Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-20T05:13:36.812Z Has data issue: false hasContentIssue false
  • English
  • Français

Imaging auditory hallucinations in schizophrenia

Published online by Cambridge University Press:  24 June 2014

D. K. Tracy  and
S. S. Shergill
D. K. Tracy
Affiliation:
Department of Psychological Medicine, Division of Psychological Medicine, Institute of Psychiatry, Kings College London, London, UK
S. S. Shergill*
Affiliation:
Department of Psychological Medicine, Division of Psychological Medicine, Institute of Psychiatry, Kings College London, London, UK Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London, London, UK
*
Dr S. S. Shergill, Institute of Psychiatry, De Crespigny Park, London, SE5 8AF, UK. Tel and Fax: +44 20 7848 0350; E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

It is increasingly recognized that there are a heterogeneous range of symptoms within the syndrome of schizophrenia and that some of these also occur frequently within other psychiatric conditions. An approach similar to that in neuropsychology, where cases are grouped based on a discrete deficit, or in this case a discrete symptom, rather than a cause or diagnosis, may be useful in exploring the neural correlates of psychotic symptomatology. Functional neuroimaging provides an excellent tool for investigating the in vivo cortical function of patients with schizophrenia. Auditory verbal hallucinations are one of the most commonly occurring psychotic symptoms in schizophrenia; and this paper examines the progress that has been made in utilizing neuroimaging techniques to investigate auditory hallucinations in schizophrenia and review potential implications for treatment and future directions for research.

Keywords

fMRIauditory hallucinationsschizophrenia
Type
Review Article
Information
Acta Neuropsychiatrica , Volume 18 , Issue 2 , April 2006 , pp. 71 - 78
Copyright
Copyright © 2006 Blackwell Munksgaard

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Liddle, PF. The symptoms of chronic schizophrenia. A re-examination of the positive-negative dichotomy. Br J Psychiatry 1987;151: 145–151. CrossRefGoogle ScholarPubMed
Van Os, J, Gilvarry, C, Bale, Ret al. A comparison of the utility of dimensional and categorical representations of psychosis. UK700 Group. Psychol Med 1999;29: 595–606. CrossRefGoogle ScholarPubMed
Broca, P. Remarques sur le siege de la faculte du langage articule; suivies d'une observation d'aphemie. Bulletin de al Societe Anatomique de Paris 1861;6: 330–357.Google Scholar
Wernicke, C. Der aphasiche Symptomenkomplex. Breslau, Poland: Cohen and Weigert, 1874. Google Scholar
Lichteim, W. On aphasia. Brain 1885;7: 433–438. CrossRefGoogle Scholar
Price, CJ. The anatomy of language: contributions from functional neuroimaging. J Anat 2000;197 (Pt. 3):335–359. CrossRefGoogle ScholarPubMed
Penfield, W. Epilepsy and the Functional Anatomy of the Human Brain. Boston: Little, Brown, 1954. Google Scholar
Perez, MM, Trimble, MR, Murray, NM, Reider, I. Epileptic psychosis: an evaluation of PSE profiles. Br J Psychiatry 1985;146: 155–163. CrossRefGoogle ScholarPubMed
Penfield, W, Perot, P. The brain's record of auditory and visual experience. A final summary discussion. Brain 1963;86: 595–696. CrossRefGoogle Scholar
Frith, CD, Done, DJ. Towards a neuropsychology of schizophrenia. Br J Psychiatry 1988;153: 437–443. CrossRefGoogle ScholarPubMed
Shergill, SS, Brammer, MJ, Fukuda, Ret al. Engagement of brain areas implicated in processing inner speech in people with auditory hallucinations. Br J Psychiatry 2003;182: 525–531. CrossRefGoogle ScholarPubMed
