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BMC Psychiatry
Published in: BMC Psychiatry 1/2016

Open Access 01-12-2016 | Research article

Event-related potentials elicited by the Deutsch “high-low” word illusion in the patients with first-episode schizophrenia with auditory hallucinations

Authors: You Xu, Hao Chai, Bingren Zhang, Qianqian Gao, Hongying Fan, Leilei Zheng, Hongjing Mao, Yonghua Zhang, Wei Wang

Published in: BMC Psychiatry | Issue 1/2016

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Abstract

Background

The exact cerebral structural and functional mechanisms under the auditory verbal hallucinations (AVHs) in schizophrenia are still unclear. The Deutsch “high-low” word illusion might trigger attentional responses mimicking those under AVHs.

Methods

We therefore have invited 16 patients with first-episode, paranoid schizophrenia, and 16 age- and gender-matched healthy volunteers to undergo the “oddball” event-related potentials elicited by the illusion. The clinical characteristics of patients were measured with the positive and negative symptom scale.

Results

Besides the longer reaction time to the illusion, the standard P2 latency was shortened, the N2 latency was prolonged, and both N1 and P3 amplitudes were reduced in patients. The P3 source analyses showed the activated bilateral temporal lobes, parietal lobe and cingulate cortex in both groups, left inferior temporal gyrus in controls, and left postcentral gyrus in schizophrenia. Moreover, the N1 amplitude was positively correlated with the paranoid score in patients.

