Abstract
Visual and auditory stimuli are transmitted from the environment to sensory cortices with different timing, requiring the brain to encode when sensory inputs must be segregated or integrated into a single percept. The probability that different audiovisual (AV) stimuli are integrated into a single percept even when presented asynchronously is reflected in the construct of temporal binding window (TBW). There is a strong interest in testing whether it is possible to broaden or shrink TBW by using different neuromodulatory approaches that can speed up or slow down ongoing alpha oscillations, which have been repeatedly hypothesized to be an important determinant of the TBWs size. Here, we employed a web-based sensory entrainment protocol combined with a simultaneity judgment task using simple flash-beep stimuli. The aim was to test whether AV temporal acuity could be modulated trial by trial by synchronizing ongoing neural oscillations in the prestimulus period to a rhythmic sensory stream presented in the upper (∼12 Hz) or lower (∼8.5 Hz) alpha range. As a control, we implemented a nonrhythmic condition where only the first and the last entrainers were employed. Results show that upper alpha entrainment shrinks AV TBW and improves AV temporal acuity when compared with lower alpha and control conditions. Our findings represent a proof of concept of the efficacy of sensory entrainment to improve AV temporal acuity in a trial-by-trial manner, and they strengthen the idea that alpha oscillations may reflect the temporal unit of AV temporal binding.
Similar content being viewed by others
Data availability
The data and materials for this study are available upon request to the authors.
References
Albouy, P., Martinez-Moreno, Z. E., Hoyer, R. S., Zatorre, R. J., & Baillet, S. (2022). Supramodality of neural entrainment: Rhythmic visual stimulation causally enhances auditory working memory performance. Science Advances, 8(8), Article eabj9782.
Bauer, A. K. R., Debener, S., & Nobre, A. C. (2020). Synchronisation of neural oscillations and cross-modal influences. Trends in Cognitive Sciences, 24(6), 481–495.
Bastiaansen, M., Berberyan, H., Stekelenburg, J. J., Schoffelen, J. M., & Vroomen, J. (2020). Are alpha oscillations instrumental in multisensory synchrony perception? Brain Research, 1734, Article 146744.
Bedard, G., & Barnett-Cowan, M. (2016). Impaired timing of audiovisual events in the elderly. Experimental Brain Research, 234(1), 331–340.
Bridges, D., Pitiot, A., MacAskill, M. R., & Peirce, J. W. (2020). The timing mega-study: Comparing a range of experiment generators, both lab-based and online. PeerJ, 8, Article e9414.
Buhrmester, M., Kwang, T., & Gosling, S. D. (2016). Amazon’s Mechanical Turk: A new source of inexpensive, yet high-quality data? Perspectives on Psychological Science, 6(1), 3–5. https://doi.org/10.1177/17456916103939
Buergers, S., & Noppeney, U. (2022). The role of alpha oscillations in temporal binding within and across the senses. Nature Human Behaviour, 6(5), 732–742.
Cecere, R., Rees, G., & Romei, V. (2015). Individual differences in alpha frequency drive crossmodal illusory perception. Current Biology, 25(2), 231–235.
Cecere, R., Gross, J., & Thut, G. (2016). Behavioural evidence for separate mechanisms of audiovisual temporal binding as a function of leading sensory modality. European Journal of Neuroscience, 43(12), 1561–1568.
Cecere, R., Gross, J., Willis, A., & Thut, G. (2017). Being first matters: Topographical representational similarity analysis of ERP signals reveals separate networks for audiovisual temporal binding depending on the leading sense. Journal of Neuroscience, 37(21), 5274–5287.
Chiang, A. K. I., Rennie, C. J., Robinson, P. A., Van Albada, S. J., & Kerr, C. C. (2011). Age trends and sex differences of alpha rhythms including split alpha peaks. Clinical Neurophysiology, 122(8), 1505–1517.
Coldea, A., Veniero, D., Morand, S., Trajkovic, J., Romei, V., Harvey, M., & Thut, G. (2022). Effects of rhythmic transcranial magnetic stimulation in the alpha-band on visual perception depend on deviation from alpha-peak frequency: Faster relative transcranial magnetic stimulation alpha-pace improves performance. Frontiers in Neuroscience, 16, 886342. https://doi.org/10.3389/fnins.2022.886342
Colonius, H., & Diederich, A. (2004). Multisensory interaction in saccadic reaction time: A time-window-of-integration model. Journal of Cognitive Neuroscience, 16(6), 1000–1009.
Conrey, B., & Pisoni, D. B. (2006). Auditory-visual speech perception and synchrony detection for speech and nonspeech signals. The Journal of the Acoustical Society of America, 119(6), 4065–4073.
