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The Role of Memory Retrieval and Emotional Salience in the Emergence of Auditory Hallucinations

Chapter

Abstract

A number of cognitive models over the last 30 years have been put ­forward to explain auditory verbal hallucinations (AVHs). According to one of the most popular, AVHs are the result of fragmented, intrusive, unintentional memory retrieval. This has been supported by a number of lines of evidence, including phenomenological descriptions of the voices, neuroimaging data during voice hearing that equates to memory recall, problems with source memory and failures to inhibit irrelevant information. These data will be critically discussed, with future lines of enquiry highlighted as relevant. In addition, AVHs are known to be emotive in nature, leading to distress and disability for the voice hearer. Research on cognitive models of AVH has emphasised how affective information or emotional salience exacerbates abnormal patterns of responding, and that emotional information might be considering a triggering factor in the experience of AVH; where relevant these data will also be reviewed.

Keywords

Schizophrenia Patient Memory Retrieval Source Memory Primary Auditory Cortex Auditory Memory 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

AVHs

Auditory verbal hallucinations

MEG

Magnetoencephalography

MTL

Medial temporal lobe

PAC

Primary auditory cortex

RCRT

Repeated continuous recognition task

SAC

Secondary auditory cortex

SICA

Spatial independent component analysis

References

  1. Allen, P. P., Johns, L. C., Fu, C. H. Y., Broome, M. R., Vythelingum, G. N., & McGuire, P. K. (2004). Misattribution of external speech in patients with hallucinations and delusions. Schizophrenia Research, 69(2–3), 277–287.PubMedCrossRefGoogle Scholar
  2. Badcock, J. C., Badcock, D. R., Read, C., & Jablensky, A. (2008). Examining encoding imprecision in spatial working memory in schizophrenia. Schizophrenia Research, 100(1–3), 144–152.PubMedCrossRefGoogle Scholar
  3. Badcock, J. C., Waters, F. A. V., Maybery, M. T., & Michie, P. T. (2005). Auditory hallucinations: Failure to inhibit irrelevant memories. Cognitive Neuropsychiatry, 10(2), 125–136.PubMedCrossRefGoogle Scholar
  4. Bentaleb, L. A., Beauregard, M., Liddle, P., & Stip, E. (2002). Cerebral activity associated with auditory verbal hallucinations: A functional magnetic resonance imaging case study. Journal of Psychiatry & Neuroscience, 27, 110–115.Google Scholar
  5. Bentall, R. P., Baker, G. A., & Havers, S. (1991). Reality monitoring and psychotic hallucinations. British Journal of Clinical Psychology, 30(3), 213–222.PubMedCrossRefGoogle Scholar
  6. Bentall, R. P., & Slade, P. D. (1985). Reality testing and auditory hallucinations. A signal detection analysis. British Journal of Clinical Psychology, 24, 159–171.PubMedCrossRefGoogle Scholar
  7. Bozikas, V. P., Kosmidis, M. H., Anezoulaki, D., Giannakou, M., Andreou, C., & Karavatos, A. (2006). Impaired perception of affective prosody in schizophrenia. The Journal of Neuropsychiatry and Clinical Neurosciences, 18(1), 81–85.PubMedCrossRefGoogle Scholar
  8. Brébion, G., David, A. S., Bressan, R. A., Ohlsen, R. I., & Pilowsky, L. S. (2009). Hallucinations and two types of free-recall intrusion in schizophrenia. Psychological Medicine, 39(6), 917–926.PubMedCrossRefGoogle Scholar
  9. Brébion, G., David, A. S., Jones, H., & Pilowsky, L. S. (2005). Hallucinations, negative symptoms, and response bias in a verbal recognition task in schizophrenia. Neuropsychology, 19(5), 612–617.PubMedCrossRefGoogle Scholar
