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Increased Gamma Oscillations Evoked by Physically Salient Distracters are Associated with Schizotypy

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Abstract

Over the last decade, there has been growing interest in aberrant salience as a precursor of positive symptoms in schizophrenia. The present study investigates the neurophysiology of attentional capture by salient stimuli in the visual modality. Evoked oscillatory activity in the gamma frequency range (40 Hz) was assessed during visual processing of physically salient distracters and evaluated in relation to schizotypy and its positive, negative and disorganized dimension. The early evoked visual gamma-band response (GBR) was assessed for 24 healthy participants using EEG time–frequency analysis. Physical salience was constituted by colored stimuli diverting from an ongoing baseline condition. schizotypal personality traits were measured by the schizotypal personality questionnaire (SPQ; Raine in Schizophr Bull 17:555–564, 1991). The early evoked visual GBR was significantly pronounced in the physically salient distracter condition. GBR signal power was significantly correlated with positive schizotypal personality traits (r = 0.588; p = 0.024*). Our results indicate that the early evoked GBR in visual processing of physically salient distracters is associated with schizotypy. These findings refer to the phenomenology of aberrant salience by bridging the gap to neurophysiological research on early sensory selection and attentional capture in the schizophrenia spectrum.

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References

  • Andreou C, Nolte G, Leicht G, Polomac N, Hanganu-Opatz IL, Lambert M, Engel AK, Mulert C (2014). Increased resting-state gamma-band connectivity in first-episode schizophrenia. Schizophr Bull. doi:10.1093/schbul/sbu121

  • Anscombe R (1987) The disorder of consciousness in schizophrenia. Schizophr Bull 13(2):241–260

    Article  CAS  PubMed  Google Scholar 

  • Basar-Eroglu C, Brand A, Hildebrandt H, Kedzior KK, Mathes B (2007) Working memory related gamma oscillations in schizophrenia patients. Int J Psychophysiol 64:39–45

    Article  PubMed  Google Scholar 

  • Bosman CA, Schoffelen J-M, Brunet N, Oostenveld R, Bastos AM, Womelsdorf T, Rubehn B, Stieglitz T, De Weerd P, Fries P (2012) Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron 75:875–888

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Busch NA, Debener S, Kranczioch C, Engel AK, Herrmann CS (2004) Size matters: effects of stimulus size, duration and eccentricity on the visual gamma-band response. Clin Neurophysiol 115(8):1810–1820

    Article  PubMed  Google Scholar 

  • Busch NA, Schadow J, Fründ I, Herrmann CS (2006) Time-frequency analysis of target detection reveals an early interface between bottom-up and top-down processes in the gamma-band. Neuroimage 29(4):1106–1116

    Article  PubMed  Google Scholar 

  • Buzsaki G, Draghun A (2004) Neural oscillations in cortical networks. Science 304:1926–1929

    Article  CAS  PubMed  Google Scholar 

  • Carl C, Açık A, König P, Engel AK, Hipp JF (2012) The saccadic spike artifact in MEG. Neuroimage 59(2):1657–1667

    Article  PubMed  Google Scholar 

  • Chen C-M, Stanford AD, Mao X, Abi-Dargham A, Shungu DC, Lisanby SH, Schroeder CE, Kegeles LS (2014) GABA level, gamma oscillation, and working memory performance in schizophrenia. Neuroimage Clin 4:531–539

    Article  PubMed Central  PubMed  Google Scholar 

  • Gallinat J, Winterer G, Herrmann CS, Senkowski D (2004) Reduced oscillatory gamma-band responses in unmedicated schizophrenic patients indicate impaired frontal network processing. Clin Neurophysiol 115:1863–1874

    Article  PubMed  Google Scholar 

  • Gonzalez-Burgos G, Lewis D (2008) GABA neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunctions in schizophrenia. Schizophr Bull 34:944–961

    Article  PubMed Central  PubMed  Google Scholar 

  • Gordon E, Williams L, Haig AR, Wright J, Meares RA (2001) Symptom profile and “gamma” processing in schizophrenia. Cogn Neuropsychiatry 6(1):7–19