Cooke, J., Poch, C., Gillmeister, H., Costantini, M., & Romei, V. (2019). Oscillatory properties of functional connections between sensory areas mediate cross-modal illusory perception. Journal of Neuroscience, 39(29), 5711–5718.
Di Gregorio, F., Trajkovic, J., Roperti, C., Marcantoni, E., Di Luzio, P., Avenanti, A., … Romei, V. (2022). Tuning alpha rhythms to shape conscious visual perception. Current Biology, 32(5), 988–998.
De Graaf, T. A., & Duecker, F. (2022). No effects of rhythmic visual stimulation on target discrimination: An online alpha entrainment experiment. European Journal of Neuroscience, 55(11/12), 3340–3351.
De Graaf, T. A., Gross, J., Paterson, G., Rusch, T., Sack, A. T., & Thut, G. (2013). Alpha-band rhythms in visual task performance: Phase-locking by rhythmic sensory stimulation. PLOS ONE, 8(3), Article e60035.
Fenner, B., Cooper, N., Romei, V., & Hughes, G. (2020). Individual differences in sensory integration predict differences in time perception and individual levels of schizotypy. Consciousness and Cognition, 84, Article 102979.
Fiebelkorn, I. C., Saalmann, Y. B., & Kastner, S. (2013). Rhythmic sampling within and between objects despite sustained attention at a cued location. Current Biology, 23(24), 2553–2558.
Ghazanfar, A. A., & Schroeder, C. E. (2006). Is neocortex essentially multisensory? Trends in Cognitive Sciences, 10(6), 278–285.
Haegens, S., & Golumbic, E. Z. (2018). Rhythmic facilitation of sensory processing: A critical review. Neuroscience & Biobehavioral Reviews, 86, 150–165.
Hanslmayr, S., Axmacher, N., & Inman, C. S. (2019). Modulating human memory via entrainment of brain oscillations. Trends in Neurosciences, 42(7), 485–499.
Hillock-Dunn, A., & Wallace, M. T. (2012). Developmental changes in the multisensory temporal binding window persist into adolescence. Developmental Science, 15(5), 688–696.
Hillock-Dunn, A., Grantham, D. W., & Wallace, M. T. (2016). The temporal binding window for audiovisual speech: Children are like little adults. Neuropsychologia, 88, 74–82.
Huang, W. A., Stitt, I. M., Negahbani, E., Passey, D. J., Ahn, S., Davey, M., … Fröhlich, F. (2021). Transcranial alternating current stimulation entrains alpha oscillations by preferential phase synchronization of fast-spiking cortical neurons to stimulation waveform. Nature Communications, 12(1), Article 3151.
Kawashima, T., Shibusawa, S., & Amano, K. (2022). Frequency-and phase-dependent effects of auditory entrainment on attentional blink. European Journal of Neuroscience, 56(4), 4411–4424.
Keil, J., & Senkowski, D. (2018). Neural oscillations orchestrate multisensory processing. The Neuroscientist, 24(6), 609–626.
Lakatos, P., O’Connell, M. N., Barczak, A., Mills, A., Javitt, D. C., & Schroeder, C. E. (2009). The leading sense: Supramodal control of neurophysiological context by attention. Neuron, 64(3), 419–430.
Lakatos, P., Gross, J., & Thut, G. (2019). A new unifying account of the roles of neuronal entrainment. Current Biology, 29(18), R890–R905.
Landau, A. N., & Fries, P. (2012). Attention samples stimuli rhythmically. Current Biology, 22(11), 1000–1004.
Marsicano, G., Cerpelloni, F., Melcher, D., & Ronconi, L. (2022). Lower multisensory temporal acuity in individuals with high schizotypal traits: A web-based study. Scientific Reports, 12(1), 1–12.
Mason, W., & Suri, S. (2012). Conducting behavioral research on Amazon’s Mechanical Turk. Behavior Research Methods, 44(1), 1–23.
McGovern, D. P., Burns, S., Hirst, R. J., & Newell, F. N. (2022). Perceptual training narrows the temporal binding window of audiovisual integration in both younger and older adults. Neuropsychologia, 173, Article 108309. https://doi.org/10.1016/j.neuropsychologia.2022.108309
Migliorati, D., Zappasodi, F., Perrucci, M. G., Donno, B., Northoff, G., Romei, V., & Costantini, M. (2020). Individual alpha frequency predicts perceived visuotactile simultaneity. Journal of Cognitive Neuroscience, 32(1), 1–11.
Murray, M. M., Lewkowicz, D. J., Amedi, A., & Wallace, M. T. (2016). Multisensory processes: A balancing act across the lifespan. Trends in Neurosciences, 39(8), 567–579.
