The phase of ongoing oscillations mediates the causal relation between brain excitation and visual perception.
Open accessAbstract
Why does neuronal activity in sensory brain areas sometimes give rise to perception, and sometimes not? Although neuronal noise is often invoked as the key factor, a portion of this variability could also be due to the history and current state of the brain affecting cortical excitability. Here we directly test this idea by examining whether the phase of prestimulus oscillatory activity is causally linked with modulations of cortical excitability and with visual perception. Transcranial magnetic stimulation (TMS) was applied over human visual cortex to induce illusory perceptions (phosphenes) while electroencephalograms (EEGs) were simultaneously recorded. Subjects reported the presence or absence of an induced phosphene following a single pulse of TMS at perceptual threshold. The phase of ongoing alpha (∼10 Hz) oscillations within 400 ms before the pulse significantly covaried with the perceptual outcome. This effect was observed in occipital regions around the site of TMS, as well as in a distant frontocentral region. In both regions, we found a systematic relationship between prepulse EEG phase and perceptual performance: phosphene probability changed by ∼15% between opposite phases. In summary, we provide direct evidence for a chain of causal relations between the phase of ongoing oscillations, neuronal excitability, and visual perception: ongoing oscillations create periodic "windows of excitability," with sensory perception being more likely to occur at specific phases.
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In humans, there is a causal relationship between cortical excitation and phosphenes perception so that the phase of pre-stimulus oscillatory activity seems linked to visual perception.
“Moreover, it has been shown in humans that there is a causal relationship between cortical excitation and phosphenes perception so that the phase of pre-stimulus oscillatory activity seems linked to visual perception (Dugue et al., 2011)”
From Toward a personalized closed-loop stimulation of the visual cortex: Advances and challenges (2022) · cites this paper as Dugue et al., 2011
LFP phase-dependent response to stimulation has been reported in experiments in rats and using non-invasive transcranial magnetic stimulation (TMS) in sighted humans.
“This has been reported in experiments in rats (Allison-Walker et al., 2020) and using non-invasive transcranial magnetic stimulation (TMS) in sighted humans (Dugue et al., 2011), but the feasibility of LFP phase-locked stimulation with intracortical electrodes in humans still remains unexplored.”
From Toward a personalized closed-loop stimulation of the visual cortex: Advances and challenges (2022) · cites this paper as Dugue et al., 2011
The frequency of ongoing oscillations is around 10 Hz.
“it seems that the frequency of ongoing oscillations is around 10 Hz (Dugue et al., 2011)”
From Toward a personalized closed-loop stimulation of the visual cortex: Advances and challenges (2022) · cites this paper as Dugue et al., 2011
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ResultCortical brain states and corticospinal synchronization influence TMS-evoked motor potentials
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BackgroundThe phase of prestimulus alpha oscillations affects tactile perception
Ai, L., & Ro, T. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00125.2013 · Cited by 103 · see citing works
“In support of this notion, we recently showed that visual perception is modulated by the alpha phase at the time of stimulus onset (Mathewson et al. 2009), an effect that has since been replicated (Busch et al. 2009; Dugué et al. 2011; Jansen and Brandt 1991; Mathewson et al. 2011).”
Solutions for managing variability in non-invasive brain stimulation studies
Guerra, A., López-Alonso, V., Cheeran, B., & Suppa, A. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.12.060 · Cited by 103 · see citing works
“In fact, recent studies demonstrated that the oscillatory activity in cerebral cortices underlies a fluctuation in neuronal excitability, which is frequency-dependent and area-specific [32, 38-41].”
Voloh, B., & Womelsdorf, T. (2016) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2016.00018 · Cited by 96 · see citing works
“…during a variety of task contexts including attention (Voloh et al., 2015), Pavlovian conditioning (Courtin et al., 2014), perceptual detection (Dugué et al., 2011), exploration (Hoffman et al., 2013; Jutras et al., 2013), learning (Rutishauser et al., 2010), speech detection (Gross et al.,…”
BackgroundMethodInfluentialTranscranial brain stimulation: closing the loop between brain and stimulation
Karabanov, A. N., Thielscher, A., & Siebner, H. R. (2016) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000342 · Cited by 102 · see citing works
How to Evaluate Phase Differences between Trial Groups in Ongoing Electrophysiological Signals
Rufin Vanrullen, A. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00426 · Cited by 98 · see citing works
“Other analogous procedures have been described, however (Drewes & VanRullen, 2011; Dugue et al., 2011; VanRullen et al., 2011; Dugue et al., 2015; Han & VanRullen, 2015), and there exists no systematic comparison between these various measures and, consequently, no accepted practice in this field.”
