Auditory hallucinations in schizophrenia: Intrusive thoughts and forgotten memories

Introduction. This paper presents a new cognitive model of auditory hallucinations in schizophrenia. We suggest that auditory hallucinations are auditory representations derived from the unintentional activation of memories and other irrelevant current mental associations. Our model proposes that a combination of deficits in intentional inhibition and contextual memory is critical to the experience of auditory hallucinations. The failure in intentional inhibition produces unwanted and uncontrollable mental events which are not recognised because they have lost the contextual cues that would normally facilitate recognition. Methods. This article amalgamates recently published data and presents a reanalysis of the findings on 43 patients with a diagnosis of schizophrenia (Badcock, Waters, Maybery, & Michie, 2005; Waters, Badcock, Maybery, & Michie, 2003a; Waters, Maybery, Badcock, & Michie, 2004a). Relative risk was also estimated to determine whether the combination of deficits increases the risk of having auditory hallucinations. Results. Almost 90% of patients currently experiencing auditory hallucinations showed the predicted combination of deficits on both inhibition and context memory, compared to only a third of patients without hallucinations. In addition, the results showed that those patients with the specified cognitive deficits were at an especially increased risk of having auditory hallucinations relative to patients without the deficits. Conclusions. The results of our investigations strongly support the role of intentional inhibition and context memory in auditory hallucinations. Critical consideration of the findings also suggests that additional cognitive processes might be important for the expression of this symptom.

[1]  P. Woodruff,et al.  Auditory hallucinations: Insights and questions from neuroimaging , 2004, Cognitive neuropsychiatry.

[2]  Richard P. Bentall,et al.  Sensory Deception: A Scientific Analysis Of Hallucination , 1988 .

[3]  Cognitive inhibition and schizophrenic symptom subgroups. , 1996, Schizophrenia bulletin.

[4]  A. David,et al.  Positive symptomatology and source-monitoring failure in schizophrenia — an analysis of symptom-specific effects , 2000, Psychiatry Research.

[5]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[6]  Marcia K. Johnson,et al.  fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. , 2000, Brain research. Cognitive brain research.

[7]  Michael D. Rugg,et al.  The Role of the Prefrontal Cortex in Recognition Memory and Memory for Source: An fMRI Study , 1999, NeuroImage.

[8]  N. Raz,et al.  Differential effects of aging on memory for content and context: a meta-analysis. , 1995, Psychology and aging.

[9]  N Sartorius,et al.  WHO international pilot study of schizophrenia. , 1972, Psychological medicine.

[10]  P. Michie,et al.  Inhibition in schizophrenia: association with auditory hallucinations , 2003, Schizophrenia Research.

[11]  T. Shallice,et al.  Response suppression, initiation and strategy use following frontal lobe lesions , 1996, Neuropsychologia.

[12]  R. Ancill,et al.  Schizophrenia : exploring the spectrum of psychosis , 1994 .

[13]  K. Deffenbacher Effects of Arousal on Everyday Memory , 1994 .

[14]  C Frith,et al.  Brain mechanisms associated with top-down processes in perception. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  C. Brewin,et al.  Intrusive memories in depression: an index of schema activation? , 1996, Psychological Medicine.

[16]  Patricia T Michie,et al.  Context memory and binding in schizophrenia , 2004, Schizophrenia Research.

[17]  A. Beech,et al.  Reduced cognitive inhibition in obsessive-compulsive disorder. , 1993, The British journal of clinical psychology.

[18]  D. Stuss,et al.  The Frontal Lobes , 1986 .

[19]  M. Egan,et al.  Relative risk of neurological signs in siblings of patients with schizophrenia. , 2001, The American journal of psychiatry.

[20]  A. Mackinnon,et al.  On the non-significance of internal versus external auditory hallucinations , 2004, Schizophrenia Research.

[21]  J. Gray,et al.  Integrating schizophrenia. , 1998, Schizophrenia bulletin.

[22]  R. Hoffman,et al.  Selective speech perception alterations in schizophrenic patients reporting hallucinated "voices". , 1999, The American journal of psychiatry.

