Archival Report|Articles in Press

Limited consistency and strength of neural oscillations during sustained visual attention in schizophrenia

Published:February 09, 2023DOI:



      Neural oscillations support perception, attention, and higher-order decision making. Aberrations in the strength or consistency of these oscillations in response to stimuli may underlie impaired visual perception and attention in schizophrenia. Here we examine the phase and power of alpha oscillations (8-12Hz) as well as aspects of beta and theta frequency oscillations during a demanding visual sustained attention task.


      Schizophrenia patients (N=74) and healthy controls (N=68) completed the Degraded-Stimulus Continuous Performance Task (DS-CPT) during electroencephalography. We used time-frequency analysis to evaluate the consistency (inter-trial phase coherence, ITPC) of the alpha cycle shortly after stimulus presentation (50-250ms). For oscillation strength we examined event-related desynchronization (ERD) in a later window associated with decision making (360-700ms).


      Alpha ITPC was reduced in schizophrenia and similar reductions were observed in theta (4-7Hz) and beta (13-20Hz) suggesting a lack of responsiveness in slower oscillations to visual stimuli. Alpha and beta ERD were also reduced in schizophrenia and associated with worse task performance, increased symptoms, and poorer cognition, suggesting that limited responsiveness of oscillations is related to impairments in the disorder. Individuals with lower ITPC had slower resting state alpha rhythms consistent with dysfunctional oscillations persisting across default and task-related brain states.


      In schizophrenia, abnormalities in the phase consistency and strength of slower oscillations during visual perception are related to symptoms and cognitive functioning. Altered visual perception and impaired attention in the disorder may be the consequence of aberrant slower oscillations that fail to dynamically reset and modulate in response to stimuli.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


        • Fries P.
        A mechanism for cognitive dynamics: neuronal communication through neuronal coherence.
        Trends Cogn Sci. 2005; 9: 474-480
        • VanRullen R.
        Perceptual Cycles.
        Trends Cogn Sci. 2016; 20: 723-735
        • Spaak E.
        • de Lange F.P.
        • Jensen O.
        Local Entrainment of Alpha Oscillations by Visual Stimuli Causes Cyclic Modulation of Perception.
        J Neurosci. 2014; 34: 3536-3544
        • Samaha J.
        • Sprague T.C.
        • Postle B.R.
        Decoding and Reconstructing the Focus of Spatial Attention from the Topography of Alpha-band Oscillations.
        J Cogn Neurosci. 2016; 28: 1090-1097
        • Jensen O.
        • Bonnefond M.
        • VanRullen R.
        An oscillatory mechanism for prioritizing salient unattended stimuli.
        Trends Cogn Sci. 2012; 16: 200-206
        • Di Gregorio F.
        • Trajkovic J.
        • Roperti C.
        • Marcantoni E.
        • Di Luzio P.
        • Avenanti A.
        • et al.
        Tuning alpha rhythms to shape conscious visual perception.
        Curr Biol. 2022; 32: 988-998.e6
        • Liu S.K.
        • Chiu C.-H.
        • Chang C.-J.
        • Hwang T.-J.
        • Hwu H.-G.
        • Chen W.J.
        Deficits in sustained attention in schizophrenia and affective disorders: stable versus state-dependent markers.
        Am J Psychiatry. 2002; 159: 975-982
        • Luck S.J.
        • Gold J.M.
        The construct of attention in schizophrenia.
        Biol Psychiatry. 2008; 64: 34-39
        • Butler P.D.
        • Silverstein S.M.
        • Dakin S.C.
        Visual perception and its impairment in schizophrenia.
        Biol Psychiatry. 2008; 64: 40-47
        • Ramsay I.S.
        • Lynn P.A.
        • Schermitzler B.
        • Sponheim S.R.
        Author Correction: Individual alpha peak frequency is slower in schizophrenia and related to deficits in visual perception and cognition.
        Sci Rep. 2021; 1120497
        • Busch N.A.
        • Dubois J.
        • VanRullen R.
        The phase of ongoing EEG oscillations predicts visual perception.
        J Neurosci. 2009; 29: 7869-7876
        • Mathewson K.E.
        • Gratton G.
        • Fabiani M.
        • Beck D.M.
        • Ro T.
        To See or Not to See: Prestimulus α Phase Predicts Visual Awareness.
        J Neurosci. 2009; 29: 2725-2732
        • Vanrullen R.
        • Busch N.A.
        • Drewes J.
        • Dubois J.
        Ongoing EEG Phase as a Trial-by-Trial Predictor of Perceptual and Attentional Variability.
        Front Psychol. 2011; 2: 60
        • Fries P.
        Rhythms for Cognition: Communication through Coherence.
        Neuron. 2015; 88: 220-235
        • Hanslmayr S.
        • Klimesch W.
        • Sauseng P.
        • Gruber W.
        • Doppelmayr M.
        • Freunberger R.
        • Pecherstorfer T.
        Visual discrimination performance is related to decreased alpha amplitude but increased phase locking.
        Neurosci Lett. 2005; 375: 64-68
        • Dugué L.
        • Marque P.
        • VanRullen R.
        The phase of ongoing oscillations mediates the causal relation between brain excitation and visual perception.
        J Neurosci. 2011; 31: 11889-11893
        • Klimesch W.
        • Doppelmayr M.
        • Russegger H.
        • Pachinger T.
        • Schwaiger J.
        Induced alpha band power changes in the human EEG and attention.
        Neurosci Lett. 1998; 244: 73-76
        • Peylo C.
        • Hilla Y.
        • Sauseng P.
        Cause or consequence? Alpha oscillations in visuospatial attention.
        Trends Neurosci. 2021; 44: 705-713
        • Corcoran C.M.
        • Stoops A.
        • Lee M.
        • Martinez A.
        • Sehatpour P.
        • Dias E.C.
        • Javitt D.C.
        Developmental trajectory of mismatch negativity and visual event-related potentials in healthy controls: Implications for neurodevelopmental vs. neurodegenerative models of schizophrenia.
        Schizophr Res. 2018; 191: 101-108
      1. Wolff A, Gomez-Pilar J, Zhang J, Choueiry J, de la Salle S, Knott V, Northoff G (2021): It’s in the Timing: Reduced Temporal Precision in Neural Activity of Schizophrenia. Cereb Cortex.