Conclusions

Our results were in line with previous neurophysiological and neuroimaging reports of hallucination or auditory processing in schizophrenia, and illustrated a whole process of cerebral information processing from N1 to P3, indicating this illusion had triggered a dynamic cerebral response similar to that of the AVHs had engaged.
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Literature
1.
Kalkstein S, Hurford I, Gur RC. Neurocognition in schizophrenia. Curr Top Behav Neurosci. 2010;4:373–90.CrossRefPubMed
2.
Barch DM, Ceaser A. Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn Sci. 2012;16:27–34.CrossRefPubMed
3.
Salisbury DF. Semantic activation and verbal working memory maintenance in schizophrenic thought disorder: insights from electrophysiology and lexical ambiguity. Clin EEG Neurosci. 2008;39(2):103–7.PubMedCentralCrossRefPubMed
4.
Kuperberg GR, Kreher DA, Ditman T. What can event-related potentials tell us about language, and perhaps even thought, in schizophrenia? Int J Psychophysiol. 2010;75(2):66–76.PubMedCentralCrossRefPubMed
5.
Mohammad OM, DeLisi LE. N400 in schizophrenia patients. Curr Opin Psychiatry. 2013;26(2):196–207.CrossRefPubMed
6.
Løberg EM, Jørgensen HA, Kroken RA, Johnsen E. Auditory verbal hallucinations reflect stable auditory attention deficits: a prospective study. Cogn Neuropsychiatry. 2015;20(1):81–94.CrossRefPubMed
7.
8.
Waters F, Allen P, Aleman A, Fernyhough C, Woodward TS, Badcock JC, et al. Auditory hallucinations in schizophrenia and nonschizophrenia populations: a review and integrated model of cognitive mechanisms. Schizophr Bull. 2012;38(4):683–93.PubMedCentralCrossRefPubMed
9.
Hoskin R, Hunter MD, Woodruff PW. The effect of psychological stress and expectation on auditory perception: A signal detection analysis. Br J Psychol. 2014;105(4):524–46.CrossRefPubMed
10.
Daalman K, Verkooijen S, Derks EM, Aleman A, Sommer IE. The influence of semantic top-down processing in auditory verbal hallucinations. Schizophr Res. 2012;139(1–3):82–6.CrossRefPubMed
11.
Bentall RP. The illusion of reality: a review and integration of psychological research on hallucinations. Psychol Bull. 1990;107:82–95.CrossRefPubMed
12.
Al-Issa I. The illusion of reality or the reality of illusion. Hallucinations and culture. Br J Psychiatry. 1995;166:368–73.CrossRefPubMed
13.
14.
15.
Deutsch D. Musical illusions and paradoxes (compact disc). La Jolla: Philomel Records; 1995.
16.
Xu Y, Zhu J, Chen W, Chai H, He W, Wang W. Personality correlates of reporting Chinese words from the Deutsch “high-low” word illusion by Chinese-speaking people. Neurosci Bull. 2012;28:240–6.CrossRefPubMed
17.
Xu Y, Fan H, Gao Q, Mao H, Zhang Y, Chen WZ, et al. Reporting meaningful Chinese words while listening to the Deutsch word illusions in Chinese patients with cluster A personality disorders. J Psychiatry. 2015;18:1000197.
18.
Stephane M, Barton S, Boutros NN. Auditory verbal hallucinations and dysfunction of the neural substrates of speech. Schizophr Res. 2001;50:61–78.CrossRefPubMed
19.
Jardri R, Pouchet A, Pins D, Thomas P. Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. Am J Psychiatry. 2011;168:73–81.CrossRefPubMed
20.
Kuhn S, Gallina J. Quantitative meta-analysis on state and trait aspects of auditory verbal hallucinations in schizophrenia. Schizophr Bull. 2012;38:779–86.PubMedCentralCrossRefPubMed
21.
Lennox BR, Bert S, Park G, Jones PB, Morris PG. Spatial and temporal mapping of neural activity associated with auditory hallucinations. Lancet. 1999;353:644.CrossRefPubMed
22.
Lennox BR, Park SB, Medley I, Morris PG, Jones PB. The functional anatomy of auditory hallucinations in schizophrenia. Psychiatry Res. 2000;100:13–20.CrossRefPubMed
23.
Shergill SS, Brammer MJ, Williams SC, Murray RM, McGuire PK. Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Arch Gen Psychiatry. 2000a;57:1033–8.CrossRefPubMed
24.
van de Ven VG, Formisano E, Roder CH, Prvulovic D, Bittner RA, Dietz MG, et al. The spatiotemporal pattern of auditory cortical responses during verbal hallucinations. Neuroimage. 2005;27:644–55.CrossRefPubMed
