Noninvasive brain stimulation for the treatment of auditory verbal hallucinations in schizophrenia: Methods, effects and challenges

Frontiers in Systems Neuroscience

Volumn 9, Issue OCT, 2015, Pages

  Kubera, Katharina M ^a   Barth, Anja ^a   Hirjak, Dusan ^a   Thomann, Philipp A ^a   Wolf, Robert C ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

Auditory verbal hallucinations; Brain function; Brain stimulation; Phenotypes; Schizophrenia; Transcranial magnetic stimulation

Indexed keywords

ANTERIOR CINGULATE; AUDITORY HALLUCINATION; AUDITORY HALLUCINATION RATING SCALE; AUDITORY PROCESSING DISORDER; AUDITORY VERBAL HALLUCINATION; BRAIN DEPTH STIMULATION; BRIEF PSYCHIATRIC RATING SCALE; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NON INVASIVE MEASUREMENT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPIC VARIATION; REVIEW; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION; TEMPORAL CORTEX; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84944457258     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2015.00131     Document Type: Review

References (63)

1. Alderson-Day, B., McCarthy-Jones, S., and Fernyhough, C. (2015). Hearing voices in the resting brain: A review of intrinsic functional connectivity research on auditory verbal hallucinations. Neurosci. Biobehav. Rev. 55, 78–87. doi: 10.1016/j.neubiorev.2015.04.016
2. Aleman, A. (2013). Use of repetitive transcranial magnetic stimulation for treatment in psychiatry. Clin. Psychopharmacol. Neurosci. 11, 53–59. doi: 10.9758/cpn.2013.11.2.53
3. Aleman, A., and de Haan, E. H. (1998). On redefining hallucination. Am. J. Orthopsychiatry. 68, 656–659. doi: 10.1037/h0080376
4. Aleman, A., Sommer, I. E., and Kahn, R. S. (2007). Efficacy of slow repetitive transcranial magnetic stimulation in the treatment of resistant auditory hallucinations in schizophrenia: a meta-analysis. J. Clin. Psychiatry. 68, 416–421. doi: 10.4088/jcp.v68n0310
5. Allen, P., Aleman, A., and McGuire, P. K. (2007). Inner speech models of auditory verbal hallucinations: evidence from behavioural and neuroimaging studies. Int. Rev. Psychiatry. 19, 407–415. doi: 10.1080/09540260701486498
6. Allen, P., Larøi, F., McGuire, P. K., and Aleman, A. (2008). The hallucinating brain: a review of structural and functional neuroimaging studies of hallucinations. Neurosci. Biobehav. Rev. 32, 175–191. doi: 10.1016/j.neubiorev.2007.07.012
7. Alonso-Solís, A., Vives-Gilabert, Y., Grasa, E., Portella, M. J., Rabella, M., Sauras, R. B., et al. (2015). Resting-state functional connectivity alterations in the default network of schizophrenia patients with persistent auditory verbal hallucinations. Schizophr. Res. 161, 261–268. doi: 10.1016/j.schres.2014.10.047
8. Andrews-Hanna, J. R., Reidler, J. S., Sepulcre, J., Poulin, R., and Buckner, R. L. (2010). Functional-anatomic fractionation of the brain’s default network. Neuron. 65, 550–562. doi: 10.1016/j.neuron.2010.02.005
9. Bais, L., Vercammen, A., Stewart, R., van Es, F., Visser, B., Aleman, A., et al. (2014). Short and long term effects of left and bilateral repetitive transcranial magnetic stimulation in schizophrenia patients with auditory verbal hallucinations: a randomized controlled trial. PLoS One. 9:e108828. doi: 10.1371/journal.pone.0108828
10. Barker, A. T., Jalinous, R., and Freeston, I. L. (1985). Non-invasive magnetic stimulation of human motor cortex. Lancet 1, 1106–1107. doi: 10.1016/S0140-6736(85)92413-4