Newman, A., Bavik, Y. L., Mount, M., & Shao, B. (2021). Data collection via online platforms: Challenges and recommendations for future research. Applied Psychology, 70(3), 1380–1402.
Noel, J. P., Łukowska, M., Wallace, M., & Serino, A. (2016). Multisensory simultaneity judgment and proximity to the body. Journal of Vision, 16(3), 21–21.
Noel, J. P., De Niear, M. A., Stevenson, R., Alais, D., & Wallace, M. T. (2017). Atypical rapid audio-visual temporal recalibration in autism spectrum disorders. Autism Research, 10(1), 121–129.
Notbohm, A., Kurths, J., & Herrmann, C. S. (2016). Modification of brain oscillations via rhythmic light stimulation provides evidence for entrainment but not for superposition of event-related responses. Frontiers in Human Neuroscience, 10, 10.
Pasqualotto, A., Dumitru, M. L., & Myachykov, A. (2016). Multisensory integration: Brain, body, and world. Frontiers in Psychology, 6, Article 2046.
Peirce, J. W. (2007). PsychoPy—Psychophysics software in Python. Journal of Neuroscience Methods, 162(1/2), 8–13.
Pikovsky, A., Rosenblum, M., Kurths, J., & Strogatz, S. (2003). Books-synchronization: A universal concept in nonlinear sciences. Physics Today, 56(1), 47.
Powers, A. R., Hillock, A. R., & Wallace, M. T. (2009). Perceptual training narrows the temporal window of multisensory binding. Journal of Neuroscience, 29(39), 12265–12274.
Recanzone, G. H. (2009). Interactions of auditory and visual stimuli in space and time. Hearing Research, 258(1/2), 89–99.
Regan, D. (1982). Comparison of transient and steady-state methods. Annals of the New York Academy of Sciences, 388, 45–71. https://doi.org/10.1111/j.1749-6632.1982.tb50784.x
Reips, U. D. (2002). Standards for Internet-based experimenting. Experimental Psychology, 49(4), 243.
Roach, N. W., Heron, J., Whitaker, D., & McGraw, P. V. (2011). Asynchrony adaptation reveals neural population code for audio-visual timing. Proceedings of the Royal Society B: Biological Sciences, 278(1710), 1314–1322.
Romei, V., Gross, J., & Thut, G. (2012). Sounds reset rhythms of visual cortex and corresponding human visual perception. Current Biology, 22(9), 807–813.
Ronconi, L., & Melcher, D. (2017). The role of oscillatory phase in determining the temporal organization of perception: Evidence from sensory entrainment. Journal of Neuroscience, 37(44), 10636–10644.
Ronconi, L., Pincham, H. L., Cristoforetti, G., Facoetti, A., & Szűcs, D. (2016a). Shaping prestimulus neural activity with auditory rhythmic stimulation improves the temporal allocation of attention. NeuroReport, 27(7), 487.
Ronconi, L., Pincham, H. L., Szűcs, D., & Facoetti, A. (2016b). Inducing attention not to blink: Auditory entrainment improves conscious visual processing. Psychological Research, 80, 774–784.
Ronconi, L., Busch, N. A., & Melcher, D. (2018). Alpha-band sensory entrainment alters the duration of temporal windows in visual perception. Scientific Reports, 8(1), 1–10.
Ronconi, L., Vitale, A., Federici, A., Mazzoni, N., Battaglini, L., Molteni, M., & Casartelli, L. (2023). Neural dynamics driving audio-visual integration in autism. Cerebral Cortex, 33(3), 543–556.
Samaha, J., & Postle, B. R. (2015). The speed of alpha-band oscillations predicts the temporal resolution of visual perception. Current Biology, 25(22), 2985–2990.
Sauter, M., Draschkow, D., & Mack, W. (2020). Building, hosting and recruiting: A brief introduction to running behavioral experiments online. Brain Sciences, 10(4), 251.
Scally, B., Burke, M. R., Bunce, D., & Delvenne, J. F. (2018). Resting-state EEG power and connectivity are associated with alpha peak frequency slowing in healthy aging. Neurobiology of Aging, 71, 149–155.
Senkowski, D., Schneider, T. R., Foxe, J. J., & Engel, A. K. (2008). Crossmodal binding through neural coherence: Implications for multisensory processing. Trends in Neurosciences, 31(8), 401–409.
Simon, D. M., Noel, J. P., & Wallace, M. T. (2017). Event related potentials index rapid recalibration to audiovisual temporal asynchrony. Frontiers in Integrative Neuroscience, 11, 8.