  • Gradin VB, Waiter G, O’Connor A, Romaniuk L, Stickle C, Matthews K, Hall J, Steele JD (2012) Salience network-midbrain dysconnectivity and blunted reward signals in schizophrenia. Psychiatry Res 211:104–111

    Article  PubMed  Google Scholar 

  • Gruber T, Müller MM, Keil A, Elbert T (1999) Selective visual-spatial attention alters induced gamma band responses in the human EEG. Clin Neurophysiol 110(12):2074–2085

    Article  CAS  PubMed  Google Scholar 

  • Haenschel C, Bittner RA, Waltz J, Haertling F, Wibral M, Singer W, Linden DEJ, Rodriguez E (2009) Cortical oscillatory activity is critical for working memory as revealed by deficits in early-onset schizophrenia. J Neurosci 29(30):9481–9489

    Article  CAS  PubMed  Google Scholar 

  • Hahn B, Robinson BM, Kaiser ST, Harvey AN, Beck VM, Leonard CJ, Kappenman ES, Luck SJ, Gold JM (2010) Failure of schizophrenia patients to overcome salient distractors during working memory encoding. Biol Psychiatry 68(7):603–609

    Article  PubMed Central  PubMed  Google Scholar 

  • Herrmann CS, Mecklinger A (2001) Gamma activity in human EEG is related to highspeed memory comparisons during object selective attention. Vis Cogn 8(3–5):593–608

    Article  Google Scholar 

  • Herrmann CS, Mecklinger AM, Pfeifer E (1999) Gamma responses and ERPs in a visual classification task. Clin Neurophysiol 110:636–642

  • Herrmann CS, Munk MHJ, Engel AK (2004) Cognitive functions of gamma-band activity: memory match and utilization. Trends in Cogn Sci 8(8):347–355

    Article  Google Scholar 

  • Herrmann CS, Grigutsch M, Busch NA (2005) EEG oscillations and wavelet analysis. In: Todd CH (ed) Event-related potentials: a methods handbook. MIT Press, Cambridge

    Google Scholar 

  • Jokeit H, Makeig S (1994) Different event-related patterns of γ-band power in brain waves of fast and slow-reacting subjects. Proc Natl Acad Sci USA 91:6339–6343

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kapur S (2003) Psychosis as a state of aberrant salience: a framework linking biology, phenomenolo-gy, and pharmacology in schizophrenia. Am J Psychiatry 160(1):13–23

    Article  PubMed  Google Scholar 

  • Kapur S (2005) From dopamine to salience to psychosis—linking biology, pharmacology and phenomenology of psychosis. Schizophr Res 79:59–68

    Article  PubMed  Google Scholar 

  • Karakas S, Basar E (1998) Early gamma response is sensory in origin: a conclusion based on cross-comparison of results from multiple experimental paradigms. Int J Psychophysiol 31(1):13–31

    Article  CAS  PubMed  Google Scholar 

  • Karakas S, Basar-Eroglu C, Özesmi C, Kafadar H, Erzengin ÖÜ (2001) Gamma response of the brain: a multifunctional oscillation that represents bottom-up with top-down processing. Int J Psychophysiol 39:137–150

    Article  CAS  PubMed  Google Scholar 

  • Klosterkötter J, Hellmich M, Steinmeyer EM, Schultze-Luttner F (2001) Diagnosing schizophrenia in the initial prodromal phase. Arch Gen Psychiatry 58:158–164

    Article  PubMed  Google Scholar 

  • Kömek K, Ermentrout GB, Walter CP, Cho RY (2012) Dopamine and gamma band synchrony in schizophrenia—insights from computational and empirical studies. Eur J Neurosci 36:2146–2155

    Article  PubMed Central  PubMed  Google Scholar 

  • Koychev I, Deakin JFW, Haenschel C, El-Deredy W (2011) Abnormal neural oscillations in schizotypy during a visual working memory task: support for a deficient top-down network? Neuropsychologia 49(10):2866–2873