11. Blumberger, D. M., Christensen, B. K., Zipursky, R. B., Moller, B., Chen, R., Fitzgerald, P. B., et al. (2012). MRI-targeted repetitive transcranial magnetic stimulation of Heschl’s gyrus for refractory auditory hallucinations. Brain Stimul. 5, 577–585. doi: 10.1016/j.brs.2011.12.002
12. Brunelin, J., Mondino, M., Gassab, L., Haesebaert, F., Gaha, L., Suaud-Chagny, M. F., et al. (2012). Examining transcranial direct-current stimulation (tDCS) as a treatment for hallucinations in schizophrenia. Am. J. Psychiatry. 169, 719–724. doi: 10.1176/appi.ajp.2012.11071091
13. Chervyakov, A. V., Chernyavsky, A. Y., Sinitsyn, D. O., and Piradov, M. A. (2015). Possible Mechanisms Underlying the Therapeutic Effects of Transcranial Magnetic Stimulation. Front. Hum. Neurosci. 9:303. doi: 10.3389/fnhum.2015.00303
14. Diederen, K. M., Neggers, S. F., de Weijer, A. D., van Lutterveld, R., Daalman, K., Eickhoff, S. B., et al. (2013). Aberrant resting-state connectivity in non-psychotic individuals with auditory hallucinations. Psychol. Med. 43, 1685–1696. doi: 10.1017/s0033291712002541
15. Ford, J. M., and Mathalon, D. H. (2005). Corollary discharge dysfunction in schizophrenia: can it explain auditory hallucinations? Int. J. Psychophysiol. 58, 179–189. doi: 10.1016/j.ijpsycho.2005.01.014
16. Freitas, C., Fregni, F., and Pascual-Leone, A. (2009). Meta-analysis of the effects of repetitive transcranial magnetic stimulation (rTMS) on negative and positive symptoms in schizophrenia. Schizophrenia Research. 108, 11–24. doi: 10.1016/j.schres.2008.11.027
17. George, M. S., and Aston-Jones, G. (2010). Noninvasive techniques for probing neurocircuitry and treating illness: vagus nerve stimulation (VNS), transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS). Neuropsychopharmacology. 35, 301–316. doi: 10.1038/npp.2009.87
18. Hoffman, R. E., Wu, K., Pittman, B., Cahill, J. D., Hawkins, K. A., Fernandez, T., et al. (2013). Transcranial magnetic stimulation of Wernicke’s and Right homologous sites to curtail “voices”: a randomized trial. Biol. Psychiatry. 73, 1008–1014. doi: 10.1016/j.biopsych.2013.01.016
19. Homan, P., Kindler, J., Hauf, M., Hubl, D., and Dierks, T. (2012). Cerebral blood flow identifies responders to transcranial magnetic stimulation in auditory verbal hallucinations. Transl. Psychiatry. 2:e189. doi: 10.1038/tp.2012.114
20. Hugdahl, K., Løberg, E. M., Specht, K., Steen, V. M., van Wageningen, H., and Jørgensen, H. A. (2008). Auditory hallucinations in schizophrenia: the role of cognitive, brain structural and genetic disturbances in the left temporal lobe. Front. Hum. Neurosci. 1:6. doi: 10.3389/neuro.09.006.2007
21. Jandl, M., Steyer, J., Weber, M., Linden, D. E., Rothmeier, J., Maurer, K., et al. (2006). Treating auditory hallucinations by transcranial magnetic stimulation: a randomized controlled cross-over trial. Neuropsychobiology. 53, 63–69. doi: 10.1159/000091721
22. Kindler, J., Homan, P., Jann, K., Federspiel, A., Flury, R., Hauf, M., et al. (2013). Reduced neuronal activity in language-related regions after transcranial magnetic stimulation therapy for auditory verbal hallucinations. Biological Psychiatry. 73, 518–524. doi: 10.1016/j.biopsych.2012.06.019
23. Koops, S., van den Brink, H., and Sommer, I. E. (2015). Transcranial direct current stimulation as a treatment for auditory hallucinations. Front. Psychol. 6:244. doi: 10.3389/fpsyg.2015.00244