25.
Ford JM, Dierks T, Fisher DJ, Herrmann CS, Hubl D, Kindler J, et al. Neurophysiological studies of auditory verbal hallucinations. Schizophr Bull. 2012;38:715–23.PubMedCentralCrossRefPubMed
26.
Boyd JE, Patriciu I, McKinnon MC, Kiang M. Test-retest reliability of N400 event-related brain potential measures in a word-pair semantic priming paradigm in patients with schizophrenia. Schizophr Res. 2014;158(1–3):195–203.CrossRefPubMed
27.
Besche-Richard C, Iakimova G, Hardy-Baylé MC, Passerieux C. Behavioral and brain measures (N400) of semantic priming in patients with schizophrenia: test-retest effect in a longitudinal study. Psychiatry Clin Neurosci. 2014;68(5):365–73.CrossRefPubMed
28.
Armstrong GA, Singhal A. Neural markers of automatic and controlled attention during immediate and delayed action. Exp Brain Res. 2011;213(1):35–48.CrossRefPubMed
29.
Dima D, Dillo W, Bonnemann C, Emrich HM, Dietrich DE. Reduced P300 and P600 amplitude in the hollow-mask illusion in patients with schizophrenia. Psychiatry Res. 2011;191(2):145–51.CrossRefPubMed
30.
Jeon YW, Polich J. Meta-analysis of P300 and schizophrenia: patients, paradigms, and practical implications. Psychophysiology. 2003;40:684–701.CrossRefPubMed
31.
Bramon E, Rabe-Hesketh S, Sham P, Murray RM, Frangou S. Meta-analysis of the P300 and P50 waveforms in schizophrenia. Schizophr Res. 2004;70:315–29.CrossRefPubMed
32.
Fisher DJ, Labelle A, Knott VJ. Auditory hallucinations and the P3a: attention-switching to speech in schizophrenia. Biol Psychol. 2010;85(3):417–23.CrossRefPubMed
33.
McCarley RW, Faux SF, Shenton ME, Nestor PG, Adams J. Event-related potentials in schizophrenia: their biological and clinical correlates and a new model of schizophrenic pathophysiology. Schizophr Res. 1991;4:209–31.CrossRefPubMed
34.
Turetsky B, Colbath EA, Gur RE. P300 subcomponent abnormalities in schizophrenia: II. Longitudinal stability and relationship to symptom change. Biol Psychiatry. 1998;43:31–9.CrossRefPubMed
35.
Bruder G, Kayser J, Tenke C, Amador X, Friedman M, Sharif Z, et al. Left temporal lobe dysfunction in schizophrenia: event-related potential and behavioral evidence from phonetic and tonal dichotic listening tasks. Arch Gen Psychiatry. 1999;56:267–76.CrossRefPubMed
36.
O’Donnell BF, McCarley RW, Potts GF, Salisbury DF, Nestor PG, Hirayasu Y, et al. Identification of neural circuits underlying P300 abnormalities in schizophrenia. Psychophysiology. 1999;36:388–98.PubMedCentralCrossRefPubMed
37.
McCarley RW, Salisbury DF, Hirayasu Y, Yurgelun-Todd DA, Tohen M, Zarate C, et al. Association between smaller left posterior superior temporal gyrus volume on magnetic resonance imaging and smaller left temporal P300 amplitude in first-episode schizophrenia. Arch Gen Psychiatry. 2002;59:321–31.CrossRefPubMed
38.
Turetsky BI, Calkins ME, Light GA, Olincy A, Radant AD, Swerdlow NR. Neurophysiological endophenotypes of schizophrenia: the viability of selected candidate measures. Schizophr Bull. 2007;33:69–94.PubMedCentralCrossRefPubMed
39.
World Health Organization. The ICD-10 Classification of Mental and Behavioural Disorders: Clinical Descriptions and Diagnostic Guidelines. Geneva: WHO; 1992.
40.
Kay SR, Flszbein A, Opfer LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 1987;13(2):261–76.CrossRefPubMed
41.
Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113.CrossRefPubMed
42.
Ille N, Berg P, Scherg M. Artifact correction of the ongoing EEG using spatial filters based on artifact and brain signal topographies. J Clin Neurophysiol. 2002;19:113–24.CrossRefPubMed
43.
Friston K, Harrison L, Daunizeau J, Kiebel S, Phillips C, Trujillo-Barreto N, et al. Multiple sparse priors for the M/EEG inverse problem. NeuroImage. 2008;39:1104–20.CrossRefPubMed
44.
Litvak V, Mattout J, Kiebel S, Phillips C, Henson R, Kilner J et al. EEG and MEG data analysis in SPM8. Comput Intell Neurosci. 2011. doi: 10.1155/2011/852961
45.