Spaak, E., de Lange, F. P., & Jensen, O. (2014). Local entrainment of alpha oscillations by visual stimuli causes cyclic modulation of perception. Journal of Neuroscience, 34(10), 3536–3544.
Spence, C. (2007). Audiovisual multisensory integration. Acoustical Science and Technology, 28(2), 61–70.
Stecker, G. C. (2018). Temporal binding of auditory spatial information across dynamic binaural events. Attention, Perception, & Psychophysics, 80(1), 14–20.
Stein, B. E., & Stanford, T. R. (2008). Multisensory integration: Current issues from the perspective of the single neuron. Nature Reviews Neuroscience, 9(4), 255–266.
Stevenson, R. A., & Wallace, M. T. (2013). Multisensory temporal integration: Task and stimulus dependencies. Experimental Brain Research, 227(2), 249–261.
Stevenson, R. A., Fister, J. K., Barnett, Z. P., Nidiffer, A. R., & Wallace, M. T. (2012). Interactions between the spatial and temporal stimulus factors that influence multisensory integration in human performance. Experimental Brain Research, 219(1), 121–137.
Stevenson, R. A., Wilson, M. M., Powers, A. R., & Wallace, M. T. (2013). The effects of visual training on multisensory temporal processing. Experimental Brain Research, 225(4), 479–489.
Stevenson, R. A., Park, S., Cochran, C., McIntosh, L. G., Noel, J. P., Barense, M. D., … Wallace, M. T. (2017). The associations between multisensory temporal processing and symptoms of schizophrenia. Schizophrenia Research, 179, 97–103.
Surwillo, W. W. (1961). Frequency of the ‘alpha’ rhythm, reaction time and age. Nature, 191, 823–824.
Thorne, J. D., & Debener, S. (2014). Look now and hear what’s coming: On the functional role of cross-modal phase reset. Hearing Research, 307, 144–152.
Thut, G., Schyns, P. G., & Gross, J. (2011). Entrainment of perceptually relevant brain oscillations by non-invasive rhythmic stimulation of the human brain. Frontiers in Psychology, 2, 170.
Van der Burg, E., Alais, D., & Cass, J. (2013). Rapid recalibration to audiovisual asynchrony. Journal of Neuroscience, 33(37), 14633–14637.
van Wassenhove, V. (2013). Speech through ears and eyes: Interfacing the senses with the supramodal brain. Frontiers in Psychology, 4, 388.
Vatakis, A., Navarra, J., Soto-Faraco, S., & Spence, C. (2008). Audiovisual temporal adaptation of speech: Temporal order versus simultaneity judgments. Experimental Brain Research, 185(3), 521–529.
Venskus, A., & Hughes, G. (2021). Individual differences in alpha frequency are associated with the time window of multisensory integration, but not time perception. Neuropsychologia, 159, 107919.
Venskus, A., Ferri, F., Migliorati, D., Spadone, S., Costantini, M., & Hughes, G. (2021). Temporal binding window and sense of agency are related processes modifiable via occipital tACS. PLOS ONE, 16(9), Article e0256987.
Vroomen, J., & Keetels, M. (2010). Perception of intersensory synchrony: A tutorial review. Attention, Perception, & Psychophysics, 72(4), 871–884.
Wallace, M. T., & Stevenson, R. A. (2014). The construct of the multisensory temporal binding window and its dysregulation in developmental disabilities. Neuropsychologia, 64, 105–123.
Zampini, M., Guest, S., Shore, D. I., & Spence, C. (2005). Audio-visual simultaneity judgments. Perception & Psychophysics, 67(3), 531–544.
Zerr, M., Freihorst, C., Schütz, H., Sinke, C., Müller, A., Bleich, S., … Szycik, G. R. (2019). Brief sensory training narrows the temporal binding window and enhances long-term multimodal speech perception. Frontiers in Psychology, 10, Article 2489.
Zhou, H. Y., Cai, X. L., Weigl, M., Bang, P., Cheung, E. F., & Chan, R. C. (2018). Multisensory temporal binding window in autism spectrum disorders and schizophrenia spectrum disorders: A systematic review and meta-analysis. Neuroscience & Biobehavioral Reviews, 86, 66–76.
Acknowledgments and funding information
G.M. and C.B. were supported by Ministero dell’Istruzione, dell’Università e della Ricerca, PRIN 2017 (2017TBA4KS_003).
The data and materials for this study are available upon request to the authors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open practices statement
The data and materials for this study are available upon request to the authors.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Marsicano, G., Bertini, C. & Ronconi, L. Alpha-band sensory entrainment improves audiovisual temporal acuity. Psychon Bull Rev 31, 874–885 (2024). https://doi.org/10.3758/s13423-023-02388-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.3758/s13423-023-02388-x