Wolpert, DM, Ghahramani, Z, Jordan, MI. An internal model for sensorimotor integration. Science 1995;269: 1880–1882. CrossRefGoogle ScholarPubMed
Blakemore, SJ, Wolpert, DM, Frith, CD. Central cancellation of self-produced tickle sensation. Nat Neurosci 1998;1: 635–640. CrossRefGoogle ScholarPubMed
Shergill, SS, Bays, PM, Frith, CD, Wolpert, DM. Two eyes for an eye: the neuroscience of force escalation. Science 2003;301: 187. CrossRefGoogle ScholarPubMed
Frith, CD, Blakemore, S, Wolpert, DM. Explaining the symptoms of schizophrenia: abnormalities in the awareness of action. Brain Res Brain Res Rev 2000;31: 357–363. CrossRefGoogle ScholarPubMed
Shergill, SS, Samson, G, Bays, PM, Frith, CD, Wolpert, DM. Evidence for sensory prediction deficits in schizophrenia. Am J Psychiatry 2005;162: 2384–2386. CrossRefGoogle Scholar
McGuire, PK, Shah, GM, Murray, RM. Increased blood flow in Broca's area during auditory hallucinations in schizophrenia. Lancet 1993;342: 703–706. CrossRefGoogle Scholar
Suzuki, M, Yuasa, S, Minabe, Y, Murata, M, Kurachi, M. Left superior temporal blood flow increases in schizophrenic and schizophreniform patients with auditory hallucination: a longitudinal case study using 123I-IMP SPECT. Eur Arch Psychiatry Clin Neurosci 1993;242: 257–261. CrossRefGoogle ScholarPubMed
Cleghorn, JM, Franco, S, Szechtman, Bet al. Toward a brain map of auditory hallucinations. Am J Psychiatry 1992;149: 1062–1069. Google Scholar
Silbersweig, DA, Stern, E, Frith, Cet al. A functional neuroanatomy of hallucinations in schizophrenia. Nature 1995;378: 176–179. CrossRefGoogle Scholar
Liddle, PF, Friston, KJ, Frith, CD, Frackowiak, RS. Cerebral blood flow and mental processes in schizophrenia. J R Soc Med 1992;85: 224–227. Google Scholar
Dierks, T, Linden, DE, Jandl, Met al. Activation of Heschl's gyrus during auditory hallucinations. Neuron 1999;22: 615–621. CrossRefGoogle ScholarPubMed
Shergill, SS, Brammer, MJ, Williams, SC, Murray, RM, McGuire, PK. Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Arch Gen Psychiatry 2000;57: 1033–1038. CrossRefGoogle ScholarPubMed
Rao, SM, Bandettini, PA, Binder, JRet al. Relationship between finger movement rate and functional magnetic resonance signal change in human primary motor cortex. J Cereb Blood Flow Metab 1996;16: 1250–1254. CrossRefGoogle ScholarPubMed
Guimaraes, AR, Melcher, JR, Talavage, TMet al. Imaging subcortical auditory activity in humans. Hum Brain Mapp 1998;6: 33–41. 3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Hall, DA, Haggard, MP, Akeroyd, MAet al. “Sparse” temporal sampling in auditory fMRI. Hum Brain Mapp 1999;7: 213–223. 3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Bandettini, PA, Jesmanowicz, A, Van Kylen, J, Birn, RM, Hyde, JS. Functional MRI of brain activation induced by scanner acoustic noise. Magn Reson Med 1998;39: 410–416. CrossRefGoogle ScholarPubMed
McGuire, PK, Silbersweig, DA, Frith, CD. Functional neuroanatomy of verbal self-monitoring. Brain 1996;119 (Pt. 3):907–917. CrossRefGoogle ScholarPubMed
Shergill, SS, Bullmore, ET, Brammer, MJet al. A functional study of auditory verbal imagery. Psychol Med 2001;31: 241–253. CrossRefGoogle ScholarPubMed
Shergill, SS, Brammer, MJ, Fukuda, Ret al. Modulation of activity in temporal cortex during generation of inner speech. Hum Brain Mapp 2002;16: 219–227. CrossRefGoogle ScholarPubMed
Woodruff, P, Brammer, MJ, Mellers, Jet al. Auditory hallucinations and perception of external speech. Lancet 1995;346: 1035. CrossRefGoogle ScholarPubMed