    Article  PubMed  Google Scholar 

  • Krishnan GP, Vohs JL, Hetrick WP, Carroll CA, Shekhar A, Bockbrader MA, O’Donnell BF (2005) Steady state visual evoked potential abnormalities in schizophrenia. Clin Neurophysiol 116(3):614–624

    Article  PubMed  Google Scholar 

  • Lee K-H, Williams LM, Breakspear M, Gordon E (2003) Synchronous gamma activity: a review and contribution to an integrative neuroscience model of schizophrenia. Brain Res Rev 41(1):57–78

    Article  PubMed  Google Scholar 

  • Leicht G, Kirsch V, Giegling I, Karch S, Hantschk I, Möller H-J, Pogarell O, Hegerl U, Rujescu D, Mulert C (2010) Reduced early auditory evoked gamma-band response in patients with schizophrenia. Biol Psychiatry 67(3):224–231

    Article  PubMed  Google Scholar 

  • Leicht G, Karch S, Karamatskos E, Giegling I, Möller H-J, Hegerl U, Pogarell O, Rujescu D, Mulert C (2011) Alterations of the early auditory evoked gamma-band response in first-degree relatives of patients with schizophrenia: hints to a new intermediate phenotype. J Psychiatr Res 45:699–705

    Article  PubMed  Google Scholar 

  • Linney YM, Murray RM, Peters ER, MacDonald AM, Rijsdijk F, Sham PC (2003) A quantitative genetic analysis of schizotypal personality traits. Psychol Med 33(5):803–816

    Article  CAS  PubMed  Google Scholar 

  • Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S, Grace AA (2008) Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 31(5):234–242

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Minzenberg MJ, Firl AJ, Yoon JH, Gomes GC, Reinking G, Carter CS (2010) Gamma oscillatory power is impaired during cognitive control independent of medication status in first-episode schizophrenia. Neuropsychopharmacology 35:2590–2599

    Article  PubMed Central  PubMed  Google Scholar 

  • Mishara AL, Fusar-Poli P (2013) The phenomenology and neurobiology of delusion formation during psychosis onset: Jaspers, Truman symptoms, and aberrant salience. Schizophr Bull 39(2):278–286

    Article  PubMed Central  PubMed  Google Scholar 

  • Mulert C, Leicht G, Pogarell O, Mergl R, Karch S, Juckel G, Möller H-J, Hegerl U (2007) Auditory cortex and anterior cingulate cortex sources of the early evoked gamma-band response: relationship to task difficulty and mental effort. Neuropsychologia 45:2294–2306

    Article  PubMed  Google Scholar 

  • Mulert C, Leicht G, Hepp P, Kirsch V, Karch S, Pogarell O, Reiser M, Hegerl U, Jäger L, Moller HJ, McCarley RW (2010) Single-trial coupling of the gamma-band response and the corresponding BOLD signal. Neuroimage 49:2238–2247

    Article  CAS  PubMed  Google Scholar 

  • Mulert C, Kirsch V, Pascual-Marqui R, McCarley RW, Spencer KM (2011) Long-range synchrony of gamma oscillations and auditory hallucination symptoms in schizophrenia. Int J Psychophysiol 79(1):55–63

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murray GK, Corlett PR, Clark L, Pessiglione M, Blackwell AD, Honey G, Jones PB, Bullmore ET, Robbins TW, Fletcher PC (2008) Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol Psychiatry 13:267–276

    Article  CAS  Google Scholar 

  • Palaniyappan L, Liddle PF (2012) Does the salience network play a cardinal role in psychosis? An emerging hypothesis of insular dysfunction. J Psychiatry Neurosci 37(1):17–27

    Article  PubMed Central  PubMed  Google Scholar 

  • Raine A (1991) The SPQ: a scale for the assessment of schizotypal personality based on DSM-III-R criteria. Schizophr Bull 17(4):555–564

    Article  CAS  PubMed  Google Scholar 

  • Raine A, Reynolds C, Lencz T, Scerbo A, Triphon N, Kim D (1994) Cognitive-perceptual, interpersonal and disorganized features of schizotypal personality. Schizophr Bull 20(1):191–201

