Mechanisms of sustained perceptual entrainment after stimulus offset.

EEG attention beat oscillation synchronization

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:
Mar 2024
Historique:
revised: 21 04 2023
received: 12 03 2021
accepted: 22 04 2023
pubmed: 8 5 2023
medline: 8 5 2023
entrez: 7 5 2023
Statut: ppublish

Résumé

Temporal alignment of neural activity to rhythmic stimulation has been suggested to result from a resonating internal neural oscillator mechanism, but can also be explained by interval-based temporal prediction. Here, we investigate behavioural and brain responses in the post-stimulation period to compare an oscillatory versus an interval-based account. Hickok et al.'s (2015) behavioural paradigm yielded results that relate to a neural oscillatory entrainment mechanism. We adapted the paradigm to an event-related potential (ERP) suitable design: a periodic sequence was followed, in half of the trials, by near-threshold targets embedded in noise. The targets were played in various phases in relation to the preceding sequences' period. Participants had to detect whether targets were played or not, and their EEG was recorded. Both behavioural results and the P300 component of the ERP were not only partially consistent with an oscillatory mechanism but also partially consistent with an interval-based attentional gain mechanism. Instead, data obtained in the post-entrainment period can best be explained with a combination of both mechanisms.

Identifiants

pubmed: 37150801
doi: 10.1111/ejn.16032
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1047-1060

Subventions

Organisme : Deutsche Forschungsgemeinschaft

Informations de copyright

© 2023 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd.

