Prestimulus alpha power but not phase influences visual discrimination of long-duration visual stimuli.


Journal

The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110

Informations de publication

Date de publication:
06 2022
Historique:
revised: 10 02 2021
received: 27 07 2020
accepted: 28 02 2021
pubmed: 6 3 2021
medline: 1 7 2022
entrez: 5 3 2021
Statut: ppublish

Résumé

Occipital oscillations in the alpha band are closely related to visual perception and attention. In multiple studies, increased alpha power has been shown to reduce detection rates of hard-to-detect visual stimuli. Recent studies explain this finding by a shift in perceptual bias. Moreover, the phase of alpha oscillations prior to stimulus onset appears to be critical for the detection of visual stimuli. This is explained by a shift in cortical excitability over the course of each alpha cycle. However, prior studies often used short presentation times of visual stimuli at the perceptual threshold. Here, we use longer presentation times to elucidate whether the same mechanisms hold for the perception of salient but challenging visual stimuli presented for up to 1,500 ms. To this end, we presented participants with hard to distinguish but salient upright or tilted Gaussian gratings in a two-alternative forced choice task, while recording occipital electroencephalographic activity. Previous reports link alpha power to stimulus detection hit rates, and we found that low prestimulus power at the individual alpha frequency relates to higher perceptual accuracy. Contrary to recent findings, we neither found an influence of alpha power on criterion, nor an influence of alpha phase on perception or response speed. We argue that longer presentation times might attenuate a possible response bias, and increased excitability might sharpen the discrimination ability, thereby leading to increased perceptual accuracy and unaffected response criterion.

Identifiants

pubmed: 33666291
doi: 10.1111/ejn.15169
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3141-3153

Informations de copyright

© 2021 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd.