  10. Brébion, G., David, A. S., Ohlsen, R., Jones, H. M., & Pilowsky, L. S. (2007). Visual memory errors in schizophrenic patients with auditory and visual hallucinations. Journal of the International Neuropsychological Society, 13(5), 832–838.PubMedCrossRefGoogle Scholar
  11. Brébion, G., Smith, M. J., Amador, X., Malaspina, D., & Gorman, J. M. (1998). Word recognition, discrimination accuracy, and decision bias in schizophrenia: Association with positive symptomatology and depressive symptomatology. The Journal of Nervous and Mental Disease, 186(10), 604–609.PubMedCrossRefGoogle Scholar
  12. Copolov, D. L., Mackinnon, A., & Trauer, T. (2004). Correlates of the affective impact of auditory hallucinations in psychotic disorders. Schizophrenia Bulletin, 30(1), 163–171.PubMedCrossRefGoogle Scholar
  13. Copolov, D. L., Seal, M. L., Maruff, P., Ulusoy, R., Wong, M. T., Tochon-Danguy, H. J., et al. (2003). Cortical activation associated with the experience of auditory hallucinations and perception of human speech in schizophrenia: A PET correlation study. Psychiatry Research, 122, 139–152.PubMedCrossRefGoogle Scholar
  14. Danion, J.-M., Rizzo, L., & Bruant, A. (1999). Functional mechanisms underlying impaired recognition memory and conscious awareness in patients with schizophrenia. Archives of General Psychiatry, 56(7), 639–648.PubMedCrossRefGoogle Scholar
  15. David, A. S. (1999). Auditory hallucinations: Phenomenology, neuropsychology and neuroimaging update. Acta Psychiatrica Scandinavica, Supplement, 99(395), 95–104.CrossRefGoogle Scholar
  16. Diaz-Asper, C., Malley, J., Genderson, M., Apud, J., & Elvevåg, B. (2008). Context binding in schizophrenia: Effects of clinical symptomatology and item content. Psychiatry Research, 159(3), 259–270.PubMedCrossRefGoogle Scholar
  17. Diederen, K. M. J., Neggers, S. F. W., Daalman, K., Blom, J. D., Goekoop, R., & Kahn, I. E. C. (2010). Deactivation of the parahippocampal gyrus preceding auditory hallucinations in schizophrenia. The American Journal of Psychiatry, 167, 427–435.PubMedCrossRefGoogle Scholar
  18. Dierks, T., Linden, D. E. J., Jandl, M., Formisano, E., Goebel, R., Lanfermann, H., et al. (1999). Activation of heschl’s gyrus during auditory hallucinations. Neuron, 22(3), 615–621.PubMedCrossRefGoogle Scholar
  19. Doré, M., Caza, N., Gingras, N., & Rouleau, N. (2007). Deficient relational binding processes in adolescents with psychosis: Evidence from impaired memory for source and temporal context. Cognitive Neuropsychiatry, 12(6), 511–536.PubMedCrossRefGoogle Scholar
  20. Edwards, J., Jackson, H. J., & Pattison, P. E. (2002). Emotion recognition via facial expression and affective prosody in schizophrenia: A methodological review. Clinical Psychology Review, 22(6), 789–832.PubMedCrossRefGoogle Scholar
  21. Escartí, M. J., de la Iglesia-Vayá, M., Martí-Bonmatí, L., Robles, M., Carbonell, J., Lull, J. J., et al. (2010). Increased amygdala and parahippocampal gyrus activation in schizophrenic patients with auditory hallucinations: An fMRI study using independent component analysis. Schizophrenia Research, 117(1), 31–41.PubMedCrossRefGoogle Scholar
  22. Favrod, J., Grasset, F., Spreng, S., Grossenbacher, B., & Hodé, Y. (2004). Benevolent voices are not so kind: The functional significance of auditory hallucinations. Psychopathology, 37(6), 304–308.PubMedCrossRefGoogle Scholar
  23. Frith, C. D. (1999). When conscious recollection disrupts memory. Archives of General Psychiatry, 56, 645–646.PubMedCrossRefGoogle Scholar
  24. Gavrilescu, M., Rossell, S., Stuart, G. W., Shea, T. L., Innes-Brown, H., Henshall, K., et al. (2010). Reduced connectivity of the auditory cortex in patients with auditory hallucinations: A resting state functional magnetic resonance imaging study. Psychological Medicine, 40(7), 1149–1158.PubMedCrossRefGoogle Scholar