MethodInfluentialThalamocortical excitability modulation guides human perception under uncertainty
Kosciessa, J. Q., Lindenberger, U., & Garrett, D. D. (2021) · Nature Communications · doi:10.1038/s41467-021-22511-7 · Cited by 101 · see citing works
Probing cortical excitability using rapid frequency tagging
Zhigalov, A., Herring, J., Herpers, J., Bergmann, T. O., & Jensen, O. B. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.03.056 · Cited by 99 · see citing works
“Additionally, the phase of alpha has been shown to modulate perception (Mathewson et al., 2011; Vanrullen et al., 2011) and cortical excitability (Dugu e et al., 2011; Scheeringa et al., 2011; Spaak et al., 2012).”
BackgroundThe role of alpha oscillations for illusory perception
Lange, J., KEIL, J. E., Schnitzler, A., van Dijk, H., & Weisz, N. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.06.015 · Cited by 98 · see citing works
Illusory Jitter Perceived at the Frequency of Alpha Oscillations
Minami, S., & Amano, K. (2017) · Current Biology · doi:10.1016/j.cub.2017.06.033 · Cited by 97 · see citing works
Kienitz, R., Schmiedt, J. T., Shapcott, K. A., Kouroupaki, K., Saunders, R. C., & Schmid, M. C. (2018) · Current Biology · doi:10.1016/j.cub.2018.05.086 · Cited by 95 · see citing works
“This is consistent with a wide set of findings that the phase of oscillations is predictive of performance and RT fluctuations for near-threshold stimuli ([9, 52–55]; however, see [56, 57]) and reflect fluctuations in neural excitability [50, 58, 59].”
Cortical cross-frequency coupling predicts perceptual outcomes
Fiebelkorn, I. C., Snyder, A. C., Mercier, M. R., Butler, J. S., Molholm, S., & Foxe, J. J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.11.021 · Cited by 94 · see citing works
“Several studies have now established that the prestimulus phase of cortical oscillations influences perceptual outcomes (Busch et al., 2009; Dugue et al., 2011; Mathewson et al., 2009).”
BackgroundResultInfluentialKosciessa, J. Q., Kloosterman, N. A., & Garrett, D. D. (2020) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007885 · Cited by 93 · see citing works
Detection of Near-Threshold Sounds is Independent of EEG Phase in Common Frequency Bands
Zoefel, B., & Heil, P. F. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00262 · Cited by 92 · see citing works
“Similarly, the probability of eliciting phosphenes by transcranial magnetic stimulation of occipital cortex varied with α-phase (Dugué et al., 2011; Romei et al., 2012).”
BackgroundFlexible frequency control of cortical oscillations enables computations required for working memory
Dipoppa, M., & Gutkin, B. S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303270110 · Cited by 88 · see citing works
Cortical layers, rhythms and BOLD signals
Scheeringa, R., & Fries, P. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2017.11.002 · Cited by 88 · see citing works
The direction of theta and alpha travelling waves modulates human memory processing
Mohan, U. R., Zhang, H., Ermentrout, B., & Jacobs, J. (2024) · Nature Human Behaviour · doi:10.1038/s41562-024-01838-3 · Cited by 96 · see citing works
“This heightened relevance of alpha-band TWs prior to encoding indicates a distinct role in priming relevant brain regions to be in an optimal state for successfully encoding an item into memory 68–73 .”
