Cited by 366Neural dynamics and brain functionTranscranial Magnetic Stimulation StudiesVisual perception and processing mechanisms

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The phase of ongoing oscillations mediates the causal relation between brain excitation and visual perception.

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Dugué, Laura, Marque, Philippe, VanRullen, Rufin·2011·The Journal of Neuroscience

DOI 10.1523/jneurosci.1161-11.2011PMC PMC6623205

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Abstract

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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Figure 1 Prepulse phase predicts phosphene perception. A , Statistical comparison between phase-locking values for trials grouped according to perception (phosphene/nophosphene, averaged over 64 electrodes and 9 subjects) and surrogate phase-locking values computed over random subsets of trials. A significant effect indicates that ongoing phase differs statistically for phosphene and no-phosphene trials. The color map represents uncorrected p values (similar in B and C ) and the white outline indicates significant effects corrected for multiple comparisons using the FDR method. There is a strongly significant phase effect (FDR = 10 -5 ; corresponding to a p value threshold of 6.4 × 10 -7 ) in the last 400 ms preceding the pulse, ranging in frequency from 7 to 17 Hz. The topography shows the scalp distribution of phase-locking values in the time-frequency range of 7 to 17 Hz and -400 to -50 ms. Further analyses are performed on two regions of interest: a frontal and an occipital one. B , Statistical significance of the phase difference between phosphene and no-phosphene trials, in the frontal region of interest at each time-frequency point. There is a strongly significant phase effect (FDR = 10 -3 ; corresponding to a p value threshold of 6.2 × 10 -5 ) in the 400 ms preceding the pulse and in the alpha frequency range ( ∼ 10 Hz). C , Same as B , but for the occipital region of interest.CC-BY-NC-SA · From the PDF

Figure 2 Differential activity (top), and periodic fluctuations of phosphene probability (bottom). A , Difference of ERPs between phosphene trials and no-phosphene trials for an occipital electrode (PO3). B , Difference of ERPs for a frontal electrode (AFz). The shaded area around the ERP difference corresponds to the SEM across nine subjects (SEM). The gray rectangle from -1 ms to 150 ms masks the duration of electrical artifacts induced by the TMS pulse. The black line at 0 ms corresponds to the pulse onset and at 600 ms to the onset of the response screen, asking subjects to report the presence or absence of a phosphene. The ERP difference diverges from zero between 250 and 600 ms after the pulse, supporting the notion that the two conditions differ at the perceptual level. In addition, the difference oscillates during the 400 ms before the pulse onset, suggesting that the two conditions correspond to different prepulse phases. C , Relationship between the prepulse occipital EEG phase (expressed in radians) at -77 ms and 10.7 Hz (time-frequency point of maximal significance), and phosphene perception (expressed as a modulation of average phosphene probability). Single trials were sorted in 10 phase bins. Phosphene probability was computed for each phase bin, then averaged over all electrodes in the occipital region of interest and over all subjects (error bars represent SEM across subjects). For enhanced readability, the curve is plotted over two consecutive cycles (phase values that were replicated are represented over shaded backgrounds). The curve demonstrates that phosphene report probability significantly oscillates along with ongoing EEG phase (one-way ANOVA over the 10 phase values, F (9,89) = 2.35, p = 0.021). The magnitude of this periodic modulation (measured between optimal and opposite phase values) is ∼ 13%. D , Relationship between the prepulse EEG phase at -40 ms and 12.6 Hz (time-frequency point of maximal significance) and phosphene perception, averaged over all electrodes of the frontal region of interest. Plotting conventions are similar to those in C . As previously, phosphene probability significantly oscillates along with ongoing EEG phase (one-way ANOVA, F (9,89) = 2.72, p = 0.008). The magnitude of this periodic modulation is ∼ 15%.CC-BY-NC-SA · From the PDF