Références

Bauer, A.-K. R., Jaeger, M., Thorne, J. D., Bendixen, A., & Debener, S. (2015). The auditory dynamic attending theory revisited: A closer look at the pitch comparison task. Brain Research, 1626, 198-210. https://doi.org/10.1016/j.brainres.2015.04.032
Bolger, D., Coull, J. T., & Schön, D. (2014). Metrical rhythm implicitly orients attention in time as indexed by improved target detection and left inferior parietal activation. Journal of Cognitive Neuroscience, 26(3), 593-605. https://doi.org/10.1162/jocn_a_00511
Bouwer, F. L., Honing, H., & Slagter, H. A. (2020). Beat-based and memory-based temporal expectations in rhythm: Similar perceptual effects, different underlying mechanisms. Journal of Cognitive Neuroscience, 32(7), 1221-1241. https://doi.org/10.1162/jocn_a_01529
Brainard, D. H. (1997). The psychophysics toolbox. Spatial Vision, 10(4), 433-436. https://doi.org/10.1163/156856897X00357
Breska, A., & Deouell, L. Y. (2017). Neural mechanisms of rhythm-based temporal prediction: Delta phase-locking reflects temporal predictability but not rhythmic entrainment. PLoS Biology, 15(2), e2001665. https://doi.org/10.1371/journal.pbio.2001665
Breska, A., & Ivry, R. B. (2018). Double dissociation of single-interval and rhythmic temporal prediction in cerebellar degeneration and Parkinson's disease. Proceedings of the National Academy of Sciences of the United States of America, 115(48), 12283-12288. https://doi.org/10.1073/pnas.1810596115
Breska, A., & Ivry, R. B. (2020). Context-specific control over the neural dynamics of temporal attention by the human cerebellum. Science Advances, 6(49), eabb1141. https://doi.org/10.1126/sciadv.abb1141
Capilla, A., Pazo-Alvarez, P., Darriba, A., Campo, P., & Gross, J. (2011). Steady-state visual evoked potentials can be explained by temporal superposition of transient event-related responses. PLoS ONE, 6(1), e14543. https://doi.org/10.1371/journal.pone.0014543
Costa-Faidella, J., Baldeweg, T., Grimm, S., & Escera, C. (2011). Interactions between ‘what’ and ‘when’ in the auditory system: Temporal predictability enhances repetition suppression. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 31(50), 18590-18597. https://doi.org/10.1523/JNEUROSCI.2599-11.2011
Coull, J. T., & Nobre, A. C. (1998). Where and when to pay attention: The neural Systems for Directing Attention to spatial locations and to time intervals as revealed by both PET and fMRI. In. The Journal of Neuroscience, 18(18), 7426-7435. https://doi.org/10.1523/jneurosci.18-18-07426.1998
Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134(1), 9-21. https://doi.org/10.1016/j.jneumeth.2003.10.009
Drake, C., Jones, M. R., & Baruch, C. (2000). The development of rhythmic attending in auditory sequences: Attunement, referent period, focal attending. Cognition, 77(3), 251-288. https://doi.org/10.1016/S0010-0277(00)00106-2
Ellis, R. J., & Jones, M. R. (2010). Rhythmic context modulates foreperiod effects. Attention, Perception, & Psychophysics, 72(8), 2274-2288. https://doi.org/10.3758/bf03196701
Farahbod, H., Saberi, K., & Hickok, G. (2020). The rhythm of attention: Perceptual modulation via rhythmic entrainment is lowpass and attention mediated. Attention, Perception & Psychophysics, 82(7), 3558-3570. https://doi.org/10.3758/s13414-020-02095-y
Font, F., Roma, G., & Serra, X. (2013). Freesound technical demo. In Proceedings of the 21st ACM international conference on multimedia - MM '13, Association for Computiting Machinery. https://doi.org/10.1145/2502081.2502245
Haegens, S., & Zion Golumbic, E. (2018). Rhythmic facilitation of sensory processing: A critical review. Neuroscience and Biobehavioral Reviews, 86, 150-165. https://doi.org/10.1016/j.neubiorev.2017.12.002
Helfrich, R. F., Breska, A., & Knight, R. T. (2019). Neural entrainment and network resonance in support of top-down guided attention. Current Opinion in Psychology, 29, 82-89. https://doi.org/10.1016/j.copsyc.2018.12.016
Henry, M. J., Herrmann, B., & Grahn, J. A. (2017). What can we learn about beat perception by comparing brain signals and stimulus envelopes? PLoS ONE, 12(2), e0172454. https://doi.org/10.1371/journal.pone.0172454
Henry, M. J., & Obleser, J. (2012). Frequency modulation entrains slow neural oscillations and optimizes human listening behavior. Proceedings of the National Academy of Sciences of the United States of America, 109(49), 20095-20100. https://doi.org/10.1073/pnas.1213390109
Hickok, G., Farahbod, H., & Saberi, K. (2015). The rhythm of perception: Entrainment to acoustic rhythms induces subsequent perceptual oscillation. Psychological Science, 26(7), 1006-1013. https://doi.org/10.1177/0956797615576533
Jones, M. R. (1976). Time, our lost dimension: Toward a new theory of perception, attention, and memory. Psychological Review, 83(5), 323-355. https://doi.org/10.1037/0033-295X.83.5.323
Jones, M. R., Moynihan, H., MacKenzie, N., & Puente, J. (2002). Temporal aspects of stimulus-driven attending in dynamic arrays. Psychological Science, 13(4), 313-319. https://doi.org/10.1111/1467-9280.00458