[23]  D. Bjorklund,et al.  The evolution of inhibition mechanisms and their role in human cognition and behavior , 1995 .

[24]  P. Michie,et al.  Auditory hallucinations: Failure to inhibit irrelevant memories , 2005, Cognitive neuropsychiatry.

[25]  C. Bell Oxford Textbook of Psychiatry , 1996 .

[26]  P. Woodruff,et al.  Characteristics of functional auditory hallucinations. , 2004, The American journal of psychiatry.

[27]  A. David The cognitive neuropsychiatry of auditory verbal hallucinations: an overview. , 2004, Cognitive neuropsychiatry.

[28]  J. Gorman,et al.  Source monitoring impairments in schizophrenia: characterisation and associations with positive and negative symptomatology , 2002, Psychiatry Research.

[29]  P. Belin,et al.  Thinking the voice: neural correlates of voice perception , 2004, Trends in Cognitive Sciences.

[30]  A. David,et al.  Auditory-verbal hallucinations and the phonological loop: a cognitive neuropsychological study. , 1993, The British journal of clinical psychology.

[31]  G. Egan,et al.  Cortical activation associated with the experience of auditory hallucinations and perception of human speech in schizophrenia: a PET correlation study , 2003, Psychiatry Research: Neuroimaging.

[32]  J. Vasterling,et al.  Attention and memory dysfunction in posttraumatic stress disorder. , 1998, Neuropsychology.

[33]  N. Hunkin,et al.  Memory for single items, word pairs, and temporal order of different kinds in a patient with selective hippocampal lesions , 2001, Cognitive neuropsychology.

[34]  J. Gorman,et al.  Opposite links of positive and negative symptomatology with memory errors in schizophrenia , 1999, Psychiatry Research.

[35]  Michael Petrides,et al.  Source versus content memory in patients with a unilateral frontal cortex or a temporal lobe excision. , 2003, Brain : a journal of neurology.

[36]  M. Egan,et al.  Relative risk of attention deficits in siblings of patients with schizophrenia. , 2000, The American journal of psychiatry.

[37]  Armin Schnider,et al.  Spontaneous confabulators fail to suppress currently irrelevant memory traces , 1999, Nature Neuroscience.

[38]  G. Tucker Oxford Textbook of Psychiatry, 2nd ed , 1992 .

[39]  J. Rauschecker,et al.  Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans , 1999, Nature Neuroscience.

[40]  T. Shallice,et al.  Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. , 1999, Brain : a journal of neurology.

[41]  P. Garety,et al.  Cognitive assessment of voices: further developments in understanding the emotional impact of voices. , 1998, The British journal of clinical psychology.

[42]  J. Nigg On inhibition/disinhibition in developmental psychopathology: views from cognitive and personality psychology and a working inhibition taxonomy. , 2000, Psychological bulletin.

[43]  J. Henderson,et al.  Inhibitory processes in adults with persistent childhood onset ADHD. , 2002, Journal of consulting and clinical psychology.

[44]  R. Bentall,et al.  Paranoia and social reasoning: an attribution theory analysis. , 1991, The British journal of clinical psychology.

[45]  M. Hardy-Bayle,et al.  Context-dependent information processing in patients with schizophrenia , 2000, Schizophrenia Research.

[46]  M. Hunter Locating voices in space: A perceptual model for auditory hallucinations? , 2004, Cognitive neuropsychiatry.

[47]  B. Shapiro,et al.  Hallucinations: theoretical and clinical overview. , 1986, The American journal of psychiatry.

[48]  Katherine Kipp,et al.  The Development of Efficient Inhibition: Evidence from Directed-Forgetting Tasks. , 1998 .

[49]  D. Hemsley A simple (or simplistic?) cognitive model for schizophrenia. , 1993, Behaviour research and therapy.

[50]  R. Dworkin,et al.  Positive and negative schizophrenic symptoms, attention, and information processing. , 1985, Schizophrenia bulletin.