Références

Achim, A., Bouchard, J., & Braun, C. M. J. (2013). EEG amplitude spectra before near threshold visual presentations differentially predict detection/omission and short-long reaction time outcomes. International Journal of Psychophysiology, 89, 88-98. https://doi.org/10.1016/j.ijpsycho.2013.05.016
Aczel, B., Palfi, B., & Szaszi, B. (2017). Estimating the evidential value of significant results in psychological science. PLoS One, 12.e0182651. https://doi.org/10.1371/journal.pone.0182651
Baumgarten, T. J., Schnitzler, A., & Lange, J. (2016). Prestimulus alpha power influences tactile temporal perceptual discrimination and confidence in decisions. Cerebral Cortex, 26, 891-903. https://doi.org/10.1093/cercor/bhu247
Becker, R., Ritter, P., & Villringer, A. (2008). Influence of ongoing alpha rhythm on the visual evoked potential. NeuroImage, 39, 707-716. https://doi.org/10.1016/j.neuroimage.2007.09.016
Benwell, C. S. Y., London, R. E., Tagliabue, C. F., Veniero, D., Gross, J., Keitel, C., & Thut, G. (2019). Frequency and power of human alpha oscillations drift systematically with time-on-task. NeuroImage, 192, 101-114. https://doi.org/10.1016/j.neuroimage.2019.02.067
Busch, N. A., Dubois, J., & Vanrullen, R. (2009). The phase of ongoing EEG oscillations predicts visual perception. Journal of Neuroscience, 29, 7869-7876. https://doi.org/10.1523/JNEUROSCI.0113-09.2009.
Busch, N. A., & Vanrullen, R. (2010). Spontaneous EEG oscillations reveal periodic sampling of visual attention. Proceedings of the National Academy of Sciences of the United States of America, 107, 16048-16053. https://doi.org/10.1073/pnas.1004801107
Callaway, E., & Yeager, C. L. (1960). Relationship between reaction time and electroencephalographic alpha phase. Science, 132, 1765-1766. https://doi.org/10.1126/science.132.3441.1765
Dugué, L., Marque, P., & Vanrullen, R. (2011). The phase of ongoing oscillations mediates the causal relation between brain excitation and visual perception. Journal of Neuroscience, 31, 11889-11893. https://doi.org/10.1523/JNEUROSCI.1161-11.2011
Dustman, R. E., & Beck, E. C. (1965). Phase of alpha brain waves, reaction time and visually evoked potentials. Electroencephalography and Clinical Neurophysiology, 18, 433-440. https://doi.org/10.1016/0013-4694(65)90123-9.
Ergenoglu, T., Demiralp, T., Bayraktaroglu, Z., Ergen, M., Beydagi, H., & Uresin, Y. (2004). Alpha rhythm of the EEG modulates visual detection performance in humans. Cognitive Brain Research, 20, 376-383. https://doi.org/10.1016/j.cogbrainres.2004.03.009
Haegens, S., Cousijn, H., Wallis, G., Harrison, P. J., & Nobre, A. C. (2014). Inter- and intra-individual variability in alpha peak frequency. NeuroImage, 92, 46-55. https://doi.org/10.1016/j.neuroimage.2014.01.049.
Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65-70.
Hussain, S. J., Claudino, L., Bönstrup, M., Norato, G., Cruciani, G., Thompson, R., Zrenner, C., Ziemann, U., Buch, E., & Cohen, L. G. (2018). Sensorimotor oscillatory phase-power interaction gates resting human corticospinal output. Cerebral Cortex, 29, 3766-3777. https://doi.org/10.1093/cercor/bhy255.
Iemi, L., & Busch, N. A. (2018). Moment-to-moment fluctuations in neuronal excitability bias subjective perception rather than strategic decision-making. eNeuro, 5, ENEURO.0430-17.2018-13. 10.1523/ENEURO.0430-17.2018
Iemi, L., Busch, N. A., Laudini, A., Haegens, S., Samaha, J., Villringer, A., & Nikulin, V. V. (2019). Multiple mechanisms link prestimulus neural oscillations to sensory responses. Elife, 8, 1300. https://doi.org/10.7554/eLife.43620
Iemi, L., Chaumon, M., Crouzet, S. M., & Busch, N. A. (2017). Spontaneous neural oscillations bias perception by modulating baseline excitability. Journal of Neuroscience, 37, 807-819. https://doi.org/10.1523/JNEUROSCI.1432-16.2016.
Jensen, O., Bonnefond, M., & Vanrullen, R. (2012). An oscillatory mechanism for prioritizing salient unattended stimuli. Trends in Cognitive Sciences, 16, 200-206. https://doi.org/10.1016/j.tics.2012.03.002.
