Seeing in the dark: Phosphene thresholds with eyes open versus closed in the absence of visual inputs

  • Author Footnotes
    1 Equal contribution.
    T.A. de Graaf
    Corresponding author. Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, PO Box 616, 6200 MD, Maastricht, The Netherlands.
    1 Equal contribution.
    Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, The Netherlands

    Maastricht Brain Imaging Centre, Maastricht, The Netherlands
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  • Author Footnotes
    1 Equal contribution.
    F. Duecker
    1 Equal contribution.
    Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, The Netherlands

    Maastricht Brain Imaging Centre, Maastricht, The Netherlands
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  • Y. Stankevich
    Department of Psychology, Institute of Clinical Psychology and Psychotherapy, Technische Universität Dresden, Dresden, Germany
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  • S. ten Oever
    Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, The Netherlands

    Maastricht Brain Imaging Centre, Maastricht, The Netherlands
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  • A.T. Sack
    Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, The Netherlands

    Maastricht Brain Imaging Centre, Maastricht, The Netherlands
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  • Author Footnotes
    1 Equal contribution.


      • We measured phosphene thresholds (PT) with eyes closed or opened, in complete darkness.
      • PT staircases were interleaved, a staircase algorithm controlled TMS intensity.
      • PT was lower with eyes closed than with eyes open.
      • We also measured parieto-occipital alpha power with EEG.
      • EEG alpha power was higher with eyes closed versus eyes open.



      Voluntarily opening or closing our eyes results in fundamentally different input patterns and expectancies. Yet it remains unclear how our brains and visual systems adapt to these ocular states.
      Objective/Hypothesis: We here used transcranial magnetic stimulation (TMS) to probe the excitability of the human visual system with eyes open or closed, in the complete absence of visual inputs.


      Combining Bayesian staircase procedures with computer control of TMS pulse intensity allowed interleaved determination of phosphene thresholds (PT) in both conditions. We measured parieto-occipital EEG baseline activity in several stages to track oscillatory power in the alpha (8–12 Hz) frequency-band, which has previously been shown to be inversely related to phosphene perception.


      Since closing the eyes generally increases alpha power, one might have expected a decrease in excitability (higher PT). While we confirmed a rise in alpha power with eyes closed, visual excitability was actually increased (PT was lower) with eyes closed.


      This suggests that, aside from oscillatory alpha power, additional neuronal mechanisms influence the excitability of early visual cortex. One of these may involve a more internally oriented mode of brain operation, engaged by closing the eyes. In this state, visual cortex may be more susceptible to top-down inputs, to facilitate for example multisensory integration or imagery/working memory, although alternative explanations remain possible.


