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Decreased entropy modulation of EEG response to novelty and relevance in schizophrenia during a P300 task

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Abstract

The analysis of the interaction between novelty and relevance may be of interest to test the aberrant salience hypothesis of schizophrenia (SCH). In comparison with other neuroimaging techniques, such as functional magnetic resonance imaging, electroencephalography (EEG) provides high temporal resolution. Therefore, EEG is useful to analyze transient dynamics in neural activity, even in the range of milliseconds. In this study, EEG activity from 31 patients with SCH and 38 controls was analyzed using Shannon spectral entropy (SE) and median frequency (MF). The aim of the study was to quantify differences between distractor (i.e., novelty) and target (i.e., novelty and relevance) tones in an auditory oddball paradigm. Healthy controls displayed a larger SE decrease in response to target stimulus than in response to distractor tones. SE decrease was accompanied by a significant and widespread reduction of MF (i.e., a significant slowing of EEG activity). In comparison with controls, patients showed a significant reduction of changes in SE in response to both target and distractor tones. These differences were also observed in patients that only received a minimal treatment prior to EEG recording. Furthermore, significant changes in SE were inversely correlated to positive and total symptoms severity for SCH patients. Our findings support the notion that SCH is associated with a reduced response to both novelty and relevance during an auditory P300 task.

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References

  1. American Psychiatric Association APA (2013) Diagnostic and statistical manual of mental disorders: Dsm-v. American Psychiatric Association, Washington, DC

    Book  Google Scholar 

  2. Ardekani BA, Choi SJ, Hossein-Zadeh GA, Porjesz B, Tanabe JL, Lim KO, Bilder R, Helpern JA, Begleiter H (2002) Functional magnetic resonance imaging of brain activity in the visual oddball task. Brain Res Cogn Brain Res 14:347–356

    Article  PubMed  Google Scholar 

  3. Atkinson RJ, Michie PT, Schall U (2012) Duration mismatch negativity and p3a in first-episode psychosis and individuals at ultra-high risk of psychosis. Biol Psychiatry 71:98–104

    Article  PubMed  Google Scholar 

  4. Aviyente S, Brakel LA, Kushwaha RK, Snodgrass M, Shevrin H, Williams WJ (2004) Characterization of event related potentials using information theoretic distance measures. IEEE Trans Biomed Eng 51:737–743

    Article  PubMed  Google Scholar 

  5. Bachiller A, Diez A, Suazo V, Dominguez C, Ayuso M, Hornero R, Poza J, Molina V (2014) Decreased spectral entropy modulation in patients with schizophrenia during a p300 task. Eur Arch Psychiatry Clin Neurosci 264:533–543. doi:10.1007/s00406-014-0488-6

  6. Berezianos A, Tong S, Thakor N (2003) Time-dependant entropy estimation of eeg rhythm changes following brain ischemia. Ann Biomed Eng 31:221–232

    Article  Google Scholar 

  7. Blanco S, García H, Quiroga RQ, Romanelli L, Rosso OA (1995) Stationarity of the eeg series. IEEE Eng Med Biol Mag 14:395–399

    Article  Google Scholar 

  8. Bledowski C, Prvulovic D, Hoechstetter K, Scherg M, Wibral M, Goebel R, Linden DE (2004) Localizing p300 generators in visual target and distractor processing: a combined event-related potential and functional magnetic resonance imaging study. J Neurosci 24:9353–9360

    Article  CAS  PubMed  Google Scholar 

  9. Bramon E, Rabe-Hesketh S, Sham P, Murray RM, Frangou S (2004) Meta-analysis of the p300 and p50 waveforms in schizophrenia. Schizophr Res 70:315–329

    Article  PubMed  Google Scholar 

  10. Casey BJ, Forman SD, Franzen P, Berkowitz A, Braver TS, Nystrom LE, Thomas KM, Noll DC (2001) Sensitivity of prefrontal cortex to changes in target probability: a functional mri study. Hum Brain Mapp 13:26–33

    Article  CAS  PubMed  Google Scholar 

  11. Cortinas M, Corral MJ, Garrido G, Garolera M, Pajares M, Escera C (2008) Reduced novelty-p3 associated with increased behavioral distractibility in schizophrenia. Biol Psychol 78:253–260

    Article  PubMed  Google Scholar 

  12. Davis KL, Kahn RS, Ko G, Davidson M (1991) Dopamine in schizophrenia: a review and reconceptualization. Am J Psychiatry 148:1474–1486

    Article  CAS  PubMed  Google Scholar 

  13. Delorme A, Makeig S (2004) Eeglab: an open source toolbox for analysis of single-trial eeg dynamics including independent component analysis. J Neurosci Methods 134:9–21

