19 - Disorders of self-monitoring and the symptoms of schizophrenia  pp. 407-424

Disorders of self-monitoring and the symptoms of schizophrenia

By Sarah-Jayne Blakemore

Image View Previous Chapter Next Chapter


In this chapter we attempt to explain one class of symptoms associated with schizophrenia. We concentrate on symptoms that are characterized by a confusion between the self and other, such as auditory hallucinations and delusions of control. We propose that such symptoms arise because of a failure in the mechanism by which the predicted consequences of self-produced actions are derived from an internal forward model. Normally the forward model predicts and cancels the sensory consequences of self-produced actions. We argue that an impairment in this prediction and cancellation mechanism can cause self-produced sensations to be classified as externally produced. This problem leads to a number of behavioural consequences, such as a lack of central error correction, many of which have been observed in patients with delusions of control and related symptoms. At the physiological level, delusions of control are associated with overactivity in the parietal cortex. We suggest that this overactivity results from a failure to attenuate responses to sensations of limb movements even though these sensations can be anticipated on the basis of the movements intended. The lack of attenuation may arise from corticocortical disconnections which prevent inhibitory signals arising in the frontal areas which generate motor commands from reaching the appropriate sensory areas.


Auditory hallucinations and passivity symptoms in schizophrenia

Rather than attempting to elucidate a biological basis for schizophrenia, our aim in this chapter is to try and explain one class of symptoms.

Andersson, G. & Armstrong, D. M. (1985). Climbing fibre input to b zone Purkinje cells during locomotor perturbation in the cat. Neuroscience Letters Supplement, 22, S27
Andersson, G. & Armstrong, D. M. (1987). Complex spikes in Purkinje cells in the lateral vermis of the cat cerebellum during locomotion. Journal of Physiology (London), 385, 107–34
Angel, R. W. & Malenka, R. C. (1982). Velocity-dependent suppression of cutaneous sensitivity during movement. Experimental Neurology, 77, 266–74
Barresi, J. & Moore, C. (1996). Intentional relations and social understanding. Behaviour and Brain Science, 19, 107–54
Bentall, R. P., Baker, G. A. & Havers, S. (1991). Reality monitoring and psychotic hallucinations. British Journal of Clinical Psychology, 30, 213–22
Bick, P. A. & Kinsbourne, M. (1987). Auditory hallucinations and subvocal speech in schizophrenic patients. American Journal of Psychiatry, 144, 222–5
Blakemore, S.-J., Frith, C. D. & Wolpert, D. W. (1999a). Spatiotemporal prediction modulates the perception of self-produced stimuli. Journal of Cognitive Neuroscience, 11, 551–9
Blakemore, S.-J., Frith, C. D. & Wolpert, D. W. (2001). The cerebellum is involved in predicting the sensory consequences of action. NeuroReport, 12, 1879–85
Blakemore, S.-J., Smith, J., Steel, R., Johnstone, E. & Frith, C. D. (2000). The perception of self-produced sensory stimuli in patients with auditory hallucinations and passivity experiences: evidence for a breakdown in self-monitoring. Psychological Medicine, 30, 1131–9
Blakemore, S.-J., Wolpert, D. M. & Frith, C. D. (1998). Central cancellation of self-produced tickle sensation. Nature Neuroscience, 1, 635–40
Blakemore, S.-J., Wolpert, D. M. & Frith, C. D. (1999b). The cerebellum contributes to somatosensory cortical activity during self-produced tactile stimulation. NeuroImage, 10, 448–59
Cahill, C., Silbersweig, D. & Frith, C. D. (1996). Psychotic experiences induced in deluded patients using distorted auditory feedback. Cognitive Neuropsychiatry, 1, 201–11
Chapin, J. K. & Woodward, D. J. (1982). Somatic sensory transmission to the cortex during movement: gating of single cell responses to touch. Experimental Neurology, 78, 654–69
Chapman, C. E. & Ageranioti-Belanger, S. A. (1991). Comparison of the discharge of primary somatosensory cortical (SI) neurones during active and passive tactile discrimination. Proceedings of the Third IBRO World Congress of Neuroscience, p. 317. Oxford: Pergamon
Chapman, C. E. (1994). Active versus passive touch: factors influencing the transmission of somatosensory signals to primary somatosensory cortex. Canadian Journal of Physiology and Pharmacology, 72, 558–70
Chapman, C. E., Bushnell, M. C., Miron, D., Duncan, G. H. & Lund, J. P. (1987). Sensory perception during movement in man. Experimental Brain Research, 68, 516–24
Claxton, G. (1975). Why can't we tickle ourselves? Perceptual and Motor Skills, 41, 335–8
Collins, D. F., Cameron, T., Gillard, D. M. & Prochazka, A. (1998). Muscular sense is attenuated when humans move. Journal of Physiology, 508, 635–43
Daprati, E., Franck, N., Georgieff, N. et al. (1997). Looking for the agent: an investigation into consciousness of action and self-consciousness in schizophrenic patients. Cognition, 65, 71–86
Decety, J. (1996). Neural representation for action. Reviews in the Neurosciences, 7, 285–97
Dolan, R. J., Fletcher, P., Frith, C. D. et al. (1995). Dopaminergic modulation of an impaired cognitive activation in the anterior cingulate cortex in schizophrenia. Nature, 378, 180–3
Ebmeier, K. P., Steele, J. D., MacKenzie, D. M. et al. (1995). Cognitive brain potentials and regional cerebral blood flow equivalents during two- and three-sound auditory ‘oddball tasks’. Electroencephalography and Clinical Neurophysiology, 95, 434–43
Feinberg, I. (1978). Efference copy and corollary discharge: implications for thinking and its disorders. Schizophrenia Bulletin, 4, 636–40
Franck, N., Rouby, P., Daprati, E. et al. (2000). Confusion between silent and overt reading in schizophrenia. Schizophrenia Research, 41, 357–64
Frith, C. D. & Done, D. J. (1989). Experiences of alien control in schizophrenia reflect a disorder in the central monitoring of action. Psychological Medicine, 19, 359–63
Frith, C. D. & Frith, U. (1999). Interacting minds – a biological basis. Science, 286, 1692–5
Frith, C. D. (1987). The positive and negative symptoms of schizophrenia reflect impairments in the perception and initiation of action. Psychological medicine, 17, 631–48
Frith, C. D. (1992). The Cognitive Neuropsychology of Schizophrenia. Hove, Sussex: Lawrence Erlbaum Associates
Frith, C. D. (1995). Consciousness is for other people. Behavioural and Brain Sciences, 18, 682–3
Frith, C. D., Blakemore, S.-J. & Wolpert, D. M. (2000a). Explaining the symptoms of schizophrenia: abnormalities in the awareness of action. Brain Research Reviews, 31, 357–63
Frith, C. D., Blakemore, S.-J. & Wolpert, D. M. (2000b). Abnormalities in the awareness and control of action. Philosophical Transactions of the Royal Society of London: Biological Sciences, 355, 1771–88
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, 343–9
Gellman, R., Gibson, A. R. & Houk, J. C. (1985). Inferior olivary neurons in the awake cat: detection of contact and passive body displacement. Journal of Neurophysiology, 54, 40–60
Gould, L. N. (1949). Auditory hallucinations and subvocal speech. Journal of Nervous and Mental Disease, 109, 418–27
Green, P. & Preston, M. (1981). Reinforcement of vocal correlates of auditory hallucinations by auditory feedback: a case study. British Journal of Psychiatry, 139, 204–8
Hoffman, R. E. (1986). Verbal hallucinations and language production processes in schizophrenia. Behavioral and Brain Sciences, 9, 503–17
Hughlings Jackson, J. (1932). Selected Writings of John Hughlings Jackson. London: Hodder & Stoughton
Imamizu, H., Miyauchi, S., Tamada, T. et al. (2000). Human cerebellar activity reflecting an acquired internal model of a new tool. Nature, 403, 192–5
Ito, M. (1970). Neurophysiological aspects of the cerebellar motor control system. International Journal of Neurology, 7, 162–76
Jeannerod, M. (1988). The Neural and Behaviourial Organisation of Goal-directed Movements. Oxford: OUP
Jeannerod, M. (1994). The representing brain – neural correlates of motor intention and imagery. Behavioral and Brain Sciences, 17, 187–202
Jeannerod, M. (1997). The Cognitive Neuropsychology of Action. Cambridge: Blackwell
Jeannerod, M. (1999). To act or not to act: perspectives on the representation of actions. Quarterly Journal of Experimental Psychology A, 52, 981–1020
Jiang, W., Chapman, C. E. & Lamarre, Y. (1991). Modulation of the cutaneous responsiveness of neurones in the primary somatosensory cortex during conditioned arm movements in the monkey. Experimental Brain Research, 84, 342–54
Johns, L. C. & McGuire, P. K. (1999). Verbal self-monitoring and auditory hallucinations in schizophrenia. Lancet, 353, 469–70
Johns, L. C., Rossell, S., Frith, C. et al. (2001). Verbal self-monitoring and auditory verbal hallucinations in patients with schizophrenia. Psychological Medicine, 31, 705–15
Johnstone, E. C. (1991). Defining characteristics of schizophrenia. British Journal of Psychiatry, 13, (suppl.) 5–6
Kay, S., Fiszbein, A. & Opler, L. (1987). The positive and negative symptom scale for schizophrenia. Schizophrenia Bulletin, 13, 261–76
Lane, R. D., Fink, G. R., Chua, P. M. & Dolan, R. J. (1997). Neural activation during selective attention to subjective emotional responses. Neuroreport, 8, 3969–72
Locke, J. (1690). Essay Concerning Human Understanding, II.VI.2. Oxford: Clarendon Press (reprinted 1989)
Malenka, R. C., Angel, R. W., Hampton, B. & Berger, P. A. (1982). Impaired central error-correcting behavior in schizophrenia. Archives of General Psychiatry, 39, 101–7
McGuire, P. K. & Frith, C. D. (1996). Disordered functional connectivity in schizophrenia. Psychological Medicine, 26, 663–7
Mellors, C. S. (1970). First-rank symptoms of schizophrenia. British Journal of Psychiatry, 117, 15–23
Miall, R. C., Weir, D. J., Wolpert, D. M. & Stein, J. F. (1993). Is the cerebellum a Smith predictor? Journal of Motor Behaviour, 25, 203–16
Milne, R. J., Aniss, A. M., Kay, N. E. & Gandevia, S. C. (1988). Reduction in perceived intensity of cutaneous stimuli during movement: a quantitative study. Experimental Brain Research, 70, 569–76
Mlakar, J., Jensterle, J. & Frith, C. D. (1994). Central monitoring deficiency and schizophrenic symptoms. Psychological Medicine, 24, 557–64
Oscarsson, O. (1980). Functional organization of olivary projection to the cerebellar anterior lobe. In The Inferior Olivary Nucleus: Anatomy and Physiology, ed. J. Courville, C. DeMontigny & Y. Lamarre. New York: Raven Press
Paulin, M. G. (1989). A Kalman filter theory of the cerebellum. In Dynamic Interactions in Neural Networks: Models and Data, ed. E. M. A. Arbib & E. S. Amari, pp. 241–59. Berlin: Springer-Verlag
Porrino, L. J. (1993). Functional consequences of acute cocaine treatment depend on route of administration. Psychopharmacology Berlin, 112, 343–51
Schneider, K. (1959). Clinical Psychopathology. New York: Grune & Stratton
Simpson, J. L., Wylie, D. R. & De Zeeuw, C. I. (1995). On climbing fiber signals and their consequence(s). Behavioural and Brain Sciences, 19, 384
Spence, S. A. (1996). Free will in the light of neuropsychiatry. Philosophy, Psychiatry and Psychology, 3, 75–90
Spence, S. A., Brooks, D. J., Hirsch, S. R. et al. (1997). A PET study of voluntary movement in schizophrenic patients experiencing passivity phenomena (delusions of alien control). Brain, 120, 1997–2011
Spence, S. A., Hirsch, S. R., Brooks, D. J. & Grasby, P. M. (1998). Prefrontal cortex activity in people with schizophrenia and control subjects. Evidence from positron emission tomography for remission of ‘hypofrontality’ with recovery from acute schizophrenia. British Journal of Psychiatry, 172, 316–23
Sperry, R. W. (1950). Neural basis of spontaneous optokinetic responses produced by visual inversion. Journal of Comparative Physiological Psychology, 43, 483–9
Stirling, J. D., Hellewell, J. S. E. & Quraishi, N. (1998). Self-monitoring dysfunction and the schizophrenic symptoms of alien control. Psychological Medicine, 28, 675–83
Vogt, B. A., & Gabriel, M. (eds) (1993). Neurobiology of Cingulate Cortex and Limbic Thalamus. Boston: Birkauser
Vogt, B. A., Finch, D. M. & Olson, C. R. (1992). Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cerebral Cortex, 2, 435–43
Von Helmholtz, H. (1867). Handbuch der Physiologischen Optik, 1st edn. Hamburg, Germany: Voss
Von Holst, E. (1954). Relations between the central nervous system and the peripheral organs. British Journal of Animal Behaviour, 2, 89–94
Watson, J. B. (1914). Behavior: An Introduction to Comparative Psychology. New York: Holt
Weiller, C., Juptner, M., Fellows, S. et al. (1996). Brain representation of active and passive movement. NeuroImage, 4, 105–10
Weiskrantz, L., Elliot, J. & Darlington, C. (1971). Preliminary observations of tickling oneself. Nature, 230, 598–9
Wing, J. K., Cooper, J. E. & Sartorius, N. (1974). Description and Classification of Psychiatric Symptoms. London: Cambridge University Press
Wolpert, D. M. (1997). Computational approaches to motor control. Trends in Cognitive Sciences, 1, 209–16
Wolpert, D. M., Ghahramani, Z. & Flanagan, R. (2001). Perspectives and problems in motor learning. Trends in Cognitive Sciences, 5, 487–94
Wolpert, D. M., Ghahramani, Z. & Jordan, M. I. (1995). An internal model for sensorimotor integration. Science, 269, 1880–2
Wolpert, D. M., Miall, R. C. & Kawato, M. (1998). Internal models in the cerebellum. Trends in Cognitive Sciences, 2, 338–47
Zahavi, D. (ed.) (2000). Advances in Consciousness Research. Amsterdam: John Benjamins