Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-13T01:37:42.017Z Has data issue: false hasContentIssue false
  • English
  • Français

The Neural Correlates of Inner Speech and Auditory Verbal Imagery in Schizophrenia: Relationship to Auditory Verbal Hallucinations

Published online by Cambridge University Press:  02 January 2018

P. K. McGuire ,
D. A. Silbersweig ,
I. Wright ,
R. M. Murray ,
R. S. J. Frackowiak  and
C. D. Frith
P. K. McGuire*
Affiliation:
Institute of Psychiatry and Wellcome Department of Cognitive Neurology, Institute of Neurology, London
D. A. Silbersweig
Affiliation:
Departments of Psychiatry & Neurology, Cornell Medical Centre, New York, USA
I. Wright
Affiliation:
Department of Psychological Medicine, Institute of Psychiatry
R. M. Murray
Affiliation:
Professor of Psychological Medicine, Institute of Psychiatry
R. S. J. Frackowiak
Affiliation:
Wellcome Department of Cognitive Neurology, Institute of Neurology, London
C. D. Frith
Affiliation:
Wellcome Department of Cognitive Neurology, Institute of Neurology, London
*
Dr P. K. McGuire, Department of Psychological Medicine, Institute of Psychiatry, London SE5 8AF
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Auditory verbal hallucinations are thought to arise from the disordered monitoring of inner speech (thinking in words). We tested the hypothesis that a predisposition to verbal auditory hallucinations would be associated with an abnormal pattern of brain activation during tasks which involved the generation and monitoring of inner speech.

Method

The neural correlates of tasks which engaged inner speech and auditory verbal imagery were examined using positron emission tomography in (a) schizophrenic patients with a strong predisposition to auditory verbal hallucinations (hallucinators), (b) schizophrenic patients with no history of hallucinations (nonhallucinators), and (c) normal controls.

Results

There were few between-group differences in activation during the inner speech task. However, when imagining sentences spoken in another person's voice, which entails the monitoring of inner speech, hallucinators showed reduced activation in the left middle temporal gyrus and the rostral supplementary motor area, regions which were strongly activated by both normal subjects and nonhallucinators (P<0.001). Conversely, when nonhallucinators imagined speech, they differed from both hallucinators and controls in showing reduced activation in the right parietal operculum.

Conclusions

A predisposition to verbal hallucinations in schizophrenia is associated with a failure to activate areas implicated in the normal monitoring of inner speech, whereas the absence of a history of hallucinations may be linked to reduced activation in an area concerned with verbal prosody.

Type
Papers
Information
The British Journal of Psychiatry , Volume 169 , Issue 2 , August 1996 , pp. 148 - 159
Copyright
Copyright © 1996 The Royal College of Psychiatrists 