Joos, K., Gilles, A., Van de Heyning, P., De Ridder, D., & Vanneste, S. (2014). From sensation to percept: The neural signature of auditory event-related potentials. Neuroscience and Biobehavioral Reviews, 42, 148-156. https://doi.org/10.1016/j.neubiorev.2014.02.009
Kaernbach, C. (1991). Simple adaptive testing with the weighted up-down method. Perception & Psychophysics, 49(3), 227-229. https://doi.org/10.3758/BF03214307
Kayser, S. J., Ince, R. A. A., Gross, J., & Kayser, C. (2015). Irregular speech rate dissociates auditory cortical entrainment, evoked responses, and frontal alpha. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 35(44), 14691-14701. https://doi.org/10.1523/JNEUROSCI.2243-15.2015
Kujala, T., Tervaniemi, M., & Schröger, E. (2007). The mismatch negativity in cognitive and clinical neuroscience: Theoretical and methodological considerations. Biological Psychology, 74(1), 1-19. https://doi.org/10.1016/j.biopsycho.2006.06.001
Lakatos, P., Karmos, G., Mehta, A. D., Ulbert, I., & Schroeder, C. E. (2008). Entrainment of neuronal oscillations as a mechanism of attentional selection. Science, 320(5872), 110-113. https://doi.org/10.1126/science.1154735
Lakatos, P., Musacchia, G., O'Connel, M. N., Falchier, A. Y., Javitt, D. C., & Schroeder, C. E. (2013). The spectrotemporal filter mechanism of auditory selective attention. Neuron, 77(4), 750-761. https://doi.org/10.1016/j.neuron.2012.11.034
Lakatos, P., Shah, A. S., Knuth, K. H., Ulbert, I., Karmos, G., & Schroeder, C. E. (2005). An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. Journal of Neurophysiology, 94(3), 1904-1911.
Lange, K. (2010). Can a regular context induce temporal orienting to a target sound? International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology, 78(3), 231-238. https://doi.org/10.1016/j.ijpsycho.2010.08.003
Large, E. W. (2000). On synchronizing movements to music. Human Movement Science, 19(4), 527-566. https://doi.org/10.1016/s0167-9457(00)00026-9
Large, E. W., & Kolen, J. F. (1994). Resonance and the perception of musical meter. Connection Science, 6(2-3), 177-208. https://doi.org/10.1080/09540099408915723
Lütkenhöner, B., Krumbholz, K., Lammertmann, C., Seither-Preisler, A., Steinsträter, O., & Patterson, R. D. (2003). Localization of primary auditory cortex in humans by magnetoencephalography. NeuroImage, 18(1), 58-66. https://doi.org/10.1006/nimg.2002.1325
Marzecová, A., Schettino, A., Widmann, A., SanMiguel, I., Kotz, S. A., & Schröger, E. (2018). Attentional gain is modulated by probabilistic feature expectations in a spatial cueing task: ERP evidence. Scientific Reports, 8(1), 54. https://doi.org/10.1038/s41598-017-18347-1
Marzecová, A., Widmann, A., SanMiguel, I., Kotz, S. A., & Schröger, E. (2017). Interrelation of attention and prediction in visual processing: Effects of task-relevance and stimulus probability. Biological Psychology, 125, 76-90. https://doi.org/10.1016/j.biopsycho.2017.02.009
Mcauley, J. D. (1995). On the perception of time as phase: Toward an adaptive oscillator model of rhythm. Retrieved from http://citeseerx.ist.psu.edu/viewdoc/summary?doi=10.1.1.142.5482
Miniussi, C., Wilding, E. L., Coull, J. T., & Nobre, A. C. (1999). Orienting attention in time. Modulation of brain potentials. Brain: a Journal of Neurology, 122(Pt 8), 1507-1518.
Morillon, B., Schroeder, C. E., Wyart, V., & Arnal, L. H. (2016). Temporal prediction in lieu of periodic stimulation. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 36(8), 2342-2347. https://doi.org/10.1523/JNEUROSCI.0836-15.2016
Mulert, C., Pogarell, O., Juckel, G., Rujescu, D., Giegling, I., Rupp, D., Mavrogiorgou, P., Bussfeld, P., Gallinat, J., Möller, H. J., & Hegerl, U. (2004). The neural basis of the P300 potential. Focus on the time-course of the underlying cortical generators. European Archives of Psychiatry and Clinical Neuroscience, 254(3), 190-198. https://doi.org/10.1007/s00406-004-0469-2
Novembre, G., & Iannetti, G. D. (2018). Tagging the musical beat: Neural entrainment or event-related potentials? Proceedings of the National Academy of Sciences of the United States of America, 115(47), E11002-E11003. https://doi.org/10.1073/pnas.1815311115
Nozaradan, S., Peretz, I., & Mouraux, A. (2012). Selective neuronal entrainment to the beat and meter embedded in a musical rhythm. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 32(49), 17572-17581. https://doi.org/10.1523/JNEUROSCI.3203-12.2012
Nozaradan, S., Peretz, I., & Keller, P. E. (2016a). Individual differences in rhythmic cortical entrainment correlate with predictive behavior in sensorimotor synchronization. Scientific Reports, 6, 20612. https://doi.org/10.1038/srep20612
Nozaradan, S., Schönwiesner, M., Caron-Desrochers, L., & Lehmann, A. (2016b). Enhanced brainstem and cortical encoding of sound during synchronized movement. NeuroImage, 142, 231-240. https://doi.org/10.1016/j.neuroimage.2016.07.015