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        • Berger H.
        Über das Elektroenkephalogramm des Menschen.
        Arch Psychiatr Nervenkr. 1929; 87: 527-570
        • Romei V.
        • Brodbeck V.
        • Michel C.
        • Amedi A.
        • Pascual-Leone A.
        • Thut G.
        Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas.
        Cereb Cortex. 2008; 18: 2010-2018
        • Marx E.
        • Stephan T.
        • Nolte A.
        • Deutschländer A.
        • Seelos K.C.
        • Dieterich M.
        • et al.
        Eye closure in darkness animates sensory systems.
        Neuroimage. 2003; 19: 924-934
        • Bianciardi M.
        • Fukunaga M.
        • van Gelderen P.
        • Horovitz S.G.
        • de Zwart J.A.
        • Duyn J.H.
        Modulation of spontaneous fMRI activity in human visual cortex by behavioral state.
        Neuroimage. 2009; 45: 160-168
        • Liu D.
        • Dong Z.
        • Zuo X.
        • Wang J.
        • Zang Y.
        Eyes-open/eyes-closed dataset sharing for reproducibility evaluation of resting state fMRI data analysis methods.
        Neuroinformatics. 2013; 11: 469-476
        • Marx E.
        • Deutschländer A.
        • Stephan T.
        • Dieterich M.
        • Wiesmann M.
        • Brandt T.
        Eyes open and eyes closed as rest conditions: impact on brain activation patterns.
        Neuroimage. 2004; 21: 1818-1824
        • McAvoy M.
        • Larson-Prior L.
        • Nolan T.S.
        • Vaishnavi S.N.
        • Raichle M.E.
        d'Avossa G. Resting states affect spontaneous BOLD oscillations in sensory and paralimbic cortex.
        J Neurophysiol. 2008; 100: 922-931
        • Yang H.
        • Long X.-Y.
        • Yang Y.
        • Yan H.
        • Zhu C.-Z.
        • Zhou X.-P.
        • et al.
        Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI.
        Neuroimage. 2007; 36: 144-152
        • Zang Y.-F.
        • He Y.
        • Zhu C.-Z.
        • Cao Q.-J.
        • Sui M.-Q.
        • Liang M.
        • et al.
        Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI.
        Brain Dev. 2007; 29: 83-91
        • Patriat R.
        • Molloy E.K.
        • Meier T.B.
        • Kirk G.R.
        • Nair V.A.
        • Meyerand M.E.
        • et al.
        The effect of resting condition on resting-state fMRI reliability and consistency: a comparison between resting with eyes open, closed, and fixated.
        Neuroimage. 2013; 78: 463-473
        • Van Dijk K.R.A.
        • Hedden T.
        • Venkataraman A.
        • Evans K.C.
        • Lazar S.W.
        • Buckner R.L.
        Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization.
        J Neurophysiol. 2010; 103: 297-321
        • Yan C.
        • Liu D.
        • He Y.
        • Zou Q.
        • Zhu C.
        • Zuo X.
        • et al.
        Spontaneous brain activity in the default mode network is sensitive to different resting-state conditions with limited cognitive load.
        PLoS One. 2009; 4: e5743
        • Zou Q.
        • Long X.
        • Zuo X.
        • Yan C.
        • Zhu C.
        • Yang Y.
        • et al.
        Functional connectivity between the thalamus and visual cortex under eyes closed and eyes open conditions: a resting-state fMRI study.
        Hum Brain Mapp. 2009; 30: 3066-3078
        • Hüfner K.
        • Stephan T.
        • Glasauer S.
        • Kalla R.
        • Riedel E.
        • Deutschländer A.
        • et al.
        Differences in saccade-evoked brain activation patterns with eyes open or eyes closed in complete darkness.
        Exp Brain Res. 2008; 186: 419-430
        • Hüfner K.
        • Stephan T.
        • Flanagin V.L.
        • Deutschländer A.
        • Stein A.
        • Kalla R.
        • et al.
        Differential effects of eyes open or closed in darkness on brain activation patterns in blind subjects.
        Neurosci Lett. 2009; 466: 30-34
        • Niven J.E.
        • Laughlin S.B.
        Energy limitation as a selective pressure on the evolution of sensory systems.
        J Exp Biol. 2008; 211: 1792-1804
        • Xu P.
        • Huang R.
        • Wang J.
        • Van Dam N.T.
        • Xie T.
        • Dong Z.
        • et al.
        Different topological organization of human brain functional networks with eyes open versus eyes closed.
        Neuroimage. 2014; 90: 246-255
        • Wiesmann M.
        • Kopietz R.
        • Albrecht J.
        • Linn J.
        • Reime U.
        • Kara E.
        • et al.
        Eye closure in darkness animates olfactory and gustatory cortical areas.
        Neuroimage. 2006; 32: 293-300
        • Hallett M.
        Transcranial magnetic stimulation: a primer.
        Neuron. 2007; 55: 187-199