  25. Hemsley, D. R. (1987a). Hallucinations: Unintended or unexpected? The Behavioral and Brain Sciences, 10, 532–533.CrossRefGoogle Scholar
  26. Hemsley, D. R. (1987b). An experimental psychological model for schizophrenia. In H. Hafner, W. F. Gattaz, & W. Janzarik (Eds.), Search for the causes of schizophrenia. Heidelberg: Springer.Google Scholar
  27. Hemsley, D. R. (1993). A simple (or simplistic?) cognitive model for schizophrenia. Behaviour Research and Therapy, 31(7), 633–645.PubMedCrossRefGoogle Scholar
  28. Henquet, C., Krabbendam, L., Dautzenberg, J., Jolles, J., & Merckelbach, H. (2005). Confusing thoughts and speech: Source monitoring and psychosis. Psychiatry Research, 133(1), 57–63.PubMedCrossRefGoogle Scholar
  29. Hoffman, R. E., Anderson, A. W., Varanko, M., Gore, J. C., & Hampson, M. (2008). Time course of regional brain activity accompanying auditory/verbal hallucinations. The British Journal of Psychiatry, 193, 424–425.PubMedCrossRefGoogle Scholar
  30. Hoffman, R. E., Pittman, B., Constable, T., Bhagwager, Z., & Hampson, M. (2011). Time course of regional brain activity accompanying auditory verbal hallucinations in schizophrenia. The British Journal of Psychiatry, 198, 277–283.PubMedCrossRefGoogle Scholar
  31. Hoffman, R. E., Rapaport, J., Mazure, C. M., & Quinlan, D. M. (1999). Selective speech perception alterations in schizophrenic patients reporting hallucinated ‘voices’. The American Journal of Psychiatry, 156(3), 393–399.PubMedGoogle Scholar
  32. Huron, C., Danion, J., Giacomoni, F., Grange, D., Robert, P., & Rizzo, L. (1995). Impairment of recognition memory with, but not without, conscious recollection in schizophrenia. The American Journal of Psychiatry, 152(12), 1737–1742.PubMedGoogle Scholar
  33. Jardri, R., Pouchet, A., Pins, D., & Thomas, P. (2011). Cortical activations during auditory verbal hallucinations in schizophrenia: A coordinate-based meta-analysis. The American Journal of Psychiatry, 168, 73–81.PubMedCrossRefGoogle Scholar
  34. Johns, L. C., Gregg, L., Allen, P., & McGuire, P. K. (2006). Impaired verbal self-monitoring in psychosis: Effects of state, trait and diagnosis. Psychological Medicine, 36(4), 465–474.PubMedCrossRefGoogle Scholar
  35. Johns, L. C., Hemsley, D., & Kuipers, E. (2002). A comparison of auditory hallucinations in a psychiatric and non-psychiatric group. British Journal of Clinical Psychology, 41(1), 81–86.PubMedCrossRefGoogle Scholar
  36. Johns, L. C., & McGuire, P. K. (1999). Verbal self-monitoring and auditory hallucinations in schizophrenia. Lancet, 353(9151), 469–470.PubMedCrossRefGoogle Scholar
  37. Johns, L. C., Rossell, S., Frith, C., Ahmad, F., Hemsley, D., Kuipers, E., et al. (2001). Verbal self-monitoring and auditory verbal hallucinations in patients with schizophrenia. Psychological Medicine, 31(4), 705–715.PubMedCrossRefGoogle Scholar
  38. Johns, L. C., & van Os, J. (2001). The continuity of psychotic experiences in the general population. Clinical Psychology Review, 21(8), 1125–1141.PubMedCrossRefGoogle Scholar
  39. Keefe, R. S. E., Arnold, M. C., Bayen, U. J., & Harvey, P. D. (1999). Source monitoring deficits in patients with schizophrenia; a multinomial modelling analysis. Psychological Medicine, 29(4), 903–914.PubMedCrossRefGoogle Scholar
  40. Kent, G., & Wahass, S. (1996). The content and characteristics of auditory hallucinations in Saudi Arabia and the UK: A cross-cultural comparison. Acta Psychiatrica Scandinavica, 94(6), 433–437.PubMedCrossRefGoogle Scholar
  41. Larøi, F., Collignon, O., & van Der Linden, M. (2005). Source monitoring for actions in hallucination proneness. Cognitive Neuropsychiatry, 10(2), 105–123.PubMedCrossRefGoogle Scholar