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

Andreasen, N. C. (1986) Comprehensive Assessment of Symptoms and History. Iowa: College of Medicine, University College of Iowa.Google Scholar
Bailey, D. L., Jones, T., Friston, K. J., et al (1991) Physical validation of statistical parametric mapping. Journal of Cerebral Blood Flow and Metabolism, 11, S150.Google Scholar
Barta, P. E., Pearlson, G. D., Powers, R. E., et al (1990) Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. American Journal of Psychiatry, 39, 784–788.Google Scholar
Bub, D. & Gum, T. (1988) PsychLab Experimental Software. Montreal: McGill University.Google Scholar
Cleghorn, J. M., Franco, S., Szetchman, B., et al (1992) Towards a brain map of auditory hallucinations. American Journal of Psychiatry, 149, 1062–1069.Google Scholar
Creutzfeldt, O., Ojemann, G. & Lettich, E. (1989) Neuronal activity in the human lateral temporal lobe II. Responses to own voice. Experimental Brain Research, 77, 475–489.Google Scholar
Delisi, L., Hofp, A. L., Neale, C., et al (1994) Asymmetries in the superior temporal lobe in male and female first-episode schizophrenic patients: measures of the planum temporale and superior temporal gyrus by MRI. Schizophrenia Research, 12, 19–28.Google Scholar
Demonet, J.-F., Chollet, F., Ramsay, S., et al (1992) The anatomy of phonological and semantic processing in normal subjects. Brain, 115, 1753–1768.Google Scholar
Farah, M. J. (1984) The neural basis of mental imagery. Trends In Neurosciences, 12, 395–399.CrossRefGoogle Scholar
Frackowiak, R. S. J. & Friston, K. J. (1994) Functional anatomy of the human brain: positron emission tomography – a new neuroanatomical technique. Journal of Anatomy, 184, 211–225.Google ScholarPubMed
Friston, K. J., Passinoham, R. E., Nutt, J. G., et al (1989) Localisation in PET images: direct fitting of the intercommisural (AC-PC) line. Journal of Cerebral Blood Flow and Metabolism, 9, 690–695.Google Scholar
Friston, K. J., Frith, C. D., Liddle, P. F., et al (1990) The relationship between global and local changes in PET scans. Journal of Cerebral Blood Flow and Metabolism, 10, 458–466.Google Scholar
Frith, C. D. & Done, D. J. (1987) Towards a neuropsychology of schizophrenia. British Journal of Psychiatry, 153, 437–443.CrossRefGoogle Scholar
Frith, C. D., Friston, K. J., Herold, S., et al (1995) Regional brain activity in chronic schizophrenic patients during the performance of a verbal fluency task. British Journal of Psychiatry, 167, 343–349.CrossRefGoogle ScholarPubMed
Gasquoine, P. G. (1993) Alien hand sign. Journal of Clinical and Experimental Neuropsychology, 15, 653–667.CrossRefGoogle ScholarPubMed
Goldberg, G. (1985) Supplementary motor area structure and function: review and hypothesis. Behavioural and Brain Sciences, 8, 567–615.CrossRefGoogle Scholar
Grasby, P. M., Fletcher, P., Frith, C. D., et al (1994) Anterior cingulate rCBF responses in volunteers and schizophrenic patients. Schizophrenia Research, 11, 170.Google Scholar
Hyde, T. M., Ziegler, J. C. & Weinberger, D. R. (1992) Psychiatric disturbances in metachromatic leukodystrophy. Archives of Neurology, 49, 401–406.Google Scholar
Liddle, P. F., Friston, K. J., Frith, C. D., et al (1992) Patterns of regional cerebral blood flow in schizophrenia. British Journal of Psychiatry, 160, 179–186.Google Scholar
List, S. J. & Cleghorn, J. M. (1993) Implications of positron emission tomography research for the investigation of the actions of antipsychotic drugs. British Journal of Psychiatry, Suppl. 22, 25 30.Google Scholar
Luppino, G., Matelli, M., Camarda, R., et al (1993) Corticocortical connections of area F3 (SMA-Proper) and area F (Pre-SMA) in the macaque monkey. Journal of Comparative Neurology, 338, 114–140.Google Scholar
McGuire, P. K., Bates, J. F. & Goldman-Rakic, P. S. (1991) Interhemispheric Integration: I. Symmetry and convergence of the corticocortical connections of the left and right principal sulcus and the left and right SMA in the rhesus monkey. Cerebral Cortex, 1, 390–407.Google Scholar
McGuire, P. K., Shah, G. M. S. & Murray, R. M. (1993) Increased blood flow in Broca's area during auditory hallucinations in schizophrenia. Lancet, 342, 703–706.CrossRefGoogle ScholarPubMed
McGuire, P. K., Silbersweig, D. A., Wright, I., et al (1995) Abnormal perception of inner speech: a physiological basis for auditory hallucinations. Lancet, 346, 596–600.CrossRefGoogle ScholarPubMed
McGuire, P. K., Silbersweig, D. A., Murray, R. M., et al (1996a) Functional anatomy of inner speech and auditory verbal imagery. Psychological Medicine, 26, 29–38.CrossRefGoogle ScholarPubMed