24. Kronmüller, K. T., von Bock, A., Grupe, S., Büche, L., Gentner, N. C., Rückl, S., et al. (2011). Psychometric evaluation of the Psychotic Symptom Rating Scales. Compr. Psychiatry. 52, 102–108. doi: 10.1016/j.comppsych.2010.04.014
25. Kubera, K. M., Sambataro, F., Vasic, N., Wolf, N. D., Frasch, K., Hirjak, D., et al. (2014). Source-based morphometry of gray matter volume in patients with schizophrenia who have persistent auditory verbal hallucinations. Prog. Neuropsychopharmacol. Biol. Psychiatry. 50, 102–109. doi: 10.1016/j.pnpbp.2013.11.015
26. Kuhn, S., and Gallinat, J. (2012). Quantitative meta-analysis on state and trait aspects of auditory verbal hallucinations in schizophrenia. Schizophr. Bull. 38, 779–786. doi: 10.1093/schbul/sbq152
27. Lavigne, K. M., Rapin, L. A., Metzak, P. D., Whitman, J. C., Jung, K., Dohen, M., et al. (2015). Left-dominant temporal-frontal hypercoupling in schizophrenia patients with hallucinations during speech perception. Schizophr. Bull. 41, 259–567. doi: 10.1093/schbul/sbu004
28. Lawrie, S. M., Buechel, C., Whalley, H. C., Frith, C. D., Friston, K. J., and Johnstone, E. C. (2002). Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations. Biol. Psychiatry. 51, 1008–1011. doi: 10.1016/s0006-3223(02)01316-1
29. Lee, S. H., Kim, W., Chung, Y. C., Jung, K. H., Bahk, W. M., Jun, T. Y., et al. (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. doi: 10.1016/j.neulet.2004.11.048
30. Lefaucheur, J. P., Andre-Obadia, N., Antal, A., Ayache, S. S., Baeken, C., Benninger, D. H., et al. (2014). Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin. Neurophysiol. 125, 2150–2206. doi: 10.1016/j.clinph.2014.05.021
31. Leff, J., Williams, G., Huckvale, M. A., Arbuthnot, M., and Leff, A. P. (2013). Computer-assisted therapy for medication-resistant auditory hallucinations: proof-of-concept study. Br. J. Psychiatry. 202, 428–433. doi: 10.1192/bjp.bp.112.124883
32. Loo, C. K., Sainsbury, K., Mitchell, P., Hadzi-Pavlovic, D., and Sachdev, P. S. (2010). A sham-controlled trial of left and right temporal rTMS for the treatment of auditory hallucinations. Psychol. Med. 40, 541–546. doi: 10.1017/s0033291709990900
33. McCarthy-Jones, S., Thomas, N., Strauss, C., Dodgson, G., Jones, N., Woods, A., et al. (2014). Better than mermaids and stray dogs? Subtyping auditory verbal hallucinations and its implications for research and practice. Schizophr. Bull. 4, S275–S284. doi: 10.1093/schbul/sbu018
34. Mechelli, A., Allen, P., Amaro, E., Jr., Fu, C. H., Williams, S. C., Brammer, M. J., et al. (2007). Misattribution of speech and impaired connectivity in patients with auditory verbal hallucinations. Hum. Brain Mapp. 28, 1213–1222. doi: 10.1002/hbm.20341
35. Modinos, G., Costafreda, S. G., van Tol, M. J., McGuire, P. K., Aleman, A., and Allen, P. (2013). Neuroanatomy of auditory verbal hallucinations in schizophrenia: a quantitative meta-analysis of voxel-based morphometry studies. Cortex. 49, 1046–1055. doi: 10.1016/j.cortex.2012.01.009
36. Mondino, M., Haesebaert, F., Poulet, E., Suaud-Chagny, M. F., and Brunelin, J. (2015). Fronto-temporal transcranial Direct Current Stimulation (tDCS) reduces source-monitoring deficits and auditory hallucinations in patients with schizophrenia. Schizophr. Res. 161, 515–516. doi: 10.1016/j.schres.2014.10.054