    Article  PubMed  Google Scholar 

  14. Demiralp T, Ademoglu A, Comerchero M, Polich J (2001) Wavelet analysis of p3a and p3b. Brain Topogr 13:251–267

    Article  CAS  PubMed  Google Scholar 

  15. Gralewicz S, Lutz P, Wiaderna D, Tomas T (2003) Alteration in behavioral sensitivity to amphetamine after treatment with oxotremorine. Effect of dose and test environment. Behav Brain Res 147:163–173

    Article  CAS  PubMed  Google Scholar 

  16. Grondin R, Cass WA, Zhang Z, Stanford JA, Gash DM, Gerhardt GA (2003) Glial cell line-derived neurotrophic factor increases stimulus-evoked dopamine release and motor speed in aged rhesus monkeys. J Neurosci 23:1974–1980

    CAS  PubMed  Google Scholar 

  17. Gur RE, Turetsky BI, Loughead J, Snyder W, Kohler C, Elliott M, Pratiwadi R, Ragland JD, Bilker WB, Siegel SJ, Kanes SJ, Arnold SE, Gur RC (2007) Visual attention circuitry in schizophrenia investigated with oddball event-related functional magnetic resonance imaging. A J Psychiatry 164:442–449

    Article  Google Scholar 

  18. Hattori S, Li Q, Matsui N, Nishino H (1993) Treadmill running test for evaluating locomotor activity after 6-ohda lesions and dopaminergic cell grafts in the rat. Brain Res Bull 31:433–435

    Article  CAS  PubMed  Google Scholar 

  19. Heitland I, Kenemans JL, Oosting RS, Baas JM, Bocker KB (2013) Auditory event-related potentials (p3a, p3b) and genetic variants within the dopamine and serotonin system in healthy females. Behav Brain Res 249:55–64

    Article  CAS  PubMed  Google Scholar 

  20. Hermens DF, Ward PB, Hodge MA, Kaur M, Naismith SL, Hickie IB (2010) Impaired mmn/p3a complex in first-episode psychosis: cognitive and psychosocial associations. Prog Neuropsychopharmacol Biol Psychiatry 34:822–829

    Article  CAS  PubMed  Google Scholar 

  21. Inouye T, Shinosaki K, Sakamoto H, Toi S, Ukai S, Iyama A, Katsuda Y, Hirano M (1991) Quantification of eeg irregularity by use of the entropy of the power spectrum. Electroencephalogr Clin Neurophysiol 79:204–210

    Article  CAS  PubMed  Google Scholar 

  22. Kapur S (2003) Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. Am J Psychiatry 160:13–23

    Article  PubMed  Google Scholar 

  23. Kaur M, Battisti RA, Ward PB, Ahmed A, Hickie IB, Hermens DF (2011) Mmn/p3a deficits in first episode psychosis: comparing schizophrenia-spectrum and affective-spectrum subgroups. Schizophr Res 130:203–209

    Article  PubMed  Google Scholar 

  24. Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (panss) for schizophrenia. Schizophr Bull 13:261–276

    Article  CAS  PubMed  Google Scholar 

  25. Keren AS, Yuval-Greenberg S, Deouell LY (2010) Saccadic spike potentials in gamma-band eeg: characterization, detection and suppression. Neuroimage 49:2248–2263

    Article  PubMed  Google Scholar 

  26. Laurens KR, Kiehl KA, Ngan ET, Liddle PF (2005) Attention orienting dysfunction during salient novel stimulus processing in schizophrenia. Schizophr Res 75:159–171

    Article  PubMed  Google Scholar 

  27. Mondragon-Maya A, Solis-Vivanco R, Leon-Ortiz P, Rodriguez-Agudelo Y, Yanez-Tellez G, Bernal-Hernandez J, Cadenhead KS, de la Fuente-Sandoval C (2013) Reduced p3a amplitudes in antipsychotic naive first-episode psychosis patients and individuals at clinical high-risk for psychosis. J Psychiatr Res 47:755–761

    Article  PubMed  Google Scholar 

  28. Monville C, Torres EM, Dunnett SB (2006) Comparison of incremental and accelerating protocols of the rotarod test for the assessment of motor deficits in the 6-ohda model. J Neurosci Methods 158:219–223

    Article  PubMed  Google Scholar 

  29. Okubo Y, Suhara T, Suzuki K, Kobayashi K, Inoue O, Terasaki O, Someya Y, Sassa T, Sudo Y, Matsushima E, Iyo M, Tateno Y, Toru M (1997) Decreased prefrontal dopamine d1 receptors in schizophrenia revealed by pet. Nature 385:634–636

