Elevated midline-parietal gamma band noise power in schizophrenia but not in bipolar patients

  • Vanessa Suazo
  • Alba Lubeiro
  • Rosa Jurado-Barba
  • Marta Moreno-Ortega
  • Mónica Dompablo
  • Isabel Morales-Muñoz
  • Roberto Rodriguez-Jimenez
  • Tomas Palomo
  • Vicente MolinaEmail author
Original Paper


Gamma oscillations are key in coordinating brain activity and seem to be altered in schizophrenia. In previous work, we studied the spatial distribution of a noise power measure (scalp-recorded electroencephalographic activity unlocked to stimuli) and found higher magnitudes in the gamma band related to symptoms and cognition in schizophrenia. In the current study, we sought to replicate those findings and to study its specificity for schizophrenia in a completely independent sample. A principal component analysis (PCA) was used to determine the factorial structure of gamma noise power acquired with an electroencephalographic recording during an odd-ball P300 paradigm in the 250- to 550-ms window in 70 patients with schizophrenia (16 patients with first episode), 45 bipolar patients and 65 healthy controls. Clinical and cognitive correlates of the resulting factors were also assessed. Three factors arose from the PCA. The first displayed a midline-parietal distribution (roughly corresponding to the default mode network), the second was centro-temporal and the third anterior–frontal. Schizophrenia but not bipolar patients showed higher gamma noise power loadings in the first factor in comparison with controls. Scores for this factor were significantly and directly associated with positive and total symptoms in patients and inversely associated with global cognition in all participants. The results of this study replicate those of our previous publication and suggest an elevated midline-parietal gamma noise power specific to schizophrenia. The gamma noise power measure seems to be a useful tool for studying background oscillatory activity during performance of cognitive tasks.


Noise power Default mode network Psychosis Positive symptoms Cognition 



The present work was supported in part by the Fondo de Investigaciones Sanitarias (Instituto de Salud Carlos III) (FIS PI080017, FIS PI1102303) and the Gerencia Regional de Salud de Castilla y León (GRS 249/A/08, GRS 613/A/11) Grants to V. Molina; a predoctoral scholarship from the University of Salamanca and Santander Bank to V. Suazo; a predoctoral scholarship from Consejería de Educación-Junta de Castilla y León and European Social Fund to A. Lubeiro; and Grants to T. Palomo and R. Rodriguez-Jimenez from the Fondo de Investigaciones Sanitarias (Instituto de Salud Carlos III) (FIS PI080514), Madrid’s Regional Government (S2010/BMD-2422 AGES) and the European Union Structural Funds, and the Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM) of the Instituto de Salud Carlos III. All authors have approved the final manuscript

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

Supplementary material

406_2016_673_MOESM1_ESM.docx (810 kb)
Supplementary material 1 (DOCX 809 kb)