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Stimulus probability affects the visual N700 component of the event-related potential
Althen, H., Banaschewski, T., Brandeis, D., & Bender, S. (2019) · Clinical Neurophysiology · doi:10.1016/j.clinph.2019.11.059 · Cited by 7
Expectance of low contrast retro-cues does not modulate anticipatory alpha power
Macedo-Pascual, J., Campo, P., Capilla, A., Hinojosa, J. A., & Poch, C. (2022) · Biological Psychology · doi:10.1016/j.biopsycho.2022.108400 · Cited by 6
Human Brain Oscillations: From Physiological Mechanisms to Analysis and Cognition
Jensen, O. B., Spaak, E., & Zumer, J. M. (2019) · Springer eBooks · doi:10.1007/978-3-319-62657-4_17-1 · Cited by 9
Pre-stimulus brain states predict and control variability in stimulation responses
Rabuffo, G., Angiolelli, M., Fukai, T., Deco, G., Sorrentino, P., & Momi, D. (2026) · Brain stimulation · doi:10.1016/j.brs.2026.103118 · Cited by 8
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Knight, R. S., Chen, T., Gratton, G., Fabiani, M., Savazzi, S., Mazzi, C., & Beck, D. M. (2024) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2024.108864 · Cited by 6
Attentional rhythmic blink: Theta/Alpha balance in neural oscillations determines the rhythmicity in visual samplingPreprint
Kawashima, T., Hayashi, M. J., & Amano, K. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.15.488436 · Cited by 4
“The reference time-point for each frequency band was defined by the time of observed minimum p-values (maximum significance) for the power (Dugué et al., 2011).”
BackgroundMethod
The Inattentional Rhythm in Audition
Lui, T. K., Boglietti, E., & Zoefel, B. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1544-24.2025 · Cited by 4
Regulation of the Functional State of the Human Brain by Real-Time Frequency−Phase Synchronization of Sensory Stimuli with the EEG Rhythm
Pushkin, A. A., Lysenko, L. V., Сухов, А. Г., Владленович, В. А., & Щербань, И. В. (2017) · Biomedical Engineering · doi:10.1007/s10527-017-9678-7 · Cited by 4
Phosphene Attributes Depend on Frequency and Intensity of Retinal tACS
Kvašňák, E., Orendáčová, M., & Vránová, J. (2022) · Physiological Research · doi:10.33549/physiolres.934887 · Cited by 4
“There are several studies that have found a link between phosphenes perception and EEG amplitude [10], phase [31], and frequency [10, 32].”
Prestimulus Alpha Phase Modulates Visual Temporal Integration
Johannknecht, M., Schnitzler, A., & Lange, J. (2024) · eNeuro · doi:10.1523/eneuro.0471-23.2024 · Cited by 4
“The reported performance effects (decreasing when deviating from the preferred phase) are smaller compared with other studies ( ∼ 7% difference between highest and lowest bin compared with ∼ 13%; Busch et al., 2009; Dugue et al., 2011; Baumgarten et al., 2015; Fakche et al., 2022).”
The effect of task‐irrelevant visual backgrounds on human transcranial magnetic stimulation‐evoked electroencephalography responses and cortical alpha activity
Rutiku, R., Einberg, A., Imanaka, K., & Bachmann, T. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12374 · Cited by 4
“This view is strengthened by results showing that phosphenes are more likely to be perceived if TMS is applied at a time when alpha power is low (Romei et al., 2008) or when its phase is optimal (Dugu e et al., 2011).”
BackgroundInfluential
Transcranial brain stimulation and EEG/MEG
Bergmann, T. O., Tomasevic, L., & Siebner, H. R. (2021) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780198832256.013.26 · Cited by 3
Individual alpha frequency appears unrelated to the latency of early visual responses
Morrow, A., Dou, W., & Samaha, J. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1118910 · Cited by 4
“This account would be consistent with a growing body of literature demonstrating that alpha-band phase modulates perceptual detection (Busch et al., 2009; Mathewson et al., 2009; Dugué et al., 2011; Ai and Ro, 2014; Samaha et al., 2015, 2017; Alexander et al., 2020) and neuronal responses (Haegens et al.”
Result
The role of neural oscillations in visuo-motor communication at the time of saccades
Burr, D. C., & Morrone, M. C. (2023) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2023.108682 · Cited by 4
Advances and Challenges in Transcranial Magnetic Stimulation (TMS) Research on Motor Systems
Chen, M., Cline, C. C., Frost, K. L., Kimberley, T. J., Nemanich, S. T., Gillick, B. T., Albott, C. S., Prudente, C. N., Lim, K. O., & He, B. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813068-1.00011-7 · Cited by 4
Neuronal synchrony and the relation between the BOLD response and the local field potentialPreprint
Winawer, J. A., Nguyen, M., & Hermes, D. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.17605/osf.io/v22bm · Cited by 4