        • Pascual-Leone A.
        • Walsh V.
        • Rothwell J.
        Transcranial magnetic stimulation in cognitive neuroscience–virtual lesion, chronometry, and functional connectivity.
        Curr Opin Neurobiol. 2000; 10: 232-237
        • Sack A.T.
        Transcranial magnetic stimulation, causal structure–function mapping and networks of functional relevance.
        Curr Opin Neurobiol. 2006; 16: 593-599
        • Amassian V.E.
        • Cracco R.Q.
        • Maccabee P.J.
        • Cracco J.B.
        • Rudell A.
        • Eberle L.
        Suppression of visual perception by magnetic coil stimulation of human occipital cortex.
        Electroencephalogr Clin Neurophysiol. 1989; 74: 458-462
        • Beckers G.
        • Hömberg V.
        Impairment of visual perception and visual short term memory scanning by transcranial magnetic stimulation of occipital cortex.
        Exp Brain Res. 1991; 87: 421-432
        • Corthout E.
        • Uttl B.
        • Walsh V.
        • Hallett M.
        • Cowey A.
        Timing of activity in early visual cortex as revealed by transcranial magnetic stimulation.
        Neuroreport. 1999; 10: 2631
        • Kammer T.
        Masking visual stimuli by transcranial magnetic stimulation.
        Psychol Res. 2007; 71: 659-666
        • Graaf T.A.
        • Koivisto M.
        • Jacobs C.
        • Sack A.T.
        The chronometry of visual perception: review of occipital TMS masking studies.
        Neurosci Biobehav Rev. 2014; 45: 295-304
        • Barker A.T.
        • Jalinous R.
        • Freeston I.L.
        Non-invasive magnetic stimulation of human motor cortex.
        Lancet. 1985; 1: 1106-1107
        • Kammer T.
        Phosphenes and transient scotomas induced by magnetic stimulation of the occipital lobe: their topographic relationship.
        Neuropsychologia. 1999; 37: 191-198
        • Marg E.
        • Rudiak D.
        Phosphenes induced by magnetic stimulation over the occipital brain: description and probable site of stimulation.
        Optom Vis Sci. 1994; 71: 301-311
        • Meyer B.U.
        • Diehl R.
        • Steinmetz H.
        • Britton T.C.
        • Benecke R.
        Magnetic stimuli applied over motor and visual cortex: influence of coil position and field polarity on motor responses, phosphenes, and eye movements.
        Electroencephalogr Clin Neurophysiol Suppl. 1991; 43: 121-134
        • Klem G.H.
        • Lüders H.O.
        • Jasper H.H.
        • Elger C.
        The ten-twenty electrode system of the international federation. The international federation of clinical neurophysiology.
        Electroencephalogr Clin Neurophysiol Suppl. 1999; 52: 3-6
        • Watson A.B.
        • Pelli D.G.
        QUEST: a Bayesian adaptive psychometric method.
        Percept Psychophys. 1983; 33: 113-120
        • Oostenveld R.
        • Fries P.
        • Maris E.
        • Schoffelen J.-M.
        FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data.
        Comput Intell Neurosci. 2011; 2011: 156869
        • Takeda M.
        • Yoshimura H.
        Lateral eye movement while eyes are closed.
        Percept Mot Ski. 1979; 48: 1227-1231
        • Romei V.
        • Rihs T.
        • Brodbeck V.
        • Thut G.
        Resting electroencephalogram alpha-power over posterior sites indexes baseline visual cortex excitability.
        Neuroreport. 2008; 19: 203-208
        • Lange J.
        • Oostenveld R.
        • Fries P.
        Reduced occipital alpha power indexes enhanced excitability rather than improved visual perception.
        J Neurosci. 2013; 33: 3212-3220
        • Volkmann F.C.
        • Riggs L.A.
        • Moore R.K.
        Eyeblinks and visual suppression.
        Science. 1980; 207: 900-902
        • Toscani M.
        • Marzi T.
        • Righi S.
        • Viggiano M.P.
        • Baldassi S.
        Alpha waves: a neural signature of visual suppression.
        Exp Brain Res. 2010; 207: 213-219
        • Volkmann F.C.
        • Riggs L.A.
        • Ellicott A.G.
        • Moore R.K.
        Measurements of visual suppression during opening, closing and blinking of the eyes.
        Vis Res. 1982; 22: 991-996
        • Thilo K.V.
        • Santoro L.
        • Walsh V.
        • Blakemore C.
        The site of saccadic suppression.
        Nat Neurosci. 2004; 7: 13-14
        • Adrian E.D.
        • Matthews B.H.C.
        The Berger Rhythm: potential changes from the occipital lobes in man.
        Brain. 2010; 133: 3-6
        • Bohdanecký Z.
        • Indra M.
        • Lánský P.
        • Radil-Weiss T.
        Alternation of EEG alpha and non-alpha periods does not differ in open and closed eye condition in darkness.
        Acta Neurobiol Exp (Wars). 1984; 44: 229-232
        • Boytsova Y.A.