        • Martínez A.
        • Gaspar P.A.
        • Hillyard S.A.
        • Bickel S.
        • Lakatos P.
        • Dias E.C.
        • Javitt D.C.
        Neural oscillatory deficits in schizophrenia predict behavioral and neurocognitive impairments.
        Front Hum Neurosci. 2015; 9: 371
        • Abeles I.Y.
        • Gomez-Ramirez M.
        Impairments in background and event-related alpha-band oscillatory activity in patients with schizophrenia.
        PLoS One. 2014; 9e91720
        • Bismark A.W.
        • Thomas M.L.
        • Tarasenko M.
        • Shiluk A.L.
        • Rackelmann S.Y.
        • Young J.W.
        • Light G.A.
        Reverse translated and gold standard continuous performance tests predict global cognitive performance in schizophrenia.
        Transl Psychiatry. 2018; 8: 80
        • Lukoff D.
        • Nuechterlein K.H.
        • Ventura J.
        Manual for the expanded brief psychiatric rating scale.
        Schizophr Bull. 1986; 12: 594-602
        • Klein S.D.
        • Shekels L.L.
        • McGuire K.A.
        • Sponheim S.R.
        Neural anomalies during vigilance in schizophrenia: Diagnostic specificity and genetic associations.
        Neuroimage Clin. 2020; 28102414
        • Sponheim S.R.
        • McGuire K.A.
        • Stanwyck J.J.
        Neural anomalies during sustained attention in first-degree biological relatives of schizophrenia patients.
        Biol Psychiatry. 2006; 60: 242-252
      2. Nuechterlein KH, Asarnow RF (1999): Degraded Stimulus Continuous Performance Test (DS-CPT) Program for IBM-Compatible Microcomputers, Version 8.12. Los Angeles, CA: Nuechterlein KH and Asarnow RF.

        • Kang S.S.
        • Lano T.J.
        • Sponheim S.R.
        Distortions in EEG interregional phase synchrony by spherical spline interpolation: causes and remedies.
        Neuropsychiatric Electrophysiology. 2015; 1: 9
      3. Cohen MX (2014): Analyzing Neural Time Series Data: Theory and Practice. MIT Press.

        • Uhlhaas P.J.
        • Singer W.
        Abnormal neural oscillations and synchrony in schizophrenia.
        Nat Rev Neurosci. 2010; 11: 100-113
        • Basar-Eroglu C.
        • Mathes B.
        • Khalaidovski K.
        • Brand A.
        • Schmiedt-Fehr C.
        Altered alpha brain oscillations during multistable perception in schizophrenia.
        Int J Psychophysiol. 2016; 103: 118-128
        • Gonzalez-Burgos G.
        • Cho R.Y.
        • Lewis D.A.
        Alterations in cortical network oscillations and parvalbumin neurons in schizophrenia.
        Biol Psychiatry. 2015; 77: 1031-1040
        • Rürup L.
        • Mathes B.
        • Schmiedt-Fehr C.
        • Wienke A.S.
        • Özerdem A.
        • Brand A.
        • Basar-Eroglu C.
        Altered gamma and theta oscillations during multistable perception in schizophrenia.
        Int J Psychophysiol. 2020; 155: 127-139
        • Basar-Eroglu C.
        • Schmiedt-Fehr C.
        • Marbach S.
        • Brand A.
        • Mathes B.
        Altered oscillatory alpha and theta networks in schizophrenia.
        Brain Res. 2008; 1235: 143-152
      4. Grove TB, Lasagna CA, Martínez-Cancino R, Pamidighantam P, Deldin PJ, Tso IF (2020): Neural Oscillatory Abnormalities During Gaze Processing in Schizophrenia: Evidence of Reduced Theta Phase Consistency and Inter-areal Theta-Gamma Coupling. Biol Psychiatry Cogn Neurosci Neuroimaging.