Phillips C, Mattout J, Rugg MD, Maquet P, Friston KJ. An empirical Bayesian solution to the source reconstruction problem in EEG. NeuroImage. 2005;24:997–1011.CrossRefPubMed
46.
Henson RN, Mattout J, Phillips C, Friston KJ. Selecting forward models for MEG source-reconstruction using model-evidence. NeuroImage. 2009;46:168–76.PubMedCentralCrossRefPubMed
47.
Worsley KJ, Friston KJ. Analysis of fMRI time-series revisited--again. NeuroImage. 1995;2:173–81.CrossRefPubMed
48.
Reinhart RM, Mathalon DH, Roach BJ, Ford JM. Relationships between pre-stimulus gamma power and subsequent P300 and reaction time breakdown in schizophrenia. Int J Psychophysiol. 2011;79(1):16–24.PubMedCentralCrossRefPubMed
49.
Ford JM, Mathalon DH, Kalba S, Marsh L, Pfefferbaum A. N1 and P300 abnormalities in patients with schizophrenia, epilepsy, and epilepsy with schizophrenialike features. Biol Psychiatry. 2001;49:848–60.CrossRefPubMed
50.
O’Donnell BF, Vohs JL, Hetrick WP, Carroll CA, Shekhar A. Auditory event-related potential abnormalities in bipolar disorder and schizophrenia. Int J Psychophysiol. 2004;53:45–55.CrossRefPubMed
51.
Calhoun V, Wu L, Kiehl K, Eichele T, Pearlson G. Aberrant processing of deviant stimuli in schizophrenia revealed by fusion of FMRI and EEG Data. Acta Neuropsychiatr. 2010;22:127–38.PubMedCentralCrossRefPubMed
52.
Salisbury DF, Collins KC, McCarley RW. Reductions in the N1 and P2 auditory event-related potentials in first-hospitalized and chronic schizophrenia. Schizophr Bull. 2010;36:991–1000.PubMedCentralCrossRefPubMed
53.
Javitt DC, Sweet RA. Auditory dysfunction in schizophrenia: integrating clinical and basic features. Nature Reviews. Neuroscience. 2015;16(9):535–50.PubMedCentralPubMed
54.
Javitt DC, Freedman R. Sensory processing dysfunction in the personal experience and neuronal machinery of schizophrenia. Am J Psychiatry. 2015;172:17–31.PubMedCentralCrossRefPubMed
55.
Gallinat J, Mulert C, Bajbouj M, Herrmann WM, Schunter J, Senkowski D, et al. Frontal and temporal dysfunction of auditory stimulus processing in schizophrenia. NeuroImage. 2002;17:110–27.CrossRefPubMed
56.
Brown K, Gordon E, Williams L, Bahramali H, Harris A, Gray J, et al. Misattribution of sensory input reflected in dysfunctional target:non-target ERPs in schizophrenia. Psychol Med. 2000;30:1443–9.CrossRefPubMed
57.
Ferreira-Santos F, Silveira C, Almeida PR, Palha A, Barbosa F, Marques-Teixeira J. The auditory P200 is both increased and reduced in schizophrenia? A meta-analytic dissociation of the effect for standard and target stimuli in the oddball task. Clin Neurophysiol. 2012;123(7):1300–8.CrossRefPubMed
58.
Demiralp T, Üçok A, Devrim M, Isoglu-Alkaç Ü, Tecer A, Polich J. N2 and P3 components of event-related potential in first-episode schizophrenic patients: scalp topography, medication, and latency effects. Psychiatry Res. 2002;111:167–79.CrossRefPubMed
59.
60.
van der Stelt O, Frye J, Lieberman JA, Belger A. Impaired P3 generation reflects high-level and progressive neurocognitive dysfunction in schizophrenia. Arch Gen Psychiatry. 2004;61:237–48.CrossRefPubMed
61.
Papageorgiou C, Oulis P, Vasios C, Kontopantelis E, Uzunoglu N, Rabavilas A, et al. P300 alterations in schizophrenic patients experiencing auditory hallucinations. Eur Neuropsychopharmacol. 2004;14(3):227–36.CrossRefPubMed
62.
Onitsuka T, Shenton ME, Salisbury DF, Dickey CC, Kasai K, Toner SK, et al. Middle and inferior temporal gyrus gray matter volume abnormalities in chronic schizophrenia: an MRI study. Am J Psychiatry. 2004;161:1603–11.PubMedCentralCrossRefPubMed
63.
O’Daly OG, Frangou S, Chitnis X, Shergill SS. Brain structural changes in schizophrenia patients with persistent hallucinations. Psychiatry Res. 2007;156:15–21.CrossRefPubMed
64.
Horacek J, Brunovsky M, Novak T, Skrdlantova L, Klirova M, Bubenikova-Valesova V, et al. Effect of low-frequency rTMS on electromagnetic tomography (LORETA) and regional brain metabolism (PET) in schizophrenia patients with auditory hallucinations. Neuropsychobiology. 2007;55:132–42.CrossRefPubMed
65.