Line, P, Silberstein, RB, Wright, JJ, Copolov, DL. Steady state visually evoked potential correlates of auditory hallucinations in schizophrenia. Neuroimage 1998;8: 370–376. CrossRefGoogle Scholar
George, MS, Parekh, PI, Rosinsky, Net al. Understanding emotional prosody activates right hemisphere regions. Arch Neurol 1996;53: 665–670. CrossRefGoogle ScholarPubMed
Mitchell, RL, Elliott, R, Barry, M, Cruttenden, A, Woodruff, PW. Neural response to emotional prosody in schizophrenia and in bipolar affective disorder. Br J Psychiatry 2004;184: 223–230. CrossRefGoogle ScholarPubMed
Buchanan, TW, Lutz, K, Mirzazade, Set al. Recognition of emotional prosody and verbal components of spoken language: an fMRI study. Brain Res Cogn Brain Res 2000;9: 227–238. CrossRefGoogle ScholarPubMed
Bottini, G, Corcoran, R, Sterzi, Ret al. The role of the right hemisphere in the interpretation of figurative aspects of language. A positron emission tomography activation study. Brain 1994;117 (Pt. 6):1241–1253. CrossRefGoogle Scholar
Canli, T, Desmond, JE, Zhao, Z, Glover, G, Gabrieli, JD. Hemispheric asymmetry for emotional stimuli detected with fMRI. Neuroreport 1998;9: 3233–3239. CrossRefGoogle ScholarPubMed
Maher, BA, Manschreck, TC, Yurgelun-Todd, DA, Tsuang, MT. Hemispheric asymmetry of frontal and temporal gray matter and age of onset in schizophrenia. Biol Psychiatry 1998;44: 413–417. CrossRefGoogle Scholar
Shapleske, J, Rossell, SL, Simmons, A, David, AS, Woodruff, PW. Are auditory hallucinations the consequence of abnormal cerebral lateralization? A morphometric MRI study of the sylvian fissure and planum temporale. Biol Psychiatry 2001;49: 685–693. CrossRefGoogle ScholarPubMed
Creutzfeldt, O, Ojemann, G, Lettich, E. Neuronal activity in the human lateral temporal lobe. II. Responses to the subjects own voice. Exp Brain Res 1989;77: 476–489. CrossRefGoogle ScholarPubMed
Reisberg, D, Wilson, M, Smith, J. Mental Images in Human Cognition. Amsterdam: Elsevier, 1991. Google Scholar
Shergill, SS, Bullmore, E, Simmons, A, Murray, R, McGuire, P. Functional anatomy of auditory verbal imagery in schizophrenic patients with auditory hallucinations. Am J Psychiatry 2000;157: 1691–1693. CrossRefGoogle ScholarPubMed
McGuire, PK, Silbersweig, DA, Wright, Iet al. The neural correlates of inner speech and auditory verbal imagery in schizophrenia: relationship to auditory verbal hallucinations. Br J Psychiatry 1996;169: 148–159. CrossRefGoogle ScholarPubMed
McGuire, PK, Silbersweig, DA, Wright, Iet al. Abnormal monitoring of inner speech: a physiological basis for auditory hallucinations. Lancet 1995;346: 596–600. CrossRefGoogle ScholarPubMed
Zatorre, RJ, Samson, S. Role of the right temporal neocortex in retention of pitch in auditory short-term memory. Brain 1991;114 (Pt. 6):2403–2417. CrossRefGoogle ScholarPubMed
Zatorre, RJ, Evans, AC, Meyer, E, Gjedde, A. Lateralization of phonetic and pitch discrimination in speech processing. Science 1992;256: 846–849. CrossRefGoogle ScholarPubMed
Pell, MD. Recognition of prosody following unilateral brain lesion: influence of functional and structural attributes of prosodic contours. Neuropsychologia 1998;36: 701–715. CrossRefGoogle ScholarPubMed
Matsumoto, K, Samson, GT, O'Daly, O, Tracy, DK, Patel, AD, Shergill, SS. Impaired prosodic discrimination in patients with schizophrenia. Br J Psychiatry 2006; in press.Google Scholar
Leiner, HC, Leiner, AL, Dow, RS. Cognitive and language functions of the human cerebellum. Trends Neurosci 1993;16: 444–447. CrossRefGoogle ScholarPubMed
Afifi, A, Bergman, R. Functional Neuroanatomy. New York: McGraw-Hill, 1998. Google Scholar