Combrisson, E., Perrone-Bertolotti, M., Soto, J. L. P., Alamian, G., Kahane, P., Lachaux, J., Guillot, A., & Jerbi, K. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2016.11.042 · Cited by 82 · see citing works
“The involvement of phase information in neuronal encoding has been extensively investigated in numerous perceptual modalities and higher-order cognitive tasks (Drewes and VanRullen, 2011; Dugue et al., 2011; Jensen et al., 2014; Klimesch et al., 2008, 2007; Montemurro et al., 2008; Palva and Palva, 2007; Sauseng and K…”
BackgroundThe role of gamma and alpha oscillations for blocking out distraction
Bonnefond, M., & Jensen, O. B. (2013) · Communicative & Integrative Biology · doi:10.4161/cib.22702 · Cited by 84 · see citing works
“More specifically, the spiking and gamma (> 30 Hz) activities, as well as the visual perception and the probability of seeing a phosphene following a TMS stimulation over the posterior cortex, have been shown to be modulated by the phase of the alpha cycle.(9-15) This phasic modulation, taken together with the inhibit…”
BackgroundSigala, R., Haufe, S., Roy, D., Dinse, H. R., & Ritter, P. (2014) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2014.00036 · Cited by 84 · see citing works
“Recent studies further highlighted the importance of ongoing oscillatory alpha phase in the perception of illusory (Dugue et al., 2011) and near-threshold visual stimuli (Mathewson et al., 2011; Vanrullen et al., 2011), as well as in the conscious access to visual stimuli (Pincham and Szucs, 2012).”
BackgroundRelationships Between Neuronal Oscillatory Amplitude and Dynamic Functional Connectivity
Tewarie, P. K. B., Hunt, B. A. E., O’Neill, G. C., Byrne, Á., Aquino, K. M., Bauer, M., Mullinger, K. J., Coombes, S., & Brookes, M. J. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy136 · Cited by 83 · see citing works
“Indeed, our findings are in strong agreement with others (Hummel and Gerloff 2006; Dugué et al. 2011; Zumer et al. 2014) in showing that alpha band oscillations are crucial in communications across brain areas.”
ResultThe shaky ground truth of real-time phase estimation
Zrenner, C., Galevska, D., Nieminen, J. O., Baur, D., Stefanou, M., & Ziemann, U. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116761 · Cited by 80 · see citing works
“In the case of real-time phase estimation, or in post-hoc estimation of phase at the time of a stimulus that affects the signal, such as a TMS pulse but also in EEG potentials evoked from sensory stimulation (Dugue et al., 2011), only data preceding the time of interest is available (Fig.”
BackgroundSensorimotor Oscillatory Phase–Power Interaction Gates Resting Human Corticospinal Output
Hussain, S. J., Claudino, L., Bönstrup, M., Norato, G., Cruciani, G., Thompson, R., Zrenner, C., Ziemann, U., Buch, E. R., & Cohen, L. G. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy255 · Cited by 79 · see citing works
Interactions between cardiac activity and conscious somatosensory perception
Motyka, P., Grund, M., Forschack, N., Al, E., Villringer, A., & Gaebler, M. (2019) · Psychophysiology · doi:10.1111/psyp.13424 · Cited by 79 · see citing works
Romei, V., Thut, G., Mok, R. M., Schyns, P. G., & Driver, J. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08020.x · Cited by 79 · see citing works
“, 2009), visual awareness (Romei et al., 2008a,b; Mathewson et al., 2009; Dugué et al., 2011), spatial”
BackgroundZoefel, B., & Rufin Vanrullen, A. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00296 · Cited by 79 · see citing works
“…target and the likelihood of perceiving a phosphene during transcranial magnetic stimulation (TMS) (Busch et al., 2009; Mathewson et al., 2009; Dugué et al., 2011; Figure 1B), and random visual input seems to reverberate in the brain at a frequency corresponding to the alpha band (VanRullen…”
BackgroundDetecting Unattended Stimuli Depends on the Phase of Prestimulus Neural Oscillations
Harris, A. M., Dux, P. E., & Mattingley, J. B. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3006-17.2018 · Cited by 77 · see citing works
“Analysis of phase dependence of perception was performed using the phase opposition sum (POS) metric (Drewes and VanRullen, 2011; Dugué, Marque, and VanRullen, 2011; VanRullen, 2016a).”
MethodAlpha Phase Determines Successful Lexical Decision in Noise
Strauß, A., Henry, M. J., Scharinger, M., & Obleser, J. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3357-14.2015 · Cited by 77 · see citing works
“On incorrect trials, the initial phonemes of the stimulus would thus coincide with suboptimal “windows” for sensory input (Dugué et al., 2011); that is, the inhibitory phase of an ongoing alpha oscillation.”