  42. Leitman, D. I., Foxe, J. J., Butler, P. D., Saperstein, A., Revheim, N., & Javitt, D. C. (2005). Sensory contributions to impaired prosodic processing in schizophrenia. Biological Psychiatry, 58(1), 56–61.PubMedCrossRefGoogle Scholar
  43. Lindstrom, L., Klockhoff, I., Svedberg, A., & Bergstrom, K. (1987). Abnormal auditory brain-stem responses in hallucinating schizophrenic patients. The British Journal of Psychiatry, 151(July), 9–14.PubMedCrossRefGoogle Scholar
  44. Lundstrom, B. N., Ingvar, M., & Petersson, K. M. (2005). The role of precuneus and left inferior frontal cortex during source memory episodic retrieval. NeuroImage, 27(4), 824–834.PubMedCrossRefGoogle Scholar
  45. Mackinnon, A., Copolov, D. L., & Trauer, T. (2004). Factors associated with compliance and resistance to command hallucinations. The Journal of Nervous and Mental Disease, 192(5), 357–362.PubMedCrossRefGoogle Scholar
  46. Maguire, E. A. (2001). The retrosplenial contribution to human navigation: A review of lesion and neuroimaging findings. Scandinavian Journal of Psychology, 42(3), 225–238.PubMedCrossRefGoogle Scholar
  47. McKay, C. M., Headlam, D. M., & Copolov, D. L. (2000). Central auditory processing in patients with auditory hallucinations. The American Journal of Psychiatry, 157(5), 759–766.PubMedCrossRefGoogle Scholar
  48. Miller, L. J., O’Connor, E., & DiPasquale, T. (1993). Patients’ attitudes toward hallucinations. The American Journal of Psychiatry, 150, 584–588.PubMedGoogle Scholar
  49. Nayani, T. H., & David, A. S. (1996). The auditory hallucination: A phenomenological survey. Psychological Medicine, 26(1), 177–189.PubMedCrossRefGoogle Scholar
  50. Oulis, P. G., Mavreas, V. G., Mamounas, J. M., & Stefanis, C. N. (1995). Clinical characteristics of auditory hallucinations. Acta Psychiatrica Scandinavica, 92(2), 97–102.PubMedCrossRefGoogle Scholar
  51. Ranganath, C., Minzenberg, M. J., & Ragland, J. D. (2008). The cognitive neuroscience of memory function and dysfunction in schizophrenia. Biological Psychiatry, 64(1), 18–25.PubMedCrossRefGoogle Scholar
  52. Rizzo, L., Danion, J. M., Grangé, D., van Linden, M. D., & Rohmer, J. G. (1996). Impairment of memory for spatial context in schizophrenia. Neuropsychology, 10(3), 376–384.CrossRefGoogle Scholar
  53. Rossell, S. L., & Boundy, C. L. (2005). Are auditory-verbal hallucinations associated with auditory affective processing deficits? Schizophrenia Research, 78(1), 95–106.PubMedCrossRefGoogle Scholar
  54. Sanjuan, J., Gonzalez, J. C., Aguilar, E. J., Leal, C., & van Os, J. (2004). Pleasurable auditory hallucinations. Acta Psychiatrica Scandinavica, 110(4), 273–278.PubMedCrossRefGoogle Scholar
  55. Seal, M. L., Aleman, A., & McGuire, P. K. (2004). Compelling imagery, unanticipated speech and deceptive memory: Neurocognitive models of auditory verbal hallucinations in schizophrenia. Cognitive Neuropsychiatry, 9(1–2), 43–72.PubMedCrossRefGoogle Scholar
  56. Shapleske, J., Rossell, S. L., Woodruff, P. W. R., Suckling, J., Bullmore, E., Simmons, A., et al. (2002). A computational morphometric MRI study of schizophrenia: Effects of hallucinations. Cerebral Cortex, 12, 1331–1341.PubMedCrossRefGoogle Scholar
  57. Shea, T. L., Sergejew, A. A., Burnham, D., Jones, C., Rossell, S. L., Copolov, D. L., et al. (2007). Emotional prosodic processing in auditory hallucinations. Schizophrenia Research, 90(1–3), 214–220.PubMedCrossRefGoogle Scholar
  58. Shergill, S. S., Brammer, M. J., Williams, S. C. R., Murray, R. M., & McGuire, P. K. (2000). Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Archives of General Psychiatry, 57(11), 1033–1038.PubMedCrossRefGoogle Scholar