37. Nieuwdorp, W., Koops, S., Somers, M., and Sommer, I. E. (2015). Transcranial magnetic stimulation, transcranial direct current stimulation and electroconvulsive therapy for medication-resistant psychosis of schizophrenia. Curr. Opin. Psychiatry. 28, 222–228. doi: 10.1097/yco.0000000000000156
38. Northoff, G., and Qin, P. (2011). How can the brain’s resting state activity generate hallucinations? A ‘resting state hypothesis’ of auditory verbal hallucinations. Schizophr. Res. 127, 202–214. doi: 10.1016/j.schres.2010.11.009
39. Plaze, M., Paillere-Martinot, M. L., Penttila, J., Januel, D., de Beaurepaire, R., Bellivier, F., et al. (2011). “Where do auditory hallucinations come from?”—a brain morphometry study of schizophrenia patients with inner or outer space hallucinations. Schizophr. Bull. 37, 212–221. doi: 10.1093/schbul/sbp081
40. Raij, T. T., Valkonen-Korhonen, M., Holi, M., Therman, S., Lehtonen, J., and Hari, R. (2009). Reality of auditory verbal hallucinations. Brain. 132, 2994–3001. doi: 10.1093/brain/awp186
41. Rosenberg, O., Gersner, R., Klein, L. D., Kotler, M., Zangen, A., and Dannon, P. (2012). Deep transcranial magnetic stimulation add-on for the treatment of auditory hallucinations: a double-blind study. Ann. Gen. Psychiatry. 11:13. doi: 10.1186/1744-859x-11-13
42. Sambataro, F., Wolf, N. D., Pennuto, M., Vasic, N., and Wolf, R. C. (2013). Revisiting default mode network function in major depression: evidence for disrupted subsystem connectivity. Psychol. Med. 44, 2041–2051. doi: 10.1017/s0033291713002596
43. Schonfeldt-Lecuona, C., Grön, G., Walter, H., Büchler, N., Wunderlich, A., Spitzer, M., et al. (2004). Stereotaxic rTMS for the treatment of auditory hallucinations in schizophrenia. Neuroreport. 15, 1669–1673. doi: 10.1097/01.wnr.0000126504.89983.ec
44. Shergill, S. S., Bullmore, E., Simmons, A., Murray, R., and McGuire, P. (2000). Functional anatomy of auditory verbal imagery in schizophrenic patients with auditory hallucinations. Am. J. Psychiatry. 157, 1691–1693. doi: 10.1176/appi.ajp.157.10.1691
45. Shergill, S. S., Murray, R. M., and McGuire, P. K. (1998). Auditory hallucinations: a review of psychological treatments. Schizophr. Res. 32, 137–150. doi: 10.1016/s0920-9964(98)00052-8
46. Slotema, C. W., Aleman, A., Daskalakis, Z. J., and Sommer, I. E. (2012). Meta-analysis of repetitive transcranial magnetic stimulation in the treatment of auditory verbal hallucinations: update and effects after one month. Schizophr. Res. 142, 40–45. doi: 10.1016/j.schres.2012.08.025
47. Slotema, C. W., Blom, J. D., de Weijer, A. D., Diederen, K. M., Goekoop, R., Looijestijn, J., et al. (2011). Can low-frequency repetitive transcranial magnetic stimulation really relieve medication-resistant auditory verbal hallucinations? Negative results from a large randomized controlled trial. Biol. Psychiatry. 69, 450–456. doi: 10.1016/j.biopsych.2010.09.051
48. Slotema, C. W., Blom, J. D., Hoek, H. W., and Sommer, I. E. (2010). Should we expand the toolbox of psychiatric treatment methods to include Repetitive Transcranial Magnetic Stimulation (rTMS)? A meta-analysis of the efficacy of rTMS in psychiatric disorders. J. Clin. Psychiatry. 71, 873–884. doi: 10.4088/jcp.08m04872gre
49. Slotema, C. W., Blom, J. D., van Lutterveld, R., Hoek, H. W., and Sommer, I. E. (2014). Review of the efficacy of transcranial magnetic stimulation for auditory verbal hallucinations. Biol. Psychiatry. 76, 101–110. doi: 10.1016/j.biopsych.2013.09.038