[51]  J. Kounios,et al.  Time-course studies of reality monitoring and recognition. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[52]  P. Chadwick,et al.  The Omnipotence of Voices II: the Beliefs About Voices Questionnaire (BAVQ) , 1995, British Journal of Psychiatry.

[53]  C. Stefanis,et al.  Clinical characteristics of auditory hallucinations , 1995, Acta psychiatrica Scandinavica.

[54]  C. Degueldre,et al.  The Functional Anatomy of Inhibition Processes Investigated with the Hayling Task , 2001, NeuroImage.

[55]  Marcia K. Johnson,et al.  Electrophysiological brain activity and memory source monitoring , 1996, Neuroreport.

[56]  J. Cohen,et al.  Schizophrenic deficits in the processing of context. A test of a theoretical model. , 1996, Archives of general psychiatry.

[57]  A. Stevens,et al.  Dissociating the cortical basis of memory for voices, words and tones. , 2004, Brain research. Cognitive brain research.

[58]  Jan Noyes,et al.  The disruption and dissolution of directed forgetting : Inhibitory control of memory , 2000 .

[59]  Jeffrey P. Toth,et al.  Dissociation of attentional processes in patients with focal frontal and posterior lesions , 1999, Neuropsychologia.

[60]  N. Tarrier,et al.  Intrusive Thoughts and Auditory Hallucinations: A Cognitive Approach , 1995, Behavioural and Cognitive Psychotherapy.

[61]  Marcia K. Johnson,et al.  Source monitoring. , 1993, Psychological bulletin.

[62]  J. Gorman,et al.  Reality monitoring failure in schizophrenia: The role of selective attention , 1996, Schizophrenia Research.

[63]  J. Gorman,et al.  Word recognition, discrimination accuracy, and decision bias in schizophrenia: association with positive symptomatology and depressive symptomatology. , 1998, The Journal of nervous and mental disease.

[64]  C. Frith,et al.  The role of the prefrontal cortex in self-consciousness: the case of auditory hallucinations. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[65]  Valerie Treyer,et al.  Selection of Currently Relevant Memories by the Human Posterior Medial Orbitofrontal Cortex , 2000, The Journal of Neuroscience.

[66]  R P Bentall,et al.  Reality monitoring and psychotic hallucinations. , 1991, The British journal of clinical psychology.

[67]  F. N. Dempster,et al.  Interference and inhibition in cognition: An historical perspective , 1995 .

[68]  M. Posner,et al.  Attention and schizophrenia: a view from cognitive neuroscience. , 1996, Cognitive neuropsychiatry.

[69]  M. Spinella CORRELATIONS AMONG BEHAVIORAL MEASURES OF ORBITOFRONTAL FUNCTION , 2002, The International journal of neuroscience.

[70]  A. Aleman,et al.  Compelling imagery, unanticipated speech and deceptive memory: Neurocognitive models of auditory verbal hallucinations in schizophrenia , 2004, Cognitive neuropsychiatry.

[71]  Mieke Verfaellie,et al.  Recollection-based memory in frontotemporal dementia: implications for theories of long-term memory. , 2002, Brain : a journal of neurology.

[72]  J. Jolles,et al.  Neuropsychological abnormalities in depression : relation between brain and behaviour , 1997 .

[73]  Richard S. J. Frackowiak,et al.  A functional neuroanatomy of hallucinations in schizophrenia , 1995, Nature.

[74]  Marcia K. Johnson,et al.  Feature memory and binding in young and older adults , 1996, Memory & cognition.

[75]  R. Hoffman,et al.  Semantic organization of hallucinated "voices" in schizophrenia. , 1994, The American journal of psychiatry.

[76]  M. Maybery,et al.  Revision of the factor structure of the Launay-Slade Hallucination Scale (LSHS-R) , 2003 .

[77]  C. Frith,et al.  The functional anatomy of verbal initiation and suppression using the Hayling Test , 1997, Neuropsychologia.

[78]  J M Fuster,et al.  Synopsis of function and dysfunction of the frontal lobe , 1999, Acta psychiatrica Scandinavica. Supplementum.