TMS entrains occipital alpha activity: Individual alpha frequency predicts the strength of entrained phase-lockingPreprint
Lin, Y.-J., Shukla, L., Dugué, L., Valero‐Cabré, A., & Carrasco, M. (2021) · Research Square · doi:10.21203/rs.3.rs-574152/v1 · Cited by 4
“In the visual cortex, the parieto-occipital alpha-band phase correlates with baseline cortical 71 excitability (phosphene threshold) [12], gamma-band (40-100 Hz) power [13], and spiking 72”
Background
Contents of Visual Predictions Oscillate at Alpha Frequencies
Hetenyi, D., Haarsma, J., & Kok, P. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0474-25.2025 · Cited by 4
“…ﬂ uence performance in visual tasks (Ergenoglu et al., 2004; van Dijk et al., 2008; Busch et al., 2009; Mathewson et al., 2009; Romei et al., 2010; Dugué et al., 2011; VanRullen et al., 2011; Hanslmayr et al., 2013; Iemi et al., 2019) and have been found to vary with experimental manipulations…”
Temporal basis function models for closed-loop neural stimulation
Bryan, M. J., Schwock, F., Yazdan-Shahmorad, A., & Rao, R. P. N. (2025) · Journal of Neural Engineering · doi:10.1088/1741-2552/ae036a · Cited by 7
“As above, the controller assumes the stimulation will be applied after a delay of 20ms and must decide whether to apply stimulation or not at the current time point based on how close a predicted trajectory will be to the reference trajectory.”
Visual awareness sharpens and accelerates attentional sampling through enhancing inhibitory neural modulation in the attention network
Yang, F., Yuan, P., Shen, L., Zhou, K., He, S., & Jiang, Y. (2025) · Nature Communications · doi:10.1038/s41467-025-64987-7 · Cited by 3
Frequency-specific attentional mechanisms phasically modulate the influence of distractors on task performance
Redding, Z. V., Ding, Y., & Fiebelkorn, I. C. (2026) · PLoS Biology · doi:10.1371/journal.pbio.3003664 · Cited by 4
Temporal Integration of Motion Streaks in Migraine
O’Hare, L. (2018) · Vision · doi:10.3390/vision2030027 · Cited by 3
“The alpha band oscillations provide a "‘window of excitability" [52]; if 209 alpha power is high at stimulus onset, then it is unlikely to be perceived, conversely, if occipital alpha 210 power is low at stimulus onset then it is more likely to be perceived [53] [54] [55].”
Background
Perceptual Illusions Caused by Discrete Sampling
Sokoliuk, R., & Rufin Vanrullen, A. (2019) · Springer eBooks · doi:10.1007/978-3-030-22048-8_17 · Cited by 3
Evidence for a theta‐band behavioural oscillation in rapid face detection
Liu, X., Balestrieri, E., & Melcher, D. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15790 · Cited by 3
Modulation of neural oscillations and associated behaviour by transcranial Alternating Current Stimulation (tACS)
Vossen, A. Y. (2017) · Enlighten: Theses (The University of Glasgow) · Cited by 4
Attention enhances LFP phase coherence in macaque visual cortex, improving sensory processingPreprint
Zareian, B., Daliri, M. R., Maboudi, K., Moghaddam, H. A., Treue, S., & Esghaei, M. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/499756 · Cited by 3
“Interestingly, it has been shown that pre-stimulus brain activity causally determines visual perception (Dugué et al., 2011).”
Background
Alpha closed-loop auditory stimulation modulates waking alpha oscillations and sleep onset dynamics in a phase-dependent manner in humansPreprint
Hebron, H., Lugli, B., Dimitrova, R., Jaramillo, V., Rhodes, E., Grossman, N., Dijk, D., & Violante, I. R. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.15.512722 · Cited by 3
“In this scenario, pre-trough locked sounds arrived at a more suitable phase at which to perturb the brain and in consequence the sleep process, in a similar vein to the cyclic excitability put forward in the visual neuroscience literature [5,6,8,14,15,52,53,59].”
Background
Detecting behavioural oscillations with increased sensitivity: A modification of Brookshire’s (2022) AR-surrogate methodPreprint
Harris, A. M., & Beale, H. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.22.609278 · Cited by 3
“…grew out of ﬁndings that the phase of rhythmic brain activity (i.e., whether brain waves are at a peak or trough) inﬂuenced neural processing and perception (Busch et al., 2009; Dugué et al., 2011; Haegens et al., 2011; Harris et al., 2018; Mathewson et al., 2009; Williams et al., 2024).”
Background
No evidence for the effect of entrainment's phase on duration reproduction and precision of regular intervals
Chatroudi, A. H., & Yotsumoto, Y. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.16071 · Cited by 2