Jensen, O., Gips, B., Bergmann, T. O., & Bonnefond, M. (2014). Temporal coding organized by coupled alpha and gamma oscillations prioritize visual processing. Trends in Neurosciences, 37, 357-369. https://doi.org/10.1016/j.tins.2014.04.001
Jensen, O., & Mazaheri, A. (2010). Shaping functional architecture by oscillatory alpha activity: Gating by inhibition. Frontiers in Human Neuroscience, 4, 186. https://doi.org/10.3389/fnhum.2010.00186
Kaernbach, C. (1991). Simple adaptive testing with the weighted up-down method. Perception and Psychophysics, 49(3), 227-229. https://doi.org/10.3758/bf03214307
Keil, J., Timm, J., SanMiguel, I., Schulz, H., Obleser, J., & Schonwiesner, M. (2014). Cortical brain states and corticospinal synchronization influence TMS-evoked motor potentials. Journal of Neurophysiology, 111, 513-519. https://doi.org/10.1152/jn.00387.2013
Klimesch, W., Sauseng, P., & Hanslmayr, S. (2007). EEG alpha oscillations: The inhibition-timing hypothesis. Brain Research Reviews, 53, 63-88. https://doi.org/10.1016/j.brainresrev.2006.06.003
Kloosterman, N. A., de Gee, J. W., Werkle-Bergner, M., Lindenberger, U., Garrett, D. D., & Fahrenfort, J. J. (2019). Humans strategically shift decision bias by flexibly adjusting sensory evidence accumulation. eLife, 8. https://doi.org/10.7554/eLife.37321
Lange, J., Keil, J., Schnitzler, A., Van Dijk, H., & Weisz, N. (2014). The role of alpha oscillations for illusory perception. Behavioural Brain Research, 271, 294-301. https://doi.org/10.1016/j.bbr.2014.06.015.
Leske, S., Ruhnau, P., Frey, J., Lithari, C., Müller, N., Hartmann, T., & Weisz, N. (2015). Prestimulus network integration of auditory cortex predisposes near-threshold perception independently of local excitability. Cerebral Cortex, 25, 4898-4907. https://doi.org/10.1093/cercor/bhv212.
Limbach, K., & Corballis, P. M. (2016). Prestimulus alpha power influences response criterion in a detection task. Psychophysiology, 53, 1154-1164. https://doi.org/10.1111/psyp.12666
Lynn, S. K., & Barrett, L. F. (2014). “Utilizing” signal detection theory. Psychological Science, 25, 1663-1673. https://doi.org/10.1177/0956797614541991
Macmillan, N. A., & Creelman, C. D. (2005). Detection theory: A user's guide. New York: Psychology Press.
Mathewson, K. E., Fabiani, M., Gratton, G., Beck, D. M., & Lleras, A. (2010). Rescuing stimuli from invisibility: Inducing a momentary release from visual masking with pre-target entrainment. Cognition, 115, 186-191. https://doi.org/10.1016/j.cognition.2009.11.010
Mathewson, K. E., Gratton, G., Fabiani, M., Beck, D. M., & Ro, T. (2009). To see or not to see: Prestimulus alpha phase predicts visual awareness. Neuroimage, 29, 2725-2732.
Oostenveld, R., Fries, P., Maris, E., & Schoffelen, J.-M. (2011). FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Computational Intelligence and Neuroscience, 2011, 1-9. https://doi.org/10.1155/2011/156869.
Peirce, J. W. (2007). PsychoPy-Psychophysics software in Python. Journal of Neuroscience Methods, 162, 8-13. https://doi.org/10.1016/j.jneumeth.2006.11.017
Peirce, J., Gray, J. R., Simpson, S., MacAskill, M., Höchenberger, R., Sogo, H., Kastman, E., & Lindeløv, J. (2019). PsychoPy2: Experiments in behavior made easy. Behavior Research Methods, 51, 195-203. https://doi.org/10.3758/s13428-018-01193-y.
Pfurtscheller, G., Stancák, A., & Neuper, C. (1996). Event-related synchronization (ERS) in the alpha band-an electrophysiological correlate of cortical idling: A review. International Journal of Psychophysiology, 24, 39-46. https://doi.org/10.1016/S0167-8760(96)00066-9.
Rahn, E., & Başar, E. (2009). Enhancement of visual evoked potentials by stimulation during low prestimulus EEG stages. International Journal of Neuroscience, 72, 123-136.
Roberts, D. M., Fedota, J. R., Buzzell, G. A., Parasuraman, R., & McDonald, C. G. (2014). Prestimulus oscillations in the alpha band of the EEG are modulated by the difficulty of feature discrimination and predict activation of a sensory discrimination process. Journal of Cognitive Neuroscience, 26, 1615-1628. https://doi.org/10.1162/jocn_a_00569.