    Article  CAS  PubMed  Google Scholar 

  30. Olsson M, Nikkhah G, Bentlage C, Bjorklund A (1995) Forelimb akinesia in the rat parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J Neurosci 15:3863–3875

    CAS  PubMed  Google Scholar 

  31. Polich J (2007) Updating p300: an integrative theory of p3a and p3b. Clin Neurophysiol 118:2128–2148

    Article  PubMed Central  PubMed  Google Scholar 

  32. Poza J, Hornero R, Abasolo D, Fernandez A, Garcia M (2007) Extraction of spectral based measures from meg background oscillations in alzheimer’s disease. Med Eng Phys 29:1073–1083

    Article  PubMed  Google Scholar 

  33. Poza J, Hornero R, Escudero J, Fernandez A, Sanchez CI (2008) Regional analysis of spontaneous meg rhythms in patients with alzheimer’s disease using spectral entropies. Ann Biomed Eng 36:141–152

    Article  PubMed  Google Scholar 

  34. Rangel-Gomez M, Hickey C, van Amelsvoort T, Bet P, Meeter M (2013) The detection of novelty relies on dopaminergic signaling: evidence from apomorphine’s impact on the novelty n2. PLoS One 8:e66469

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Redgrave P, Gurney K (2006) The short-latency dopamine signal: a role in discovering novel actions? Nat Rev Neurosci 7:967–975

    Article  CAS  PubMed  Google Scholar 

  36. Rissling AJ, Park SH, Young JW, Rissling MB, Sugar CA, Sprock J, Mathias DJ, Pela M, Sharp RF, Braff DL, Light GA (2013) Demand and modality of directed attention modulate “pre-attentive” sensory processes in schizophrenia patients and nonpsychiatric controls. Schizophr Res 146:326–335

    Article  PubMed Central  PubMed  Google Scholar 

  37. Roach BJ, Mathalon DH (2008) Event-related eeg time-frequency analysis: an overview of measures and an analysis of early gamma band phase locking in schizophrenia. Schizophr Bull 34:907–926

    Article  PubMed Central  PubMed  Google Scholar 

  38. Rozas G, Labandeira Garcia JL (1997) Drug-free evaluation of rat models of parkinsonism and nigral grafts using a new automated rotarod test. Brain Res 749:188–199

    Article  CAS  PubMed  Google Scholar 

  39. Sabeti M, Katebi S, Boostani R (2009) Entropy and complexity measures for eeg signal classification of schizophrenic and control participants. Artif Intell Med 47:263–274

    Article  PubMed  Google Scholar 

  40. Schoen W, Chang JS, Lee U, Bob P, Mashour GA (2011) The temporal organization of functional brain connectivity is abnormal in schizophrenia but does not correlate with symptomatology. Conscious Cogn 20:1050–1054

    Article  PubMed  Google Scholar 

  41. Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech 27:379–423, 623–656

  42. TEA Ediciones SA (1999) Escala wechsler de inteligencia para adultos. TEA Ediciones, S.A, Madrid, España

    Google Scholar 

  43. Uhlhaas PJ, Singer W (2010) Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11:100–113

    Article  CAS  PubMed  Google Scholar 

  44. von Stein A, Chiang C, Konig P (2000) Top-down processing mediated by interareal synchronization. Proc Natl Acad Sci USA 97:14748–14753

    Article  Google Scholar 

Download references

Acknowledgments

The present work was supported in part by: ‘Ministerio de Economía y Competitividad’ and FEDER under project TEC2011-22987 and by the ‘Project Cero 2011 on Ageing’ from ‘Fundación General CSIC,’ ‘Obra Social La Caixa’ and CSIC; ‘Fondo de Investigaciones Sanitarias (Instituto de Salud Carlos III)’ (FIS PI1102203) and the ‘Gerencia Regional de Salud de Castilla y León’ (GRS 613/A/11) Grants; a Marie Curie Intra European Fellowship within the 7th European Community Framework Programme (330156-CODIP) to A. Díez; a predoctoral scholarship from the University of Salamanca and Santander Bank to V. Suazo; and a PIF-UVA grant from the University of Valladolid to A. Bachiller.

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All authors have approved the final manuscript. On behalf of all authors, the corresponding author states that there is no conflict of interest.

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The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008.

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Correspondence to Vicente Molina.

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Bachiller, A., Lubeiro, A., Díez, Á. et al. Decreased entropy modulation of EEG response to novelty and relevance in schizophrenia during a P300 task. Eur Arch Psychiatry Clin Neurosci 265, 525–535 (2015). https://doi.org/10.1007/s00406-014-0525-5

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