Desmond, JE, Gabrieli, JD, Wagner, AD, Ginier, BL, Glover, GH. Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J Neurosci 1997;17: 9675–9685. Google ScholarPubMed
Levelt, WJ. Monitoring and self-repair in speech. Cognition 1983;14: 41–104. CrossRefGoogle Scholar
Johns, LC, McGuire, PK. Verbal self-monitoring and auditory hallucinations in schizophrenia. Lancet 1999;353: 469–470. CrossRefGoogle Scholar
Shergill, SS, Murray, RM, McGuire, PK. Auditory hallucinations: a review of psychological treatments. Schizophr Res 1998;32: 137–150. CrossRefGoogle ScholarPubMed
Woodruff, PW, Wright, IC, Bullmore, ETet al. Auditory hallucinations and the temporal cortical response to speech in schizophrenia: a functional magnetic resonance imaging study. Am J Psychiatry 1997;154: 1676–1682. CrossRefGoogle ScholarPubMed
Haraldsson, HM, Ferrarelli, F, Kalin, NH, Tononi, G. Transcranial magnetic stimulation in the investigation and treatment of schizophrenia: a review. Schizophr Res 2004;71: 1–16. CrossRefGoogle ScholarPubMed
Hoffman, RE, Gueorguieva, R, Hawkins, KAet al. Temporoparietal transcranial magnetic stimulation for auditory hallucinations: safety, efficacy and moderators in a fifty patient sample. Biol Psychiatry 2005;58: 97–104. CrossRefGoogle Scholar
Hoffman, RE, Boutros, NN, Hu, Set al. Transcranial magnetic stimulation and auditory hallucinations in schizophrenia. Lancet 2000;355: 1073–1075. CrossRefGoogle Scholar
Figiel, GS, Epstein, C, Mcdonald, WMet al. The use of rapid-rate transcranial magnetic stimulation (rTMS) in refractory depressed patients. J Neuropsychiatry Clin Neurosci 1998;10: 20–25. CrossRefGoogle Scholar
Paus, T, Barrett, J. Transcranial magnetic stimulation (TMS) of the human frontal cortex: implications for repetitive TMS treatment of depression. J Psychiatry Neurosci 2004;29: 268–279. Google ScholarPubMed
Alonso, P, Pujol, J, Cardoner, Net al. Right prefrontal repetitive transcranial magnetic stimulation in obsessive-compulsive disorder: a double-blind, placebo-controlled study. Am J Psychiatry 2001;158: 1143–1145. CrossRefGoogle ScholarPubMed
Greenberg, BD, George, MS, Martin, JDet al. Effect of prefrontal repetitive transcranial magnetic stimulation in obsessive-compulsive disorder: a preliminary study. Am J Psychiatry 1997;154: 867–869. Google ScholarPubMed
Grisaru, N, Chudakov, B, Yaroslavsky, Y, Belmaker, RH. Transcranial magnetic stimulation in mania: a controlled study. Am J Psychiatry 1998;155: 1608–1610. CrossRefGoogle ScholarPubMed
Grisaru, N, Amir, M, Cohen, H, Kaplan, Z. Effect of transcranial magnetic stimulation in posttraumatic stress disorder: a preliminary study. Biol Psychiatry 1998;44: 52–55. CrossRefGoogle ScholarPubMed
Poulet, E, Brunelin, J, Bediou, Eet al. Slow transcranial magnetic stimulation can rapidly reduce resistant auditory hallucinations in schizophrenia. Biol Psychiatry 2005;57: 188–191. CrossRefGoogle Scholar
D'Alfonso, AA, Aleman, A, Kessels, RPet al. Transcranial magnetic stimulation of left auditory cortex in patients with schizophrenia: effects on hallucinations and neurocognition. J Neuropsychiatry Clin Neurosci 2002;14: 77–79. CrossRefGoogle ScholarPubMed
Chibbaro, G, Daniele, M, Alagona, Get al. Repetitive transcranial magnetic stimulation in schizophrenic patients reporting auditory hallucinations. Neurosci Lett 2005;383: 54–57. CrossRefGoogle ScholarPubMed
Lee, SH, Kim, W, Chung, YCet al. 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 2005;376: 177–181. CrossRefGoogle ScholarPubMed