[79]  Hélène Amieva,et al.  Inhibitory functioning in Alzheimer's disease. , 2004, Brain : a journal of neurology.

[80]  A. Pfefferbaum,et al.  Patterns of content, contextual, and working memory impairments in schizophrenia and nonamnesic alcoholism. , 1997, Neuropsychology.

[81]  I. Leudar,et al.  Hearing voices: A phenomenological-hermeneutic approach , 2004, Cognitive neuropsychiatry.

[82]  Philip K McGuire,et al.  Verbal self-monitoring and auditory hallucinations in schizophrenia , 1999, The Lancet.

[83]  P. Rankin,et al.  Reality discrimination, reality monitoring and disposition towards hallucination. , 1995, The British journal of clinical psychology.

[84]  N. Mori,et al.  Unilateral auditory hallucinations in schizophrenia after damage to the right hippocampus , 2002, Schizophrenia Research.

[85]  R. Murray,et al.  Increased blood flow in Broca's area during auditory hallucinations in schizophrenia , 1993, The Lancet.

[86]  M. Romme,et al.  Auditory hallucinations: a comparison between patients and nonpatients. , 1998, The Journal of nervous and mental disease.

[87]  D. Hemsley,et al.  Schizophrenia: a failure to control the contents of consciousness? , 1987, The British journal of clinical psychology.

[88]  David L. Strayer,et al.  Aging and inhibition: beyond a unitary view of inhibitory processing in attention. , 1994, Psychology and aging.

[89]  A. Pickering,et al.  The relationship between cognitive inhibition and psychotic symptoms. , 2000, Journal of abnormal psychology.

[90]  Michael C. Anderson,et al.  Inhibitory processes and the control of memory retrieval , 2002, Trends in Cognitive Sciences.

[91]  M. Van der Linden,et al.  Patients with Schizophrenia Remember that an Event has Occurred, but not When , 1996, British Journal of Psychiatry.

[92]  A. David,et al.  The auditory hallucination: a phenomenological survey , 1996, Psychological Medicine.

[93]  Heather M. Kleider,et al.  The marriage of perception and memory: Creating two-way illusions with words and voices , 1999, Memory & cognition.

[94]  K. K. Harnishfeger,et al.  The development of cognitive inhibition: Theories, definitions, and research evidence , 1995 .

[95]  Peter B. Jones,et al.  Spatial and temporal mapping of neural activity associated with auditory hallucinations , 1999, The Lancet.

[96]  A. Crider Perseveration in schizophrenia. , 1997, Schizophrenia bulletin.

[97]  E. Glisky,et al.  Source memory in older adults: an encoding or retrieval problem? , 2001, Journal of experimental psychology. Learning, memory, and cognition.

[98]  E. Daprati,et al.  Confusion between silent and overt reading in schizophrenia , 2000, Schizophrenia Research.

[99]  C. Frith,et al.  Consciousness, Information Processing and Schizophrenia , 1979, British Journal of Psychiatry.

[100]  A. Morrison,et al.  Cognitive processes in auditory hallucinations: attributional biases and metacognition , 1998, Psychological Medicine.

[101]  F. Guillem,et al.  The cognitive and anatomo-functional basis of reality distortion in schizophrenia: A view from memory event-related potentials , 2003, Psychiatry Research.

[102]  Lars Nyberg,et al.  Brain Regions Differentially Involved in Remembering What and When: a PET Study , 1997, Neuron.

[103]  D. Servan-Schreiber,et al.  A Neural Network Model of Disturbances in the Processing of Context in Schizophrenia , 1992 .

[104]  A. Morrison,et al.  Intrusive thoughts and auditory hallucinations: a comparative study of intrusions in psychosis. , 2000, Behaviour research and therapy.

[105]  A. Morrison THE INTERPRETATION OF INTRUSIONS IN PSYCHOSIS: AN INTEGRATIVE COGNITIVE APPROACH TO HALLUCINATIONS AND DELUSIONS , 2001, Behavioural and Cognitive Psychotherapy.