“In recent years, in addition to studies that have reported positive findings (e.g., Busch et al., 2009; de Graaf et al., 2013; Dugué et al., 2011; Fakche et al., 2022; Mathewson et al., 2009; Ronconi et al., 2018), there has been a trend in reporting null results regarding the role of inhibitory…”
BackgroundResult
Mathematical Psychiatry: On Cortical Spreading Depression—A Review
Nsugbe, E. (2023) · Brain Sciences · doi:10.3390/brainsci13091241 · Cited by 2
Pre-stimulus EEG phase coherence predicts visual target detection failures in schizophrenia: A pilot study
Reavis, E. A., Wynn, J. K., & Green, M. F. (2024) · Schizophrenia Research · doi:10.1016/j.schres.2024.08.016 · Cited by 2
Performance Evaluation of a Real-Time Phase Estimation Algorithm Applied to Intracortical Signals from Human Visual Cortex
Grani, F., Soto‐Sánchez, C., Doblado, A. R., Grima, M. D., Farfán, F. D., Calvo, M. V., Soo, L., Wacławczyk, D., Ferrandez, J., González, P., et al. (2022) · Lecture notes in computer science · doi:10.1007/978-3-031-06242-1_51 · Cited by 2
Recognizing an Object from the Sum of Its Parts: An Intracranial Study on Alpha Rhythms
Bertrand, J., Tremblay, J., Lassonde, M. C., Vannasing, P., Nguyen, D. K., Robert, M., Bouthillier, A., & Leporé, F. (2014) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00582 · Cited by 2
“This is speculative but relates to the resonance concept proposed by Grossberg (1995) and to Bar et al.”
The neurodynamic bases of imitating learning and episodic memory
Давидович, Ц. В. (2016) · BIOPHYSICS · doi:10.1134/s0006350916020226 · Cited by 2
Oscillations and Synchrony in Attention
Keitel, C., Thut, G., & Groß, J. (2020) · Springer eBooks · doi:10.1007/978-1-0716-0653-7_3 · Cited by 2
Flexible allocation of attention in time or space across the life span : Theta and alpha oscillatory signatures of age-related decline and compensation as revealed by MEG
Callaghan, E., Holland, C., & Kessler, K. (2018) · Lancaster EPrints (Lancaster University) · Cited by 2
Visual Entrainment at 10 Hz causes periodic modulation of the Flash Lag IllusionPreprint
Chota, S., & Rufin Vanrullen, A. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/515114 · Cited by 2
Neuronal synchrony and the relation between the BOLD response and the local field potentialPreprint
Hermes, D., Nguyen, M., & Winawer, J. A. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/083840 · Cited by 2
“This is consistent with the observations that the threshold for eliciting a phosphene with TMS changes with alpha phase [72,73] and that the alpha phase at the time of stimulus presentation influences the size of the BOLD response in visual cortex [74].”
Result
Transcranial magnetic stimulation to frontal but not occipital cortex disrupts endogenous attentionPreprint
Fernández, A., Hanning, N. M., & Carrasco, M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.01.514715 · Cited by 2
Cross-modal interaction of Alpha Activity does not reflect inhibition of early sensory processing: A frequency tagging study using EEG and MEGPreprint
Brickwedde, M., Limachya, R., Markiewicz, R., Sutton, E., Postzich, C., Shapiro, K. L., Jensen, O. B., & Mazaheri, A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.19.488727 · Cited by 2
“Alpha inhibition is believed to be transmitted in a phasic manner, as phosphene perception as well as high-frequency and spiking activity vary in line with the alpha cycle (Dugué et al., 2011; Haegens et al., 2011; Spaak et al., 2012).”
Background
Cross-modal interaction of Alpha Activity does not reflect inhibition of early sensory processing: A frequency tagging study using EEG and MEGPreprint
Brickwedde, M., Limachya, R., Markiewicz, R., Sutton, E., Postzich, C., Shapiro, K. L., Jensen, O. B., & Mazaheri, A. (2025) · eLife · doi:10.7554/elife.106050.1 · Cited by 2
Cross-modal interaction of Alpha Activity does not reflect inhibition of early sensory processing: A frequency tagging study using EEG and MEGPreprint
Brickwedde, M., Limachya, R., Markiewicz, R., Sutton, E., Postzich, C., Shapiro, K. L., Jensen, O. B., & Mazaheri, A. (2025) · eLife · doi:10.7554/elife.106050.3 · Cited by 2
Phase-Dependent EEG Decoding of Continuous Visual StimuliPreprint
Deodato, M., & Melcher, D. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.10.687532 · Cited by 2
Neural oscillatory dynamics of spoken word recognition
Strauß, A. (2015) · Cited by 2

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
DOI: 10.1523/jneurosci.1161-11.2011
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: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 184 d)
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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The phase of ongoing oscillations mediates the causal relation between brain excitation and visual perception.

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