BackgroundInfluentialLow pre‐stimulus EEG alpha power amplifies visual awareness but not visual sensitivity
Benwell, C., Coldea, A., Harvey, M., & Thut, G. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15166 · Cited by 75 · see citing works
“…alpha power reflect an increase in global baseline excitability levels (see also evidence from transcranial magnetic stimulation [TMS]- EEG studies; Dugué et al., 2011; Romei et al., 2008; Samaha et al., 2017), then low alpha power may lead to a more liberal decision criterion, leaving perceptual…”
BackgroundGonzález-Rosa, J. J., Soto-León, V., Real, P., Carrasco-López, C., Foffani, G., Strange, B. A., & Oliviero, A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4232-14.2015 · Cited by 74 · see citing works
“sual selective attention tasks (Dugué et al., 2011; Foxe and Snyder, 2011), with higher prestimulus alpha power associated with less likely, or slower, visual target detection (Thut et al.”
BackgroundKizuk, S. A. D., & Mathewson, K. E. (2016) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01058 · Cited by 68 · see citing works
EEG-microstate dependent emergence of perceptual awareness
Britz, J., ndez, L. D. H., Ro, T., & Michel, C. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00163 · Cited by 70 · see citing works
“Frontiers in Behavioral Neuroscience www.frontiersin.org May 2014 | Volume 8 | Article 163 | 7 Other studies have related awareness to local differences in phase of the alpha and theta band (Busch et al., 2009; Mathewson et al., 2009; Dugué et al., 2011).”
BackgroundThe role of cortical beta oscillations in time estimation
Kulashekhar, S., Pekkola, J., Palva, J. M., & Palva, S. (2016) · Human Brain Mapping · doi:10.1002/hbm.23239 · Cited by 72 · see citing works
“…are achieved when the stimulus processing coincides with the high-excitability phases of neuronal oscillations [Besle et al., 2011; Busch et al., 2009; Busch and VanRullen, 2010; Drewes and Vanrullen, 2011; Dugue et al., 2011; Kosem et al., 2014; Lakatos et al., 2008; Stefanics et al., 2010].”
BackgroundThe Discrete and Continuous Brain: From Decisions to Movement—And Back Again
Parr, T., & Friston, K. J. (2018) · Neural Computation · doi:10.1162/neco_a_01102 · Cited by 70 · see citing works
Saccadic Suppression Is Embedded Within Extended Oscillatory Modulation of Sensitivity
Benedetto, A., & Morrone, M. C. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2390-16.2016 · Cited by 71 · see citing works
“Interestingly, saccadic reaction times to abrupt visual stimuli are highly variable and can be predicted by the phase of ongoing brain oscillations, as has been observed for many other visual functions (VanRullen and Koch, 2003; Busch et al., 2009; Dugué et al., 2011; Milton and Pleydell-Pearce, 2016).”
BackgroundStaudigl, T., Härtl, E., Noachtar, S., Doeller, C. F., & Jensen, O. B. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2003404 · Cited by 71 · see citing works
“Building on prior evidence on the cortical origins of alpha activity underlying visual information sampling [8,9], we hypothesized that higher phase locking in occipital lobe would be related to successful memory performance.”
BackgroundIndividual Alpha Frequency Relates to the Sound-Induced Flash Illusion
KEIL, J. E., & Senkowski, D. (2017) · Multisensory Research · doi:10.1163/22134808-00002572 · Cited by 70 · see citing works
Lasting connectivity increase and anxiety reduction via transcranial alternating current stimulation
Clancy, K. J., Baisley, S. K., Albizu, A., Kartvelishvili, N., Ding, M., & Li, W. (2018) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsy096 · Cited by 69 · see citing works
Gehrig, J., Wibral, M., Arnold, C., & Kell, C. A. (2012) · Frontiers in Psychology · doi:10.3389/fpsyg.2012.00169 · Cited by 68 · see citing works
“Changes in both alpha and beta oscillations have previously been shown to be behaviorally relevant (Hammond et al., 2007; Dugue et al., 2011).”
BackgroundLook now and hear what's coming: On the functional role of cross-modal phase reset
Thorne, J. D., & Debener, S. (2013) · Hearing Research · doi:10.1016/j.heares.2013.07.002 · Cited by 66 · see citing works
“Subsequent studies have used similar methodology to show phase effects on transcranial magnetic stimulation (TMS)-induced phosphene detection (Dugue et al., 2011) and saccadic reaction time (Drewes and VanRullen, 2011) in addition to further examples of threshold-stimulus detection (e.”
MethodDistinct roles of theta and alpha oscillations in the involuntary capture of goal-directed attention
Harris, A. M., Dux, P. E., Jones, C. N., & Mattingley, J. B. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.03.008 · Cited by 65 · see citing works
“, 2009), as well as the probability that transcranial magnetic stimulation (TMS) of occipital cortex will produce phosphenes (Dugue et al., 2011; Romei et al., 2012).”
