Skip to main content
×
×
Home

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

  • P. K. McGuire (a1), D. A. Silbersweig (a2), I. Wright (a3), R. M. Murray (a4), R. S. J. Frackowiak (a5) and C. D. Frith (a5)...
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.

Copyright
Corresponding author
Dr P. K. McGuire, Department of Psychological Medicine, Institute of Psychiatry, London SE5 8AF
References
Hide All
Andreasen, N. C. (1986) Comprehensive Assessment of Symptoms and History. Iowa: College of Medicine, University College of Iowa.
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.
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, 784788.
Bub, D. & Gum, T. (1988) PsychLab Experimental Software. Montreal: McGill University.
Cleghorn, J. M., Franco, S., Szetchman, B., et al (1992) Towards a brain map of auditory hallucinations. American Journal of Psychiatry, 149, 10621069.
Creutzfeldt, O., Ojemann, G. & Lettich, E. (1989) Neuronal activity in the human lateral temporal lobe II. Responses to own voice. Experimental Brain Research, 77, 475489.
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, 1928.
Demonet, J.-F., Chollet, F., Ramsay, S., et al (1992) The anatomy of phonological and semantic processing in normal subjects. Brain, 115, 17531768.
Farah, M. J. (1984) The neural basis of mental imagery. Trends In Neurosciences, 12, 395399.
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, 211225.
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, 690695.
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, 458466.
Frith, C. D. & Done, D. J. (1987) Towards a neuropsychology of schizophrenia. British Journal of Psychiatry, 153, 437443.
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, 343349.
Gasquoine, P. G. (1993) Alien hand sign. Journal of Clinical and Experimental Neuropsychology, 15, 653667.
Goldberg, G. (1985) Supplementary motor area structure and function: review and hypothesis. Behavioural and Brain Sciences, 8, 567615.
Grasby, P. M., Fletcher, P., Frith, C. D., et al (1994) Anterior cingulate rCBF responses in volunteers and schizophrenic patients. Schizophrenia Research, 11, 170.
Hyde, T. M., Ziegler, J. C. & Weinberger, D. R. (1992) Psychiatric disturbances in metachromatic leukodystrophy. Archives of Neurology, 49, 401406.
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, 179186.
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.
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, 114140.
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, 390407.
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, 703706.
McGuire, P. K., Silbersweig, D. A., Wright, I., et al (1995) Abnormal perception of inner speech: a physiological basis for auditory hallucinations. Lancet, 346, 596600.
McGuire, P. K., Silbersweig, D. A., Murray, R. M., et al (1996a) Functional anatomy of inner speech and auditory verbal imagery. Psychological Medicine, 26, 2938.
McGuire, P. K., Silbersweig, D. A., & Frith, C. D. (1996b) Functional neuroanatomy of verbal self-monitoring. Brain (in press).
Maudsley, H. (1886) Natural Causes and Supernatural Seemings. London: Kegan Paul, Trench & Co.
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, 96103.
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, 307315.
Muller-Preuss, P., & Ploog, D. (1981) Inhibition of cortical neurons during phonation. Brain Research, 215, 6176.
Murray, R. M., O'Callaghan, E. O., Castle, D. J., et al (1992) A neurodevelopmental approach to the classification of schizophrenia. Schizophrenia Research, 18, 319332.
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, 99108.
Nayani, T. H. & David, A. S. (1996) The auditory hallucination: a phenomenological survey. Psychological Medicine, 26, 177195.
Nelson, H. A. & O'Connell, A. (1978) Dementia: the estimation of premorbid intelligence levels using the New Adult Reading Test Cortex, 14, 234244.
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. 361. New York: Plenum.
Paulesu, E., Frith, C. D. & Frackowiak, R. S. J. (1993) The neural correlates of the verbal component of working memory. Nature, 362, 342344.
Price, C., Wise, R., Watson, J. D. G., et al (1994) Brain activity during reading: the effects of exposure duration and task. Brain, 117, 12551270.
Price, C., Wise, R., Warburton, E., et al (1996) Hearing & Saying: The functional neuro-anatomy of auditory word processing. Brain (in press).
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, 826.
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.
Roberts, G. W. (1991) Schizophrenia: a neuropathological perspective. British Journal of Psychiatry, 158, 817.
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, 144148.
Silbersweig, D. A., Stern, E., Frith, C., et al (1995) A functional anatomy of hallucinations in schizophrenia. Nature, 378, 176179.
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. 95120. New Jersey: Lawrence Erlbaum Associates.
Talairach, J. & Tournoux, P. (1988) Co-planar Stereotaxic Atlas of the Human Brain. Stuttgart Thieme Verlag.
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, 159180.
Wise, R., Chollet, F., Hadar, U., et al (1991) Distribution of cortical neural networks involved in word comprehension and word retrieval. Brain, 114, 18031817.
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, 620633.
Zatorre, R. J., Evans, A. C., Meyer, E., et al (1992) Lateralisation in phonetic and pitch discrimination in speech processing. Science, 256, 846849.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

The British Journal of Psychiatry
  • ISSN: 0007-1250
  • EISSN: 1472-1465
  • URL: /core/journals/the-british-journal-of-psychiatry
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 33 *
Loading metrics...

Abstract views

Total abstract views: 163 *
Loading metrics...

* Views captured on Cambridge Core between 2nd January 2018 - 16th August 2018. This data will be updated every 24 hours.

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

  • P. K. McGuire (a1), D. A. Silbersweig (a2), I. Wright (a3), R. M. Murray (a4), R. S. J. Frackowiak (a5) and C. D. Frith (a5)...
Submit a response

eLetters

No eLetters have been published for this article.

×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *