Review

Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia

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Abstract

Advances in cognitive neuroscience offer us new ways to understand the symptoms of mental illness by uniting basic neurochemical and neurophysiological observations with the conscious experiences that characterize these symptoms. Cognitive theories about the positive symptoms of schizophrenia — hallucinations and delusions — have tended to treat perception and belief formation as distinct processes. However, recent advances in computational neuroscience have led us to consider the unusual perceptual experiences of patients and their sometimes bizarre beliefs as part of the same core abnormality — a disturbance in error-dependent updating of inferences and beliefs about the world. We suggest that it is possible to understand these symptoms in terms of a disturbed hierarchical Bayesian framework, without recourse to separate considerations of experience and belief.

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References

  1. 1.

    , , & Schizophrenia: a concise overview of incidence, prevalence, and mortality. Epidemiol. Rev. 30, 67–76 (2008).

  2. 2.

    Molecular pathology of schizophrenia: more than one disease process? BMJ 280, 66–68 (1980). An influential paper that made the distinction between positive and negative symptoms.

  3. 3.

    Schizophrenic syndromes, cognitive performance and neurological dysfunction. Psychol. Med. 17, 49–57 (1987). An empirical demonstration that the signs and symptoms of schizophrenia should be described in terms of three dimensions: psychomotor poverty, disorganization and reality distortion (hallucinations and delusions).

  4. 4.

    General Psychopathology (Manchester Univ. Press, Manchester, 1962). The author of this book claimed that positive symptoms were 'not understandable'. We disagree.

  5. 5.

    Editorial: in praise of cognitive neuropsychiatry. Cognit. Neuropsychiatry 13, 1–7 (2008).

  6. 6.

    , , & Reasoning and delusions. Br. J. Psychiatry 170, 398–405 (1997).

  7. 7.

    Clinical Psychopathology (Grune & Stratton, New York, 1959). An influential attempt to list symptoms specific to schizophrenia.

  8. 8.

    , & (eds) Diagnosis and Clinical Measurement in Psychiatry. A Reference Manual for SCAN (Cambridge Univ. Press, Cambridge, UK, 1998).

  9. 9.

    Delusional thinking and perceptual disorder. J. Individ. Psychol. 30, 98–113 (1974). The original proposal that delusions are caused by anomalous perceptual experiences.

  10. 10.

    Consciousness, information processing and schizophrenia. Br. J. Psychiatry 134, 225–235 (1979). This paper used the term consciousness when doing so was neither popular nor profitable.

  11. 11.

    A simple (or simplistic?) cognitive model for schizophrenia. Behav. Res. Ther. 31, 633–645 (1993).

  12. 12.

    Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. Am. J. Psychiatry 160, 13–23 (2003). An influential synthesis of ideas concerning the role of dopamine in the generation of positive symptoms.

  13. 13.

    Efference copy and corollary discharge: implications for thinking and its disorders. Schizophr. Bull. 4, 636–640 (1978). The original proposal that positive symptoms, in particular thought insertion, might be caused by a problem with corollary discharge.

  14. 14.

    Handbuch der Physiologischen Optik (Voss, Leipzig, 1866). A work of genius that suggested, among many other things, that perception depends on inference.

  15. 15.

    , , , & Disorders of agency in schizophrenia correlate with an inability to compensate for the sensory consequences of actions. Curr. Biol. 15, 1119–1124 (2005).

  16. 16.

    , & Abnormalities in the awareness of action. Trends Cogn. Sci. 6, 237–242 (2002).

  17. 17.

    , & Inner speech models of auditory verbal hallucinations: evidence from behavioural and neuroimaging studies. Int. Rev. Psychiatry 19, 407–415 (2007).

  18. 18.

    & Reinforcement of vocal correlates of auditory hallucinations by auditory feedback: a case study. Br. J. Psychiatry 139, 204–208 (1981).

  19. 19.

    Auditory hallucinations and subvocal speech. J. Nerv. Ment. Dis. 109, 418–427 (1949). The first demonstration that hallucinations can be associated with the patient's own speech.

  20. 20.

    & Vocal activity in verbal hallucinations. J. Psychiatr. Res. 21, 101–109 (1987).

  21. 21.

    & Subvocal activity and auditory hallucinations: clues for behavioral treatments? Schizophr. Bull. 16, 617–625 (1990).

  22. 22.

    Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Cogn. Neurosci. 43, 482–489 (1950).

  23. 23.

    & Das reafferenzprinzip (Wechselwirkungen zwischen Zentralnervensystem und Peripherie). Naturwissenshaften 37, 464–476 (1950).

  24. 24.

    & Corollary discharge across the animal kingdom. Nature Rev. Neurosci. 9, 587–600 (2008).

  25. 25.

    , , , & The perception of self-produced sensory stimuli in patients with auditory hallucinations and passivity experiences: evidence for a breakdown in self-monitoring. Psychol. Med. 30, 1131–1139 (2000). A demonstration that patients with schizophrenia can tickle themselves.

  26. 26.

    , , , & Evidence for sensory prediction deficits in schizophrenia. Am. J. Psychiatry 162, 2384–2386 (2005).

  27. 27.

    & Electrophysiological evidence of corollary discharge dysfunction in schizophrenia during talking and thinking. J. Psychiatr. Res. 38, 37–46 (2004).

  28. 28.

    & Brain circuits for the internal monitoring of movements. Annu. Rev. Neurosci. 31, 317–338 (2008).

  29. 29.

    & Can neuroscience explain consciousness? J. Conscious. Stud. 11, 180–198 (2004). An attempt to forge a link between neural processes and subjective experience.

  30. 30.

    When did Bayesian inference become “Bayesian”? Bayesian Anal. 1, 1–40 (2006).

  31. 31.

    & The formation and maintenance of delusions: a Bayesian analysis. Br. J. Psychiatry 149, 51–56 (1986). An influential demonstration that patients with delusions have problems with probabilistic inferences.

  32. 32.

    , , , & A cognitive model of persecutory delusions. Br. J. Clin. Psychol. 41, 331–347 (2002).

  33. 33.

    , & Reasoning in deluded schizophrenic and paranoid patients. Biases in performance on a probabilistic inference task. J. Nerv. Ment. Dis. 179, 194–201 (1991).

  34. 34.

    , & Paranoia and social reasoning: an attribution theory analysis. Br. J. Clin. Psychol. 30, 13–23 (1991).

  35. 35.

    Reasoning and delusion proneness - confidence in decisions. J. Nerv. Ment. Dis. 196, 9–15 (2008).

  36. 36.

    , , & Belief inflexibility in schizophrenia. Cognit. Neuropsychiatry 13, 267–277 (2008).

  37. 37.

    , & Decision-making impairments in the context of intact reward sensitivity in schizophrenia. Biol. Psychiatry 64, 62–69 (2008).

  38. 38.

    Cognitive neuropsychiatry and delusional belief. Q. J. Exp. Psychol. (Colchester) 60, 1041–1062 (2007). A persuasive demonstration that perceptual anomalies are not sufficient to cause delusions.

  39. 39.

    , & Schizophrenia and monothematic delusions. Schizophr. Bull. 33, 642–647 (2007).

  40. 40.

    , , & Confabulation: damage to a specific inferior medial prefrontal system. Cortex 44, 637–648 (2008).

  41. 41.

    , & Psychotic experiences induced in deluded patients using distorted auditory feedback. Cogn. Neuropsychiatry 1, 201–211 (1996).

  42. 42.

    , & Delusions of alien control in the normal brain. Neuropsychologia 41, 1058–1067 (2003).

  43. 43.

    , , & Two eyes for an eye: the neuroscience of force escalation. Science 301, 187–187 (2003).

  44. 44.

    , , & Fine-tuning of auditory cortex during speech production. Psychophysiology 42, 180–190 (2005).

  45. 45.

    , , , & Speaking modifies voice-evoked activity in the human auditory cortex. Hum. Brain Mapp. 9, 183–191 (2000).

  46. 46.

    , , & Modulation of the auditory cortex during speech: an MEG study. J. Cogn. Neurosci. 14, 1125–1138 (2002).

  47. 47.

    , & Suppressed responses to self-triggered sounds in the human auditory cortex. Cereb. Cortex 15, 299–302 (2005).

  48. 48.

    , , , & Dissecting corollary discharge dysfunction in schizophrenia. Psychophysiology 44, 522–529 (2007).

  49. 49.

    , & Increased blood flow in Broca's area during auditory hallucinations in schizophrenia. Lancet 342, 703–706 (1993). An early demonstration that hallucinations are associated with activity in speech-production regions of the brain.

  50. 50.

    , , , & Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Arch. Gen. Psychiatry 57, 1033–1038 (2000).

  51. 51.

    , , , & Functional anatomy of auditory verbal imagery in schizophrenic patients with auditory hallucinations. Am. J. Psychiatry 157, 1691–1693 (2000).

  52. 52.

    et al. Cortical responsiveness during talking and listening in schizophrenia: an event-related brain potential study. Biol. Psychiatry 50, 540–549 (2001).

  53. 53.

    , , , & Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Arch. Gen. Psychiatry 57, 1033–1038 (2000).

  54. 54.

    et al. Modality specific neural correlates of auditory and somatic hallucinations. J. Neurol. Neurosurg. Psychiatry 71, 688–690 (2001).

  55. 55.

    et al. Temporal course of auditory hallucinations. Br. J. Psychiatry 185, 516–517 (2004).

  56. 56.

    , , , & The functional anatomy of auditory hallucinations in schizophrenia. Psychiatry Res. 100, 13–20 (2000).

  57. 57.

    , , & Synch before you speak: auditory hallucinations in schizophrenia. Am. J. Psychiatry 164, 458–466 (2007). Evidence that hallucinations are associated with a reduction of long-range connectivity in the brain.

  58. 58.

    et al. A review of diffusion tensor imaging studies in schizophrenia. J. Psychiatr. Res. 41, 15–30 (2007).

  59. 59.

    et al. Misattribution of speech and impaired connectivity in patients with auditory verbal hallucinations. Hum. Brain Mapp. 28, 1213–1222 (2007). Structural evidence for connectivity problems in schizophrenia.

  60. 60.

    The exploitation of regularities in the environment by the brain. Behav. Brain. Sci. 24, 602–607; discussion 652–671 (2001).

  61. 61.

    An essay towards solving a problem in the doctrine of chances. Philos. Trans. R. Soc. Lond. 53, 370–418 (1763). A work of genius providing the computational basis for the process of inference that underlies perception and belief formation.

  62. 62.

    Latent inhibition. Psychol. Bull. 79, 398–407 (1973).

  63. 63.

    Conditions for versatile learning, Helmholtz's unconscious inference, and the task of perception. Vision Res. 30, 1561–1571 (1990). An important proposal about the mechanism of inference in the visual system.

  64. 64.

    & Vision as Bayesian inference: analysis by synthesis? Trends Cogn. Sci. 10, 301–308 (2006). Review of the evidence that vision depends on inference.

  65. 65.

    et al. Latent inhibition and schizophrenia: Pavlovian conditioning of autonomic responses. Schizophr. Res. 55, 147–158 (2002).

  66. 66.

    in Punishment and Aversive Behaviour (eds Campbell, B. A. & Church, R. M.) 279–296 (Appleton Century Crofts, New York, 1969).

  67. 67.

    & in Classical Conditioning II (eds Black, A. H. & Prokasy, W. F.) 64–99 (Appleton Century Crofts, New York, 1972). The computational basis of learning by association.

  68. 68.

    & Neuronal coding of prediction errors. Annu. Rev. Neurosci. 23, 473–500 (2000). An important account of the role of prediction errors in learning.

  69. 69.

    , , & Disruption of the Kamin blocking effect in schizophrenia and in normal subjects following amphetamine. Behav. Brain Res. 88, 103–114 (1997).

  70. 70.

    & Dopamine neurons report an error in the temporal prediction of reward during learning. Nature Neurosci. 1, 304–309 (1998).

  71. 71.

    & Importance of unpredictability for reward responses in primate dopamine neurons. J. Neurophysiol. 72, 1024–1027 (1994).

  72. 72.

    , & Dopamine responses comply with basic assumptions of formal learning theory. Nature 412, 43–48 (2001).

  73. 73.

    , , , & Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442, 1042–1045 (2006).

  74. 74.

    et al. Dysfunction of ventral striatal reward prediction in schizophrenia. Neuroimage 29, 409–416 (2006).

  75. 75.

    et al. Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol. Psychiatry 13, 267–276 (2007). Evidence of abnormal neural correlates of prediction errors in schizophrenia.

  76. 76.

    et al. Disrupted prediction error signal in psychosis: evidence for an associative account of delusions. Brain 130, 2387–2400 (2007).

  77. 77.

    et al. The formation of abnormal associations in schizophrenia: neural and behavioral evidence. Neuropsychopharmacology 33, 473–479 (2008).

  78. 78.

    et al. Pathological gambling caused by drugs used to treat Parkinson disease. Arch. Neurol. 62, 1377–1381 (2005).

  79. 79.

    , & A free energy principle for the brain. J. Physiol. (Paris) 100, 70–87 (2006). An important proposal that the brain consists of a hierarchy of Bayesian inferencing devices.

  80. 80.

    , , , & Shape perception reduces activity in human primary visual cortex. Proc. Natl Acad. Sci. USA 99, 15164–15169 (2002).

  81. 81.

    & Hierarchical Bayesian inference in the visual cortex. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 20, 1434–1448 (2003).

  82. 82.

    & A neural representation of prior information during perceptual inference. Neuron 59, 336–347 (2008).

  83. 83.

    A theory of attention: variations in associability of stimuli with reinforcement. Psychol. Rev. 82, 276–298 (1975).

  84. 84.

    & A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychol. Rev. 87, 532–552 (1980).

  85. 85.

    , & Bayesian theories of conditioning in a changing world. Trends Cogn. Sci. 10, 294–300 (2006).

  86. 86.

    Schizophrenic psychology, associative learning and the role of forebrain dopamine. Med. Hypotheses 2, 203–211 (1976).

  87. 87.

    The development of a cognitive model of schizophrenia: placing it in context. Neurosci. Biobehav. Rev. 29, 977–988 (2005).

  88. 88.

    & Parsing reward. Trends Neurosci. 26, 507–513 (2003).

  89. 89.

    et al. Incentive motivation in first-episode psychosis: a behavioural study. BMC Psychiatry 8, 34 (2008).

  90. 90.

    et al. Do patients with schizophrenia exhibit aberrant salience? Psychol. Med. 2008 06 30 (doi:10.1017/S0033291708003863).

  91. 91.

    & Uncertainty, neuromodulation, and attention. Neuron 46, 681–692 (2005).

  92. 92.

    , & Weak suppression of visual context in chronic schizophrenia. Curr. Biol. 15, R822–R824 (2005).

  93. 93.

    , , & Compromised late-stage motion processing in schizophrenia. Biol. Psychiatry 55, 834–841 (2004).

  94. 94.

    & Disorders of attention and perception in early schizophrenia. Br. J. Psychiatry 34, 103–116 (1961). An influential survey of experiences in the early stages of psychosis.

  95. 95.

    The early symptoms of schizophrenia. Br. J. Psychiatry 112, 225–251 (1966).

  96. 96.

    The step ladder to the impossible: a first hand phenomenological account of a schizo-affective psychotic crisis. J. Ment. Health 2, 239–250 (1993). A fascinating personal account of a psychotic breakdown.

  97. 97.