Hoffman, RE, Boutros, NN, Berman, RM, et al. Transcranial magnetic stimulation of left temporoparietal cortex in three patients reporting hallucinated “voices”. Biol Psychiatry 1999;46: 130–132. CrossRefGoogle ScholarPubMed
Hoffman, RE, Hawkins, KA, Guerguieva, Ret al. Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. Arch Gen Psychiatry 2003;60: 49–56. CrossRefGoogle ScholarPubMed
Fitzgerald, PB, Benitee, J, Daskalakis, Jet al. A double-blind sham-controlled trial of repetitive transcranial magnetic stimulation in the treatment of refractory auditory hallucinations. J Clin Psychopharmacol 2005;25: 358–362. CrossRefGoogle ScholarPubMed
McIntosh, AM, Semple, D, Tasker, Ket al. Transcranial magnetic stimulation for auditory hallucinations in schizophrenia. Psychiatry Res 2004;127: 9–17. CrossRefGoogle Scholar
Paus, T. Imaging the brain before, during, and after transcranial magnetic stimulation. Neuropsychologia 1999;37: 219–224. CrossRefGoogle ScholarPubMed
Roth, BJ, Saypol, JM, Hallett, M, Cohen, LG. A theoretical calculation of the electric field induced in the cortex during magnetic stimulation. Electroencephalogr Clin Neurophysiol 1991;81: 47–56. CrossRefGoogle ScholarPubMed
Singh, KD, Hamdy, S, Aziz, Q, Thompson, DG. Topographic mapping of trans-cranial magnetic stimulation data on surface rendered MR images of the brain. Electroencephalogr Clin Neurophysiol 1997;105: 345–351. CrossRefGoogle Scholar
Peters, T, Davey, B, Munger, P, Comeau, R, Evans, A, Olivier, A. Three-dimensional multimodal image-guidance for neurosurgery. IEEE Trans Med Imaging 1996;15: 121–128. CrossRefGoogle ScholarPubMed
Neggers, SF, Langerak, TR, Schutter, DJet al. A stereotactic method for image-guided transcranial magnetic stimulation validated with fMRI and motor-evoked potentials. Neuroimage 2004;21: 1805–1817. CrossRefGoogle ScholarPubMed
Denslow, S, Bohning, DE, Bohning, PA, Lomarev, MP, George, MS. An increased precision comparison of TMS-induced motor cortex BOLD fMRI response for image-guided versus function-guided coil placement. Cogn Behav Neurol 2005;18: 119–126. CrossRefGoogle ScholarPubMed
Lotze, M, Kaethner, RJ, Erb, Met al. Comparison of representational maps using functional magnetic resonance imaging and transcranial magnetic stimulation. Clin Neurophysiol 2003;114: 306–312. CrossRefGoogle ScholarPubMed
Niyazov, DM, Butler, AJ, Kadah, YM, Epstein, CM, Hu, XP. Functional magnetic resonance imaging and transcranial magnetic stimulation: effects of motor imagery, movement and coil orientation. Clin Neurophysiol 2005;116: 1601–1610. CrossRefGoogle ScholarPubMed
Bohning, DE, Denslow, S, Bohning, PA, Walker, JA, George, MS. A TMS coil positioning/holding system for MR image-guided TMS interleaved with fMRI. Clin Neurophysiol 2003;114: 2210–2219. CrossRefGoogle ScholarPubMed
Shergill, SS, Brammer, MJ, Amaro, E, Williams, SCR, Murray, RM, McGuire, PK. The temporal course of auditory hallucinations. Br J Psychiatry 2004;185: 516–517. CrossRefGoogle ScholarPubMed
Bullmore, E, Horwitz, B, Honey, Get al. How good is good enough in path analysis of fMRI data? Neuroimage 2000 11: 289–301. CrossRefGoogle ScholarPubMed
Jones, DK, Pierpaoli, C. Confidence mapping in diffusion tensor magnetic resonance imaging tractography using a bootstrap approach. Magn Reson Med 2005;53: 1143–1149. CrossRefGoogle ScholarPubMed
Kanaan, RAA, Shergill, SS, Barker, GJet al. Tract-specific anisotropy measurements in diffusion tensor imaging. Psychiatry Res 2006;146: 73–82. CrossRefGoogle ScholarPubMed
Desmond, JE, Fiez, JA. Neuroimaging studies of the cerebellum: language, learning and memory. Tren Cog Sci 1998;2: 355–362. CrossRefGoogle ScholarPubMed