50. Sommer, I. E., de Weijer, A. D., Daalman, K., Neggers, S. F., Somers, M., Kahn, R. S., et al. (2007). Can fMRI-guidance improve the efficacy of rTMS treatment for auditory verbal hallucinations? Schizophr. Res. 93, 406–408. doi: 10.1016/j.schres.2007.03.020
51. Sommer, I. E., Diederen, K. M., Blom, J. D., Willems, A., Kushan, L., Slotema, K., et al. (2008). Auditory verbal hallucinations predominantly activate the right inferior frontal area. Brain. 131, 3169–3177. doi: 10.1093/brain/awn251
52. Sommer, I. E., Slotema, C. W., Daskalakis, Z. J., Derks, E. M., Blom, J. D., and van der Gaag, M. (2012). The treatment of hallucinations in schizophrenia spectrum disorders. Schizophr. Bull. 38, 704–714. doi: 10.1093/schbul/sbs034
53. Stephane, M., Barton, S., and Boutros, N. N. (2001). Auditory verbal hallucinations and dysfunction of the neural substrates of speech. Schizophr. Res. 50, 61–78. doi: 10.1016/s0920-9964(00)00150-x
54. Tharyan, P., and Adams, C. E. (2005). Electroconvulsive therapy for schizophrenia. Cochrane Database Syst. Rev. 18:CD000076. doi: 10.1002/9780470987353.ch27
55. Thiel, A., Schumacher, B., Wienhard, K., Gairing, S., Kracht, L. W., Wagner, R., et al. (2006). Direct demonstration of transcallosal disinhibition in language networks. J. Cereb. Blood Flow Metab. 26, 1122–1127. doi: 10.1038/sj.jcbfm.9600350
56. Tranulis, C., Sepehry, A. A., Galinowski, A., and Stip, E. (2008). Should we treat auditory hallucinations with repetitive transcranial magnetic stimulation? A metaanalysis. Can. J. Psychiatry. 53, 577–586.
57. Vlachos, A., Muller-Dahlhaus, F., Rosskopp, J., Lenz, M., Ziemann, U., and Deller, T. (2012). Repetitive magnetic stimulation induces functional and structural plasticity of excitatory postsynapses in mouse organotypic hippocampal slice cultures. J. Neurosci. 32, 17514–17523. doi: 10.1523/jneurosci.0409-12.2012
58. Wang, J. X., and Voss, J. L. (2015). Long-lasting enhancements of memory and hippocampal-cortical functional connectivity following multiple-day targeted noninvasive stimulation. Hippocampus. 25, 877–883. doi: 10.1002/hipo.22416
59. Wassermann, E. M., and Zimmermann, T.. (2012). Transcranial magnetic brain stimulation: therapeutic promises and scientific gaps. Pharmacol. Ther. 133, 98–107. doi: 10.1016/j.pharmthera.2011.09.003
60. Waters, F., Allen, P., Aleman, A., Fernyhough, C., Woodward, T. S., Badcock, J. C., et al. (2012). Auditory hallucinations in schizophrenia and nonschizophrenia populations: a review and integrated model of cognitive mechanisms. Schizophr. Bull. 38, 683–693. doi: 10.1093/schbul/sbs045
61. Wolf, N. D., Grön, G., Sambataro, F., Vasic, N., Frasch, K., Schmid, M., et al. (2012). Magnetic resonance perfusion imaging of auditory verbal hallucinations in patients with schizophrenia. Schizophr. Res. 134, 285–287. doi: 10.1016/j.schres.2011.11.018
62. Wolf, N. D., Sambataro, F., Vasic, N., Frasch, K., Schmid, M., Schönfeldt-Lecuona, C., et al. (2011). Dysconnectivity of multiple resting-state networks in patients with schizophrenia who have persistent auditory verbal hallucinations. J. Psychiatry. Neurosci. 36, 366–374. doi: 10.1503/jpn.110008
63. Woodward, T. S., Jung, K., Hwang, H., Yin, J., Taylor, L., Menon, M., et al. (2014). Symptom dimensions of the psychotic symptom rating scales in psychosis: a multisite study. Schizophr. Bull. 4, S265–S274. doi: 10.1093/schbul/sbu014