      5. Peterson EJ, Rosen BQ, Campbell AM, Belger A, Voytek B (2017, March 3): 1/f neural noise is a better predictor of schizophrenia than neural oscillations. Biorxiv. p 113449.

        • Ciullo V.
        • Spalletta G.
        • Caltagirone C.
        • Jorge R.E.
        • Piras F.
        Explicit Time Deficit in Schizophrenia: Systematic Review and Meta-Analysis Indicate It Is Primary and Not Domain Specific.
        Schizophr Bull. 2016; 42: 505-518
        • Haß K.
        • Sinke C.
        • Reese T.
        • Roy M.
        • Wiswede D.
        • Dillo W.
        • et al.
        Enlarged temporal integration window in schizophrenia indicated by the double-flash illusion.
        Cogn Neuropsychiatry. 2017; 22: 145-158
        • Norton D.
        • Ongur D.
        • Stromeyer 3rd, C.
        • Chen Y.
        Altered “three-flash” illusion in response to two light pulses in schizophrenia.
        Schizophr Res. 2008; 103: 275-282
        • Silverstein S.M.
        Visual Perception Disturbances in Schizophrenia: A Unified Model.
        Nebr Symp Motiv. 2016; 63: 77-132
        • Rassovsky Y.
        • Horan W.P.
        • Lee J.
        • Sergi M.J.
        • Green M.F.
        Pathways between early visual processing and functional outcome in schizophrenia.
        Psychol Med. 2011; 41: 487-497
        • Sergi M.J.
        • Rassovsky Y.
        • Nuechterlein K.H.
        • Green M.F.
        Social perception as a mediator of the influence of early visual processing on functional status in schizophrenia.
        Am J Psychiatry. 2006; 163: 448-454
        • Sadaghiani S.
        • Kleinschmidt A.
        Brain Networks and α-Oscillations: Structural and Functional Foundations of Cognitive Control.
        Trends Cogn Sci. 2016; 20: 805-817
        • Kustermann T.
        • Rockstroh B.
        • Kienle J.
        • Miller G.A.
        • Popov T.
        Deficient attention modulation of lateralized alpha power in schizophrenia.
        Psychophysiology. 2016; 53: 776-785
        • Becske M.
        • Marosi C.
        • Molnár H.
        • Fodor Z.
        • Tombor L.
        • Csukly G.
        Distractor filtering and its electrophysiological correlates in schizophrenia.
        Clin Neurophysiol. 2022; 133: 71-82
        • Fodor Z.
        • Marosi C.
        • Tombor L.
        • Csukly G.
        Salient distractors open the door of perception: alpha desynchronization marks sensory gating in a working memory task.
        Sci Rep. 2020; 1019179
        • Stipacek A.
        • Grabner R.H.
        • Neuper C.
        • Fink A.
        • Neubauer A.C.
        Sensitivity of human EEG alpha band desynchronization to different working memory components and increasing levels of memory load.
        Neurosci Lett. 2003; 353: 193-196
        • Kim S.
        • Jung K.H.
        • Lee J.-H.
        Characteristics of alpha power event-related desynchronization in the discrimination of spontaneous deceptive responses.
        Int J Psychophysiol. 2012; 85: 230-235
        • Borghini G.
        • Aricò P.
        • Di Flumeri G.
        • Cartocci G.
        • Colosimo A.
        • Bonelli S.
        • et al.
        EEG-Based Cognitive Control Behaviour Assessment: an Ecological study with Professional Air Traffic Controllers.
        Sci Rep. 2017; 7: 547
        • Nuechterlein K.H.
        • Green M.F.
        • Calkins M.E.
        • Greenwood T.A.
        • Gur R.E.
        • Gur R.C.
        • et al.
        Attention/vigilance in schizophrenia: performance results from a large multi-site study of the Consortium on the Genetics of Schizophrenia (COGS).
        Schizophr Res. 2015; 163: 38-46
        • Jones S.R.
        When brain rhythms aren’t “rhythmic”: implication for their mechanisms and meaning.
        Curr Opin Neurobiol. 2016; 40: 72-80