  1. 1.
    American Psychiatric Association APA (2000) Diagnostic and statistical manual of mental disorders: DSM-IV-TR. American Psychiatric Association, WashingtonGoogle Scholar
  2. 2.
    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 24:9353–9360CrossRefPubMedGoogle Scholar
  3. 3.
    British Medical Journal (1964) Human Experimentation. Code of ethics of the world medical association. Declaration of Helsinki. Br Med J 2:177–178Google Scholar
  4. 4.
    Buzsáki G (2006) Diversity of cortical functions: inhibition. In: Rhythms of the brain. Oxford University Press, New York, pp 61–79. ISBN 019804125X Google Scholar
  5. 5.
    Buzsáki G (2006) The Gamma Buzz: gluing by oscillations in the waking brain. In: Rhythms of the Brain. Oxford University Press, New York, pp 231–261. ISBN 9780198041252Google Scholar
  6. 6.
    Carl C, Acik A, Konig P, Engel AK, Hipp JF (2012) The saccadic spike artifact in MEG. Neuroimage 59:1657–1667CrossRefPubMedGoogle Scholar
  7. 7.
    Cohen J (1992) A power primer. Psychol Bull 112:155–159CrossRefPubMedGoogle Scholar
  8. 8.
    Connolly JF, Kleinman KM (1978) A single channel method for recording vertical and lateral eye movements. Electroencephalogr Clin Neurophysiol 45:128–129CrossRefPubMedGoogle Scholar
  9. 9.
    Cramer EM, Bock RD (1966) Multivariate analysis. Rev Educ Res 36:604–617Google Scholar
  10. 10.
    Chen CM, 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 4:531–539CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Del Pino I, Garcia-Frigola C, Dehorter N, Brotons-Mas JR, Alvarez-Salvado E, Martinez de Lagran M, Ciceri G, Gabaldon MV, Moratal D, Dierssen M, Canals S, Marin O, Rico B (2013) Erbb4 deletion from fast-spiking interneurons causes schizophrenia-like phenotypes. Neuron 79:1152–1168CrossRefPubMedGoogle Scholar
  12. 12.
    Diez A, Suazo V, Casado P, Martin-Loeches M, Molina V (2013) Spatial distribution and cognitive correlates of gamma noise power in schizophrenia. Psychol Med 43:1175–1185CrossRefPubMedGoogle Scholar
  13. 13.
    Diez A, Suazo V, Casado P, Martin-Loeches M, Perea MV, Molina V (2014) Frontal gamma noise power and cognitive domains in schizophrenia. Psychiatry Res 221:104–113CrossRefPubMedGoogle Scholar
  14. 14.
    Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673–9678CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Gandal MJ, Edgar JC, Klook K, Siegel SJ (2012) Gamma synchrony: towards a translational biomarker for the treatment-resistant symptoms of schizophrenia. Neuropharmacology 62:1504–1518CrossRefPubMedGoogle Scholar
  16. 16.
    Garrity AG, Pearlson GD, McKiernan K, Lloyd D, Kiehl KA, Calhoun VD (2007) Aberrant “default mode” functional connectivity in schizophrenia. Am J Psychiatry 164:450–457CrossRefPubMedGoogle Scholar
  17. 17.
    Gevins A (2002) Electrophysiological Imaging of Brain Function. In: Toga AW, Mazziotta JC (eds) Brain mapping: the methods. Academic Press, London, pp 175–186CrossRefGoogle Scholar
  18. 18.
    Goncharova II, McFarland DJ, Vaughan TM, Wolpaw JR (2003) EMG contamination of EEG: spectral and topographical characteristics. Clin Neurophysiol 114:1580–1593CrossRefPubMedGoogle Scholar
  19. 19.
    Goyal N, Praharaj SK, Desarkar P, Nizamie H (2011) Electroencephalographic abnormalities in clozapine-treated patients: a cross-sectional study. Psychiatry Investig 8:372–376CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Gratton G, Coles MG, Donchin E (1983) A new method for off-line removal of ocular artifact. Electroencephalogr Clin Neurophysiol 55:468–484CrossRefPubMedGoogle Scholar
  21. 21.
    Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100:253–258CrossRefPubMedGoogle Scholar
  22. 22.
    Howell DC (2007) Statistical methods for psychology. Thompson Wadsworth, BelmontGoogle Scholar
  23. 23.
    Jerbi K, Vidal JR, Ossandon T, Dalal SS, Jung J, Hoffmann D, Minotti L, Bertrand O, Kahane P, Lachaux JP (2010) Exploring the electrophysiological correlates of the default-mode network with intracerebral EEG. Front Syst Neurosci 4:27PubMedPubMedCentralGoogle Scholar
  24. 24.
    Kapur S (2003) Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. Am J Psychiatry 160:13–23CrossRefPubMedGoogle Scholar
  25. 25.
    Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13:261–276CrossRefPubMedGoogle Scholar
  26. 26.
    Keren AS, Yuval-Greenberg S, Deouell LY (2010) Saccadic spike potentials in gamma-band EEG: characterization, detection and suppression. Neuroimage 49:2248–2263CrossRefPubMedGoogle Scholar
  27. 27.
    Kikuchi YS, Sato W, Ataka K, Yagisawa K, Omori Y, Kanbayashi T, Shimizu T (2014) Clozapine-induced seizures, electroencephalography abnormalities, and clinical responses in Japanese patients with schizophrenia. Neuropsychiatr Dis Treat 10:1973–1978CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Lee KH, Williams LM, Breakspear M, Gordon E (2003) Synchronous gamma activity: a review and contribution to an integrative neuroscience model of schizophrenia. Brain Res Brain Res Rev 41:57–78CrossRefPubMedGoogle Scholar
  29. 29.
    Lewis DA, Sweet RA (2009) Schizophrenia from a neural circuitry perspective: advancing toward rational pharmacological therapies. J. Clin. Invest. 119:706–716CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Manoach DS (2003) Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophr Res 60:285–298CrossRefPubMedGoogle Scholar
  31. 31.
    Möcks J, Kohler W, Gasser T, Pham DT (1988) Novel approaches to the problem of latency jitter. Psychophysiology 25:217–226CrossRefPubMedGoogle Scholar
