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Auditory hallucinations, top-down processing and language perception: a general population study

  • J. N. de Boer (a1), M. M. J. Linszen (a2), J. de Vries (a1), M. J. L. Schutte (a2), M. J. H. Begemann (a2), S. M. Heringa (a1), M. M. Bohlken (a1), K. Hugdahl (a3) (a4), A. Aleman (a2), F. N. K. Wijnen (a5) and I. E. C. Sommer (a2)...

Abstract

Background

Studies investigating the underlying mechanisms of hallucinations in patients with schizophrenia suggest that an imbalance in top-down expectations v. bottom-up processing underlies these errors in perception. This study evaluates this hypothesis by testing if individuals drawn from the general population who have had auditory hallucinations (AH) have more misperceptions in auditory language perception than those who have never hallucinated.

Methods

We used an online survey to determine the presence of hallucinations. Participants filled out the Questionnaire for Psychotic Experiences and participated in an auditory verbal recognition task to assess both correct perceptions (hits) and misperceptions (false alarms). A hearing test was performed to screen for hearing problems.

Results

A total of 5115 individuals from the general Dutch population participated in this study. Participants who reported AH in the week preceding the test had a higher false alarm rate in their auditory perception compared with those without such (recent) experiences. The more recent the AH were experienced, the more mistakes participants made. While the presence of verbal AH (AVH) was predictive for false alarm rate in auditory language perception, the presence of non-verbal or visual hallucinations were not.

Conclusions

The presence of AVH predicted false alarm rate in auditory language perception, whereas the presence of non-verbal auditory or visual hallucinations was not, suggesting that enhanced top-down processing does not transfer across modalities. More false alarms were observed in participants who reported more recent AVHs. This is in line with models of enhanced influence of top-down expectations in persons who hallucinate.

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Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

Author for correspondence: Janna de Boer, E-mail: j.n.deboer-18@umcutrecht.nl

References

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Aleman, A, Böcker, KBE, Hijman, R, Kahn, RS and de Haan, EHF (2002) Hallucinations in schizophrenia: imbalance between imagery and perception? Schizophrenia Research 57, 315316.
Aleman, A, Böcker, KBE, Hijman, R, de Haan, EHF and Kahn, RS (2003) Cognitive basis of hallucinations in schizophrenia: role of top-down information processing. Schizophrenia Research 64, 175185.
Bentall, RP (1990) The illusion of reality: a review and integration of psychological research on hallucinations. Psychological Bulletin 107, 82.
Bentall, RP and Slade, PD (1985) Reality testing and auditory hallucinations: a signal detection analysis. British Journal of Clinical Psychology 24, 159169.
Bentall, RP, Baker, GA and Havers, S (1991) Reality monitoring and psychotic hallucinations. British Journal of Clinical Psychology 30, 213222.
Blank, IA and Fedorenko, E (2017) Domain-general brain regions do not track linguistic input as closely as language-selective regions. Journal of Neuroscience 37, 999910011.
Blom, JD (2009) A Dictionary of Hallucinations. New York: Springer Science & Business Media.
Böcker, KBE, Hijman, R, Kahn, RS and de Haan, EHF (2000) Perception, mental imagery and reality discrimination in hallucinating and non-hallucinating schizophrenic patients. British Journal of Clinical Psychology 39, 397406.
Brysbaert, M, Stevens, M, Mandera, P and Keuleers, E (2015) The impact of word prevalence on lexical decision times: evidence from the Dutch Lexicon Project 2. Journal of Experimental Psychology: Human Perception and Performance 150.
Cassidy, CM, Balsam, PD, Weinstein, JJ, Rosengard, RJ, Slifstein, M, Daw, ND, Abi-Dargham, A and Horga, G (2018) A perceptual inference mechanism for hallucinations linked to striatal dopamine. Current Biology 28, 503514.
Catalan, A, Simons, CJP, Bustamante, S, Drukker, M, Madrazo, A, de Artaza, MG, Gorostiza, I, Van Os, J and Gonzalez-Torres, MA (2014) Novel evidence that attributing affectively salient signal to random noise is associated with psychosis. PLoS ONE 9, e102520.
Davis, MH and Johnsrude, IS (2007) Hearing speech sounds: top-down influences on the interface between audition and speech perception. Hearing Research 229, 132147.
Dehaene, S and Cohen, L (2011) The unique role of the visual word form area in reading. Trends in Cognitive Sciences 15, 254262.
Dima, D, Dietrich, DE, Dillo, W and Emrich, HM (2010) Impaired top-down processes in schizophrenia: a DCM study of ERPs. NeuroImage 52, 824832.
Engel, AK, Fries, P and Singer, W (2001) Dynamic predictions: oscillations and synchrony in top–down processing. Nature Reviews Neuroscience 2, 704716.
Evans, JR and Mathur, A (2005) The value of online surveys. Internet Research 15, 195219.
Fenske, MJ, Aminoff, E, Gronau, N and Bar, M (2006) Top-down facilitation of visual object recognition: object-based and context-based contributions. Progress in Brain Research 155, 321.
Frost, R, Armstrong, BC, Siegelman, N and Christiansen, MH (2015) Domain generality versus modality specificity: the paradox of statistical learning. Trends in Cognitive Sciences 19, 117125.
Frost, RLA, Monaghan, P and Tatsumi, T (2017) Domain-general mechanisms for speech segmentation: the role of duration information in language learning. Journal of Experimental Psychology: Human Perception and Performance 43, 466.
Gibson, JJ (1950) The Perception of the Visual World. Boston: Houghton Mifflin.
Gibson, JJ (1966) The Senses Considered as Perceptual Systems. London: Houghton Mifflin.
Graham Scott, J, Nurcombe, B, Sheridan, J and McFarland, M (2007) Hallucinations in adolescents with post-traumatic stress disorder and psychotic disorder. Australasian Psychiatry 15, 4448.
Grossberg, S (1982) How does a brain build a cognitive code? In Cohen, R. and Wartofsky, M. (eds), Studies of Mind and Brain. Boston Studies in the Philosophy of Science, vol 70. Dordrecht: Springer, pp. 152.
Grossberg, S (2000) How hallucinations may arise from brain mechanisms of learning, attention, and volition. Journal of the International Neuropsychological Society 6, 583592.
Hauser, MD, Chomsky, N and Fitch, WT (2002) The faculty of language: what is it, who has it, and how did it evolve? Science 298, 15691579.
Honig, A, Romme, MAJ, Ensink, BJ, Escher, SD, Pennings, MHA and Devries, MW (1998) Auditory hallucinations: a comparison between patients and nonpatients. The Journal of Nervous and Mental Disease 186, 646651.
Hugdahl, K (2009) ‘Hearing voices’: auditory hallucinations as failure of top-down control of bottom-up perceptual processes. Scandinavian Journal of Psychology 50, 553560.
Hugdahl, K (2015) Auditory hallucinations: a review of the ERC “VOICE” project. World Journal of Psychiatry 5, 193.
Jardri, R, Hugdahl, K, Hughes, M, Brunelin, J, Waters, F, Alderson-Day, B, Smailes, D, Sterzer, P, Corlett, PR and Leptourgos, P (2016) Are hallucinations due to an imbalance between excitatory and inhibitory influences on the brain? Schizophrenia Bulletin 42, 11241134.
Johns, LC and Van Os, J (2001) The continuity of psychotic experiences in the general population. Clinical Psychology Review 21, 11251141.
Johns, LC, Nazroo, JY, Bebbington, P and Kuipers, E (2002) Occurrence of hallucinatory experiences in a community sample and ethnic variations. The British Journal of Psychiatry 180, 174178.
Johns, LC, Cannon, M, Singleton, N, Murray, RM, Farrell, M, Brugha, T, Bebbington, P, Jenkins, R and Meltzer, H (2004) Prevalence and correlates of self-reported psychotic symptoms in the British population. The British Journal of Psychiatry 185, 298305.
Kay, SR, Fiszbein, A and Opfer, LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261.