        • Danko S.G.
        EEG differences between resting states with eyes open and closed in darkness.
        Hum Physiol. 2010; 36: 367-369
        • Ben-Simon E.
        • Podlipsky I.
        • Okon-Singer H.
        • Gruberger M.
        • Cvetkovic D.
        • Intrator N.
        • et al.
        The dark side of the alpha rhythm: fMRI evidence for induced alpha modulation during complete darkness.
        Eur J Neurosci. 2013; 37: 795-803
        • Henning S.
        • Merboldt K.-D.
        • Frahm J.
        Task- and EEG-correlated analyses of BOLD MRI responses to eyes opening and closing.
        Brain Res. 2006; 1073–1074: 359-364
        • Compston A.
        The Berger rhythm: potential changes from the occipital lobes in man.
        Brain. 2010; 133: 3-6
        • Amochaev A.
        • Salamy A.
        • Alvarez W.
        • Peeke H.
        Topographic mapping and habituation of event related eeg alpha band desynchronization.
        Int J Neurosci. 1989; 49: 151-155
        • 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
        • Pfurtscheller G.
        • Stancák A.
        • Neuper C.
        Event-related synchronization (ERS) in the alpha band - an electrophysiological correlate of cortical idling: a review.
        Int J Psychophysiol. 1996; 24: 39-46
        • Jensen O.
        • Mazaheri A.
        Shaping functional architecture by oscillatory alpha activity: gating by inhibition.
        Front Hum Neurosci Front. 2010; 4: 186
        • Boroojerdi B.
        • Bushara K.O.
        • Corwell B.
        • Immisch I.
        • Battaglia F.
        • Muellbacher W.
        • et al.
        Enhanced excitability of the human visual cortex induced by short-term light deprivation.
        Cereb Cortex. 2000; 10: 529-534
        • Fierro B.
        • Brighina F.
        • Vitello G.
        • Piazza A.
        • Scalia S.
        • Giglia G.
        • et al.
        Modulatory effects of low- and high-frequency repetitive transcranial magnetic stimulation on visual cortex of healthy subjects undergoing light deprivation.
        J Physiol. 2005; 565: 659-665
        • Pitskel N.B.
        • Merabet L.B.
        • Ramos-Estebanez C.
        • Kauffman T.
        • Pascual-Leone A.
        Time-dependent changes in cortical excitability after prolonged visual deprivation.
        NeuroReport. 2007; 18: 1703-1707
        • Stewart L.M.
        • Walsh V.
        • Rothwell J.C.
        Motor and phosphene thresholds: a transcranial magnetic stimulation correlation study.
        Neuropsychologia. 2001; 39: 415-419
        • Oever ten S.
        • Schroeder C.E.
        • Poeppel D.
        • van Atteveldt N.
        • Zion-Golumbic E.
        Rhythmicity and cross-modal temporal cues facilitate detection.
        Neuropsychologia. 2014; 63: 43-50
        • Lovelace C.T.
        • Stein B.E.
        • Wallace M.T.
        An irrelevant light enhances auditory detection in humans: a psychophysical analysis of multisensory integration in stimulus detection.
        Brain Res Cogn Brain Res. 2003; 17: 447-453
        • Weisz N.
        • Wühle A.
        • Monittola G.
        Prestimulus oscillatory power and connectivity patterns predispose conscious somatosensory perception.
        Proc Nat Acad Sci U. S. A. 2014; 111: E417-E425
        • Leske S.
        • Ruhnau P.
        • Frey J.
        • Lithari C.
        • Müller N.
        Prestimulus network integration of auditory cortex predisposes near-threshold perception independently of local excitability.
        Cereb Cortex. 2015; 25: 4898-4907
        • Machielsen W.C.
        • Rombouts S.A.
        • Barkhof F.
        • Scheltens P.
        • Witter M.P.
        FMRI of visual encoding: reproducibility of activation.
        Hum Brain Mapp. 2000; 9: 156-164
        • Kosslyn S.M.
        • Ganis G.
        • Thompson W.L.
        Neural foundations of imagery.
        Nat Rev Neurosci. 2001; 2: 635-642
        • Kosslyn S.M.
        • Pascual-Leone A.
        • Felician O.
        • Camposano S.
        • Keenan J.P.
        • Thompson W.L.
        • et al.
        The role of area 17 in visual imagery: convergent evidence from PET and rTMS.
        Science. 1999; 284: 167-170
        • Sparing R.
        • Mottaghy F.M.
        • Ganis G.
        • Thompson W.L.
        • Töpper R.
        • Kosslyn S.M.
        • et al.
        Visual cortex excitability increases during visual mental imagery–a TMS study in healthy human subjects.
        Brain Res. 2002; 938: 92-97
        • Cattaneo Z.
        • Pisoni A.
        • Papagno C.
        • Silvanto J.
        Modulation of visual cortical excitability by working memory: effect of luminance contrast of mental imagery.
        Front Psychol Front. 2011; 2: 29