Fluctuations in instantaneous frequency predict alpha amplitude during visual perception
Nelli, S., Itthipuripat, S., Srinivasan, R., & Serences, J. T. (2017) · Nature Communications · doi:10.1038/s41467-017-02176-x · Cited by 63 · see citing works
Distinct contributions of alpha and theta rhythms to perceptual and attentional sampling
Michel, R., Dugué, L., & Busch, N. A. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15154 · Cited by 62 · see citing works
“…perceptual rhythms comes from studies demonstrating the effect of the phase of ongoing neuronal oscillations in the alpha range (8– 12 Hz) at the moment of stimulus onset on stimulus detection (Busch et al., 2009; Mathewson et al., 2009) or detection of TMS-induced pho-sphenes (Dugué et al., 2011).”
Shirinpour, S., Alekseichuk, I., Mantell, K. E., & Opitz, A. (2020) · Journal of Neural Engineering · doi:10.1088/1741-2552/ab9dba · Cited by 61 · see citing works
How to test for phasic modulation of neural and behavioural responses
Zoefel, B., Davis, M. H., Valente, G., & Riecke, L. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116175 · Cited by 61 · see citing works
Cooke, J., Poch, C., Gillmeister, H., Costantini, M., & Romei, V. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.3184-18.2019 · Cited by 60 · see citing works
“…by oscillatory activity in the alpha band (Ergenoglu et al., 2004; Hanslmayr et al., 2007; Romei et al., 2008a,b, 2010; Van Dijk et al., 2008; Dugué et al., 2011; Weisz et al., 2011; Frey et al., 2014), while somatosensory processing typically occurs within the beta band (Salenius and Hari,…”
BackgroundDirect Control of Visual Perception with Phase-specific Modulation of Posterior Parietal Cortex
Jaegle, A., & Ro, T. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00494 · Cited by 59 · see citing works
“Other results suggest that these phase-correlated behavioral effects may reflect modulations in cortical excitability following the alpha phase, with peak excitability occurring at the phase opposite to minimum excitability, as measured by the fMRI BOLD response (Scheeringa, Mazaheri, Bojak, Norris, & Kleinschmidt, 20…”
MethodInfluentialRhythmic modulation of visual contrast discrimination triggered by action
Benedetto, A., Donatella Spinelli, A., & Morrone, M. C. (2016) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2016.0692 · Cited by 57 · see citing works
“B 283 : 20160692 Brain alpha-oscillatory activity is generally linked to inhibition of cortical areas, and thus strongly coupled with stimulus processing [43–45].”
BackgroundSchaworonkow, N., Gordon, P. C., Belardinelli, P., Ziemann, U., Bergmann, T. O., & Zrenner, C. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00954 · Cited by 57 · see citing works
Herring, J., Esterer, S., Marshall, T. R., Jensen, O. B., & Bergmann, T. O. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.09.047 · Cited by 54 · see citing works
“While Mathewson et al. (2009) found reduced visual detection performance during the alpha trough of parietal electrodes, Dugue et al. (2011) found increased phosphene probability in response to transcranial magnetic stimulation (TMS) during the parietal alpha trough.”
- Authors
- Dugué, L., Marque, P., & VanRullen, R.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- ORCID
- Dugué, Laura
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-08-17
- Volume
- 31
- Issue
- 33
- Pages
- 11889-11893
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6623205
- OpenAlex
- W2003309602
- Cited by
- 364
- References
- 29
- Citations by year
- 2026: 20 · 2025: 25 · 2024: 19 · 2023: 17 · 2022: 26 · 2021: 21 · 2020: 19 · 2019: 27 · 2018: 36 · 2017: 40 · 2016: 28 · 2015: 21 · 2014: 23 · 2013: 21 · 2012: 18
- FWCI
- 10.40
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- EEG phase, alpha oscillations, cortical excitability, visual perception, phosphenes, transcranial magnetic stimulation, illusory perception, neural noise, perceptual thresholds, visual cortex
- MeSH terms
- Adult, Alpha Rhythm, Electroencephalography, Female, Humans, Male, Phosphenes, Photic Stimulation, Visual Cortex, Visual Perception, Transcranial Magnetic Stimulation, Young Adult
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