Kelleher, I, Devlin, N, Wigman, JTW, Kehoe, A, Murtagh, A, Fitzpatrick, C and Cannon, M (2014) Psychotic experiences in a mental health clinic sample: implications for suicidality, multimorbidity and functioning. Psychological Medicine 44, 16151624.
Kompus, K, Falkenberg, LE, Bless, JJ, Johnsen, E, Kroken, RA, Kråkvik, B, Larøi, F, Løberg, E-M, Vedul-Kjelsås, E and Westerhausen, R (2013) The role of the primary auditory cortex in the neural mechanism of auditory verbal hallucinations. Frontiers in Human Neuroscience 7, 144.
Korsnes, MS, Hugdahl, K, Nygård, M and Bjørnæs, H (2010) An fMRI study of auditory hallucinations in patients with epilepsy. Epilepsia 51, 610617.
Leensen, MCJ, de Laat, JAPM, Snik, AFM and Dreschler, WA (2011) Speech-in-noise screening tests by internet, part 2: improving test sensitivity for noise-induced hearing loss. International Journal of Audiology 50, 835848.
Linszen, M, de Boer, J, Schutte, J, Begemann, M, de Vries, J, Koops, S, Blom, R, Bohlken, M, Heringa, S, Blom, J and Sommer, I (2018) Phenomenology and content of hallucinations and other misperceptions in the general population: a large online survey.
Macmillan, NA (2002) Signal detection theory. Wiley Online Library Stevens’ handbook of experimental psychology.
Macmillan, NA and Creelman, CD (2004) Detection Theory: A User's Guide. New York: Psychology Press.
Moseley, P, Smailes, D, Ellison, A and Fernyhough, C (2016) The effect of auditory verbal imagery on signal detection in hallucination-prone individuals. Cognition 146, 206216.
Moskowitz, H and McGlothlin, W (1974) Effects of marihuana on auditory signal detection. Psychopharmacologia 40, 137145.
O'Callaghan, C, Kveraga, K, Shine, JM, Adams, RB and Bar, M (2017) Predictions penetrate perception: converging insights from brain, behaviour and disorder. Consciousness and Cognition 47, 6374.
Ohayon, MM (2000) Prevalence of hallucinations and their pathological associations in the general population. Psychiatry Research 97, 153164.
Oomen, PP, van Hell, HH and Bossong, MG (2018) The acute effects of cannabis on human executive function. Behavioural Pharmacology 29, 605616.
Overall, JE and Gorham, DR (1962) The brief psychiatric rating scale. Psychological Reports 10, 799812.
Posey, TB and Losch, ME (1983) Auditory hallucinations of hearing voices in 375 normal subjects. Imagination, Cognition and Personality 3, 99113.
Powers, AR, Kelley, M and Corlett, PR (2016) Hallucinations as top-down effects on perception. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging 1, 393400.
Powers, AR, Mathys, C and Corlett, PR (2017) Pavlovian conditioning-induced hallucinations result from overweighting of perceptual priors. Science 357, 596600.
Remberk, B (2017) Clinical significance of psychotic-like experiences in children and adolescents. Psychiatria Polska 51, 271282.
Rund, BR (1998) A review of longitudinal studies of cognitive functions in schizophrenia patients. Schizophrenia Bulletin 24, 425435.
Sarter, M, Hasselmo, ME, Bruno, JP and Givens, B (2005) Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Research Reviews 48, 98111.
Servan-Schreiber, D, Cohen, JD and Steingard, S (1996) Schizophrenic deficits in the processing of context: a test of a theoretical model. Archives of General Psychiatry 53, 11051112.
Shergill, SS, Murray, RM and McGuire, PK (1998) Auditory hallucinations: a review of psychological treatments. Schizophrenia Research 32, 137150.
Sommer, IEC, Daalman, K, Rietkerk, T, Diederen, KM, Bakker, S, Wijkstra, J and Boks, MPM (2008) Healthy individuals with auditory verbal hallucinations; who are they? Psychiatric assessments of a selected sample of 103 subjects. Schizophrenia Bulletin 36, 633641.
Sommer, I, Kleijer, H and Hugdahl, K (2018) Toward personalized treatment of hallucinations. Current Opinion in Psychiatry 32, 237245.
Stanislaw, H and Todorov, N (1999) Calculation of signal detection theory measures. Behavior Research Methods, Instruments, & Computers 31, 137149.
Stocker, AA and Simoncelli, EP (2006 a) Noise characteristics and prior expectations in human visual speed perception. Nature Neuroscience 9, 578.
Stocker, AA and Simoncelli, EP (2006 b) Sensory adaptation within a Bayesian framework for perception. In Proceedings of the 2005 Conference on Advances in Neural Information Processing Systems 18, NIPS 2005, Vancouver, BC, Canada, 12/5/05, pp. 12891296.
Tien, AY (1991) Distribution of hallucinations in the population. Social Psychiatry and Psychiatric Epidemiology 26, 287292.
Van Berkum, JJA (2010) The brain is a prediction machine that cares about good and bad-any implications for neuropragmatics? Italian Journal of Linguistics 22, 181208.
Vercammen, A and Aleman, A (2008) Semantic expectations can induce false perceptions in hallucination-prone individuals. Schizophrenia Bulletin 36, 151156.
Waters, F, Allen, P, Aleman, A, Fernyhough, C, Woodward, TS, Badcock, JC, Barkus, E, Johns, L, Varese, F and Menon, M (2012) Auditory hallucinations in schizophrenia and nonschizophrenia populations: a review and integrated model of cognitive mechanisms. Schizophrenia Bulletin 38, 683693.
Wigman, JTW, van Nierop, M, Vollebergh, WAM, Lieb, R, Beesdo-Baum, K, Wittchen, H-U and van Os, J (2012) Evidence that psychotic symptoms are prevalent in disorders of anxiety and depression, impacting on illness onset, risk, and severity – implications for diagnosis and ultra-high risk research. Schizophrenia Bulletin 38, 247257.
Wright, KB (2005) Researching Internet-based populations: advantages and disadvantages of online survey research, online questionnaire authoring software packages, and web survey services. Journal of Computer-Mediated Communication 10, JCMC1034.
Yarkoni, T, Balota, D and Yap, M (2008) Moving beyond Coltheart's N: a new measure of orthographic similarity. Psychonomic Bulletin & Review 15, 971979.

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