Obleser, J., & Kayser, C. (2019). Neural entrainment and attentional selection in the listening brain. Trends in Cognitive Sciences, 23(11), 913-926. https://doi.org/10.1016/j.tics.2019.08.004
ten Oever, S., Schroeder, C. E., Poeppel, D., van Atteveldt, N., & Zion-Golumbic, E. (2014). Rhythmicity and cross-modal temporal cues facilitate detection. Neuropsychologia, 63, 43-50. https://doi.org/10.1016/j.neuropsychologia.2014.08.008
ten Oever, S., Schroeder, C. E., Poeppel, D., van Atteveldt, N., Mehta, A. D., Mégevand, P., Groppe, D. M., & Zion-Golumbic, E. (2017). Low-frequency cortical oscillations entrain to subthreshold rhythmic auditory stimuli. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 37(19), 4903-4912. https://doi.org/10.1523/JNEUROSCI.3658-16.2017
Phillips-Silver, J., Aktipis, C. A., & Bryant, G. A. (2010). The ecology of entrainment: Foundations of coordinated rhythmic movement. Music Perception, 28(1), 3-14. https://doi.org/10.1525/mp.2010.28.1.3
Polich, J. (2003). Theoretical Overview of P3a and P3b. In J. Polich (Ed.), Detection of change (pp. 83-98). Boston, MA: Springer. https://doi.org/10.1007/978-1-4615-0294-4_5
Rajendran, V. G., & Schnupp, J. W. H. (2019). Frequency tagging cannot measure neural tracking of beat or meter [review of frequency tagging cannot measure neural tracking of beat or meter]. Proceedings of the National Academy of Sciences of the United States of America, 116(8), 2779-2780. https://doi.org/10.1073/pnas.1820020116
Rajendran, V. G., Teki, S., & Schnupp, J. W. H. (2018). Temporal processing in audition: Insights from music. Neuroscience, 389, 4-18. https://doi.org/10.1016/j.neuroscience.2017.10.041
Repp, B. H. (2005). Sensorimotor synchronization: A review of the tapping literature. Psychonomic Bulletin & Review, 12(6), 969-992. https://doi.org/10.3758/BF03206433
Repp, B. H., & Su, Y.-H. (2013). Sensorimotor synchronization: A review of recent research (2006-2012). Psychonomic Bulletin & Review, 20(3), 403-452. https://doi.org/10.3758/s13423-012-0371-2
Sanabria, D., & Correa, Á. (2013). Electrophysiological evidence of temporal preparation driven by rhythms in audition. Biological Psychology, 92(2), 98-105. https://doi.org/10.1016/j.biopsycho.2012.11.012
Schafer, E. W., Amochaev, A., & Russell, M. J. (1981). Knowledge of stimulus timing attenuates human evoked cortical potentials. Electroencephalography and Clinical Neurophysiology, 52(1), 9-17. https://doi.org/10.1016/0013-4694(81)90183-8
Schröger, E. (1998). Measurement and interpretation of the mismatch negativity. Behavior Research Methods, Instruments, & Computers: a Journal of the Psychonomic Society, Inc, 30(1), 131-145.
Stuckenberg, M. V., Schröger, E., & Widmann, A. (2019). Presentation probability of visual-auditory pairs modulates visually induced auditory predictions. Journal of Cognitive Neuroscience, 31(8), 1110-1125. https://doi.org/10.1162/jocn_a_01398
Summerfield, C., & Egner, T. (2009). Expectation (and attention) in visual cognition. Trends in Cognitive Sciences, 13(9), 403-409. https://doi.org/10.1016/j.tics.2009.06.003
Sun, Y., Michalareas, G., & Poeppel, D. (2021). The impact of phase entrainment on auditory detection is highly variable: Revisiting a key finding. The European Journal of Neuroscience, 55, 3373-3390. https://doi.org/10.1111/ejn.15367
Tal, I., Large, E. W., Rabinovitch, E., Wei, Y., Schroeder, C. E., Poeppel, D., & Golumbic, E. Z. (2017). Neural entrainment to the beat: The ‘missing-pulse’ phenomenon. The Journal of Neuroscience, 37(26), 6331-6341. https://doi.org/10.1523/jneurosci.2500-16.2017
Todorovic, A., Schoffelen, J.-M., van Ede, F., Maris, E., & de Lange, F. P. (2015). Temporal expectation and attention jointly modulate auditory oscillatory activity in the Beta band. PLoS ONE, 10(3), e0120288. https://doi.org/10.1371/journal.pone.0120288
Widmann. (n.d.). widmann/erptools. Retrieved January 31, 2021, from https://github.com/widmann/erptools
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
Will, U., & Berg, E. (2007). Brain wave synchronization and entrainment to periodic acoustic stimuli. Neuroscience Letters, 424(1), 55-60. https://doi.org/10.1016/j.neulet.2007.07.036
Zhao, J., Al-Aidroos, N., & Turk-Browne, N. B. (2013). Attention is spontaneously biased toward regularities. Psychological Science, 24(5), 667-677. https://doi.org/10.1177/0956797612460407
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

Auteurs

Moran Aharoni (M)

Edmund and Lilly Safra Center for Brain Science, The Hebrew University of Jerusalem, Jerusalem, Israel.
Wilhelm Wundt Institute for Psychology, Leipzig University, Leipzig, Germany.

Assaf Breska (A)

Max Planck Institute for Biological Cybernetics, Tübingen, Germany.

Matthias M Müller (MM)

Wilhelm Wundt Institute for Psychology, Leipzig University, Leipzig, Germany.

Erich Schröger (E)

Wilhelm Wundt Institute for Psychology, Leipzig University, Leipzig, Germany.

Classifications MeSH