Rouder, J. N., Speckman, P. L., Sun, D., Morey, R. D., & Iverson, G. (2009). Bayesian t tests for accepting and rejecting the null hypothesis. Psychonomic Bulletin & Review, 16, 225-237. https://doi.org/10.3758/PBR.16.2.225
Ruhnau, P., Hauswald, A., & Weisz, N. (2014). Investigating ongoing brain oscillations and their influence on conscious perception - Network states and the window to consciousness. Front. Psychology, 5, 1230.
Samaha, J., Iemi, L., Haegens, S., & Busch, N. A. (2020). Spontaneous brain oscillations and perceptual decision-making. Trends in Cognitive Sciences, 24, 639-653. https://doi.org/10.1016/j.tics.2020.05.004
Samaha, J., Iemi, L., & Postle, B. R. (2017). Prestimulus alpha-band power biases visual discrimination confidence, but not accuracy. Consciousness and Cognition, 54, 47-55. https://doi.org/10.1016/j.concog.2017.02.005.
Smith, P. L., & Ratcliff, R. (2004). Psychology and neurobiology of simple decisions. Trends in Neurosciences, 27, 161-168. https://doi.org/10.1016/j.tins.2004.01.006
Stanislaw, H., & Todorov, N. (1999). Calculation of signal detection theory measures. Behav Res Methods Instrum Comput, 31, 137-149. https://doi.org/10.3758/BF03207704.
Taylor, M. M., & Creelman, C. D. (1967). PEST: Efficient estimation provability functions. The Journal of the Acoustical Society of America, 41, 782-787.
Thut, G., Nietzel, A., Brandt, S. A., & Pascual-Leone, A. (2006). Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. Journal of neuroscience, 26(37), 9494-9502. https://doi.org/10.1523/JNEUROSCI.0875-06.2006
Trujillo-Ortiz, A., Hernandez-Walls, R., & Trujillo-Perez, R. A. (2020) RMAOV2: Two-way repeated measures ANOVA. A MATLAB file.
Van Dijk, H., Schoffelen, J.-M., Oostenveld, R., & Jensen, O. (2008). Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. Journal of Neuroscience, 28(8), 1816-1823. https://doi.org/10.1523/JNEUROSCI.1853-07.2008
van Elswijk, G., Maij, F., Schoffelen, J.-M., Overeem, S., Stegeman, D. F., & Fries, P. (2010). Corticospinal beta-band synchronization entails rhythmic gain modulation. Journal of Neuroscience, 30(12), 4481-4488. https://doi.org/10.1523/JNEUROSCI.2794-09.2010.
Van Vugt, M. K., Simen, P., Nystrom, L. E., Holmes, P., & Cohen, J. D. (2012). EEG oscillations reveal neural correlates of evidence accumulation. Frontiers in Neuroscience, 6, 106. https://doi.org/10.3389/fnins.2012.00106
Vanrullen, R. (2016). Perceptual cycles. Trends in Cognitive Sciences, 20, 723-735. https://doi.org/10.1016/j.tics.2016.07.006
Widmann, A., Schröger, E., & Maess, B. (2015). Digital filter design for electrophysiological data--a practical approach. Journal of Neuroscience Methods, 250, 34-46. https://doi.org/10.1016/j.jneumeth.2014.08.002
Zazio, A., Ruhnau, P., Weisz, N., & Wutz, A. (2021). Pre-stimulus alpha-band power and phase fluctuations originate from different neural sources and exert distinct impact on stimulus-evoked responses. The European Journal of Neuroscience, 1-13. https://doi.org/10.1111/ejn.15138
Zoefel, B., Davis, M. H., Valente, G., & Riecke, L. (2019). How to test for phasic modulation of neural and behavioural responses. NeuroImage, 202.116175. https://doi.org/10.1016/j.neuroimage.2019.116175
Zumer, J. M., Scheeringa, R., Schoffelen, J.-M., Norris, D. G., & Jensen, O. (2014). Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex. PLoS Biology, 12.e1001965. https://doi.org/10.1371/journal.pbio.1001965

Auteurs

Georgios Michail (G)

Department of Psychiatry and Psychotherapy, Multisensory Integration Lab, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Lino Toran Jenner (L)

Biological Psychology, Christian-Albrechts-University, Kiel, Germany.

Julian Keil (J)

Biological Psychology, Christian-Albrechts-University, Kiel, Germany.

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