  32. 32.
    Muthukumaraswamy SD (2013) High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations. Front Hum Neurosci 7:138CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Niessing J, Ebisch B, Schmidt KE, Niessing M, Singer W, Galuske RA (2005) Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309:948–951CrossRefPubMedGoogle Scholar
  34. 34.
    Nuechterlein KH, Green MF, Kern RS, Baade LE, Barch DM, Cohen JD, Essock S, Fenton WS, Frese FJ 3rd, Gold JM, Goldberg T, Heaton RK, Keefe RS, Kraemer H, Mesholam-Gately R, Seidman LJ, Stover E, Weinberger DR, Young AS, Zalcman S, Marder SR (2008) The MATRICS Consensus Cognitive Battery, part 1: test selection, reliability, and validity. Am J Psychiatry 165:203–213CrossRefPubMedGoogle Scholar
  35. 35.
    O’Connor BP (2000) SPSS and SAS programs for determining the number of components using parallel analysis and velicer’s MAP test. Behav Res Methods Instrum Comput 32:396–402CrossRefPubMedGoogle Scholar
  36. 36.
    O’Donnell RD, Berkhout J, Adey WR (1974) Contamination of scalp EEG spectrum during contraction of cranio-facial muscles. Electroencephalogr Clin Neurophysiol 37:145–151CrossRefPubMedGoogle Scholar
  37. 37.
    Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98:676–682CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Rodriguez-Jimenez R, Bagney A, Garcia-Navarro C, Aparicio AI, Lopez-Anton R, Moreno-Ortega M, Jimenez-Arriero MA, Santos JL, Lobo A, Kern RS, Green MF, Nuechterlein KH, Palomo T (2012) The MATRICS consensus cognitive battery (MCCB): co-norming and standardization in Spain. Schizophr Res 134:279–284CrossRefPubMedGoogle Scholar
  39. 39.
    Rolfs M (2009) Microsaccades: small steps on a long way. Vis Res 49:2415–2441CrossRefPubMedGoogle Scholar
  40. 40.
    Rolfs M, Engbert R, Kliegl R (2005) Crossmodal coupling of oculomotor control and spatial attention in vision and audition. Exp Brain Res 166:427–439CrossRefPubMedGoogle Scholar
  41. 41.
    Roye A, Schroger E, Jacobsen T, Gruber T (2010) Is my mobile ringing? Evidence for rapid processing of a personally significant sound in humans. J Neurosci 30:7310–7313CrossRefPubMedGoogle Scholar
  42. 42.
    Scheeringa R, Fries P, Petersson KM, Oostenveld R, Grothe I, Norris DG, Hagoort P, Bastiaansen MC (2011) Neuronal dynamics underlying high- and low-frequency EEG oscillations contribute independently to the human BOLD signal. Neuron 69:572–583CrossRefPubMedGoogle Scholar
  43. 43.
    Spencer KM, Nestor PG, Niznikiewicz MA, Salisbury DF, Shenton ME, McCarley RW (2003) Abnormal neural synchrony in schizophrenia. J Neurosci 23:7407–7411PubMedPubMedCentralGoogle Scholar
  44. 44.
    Suazo V, Diez A, Martin C, Ballesteros A, Casado P, Martin-Loeches M, Molina V (2012) Elevated noise power in gamma band related to negative symptoms and memory deficit in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 38:270–275CrossRefPubMedGoogle Scholar
  45. 45.
    Uhlhaas PJ, Linden DE, Singer W, Haenschel C, Lindner M, Maurer K, Rodriguez E (2006) Dysfunctional long-range coordination of neural activity during Gestalt perception in schizophrenia. J Neurosci 26:8168–8175CrossRefPubMedGoogle Scholar
  46. 46.
    Uhlhaas PJ, Singer W (2006) Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52:155–168CrossRefPubMedGoogle Scholar
  47. 47.
    Whitfield-Gabrieli S, Ford JM (2012) Default mode network activity and connectivity in psychopathology. Annu Rev Clin Psychol 8:49–76CrossRefPubMedGoogle Scholar
  48. 48.
    Winterer G, Coppola R, Goldberg TE, Egan MF, Jones DW, Sanchez CE, Weinberger DR (2004) Prefrontal broadband noise, working memory, and genetic risk for schizophrenia. Am J Psychiatry 161:490–500CrossRefPubMedGoogle Scholar
  49. 49.
    Yuval-Greenberg S, Deouell LY (2009) The broadband-transient induced gamma-band response in scalp EEG reflects the execution of saccades. Brain Topogr 22:3–6CrossRefPubMedGoogle Scholar
  50. 50.
    Yuval-Greenberg S, Deouell LY (2011) Scalp-recorded induced gamma-band responses to auditory stimulation and its correlations with saccadic muscle-activity. Brain Topogr 24:30–39CrossRefPubMedGoogle Scholar
  51. 51.
    Yuval-Greenberg S, Tomer O, Keren AS, Nelken I, Deouell LY (2008) Transient induced gamma-band response in EEG as a manifestation of miniature saccades. Neuron 58:429–441CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Vanessa Suazo
    • 1
  • Alba Lubeiro
    • 2
  • Rosa Jurado-Barba
    • 3
    • 4
  • Marta Moreno-Ortega
    • 3
    • 5
  • Mónica Dompablo
    • 3
  • Isabel Morales-Muñoz
    • 3
  • Roberto Rodriguez-Jimenez
    • 3
    • 6
    • 7
  • Tomas Palomo
    • 3
    • 6
    • 7
  • Vicente Molina
    • 2
    • 6
    • 8
    Email author
  1. 1.Psychiatry Research Unit, University Hospital of Álava, OsakidetzaCIBERSAMVitoriaSpain
  2. 2.Psychiatry Department, Faculty of MedicineUniversity of ValladolidValladolidSpain
  3. 3.Department of PsychiatryInstituto de Investigación 12 de Octubre (i+12)MadridSpain
  4. 4.Department of Psychology, Faculty of Health SciencesCamilo Jose Cela UniversityMadridSpain
  5. 5.New York State Psychiatric InstituteColumbia UniversityNew YorkUSA
  6. 6.Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM)MadridSpain
  7. 7.Psychiatry Department, Faculty of MedicineUCMMadridSpain
  8. 8.Psychiatry Service, University Hospital of ValladolidUniversity of ValladolidValladolidSpain

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