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The Role of Oscillatory Phase in Determining the Temporal Organization of Perception: Evidence from Sensory Entrainment

Recent behavioral, neuroimaging, and neurophysiological studies have renewed the idea that the information processing within different temporal windows is linked to the phase and/or frequency of the ongoing oscillations, predominantly in the theta/alpha band (∼4–7 and 8–12 Hz, respectively). However...

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Autores principales: Ronconi, Luca, Melcher, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5666584/
https://www.ncbi.nlm.nih.gov/pubmed/28972130
http://dx.doi.org/10.1523/JNEUROSCI.1704-17.2017
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author Ronconi, Luca
Melcher, David
author_facet Ronconi, Luca
Melcher, David
author_sort Ronconi, Luca
collection PubMed
description Recent behavioral, neuroimaging, and neurophysiological studies have renewed the idea that the information processing within different temporal windows is linked to the phase and/or frequency of the ongoing oscillations, predominantly in the theta/alpha band (∼4–7 and 8–12 Hz, respectively). However, being correlational in nature, this evidence might reflect a nonfunctional byproduct rather than having a causal role. A more direct link can be shown with methods that manipulate oscillatory activity. Here, we used audiovisual entrainment at different frequencies in the prestimulus period of a temporal integration/segregation task. We hypothesized that entrainment would align ongoing oscillations and drive them toward the stimulation frequency. To reveal behavioral oscillations in temporal perception after the entrainment, we sampled the segregation/integration performance densely in time. In Experiment 1, two groups of human participants (both males and females) received stimulation either at the lower or the upper boundary of the alpha band (∼8.5 vs 11.5 Hz). For both entrainment frequencies, we found a phase alignment of the perceptual oscillation across subjects, but with two different power spectra that peaked near the entrainment frequency. These results were confirmed when perceptual oscillations were characterized in the time domain with sinusoidal fittings. In Experiment 2, we replicated the findings in a within-subject design, extending the results for frequencies in the theta (∼6.5 Hz), but not in the beta (∼15 Hz), range. Overall, these findings show that temporal segregation can be modified by sensory entrainment, providing evidence for a critical role of ongoing oscillations in the temporal organization of perception. SIGNIFICANCE STATEMENT The continuous flow of sensory input is not processed in an analog fashion, but rather is grouped by the perceptual system over time. Recent studies pinpointed the phase and/or frequency of the neural oscillations in the theta/alpha band (∼4–12 Hz) as possible mechanisms underlying temporal windows in perception. Here, we combined two innovative methodologies to provide more direct support for this evidence. We used sensory entrainment to align neural oscillations to different frequencies and then characterized the resultant perceptual oscillation with a temporal dense sampling of the integration/segregation performance. Our results provide the first evidence that the frequency of temporal segregation can be modified by sensory entrainment, supporting a critical role of ongoing oscillations in the integration/segregation of information over time.
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spelling pubmed-56665842017-11-15 The Role of Oscillatory Phase in Determining the Temporal Organization of Perception: Evidence from Sensory Entrainment Ronconi, Luca Melcher, David J Neurosci Research Articles Recent behavioral, neuroimaging, and neurophysiological studies have renewed the idea that the information processing within different temporal windows is linked to the phase and/or frequency of the ongoing oscillations, predominantly in the theta/alpha band (∼4–7 and 8–12 Hz, respectively). However, being correlational in nature, this evidence might reflect a nonfunctional byproduct rather than having a causal role. A more direct link can be shown with methods that manipulate oscillatory activity. Here, we used audiovisual entrainment at different frequencies in the prestimulus period of a temporal integration/segregation task. We hypothesized that entrainment would align ongoing oscillations and drive them toward the stimulation frequency. To reveal behavioral oscillations in temporal perception after the entrainment, we sampled the segregation/integration performance densely in time. In Experiment 1, two groups of human participants (both males and females) received stimulation either at the lower or the upper boundary of the alpha band (∼8.5 vs 11.5 Hz). For both entrainment frequencies, we found a phase alignment of the perceptual oscillation across subjects, but with two different power spectra that peaked near the entrainment frequency. These results were confirmed when perceptual oscillations were characterized in the time domain with sinusoidal fittings. In Experiment 2, we replicated the findings in a within-subject design, extending the results for frequencies in the theta (∼6.5 Hz), but not in the beta (∼15 Hz), range. Overall, these findings show that temporal segregation can be modified by sensory entrainment, providing evidence for a critical role of ongoing oscillations in the temporal organization of perception. SIGNIFICANCE STATEMENT The continuous flow of sensory input is not processed in an analog fashion, but rather is grouped by the perceptual system over time. Recent studies pinpointed the phase and/or frequency of the neural oscillations in the theta/alpha band (∼4–12 Hz) as possible mechanisms underlying temporal windows in perception. Here, we combined two innovative methodologies to provide more direct support for this evidence. We used sensory entrainment to align neural oscillations to different frequencies and then characterized the resultant perceptual oscillation with a temporal dense sampling of the integration/segregation performance. Our results provide the first evidence that the frequency of temporal segregation can be modified by sensory entrainment, supporting a critical role of ongoing oscillations in the integration/segregation of information over time. Society for Neuroscience 2017-11-01 /pmc/articles/PMC5666584/ /pubmed/28972130 http://dx.doi.org/10.1523/JNEUROSCI.1704-17.2017 Text en Copyright © 2017 Ronconi and Melcher https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Ronconi, Luca
Melcher, David
The Role of Oscillatory Phase in Determining the Temporal Organization of Perception: Evidence from Sensory Entrainment
title The Role of Oscillatory Phase in Determining the Temporal Organization of Perception: Evidence from Sensory Entrainment
title_full The Role of Oscillatory Phase in Determining the Temporal Organization of Perception: Evidence from Sensory Entrainment
title_fullStr The Role of Oscillatory Phase in Determining the Temporal Organization of Perception: Evidence from Sensory Entrainment
title_full_unstemmed The Role of Oscillatory Phase in Determining the Temporal Organization of Perception: Evidence from Sensory Entrainment
title_short The Role of Oscillatory Phase in Determining the Temporal Organization of Perception: Evidence from Sensory Entrainment
title_sort role of oscillatory phase in determining the temporal organization of perception: evidence from sensory entrainment
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5666584/
https://www.ncbi.nlm.nih.gov/pubmed/28972130
http://dx.doi.org/10.1523/JNEUROSCI.1704-17.2017
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