, H. H., & Jessen, F. (2010) · Radiology · doi:10.1148/radiol.10091224 · Cited by 97 · see citing works
Reality of auditory verbal hallucinations
Raij, T. T., Valkonen-Korhonen, M., Holi, M., Therman, S., Lehtonen, J., & Hari, R. (2009) · Brain · doi:10.1093/brain/awp186 · Cited by 95 · see citing works
Functional magnetic resonance imaging of inner speech in schizophrenia
Simons, C. J. P., Tracy, D. K., Sanghera, K. K., O'Daly, O., Gilleen, J., Dominguez, M.-D.-G., Krabbendam, L., & Shergill, S. S. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.09.007 · Cited by 87 · see citing works
Hubl, D., Nyffeler, T., Wurtz, P., Chaves, S., Pflugshaupt, T., Lüthi, M., von Wartburg, R., Wiest, R., Dierks, T., Strik, W. K., et al. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.10.049 · Cited by 78 · see citing works
Self-citationKindler, J., Schumacher, R., Cazzoli, D., et al. (2012) · Stroke · doi:10.1161/strokeaha.111.647503 · Cited by 68 · see citing works
Self-citationHoman, P., Kindler, J., Federspiel, A., Flury, R., Hubl, D., Hauf, M., & Dierks, T. (2011) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.11030496 · Cited by 65 · see citing works
Self-citationHashimoto, R., Lee, K., Preus, A. P., McCarley, R. W., & Wible, C. G. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp079 · Cited by 62 · see citing works
Time course of regional brain activity accompanying auditory verbal hallucinations in schizophrenia
Hoffman, R. E., Pittman, B. P., Constable, R. T., Bhagwagar, Z., & Hampson, M. (2011) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.110.086835 · Cited by 50 · see citing works
Comparison of spatial and temporal pattern for fMRI obtained with BOLD and arterial spin labeling
Federspiel, A., Müller, T., Horn, H., Kiefer, C., & Strik, W. K. (2006) · Journal of Neural Transmission · doi:10.1007/s00702-006-0434-5 · Cited by 48 · see citing works
Self-citationAndoh, J., Eric Artiges, A., Pallier, C., Rivière, D., Mangin, J., Martinot, M. P., & Martinot, J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm047 · Cited by 46 · see citing works
Interleaved TMS/CASL: Comparison of different rTMS protocols
Moisa, M., Pohmann, R., Uludaǧ, K., & Thielscher, A. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.07.010 · Cited by 45 · see citing works
Baseline Brain Perfusion and the Serotonin Transporter Promoter Polymorphism
Viviani, R., Sim, E.-J., Lo, H., Beschoner, P., Osterfeld, N., Maier, C., Seeringer, A., Godoy, A. L. P. C., Rosa, A., Comas, D., et al. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.08.035 · Cited by 37 · see citing works
Giesel, F. L., Mehndiratta, A., Hempel, A., Hempel, E., Kress, K. R., Essig, M., & Schröder, J. (2011) · European Journal of Radiology · doi:10.1016/j.ejrad.2011.03.002 · Cited by 19 · see citing works
Neurophysiological mechanisms of psychotic symptoms
Strik, W. K., & Dierks, T. (2008) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-008-5016-0 · Cited by 15 · see citing works
Self-citationHubl, D., Hauf, M., van Swam, C., et al. (2007) · The Lancet · doi:10.1016/s0140-6736(07)61237-9 · Cited by 12 · see citing works
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Lefaucheur, J.-P., André-Obadia, N., Antal, A., Ayache, S. S., Baeken, C., Benninger, D. H., Cantello, R. M., Cincotta, M., de Carvalho, M., De Ridder, D., et al. (2014) · Clinical Neurophysiology · doi:10.1016/j.clinph.2014.05.021 · Cited by 2,119 · see citing works
Moseley, P., Fernyhough, C., & Ellison, A. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.10.001 · Cited by 113 · see citing works
Homan, P., Kindler, J., Hauf, M., Hubl, D., & Dierks, T. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.114 · Cited by 80 · see citing works
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- Authors
- Kindler, J., Homan, P., Jann, K., Federspiel, A., Flury, R., Hauf, M., Strik, W., Dierks, T., & Hubl, D.
- Affiliations
- University Hospital of Bern (CH)
- University of Bern (CH)
- Corresponding author
- Dierks, Thomas
- ORCID
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2013-03
- Volume
- 73
- Issue
- 6
- Pages
- 518-524
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W2021392104
- Cited by
- 112
- References
- 52
- Citations by year
- 2025: 9 · 2024: 9 · 2023: 7 · 2022: 8 · 2021: 10 · 2020: 6 · 2019: 12 · 2018: 5 · 2017: 14 · 2016: 10 · 2015: 8 · 2014: 7 · 2013: 6 · 2012: 1
- FWCI
- 3.54
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Bern Open Repository and Information System (University of Bern) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Swiss National Science Foundation (32003B-112578)
- Topics
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cognitive Neuroscience › Hallucinations in medical conditions
- Keywords
- transcranial magnetic stimulation, auditory verbal hallucinations, schizophrenia, schizoaffective disorder, cerebral blood flow, arterial spin labeling, primary auditory cortex, Broca's area, cingulate gyrus, language regions
- MeSH terms
- Adolescent, Adult, Aged, Auditory Cortex, Cerebral Cortex, Cerebrovascular Circulation, Female, Frontal Lobe, Gyrus Cinguli, Hallucinations, Humans, Language, Male, Middle Aged, Neurons, Psychotic Disorders, Schizophrenia, Transcranial Magnetic Stimulation, Functional Neuroimaging
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