McGuire, P. K., Silbersweig, D. A., & Frith, C. D. (1996b) Functional neuroanatomy of verbal self-monitoring. Brain (in press).Google Scholar
Maudsley, H. (1886) Natural Causes and Supernatural Seemings. London: Kegan Paul, Trench & Co.Google Scholar
Mintun, M. A., Fox, P. T. & Raichle, M. E. (1989) A highly accurate method of localising regions of neuronal activation in the human brain with positron emission tomography. Journal of Cerebral Blood Flow and Metabolism, 9, 96–103.Google Scholar
Muller-Preuss, P., Newman, J. D. & Jurgens, U. (1980) Anatomical and physiological evidence for a relationship between the angular vocalisation area and the auditory cortex in the squirrel monkey. Brain Research, 202, 307–315.Google Scholar
Muller-Preuss, P., & Ploog, D. (1981) Inhibition of cortical neurons during phonation. Brain Research, 215, 61–76.Google Scholar
Murray, R. M., O'Callaghan, E. O., Castle, D. J., et al (1992) A neurodevelopmental approach to the classification of schizophrenia. Schizophrenia Research, 18, 319–332.Google Scholar
Musalek, M., Podreka, I., Walter, H., et al (1989) Regional brain function in hallucinations: a study of regional cerebral blood flow with 99m-Tc-SPECT in patients with auditory hallucinations, tactile hallucinations and normal controls. Comprehensive Psychiatry, 30, 99–108.Google Scholar
Nayani, T. H. & David, A. S. (1996) The auditory hallucination: a phenomenological survey. Psychological Medicine, 26, 177–195.CrossRefGoogle ScholarPubMed
Nelson, H. A. & O'Connell, A. (1978) Dementia: the estimation of premorbid intelligence levels using the New Adult Reading Test Cortex, 14, 234–244.CrossRefGoogle ScholarPubMed
Pandya, D. N. & Yeterian, E. H. (1985) Architecture and connections of cortical association areas. In Cerebral Cortex, Vol. 4 (eds Peters, A. & Jones, E. G.), pp. 3–61. New York: Plenum.Google Scholar
Paulesu, E., Frith, C. D. & Frackowiak, R. S. J. (1993) The neural correlates of the verbal component of working memory. Nature, 362, 342–344.Google Scholar
Price, C., Wise, R., Watson, J. D. G., et al (1994) Brain activity during reading: the effects of exposure duration and task. Brain, 117, 1255–1270.CrossRefGoogle ScholarPubMed
Price, C., Wise, R., Warburton, E., et al (1996) Hearing & Saying: The functional neuro-anatomy of auditory word processing. Brain (in press).CrossRefGoogle Scholar
Raichle, M. E., Fiez, J. A., Videen, T. O., et al (1994) Practice-related changes in human brain functional anatomy during nonmotor learning. Cerberal Cortex, 4, 8–26.Google Scholar
Ross, R. A. (1990) A software system for interactive and quantitative analysis of biomedical images. In 3D Imaging in Medicine, Vol. F 60. (eds Hohne, K. H., Fuchs, H. & Pizer, S. M.). NATO ASI Series.Google Scholar
Roberts, G. W. (1991) Schizophrenia: a neuropathological perspective. British Journal of Psychiatry, 158, 8–17.Google Scholar
Ross, E. D. & Mesulam, M.-M. (1981) The aprosodias: functional-anatomic organisation of the affective components of language in the right hemisphere. Archives of Neurology, 36, 144–148.CrossRefGoogle Scholar
Silbersweig, D. A., Stern, E., Frith, C., et al (1995) A functional anatomy of hallucinations in schizophrenia. Nature, 378, 176–179.Google Scholar
Smith, J. D., Reisberg, D. & Wilson, M. (1992) Subvocalisation & auditory imagery: interactions between the inner ear and inner voice. In Auditory Imagery (ed. Reisberg, D.), pp. 95–120. New Jersey: Lawrence Erlbaum Associates.Google Scholar
Talairach, J. & Tournoux, P. (1988) Co-planar Stereotaxic Atlas of the Human Brain. Stuttgart Thieme Verlag.Google Scholar
Warburton, E., Wise, R. S. J., Price, C. J., et al (1996) Noun and verb retrieval by normal subjects: studies with positron emission tomography. Brain, 119, 159–180.Google Scholar
Wise, R., Chollet, F., Hadar, U., et al (1991) Distribution of cortical neural networks involved in word comprehension and word retrieval. Brain, 114, 1803–1817.CrossRefGoogle ScholarPubMed
Woods, R. P., Cherry, S. R. & Mazziotta, J. C. (1992) A rapid automated algorithm for accurately aligning and reslicing positron emission tomography images. Journal of Computer Assisted Tomography, 16, 620–633.Google Scholar
Zatorre, R. J., Evans, A. C., Meyer, E., et al (1992) Lateralisation in phonetic and pitch discrimination in speech processing. Science, 256, 846–849.Google Scholar
Submit a response

eLetters

No eLetters have been published for this article.