    Article  CAS  PubMed  Google Scholar 

  • Roiser JP, Howes OD, Chaddock CA, Joyce EM, McGuire P (2013) Neural and behavioral correlates of aberrant salience in individuals at risk for psychosis. Schizophr Bull 39(6):1328–1336

  • Roiser JP, Stephan KE, den Ouden HEM, Barnes TRE, Friston KJ, Joyce EM (2009) Do patients with schizophrenia exhibit aberrant salience? Psychol Med 39:199–209

  • Schneider TR, Debener S, Oostenveld R, Engel AK (2008) Enhanced EEG gamma-band activity reflects multisensory semantic matching in visual-to-auditory object priming. Neuroimage 42(3):1244–1254

    Article  PubMed  Google Scholar 

  • Senkowski D, Herrmann CS (2002) Effects of task difficulty on evoked gamma activity and ERPs in a visual discrimination task. Clin Neurophysiol 113(11):1742–1753

    Article  PubMed  Google Scholar 

  • Sommer IEC, Diederen KMJ, Blom J-D, Willems A, Kushan L, Slotema K, Boks KPM, Daalman K, Hoek HW, Neggers SFW (2008) Auditory verbal hallucinations predominantly activate the right inferior frontal area. Brain 131(12):3169–3177

    Article  PubMed  Google Scholar 

  • Spencer KM, Nestor PG, Perlmutter R, Niznikiewicz MA, Klump MC, Frumin M, Shenton ME, McCarley RW (2004) Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc Natl Acad Sci USA 101(49):17288–17293

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Spencer KM, Salisbury DF, Shenton ME, McCarley RW (2008) γ-Band auditory steady-state responses are impaired in first episode psychosis. Biol Psychiatry 64(5):369–375

    Article  PubMed Central  PubMed  Google Scholar 

  • Spencer KM, Niznikiewicz MA, Nestor PG, Shenton ME, McCarley RW (2009) Left auditory cortex gamma synchronization and auditory hallucination symptoms in schizophrenia. BMC Neurosci 10:85

    Article  PubMed Central  PubMed  Google Scholar 

  • Tallon-Baudry C, Bertrand O, Peronnet F, Pernier J (1998) Induced γ-band activity during the delay of a visual short-term memory task in humans. J Neurosci 18(11):4244–4254

    CAS  PubMed  Google Scholar 

  • Teising M (2005) Permeability and demarcation in the psychoanalytic process. Functions of the contact-barrier. Int J Psychoanal 86:1627–1644

    PubMed  Google Scholar 

  • Uhlhaas PJ, Singer W (2010) Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11(2):100–113

    Article  CAS  PubMed  Google Scholar 

  • Yoon JH, Maddock RJ, Rokem A, Silver MA, Minzenberg MJ, Ragland JD, Carter CS (2010) GABA concentration is reduced in visual cortex in schizophrenia and correlates with orientation-specific surround suppression. J Neurosci 30(10):3777–3781

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank the Werner Otto foundation for the financial support of L.K.; C.M. and G.L. were supported by the DFG grant for the SFB 936. We would also like to thank the anonymous reviewers for their annotations, as well as Nenad Polomac for technical support and Dr. Cornelia Stöckel as well as Mareike Pietzsch for proofreading the manuscript.

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  1. Department of Psychiatry and Psychotherapy, Center for Psychosocial Medicine, University Medical Center Hamburg-Eppendorf, Martinistr. 52, 20246, Hamburg, Germany

    Laura Kornmayer, Gregor Leicht & Christoph Mulert

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  1. Laura Kornmayer
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  2. Gregor Leicht
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  3. Christoph Mulert
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Correspondence to Christoph Mulert.

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Kornmayer, L., Leicht, G. & Mulert, C. Increased Gamma Oscillations Evoked by Physically Salient Distracters are Associated with Schizotypy. Brain Topogr 28, 153–161 (2015). https://doi.org/10.1007/s10548-014-0418-y

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  • DOI: https://doi.org/10.1007/s10548-014-0418-y

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