Whitney C, Kirk M, O’Sullivan J, Lambon Ralph MA, Jefferies E. The neural organization of semantic control: TMS evidence for a distributed network in left inferior frontal and posterior middle temporal gyrus. Cereb Cortex. 2011;21:1066–75.PubMedCentralCrossRefPubMed
66.
Mellet E, Tzourio N, Denis M, Mazoyer B. Cortical anatomy of mental imagery of concrete nouns based on their dictionary definition. Neuroreport. 1998;9:803–8.CrossRefPubMed
67.
Nakamura K, Honda M, Okada T, Hanakawa T, Toma K, Fukuyama H, et al. Participation of the left posterior inferior temporal cortex in writing and mental recall of kanji orthography: a functional MRI study. Brain. 2000;123:954–67.CrossRefPubMed
68.
Chan AHD, Liu HL, Yip V, Fox PT, Gao JH, Tan LH. Neural systems for word meaning modulated by semantic ambiguity. NeuroImage. 2004;22:1128–33.CrossRefPubMed
69.
Rowan A, Liégeois F, Vargha-Khadem F, Gadian D, Connelly A, Baldeweg T. Cortical lateralization during verb generation: a combined ERP and fMRI study. NeuroImage. 2004;22:665–75.CrossRefPubMed
70.
Kiehl KA, Stevens MC, Celone K, Kurtz M, Krystal JH. Abnormal hemodynamics in schizophrenia during an auditory oddball task. Biol Psychiatry. 2005;57:1029–40.PubMedCentralCrossRefPubMed
71.
Shergill SS, Bullmore E, Simmons A, Murray R, McGuire P. Functional anatomy of auditory verbal imagery in schizophrenic patients with auditory hallucinations. Am J Psychiatry. 2000b;157:1691–3.CrossRefPubMed
72.
Shergill SS, Cameron LA, Brammer MJ, Williams SC, Murray RM, McGuire PK. Modality specific neural correlates of auditory and somatic hallucinations. J Neurol Neurosurg Psychiatry. 2001;71:688–90.PubMedCentralCrossRefPubMed
73.
Nenadic I, Smesny S, Schlosser RG, Sauer H, Gaser C. Auditory hallucinations and brain structure in schizophrenia: voxel-based morphometric study. Br J Psychiatry. 2010;196:412–3.CrossRefPubMed
74.
Diederen KM, Neggers SF, Daalman K, Blom JD, Goekoop R, Kahn RS, et al. Deactivation of the parahippocampal gyrus preceding auditory hallucinations in schizophrenia. Am J Psychiatry. 2010;167:427–35.CrossRefPubMed
75.
van Lutterveld R, Diederen KM, Koops S, Begemann MJ, Sommer IE. The influence of stimulus detection on activation patterns during auditory hallucinations. Schizophr Res. 2013;145:27–32.CrossRefPubMed
76.
Kambeitz-Ilankovic L, Hennig-Fast K, Benetti S, Kambeitz J, Pettersson-Yeo W, O’Daly O, et al. Attentional modulation of source attribution in first-episode psychosis: A functional magnetic resonance imaging study. Schizophr Bull. 2012;39(5):1027–36.PubMedCentralCrossRefPubMed
77.
Falkenberg LE, Specht K, Westerhausen R. Attention and cognitive control networks assessed in a dichotic listening fMRI study. Brain Cogn. 2011;76(2):276–85.CrossRefPubMed
78.
Mangalathu-Arumana J, Beardsley SA, Liebenthal E. Within-subject joint independent component analysis of simultaneous fMRI/ERP in an auditory oddball paradigm. NeuroImage. 2012;60(4):2247–57.PubMedCentralCrossRefPubMed
79.
Kessler C, Steinberg A. Evoked potential variation in schizophrenic subgroups. Biol Psychiatry. 1989;26(4):372–80.CrossRefPubMed
80.
Prévost M, Rodier M, Lionnet C, Brodeur M, King S, Debruille JB. Paranoid induction reduces N400s of healthy subjects with delusional-like ideation. Psychophysiology. 2011;48(7):937–49.CrossRefPubMed
81.
Tomé D, Barbosa F, Nowak K, Marques-Teixeira J. The development of the N1 and N2 components in auditory oddball paradigms: a systematic review with narrative analysis and suggested normative values. J Neural Transm. 2015;122(3):375–91.CrossRefPubMed
Metadata
Title
Event-related potentials elicited by the Deutsch “high-low” word illusion in the patients with first-episode schizophrenia with auditory hallucinations
Authors
You Xu
Hao Chai
Bingren Zhang
Qianqian Gao
Hongying Fan
Leilei Zheng
Hongjing Mao
Yonghua Zhang
Wei Wang
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Psychiatry / Issue 1/2016
Electronic ISSN: 1471-244X
DOI
https://doi.org/10.1186/s12888-016-0747-3

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