  59. Silbersweig, D. A., Stern, E., Frith, C., Cahill, C., Holmes, A., Grootoonk, S., et al. (1995). A functional neuroanatomy of hallucinations in schizophrenia. Nature, 378(6553), 176–179.PubMedCrossRefGoogle Scholar
  60. Tendolkar, I., Ruhrmann, S., Brockhaus, A., Pukrop, R., & Klosterkötter, J. (2002). Remembering or knowing: Electrophysiological evidence for an episodic memory deficit in schizophrenia. Psychological Medicine, 32(7), 1261–1271.PubMedCrossRefGoogle Scholar
  61. Tien, A. Y. (1991). Distributions of hallucinations in the population. Social Psychiatry and Psychiatric Epidemiology, 26(6), 287–292.PubMedCrossRefGoogle Scholar
  62. Tulving, E. (1985). Ebbinghaus’s memory. What did he learn and remember? Journal of Experimental Psychology: Learning, Memory, and Cognition, 11(3), 485–490.CrossRefGoogle Scholar
  63. van de Ven, V. G., Formisano, E., Roder, C. H., Prvulovic, D., Bittner, R. A., Dietz, M. G., et al. (2005). The spatiotemporal pattern of auditory cortical responses during verbal hallucinations. NeuroImage, 27, 644–655.PubMedCrossRefGoogle Scholar
  64. van Erp, T. G. M., Lesh, T. A., Knowlton, B. J., Bearden, C. E., Hardt, M., Karlsgodt, K. H., et al. (2008). Remember and know judgments during recognition in chronic schizophrenia. Schizophrenia Research, 100(1–3), 181–190.PubMedCrossRefGoogle Scholar
  65. Waters, F. A. V., Badcock, J. C., & Maybery, M. T. (2006). The ‘who’ and ‘when’ of context memory: Different patterns of association with auditory hallucinations. Schizophrenia Research, 82(2–3), 271–273.PubMedCrossRefGoogle Scholar
  66. Waters, F. A. V., Badcock, J. C., Maybery, M. T., & Michie, P. T. (2003). Inhibition in schizophrenia: Association with auditory hallucinations. Schizophrenia Research, 62(3), 275–280.PubMedCrossRefGoogle Scholar
  67. Waters, F. A. V., Maybery, M. T., Badcock, J. C., & Michie, P. T. (2004). Context memory and binding in schizophrenia. Schizophrenia Research, 68(2–3), 119–125.PubMedCrossRefGoogle Scholar
  68. Weis, S., Klaver, P., Reul, J., Elger, C. E., & Fernandez, G. (2004). Neural correlates of successful declarative memory formation and retrieval: The anatomical overlap. Cortex, 40, 200–202.PubMedCrossRefGoogle Scholar
  69. Wing, J. K., Cooper, J. E., & Sartorius, N. (1974). Measurement and classification of psychiatric symptoms: An instruction manual for the PSE and Catego program. London: Cambridge University Press.Google Scholar
  70. Woodruff, P. W. R., Wright, I. C., Bullmore, E. T., Brammer, M., Howard, R. J., Williams, S. C. R., et al. (1997). Auditory hallucinations and the temporal cortical response to speech in schizophrenia: A functional magnetic resonance imaging study. The American Journal of Psychiatry, 154(12), 1676–1682.PubMedGoogle Scholar
  71. Woodward, T. S., Menon, M., & Whitman, J. C. (2007). Source monitoring biases and auditory hallucinations. Cognitive Neuropsychiatry, 12(6), 477–494.PubMedCrossRefGoogle Scholar
  72. Yonelinas, A. P., Otten, L. J., Shaw, R. N., & Rugg, M. D. (2005). Separating the brain regions involved in recollection and familiarity in recognition memory. Journal of Neuroscience, 25(11), 3002–3008.PubMedCrossRefGoogle Scholar
  73. Zigler, E., & Phillips, L. (1961). Psychiatric diagnosis and symptomatology. Journal of Abnormal and Social Psychology, 63(1), 69–75.CrossRefGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Brain and Psychological Sciences Research CentreSwinburne University of TechnologyMelbourneAustralia
  2. 2.Cognitive Neuropsychology LabMonash Alfred Psychiatry Research Centre (MAPrc)MelbourneAustralia

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