    Prenatal infection as a risk factor for schizophrenia. Schizophr. Bull. 32, 200–202 (2006).

  98. 98.

    , , & The schizophrenia envirome. Curr. Opin. Psychiatry 18, 141–145 (2005).

  99. 99.

    , & Psychiatric genetics: progress amid controversy. Nature Rev. Genet. 9, 527–540 (2008).

  100. 100.

    , , , & Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. Br. J. Psychiatry 188, 510–518 (2006).

  101. 101.

    , , & Altered cortical glutamate neurotransmission in schizophrenia: evidence from morphological studies of pyramidal neurons. Ann. NY Acad. Sci. 1003, 102–112 (2003).

  102. 102.

    & Half a century of antipsychotics and still a central role for dopamine D2 receptors. Prog. Neuropsychopharmacol. Biol. Psychiatry 27, 1081–1090 (2003).

  103. 103.

    , & The amphetamine-induced sensitized state as a model of schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 31, 1556–1571 (2007).

  104. 104.

    & The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 20, 201–225 (1999).

  105. 105.

    , & From prediction error to psychosis: ketamine as a pharmacological model of delusions. J. Psychopharmacol. 21, 238–252 (2007).

  106. 106.

    American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (American Psychiatric Association, Washington DC, 1994). The official definition of schizophrenia.

  107. 107.

    The dreaming sleep stage: a new neurobiological model of schizophrenia? Neuroscience 140, 1105–1115 (2006).

  108. 108.

    & Sleep imaging and the neuro-psychological assessment of dreams. Trends Cogn. Sci. 6, 23–30 (2002).

  109. 109.

    Pathways to emotional dysfunction in first-episode psychosis. Br. J. Psychiatry 182, 373–375 (2003).

  110. 110.

    , , , & Persecutory delusions: a review and theoretical integration. Clin. Psychol. Rev. 21, 1143–1192 (2001).

  111. 111.

    , , & Folie a deux and shared psychotic disorder. Curr. Psychiatry Rep. 9, 200–205 (2007).

  112. 112.

    Living with schizophrenia. Can. Med. Assoc. J. 82, 218–221 (1960).

  113. 113.

    , , , & Reduced communication between frontal and temporal lobes during talking in schizophrenia. Biol. Psychiatry 51, 485–492 (2002).

  114. 114.

    First rank symptoms of schizophrenia. Br. J. Psychiatry 117, 15–23 (1970).

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Acknowledgements

C.D.F. is supported by the Wellcome Trust and the Danish National Research Foundation. P.C.F. is supported by the Bernard Wolfe Health Neuroscience Fund and by the Wellcome Trust. We are grateful to K. Friston and E. C. Johnstone for their comments on an earlier draft of this paper.

Author information

Affiliations

  1. University of Cambridge, Department of Psychiatry, Addenbrooke's Hospital, Hills Road, Cambridge, CB2 2QQ, UK.

    • Paul C. Fletcher
  2. Centre for Functionally Integrative Neuroscience, Aarhus University Hospital, 8000 Aarhus C, Denmark.

    • Chris D. Frith
  3. Wellcome Trust Centre for Neuroimaging, Functional Imaging Laboratory, University College London, London, WC1N 3BG, UK.

    • Chris D. Frith

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Corresponding author

Correspondence to Chris D. Frith.

Glossary

Cognitive behavioural therapy

A form of psychotherapy in which the patient is encouraged to examine the cognitive processes by which they arrive at a particular state of mind, and to change these processes together with the accompanying behaviours that may reinforce them.

Corollary discharge

The estimate of sensory feedback that is derived from the internal copy of the motor signal (the efference copy).

Efference copy

An internal copy of a motor signal that can be used to predict the sensory consequences of the movement.

Latent inhibition

The phenomenon whereby a stimulus that has been previously presented but has not had any predictive value becomes more difficult to associate with an outcome when presented at a later stage at which it does have predictive value. That is, learning related to the pre-exposed stimulus is slow compared with learning related to new stimuli.