TY - JOUR
T1 - The role of oscillatory phase in determining the temporal organization of perception
T2 - Evidence from sensory entrainment
AU - Ronconi, Luca
AU - Melcher, David
N1 - Funding Information:
Received June 19, 2017; revised Aug. 17, 2017; accepted Aug. 21, 2017. Authorcontributions:L.R.andD.M.designedresearch;L.R.performedresearch;L.R.analyzeddata;L.R.andD.M. wrote the paper. The work was supported by the European Research Council (“Construction of Perceptual Space-Time” StG Agreement 313658). The authors declare no competing financial interests. CorrespondenceshouldbeaddressedtoLucaRonconi,Ph.D.,CenterforMind/BrainSciences(CIMeC),University of Trento, Corso Bettini 31, 38068 Rovereto (TN), Italy. E-mail: luca.ronconi@unitn.it. DOI:10.1523/JNEUROSCI.1704-17.2017 Copyright © 2017 Ronconi and Melcher This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in anymediumprovidedthattheoriginalworkisproperlyattributed.
Publisher Copyright:
© 2017 the authors.
PY - 2017/11/1
Y1 - 2017/11/1
N2 - 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.
AB - 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.
KW - Behavioral oscillations
KW - Oscillations
KW - Temporal perception
KW - Time perception
KW - Visual perception
KW - Visual Perception/physiology
KW - Auditory Perception/physiology
KW - Electroencephalography/methods
KW - Humans
KW - Time Perception/physiology
KW - Periodicity
KW - Acoustic Stimulation/methods
KW - Male
KW - Random Allocation
KW - Young Adult
KW - Visual Cortex/physiology
KW - Photic Stimulation/methods
KW - Adult
KW - Female
KW - Alpha Rhythm/physiology
UR - http://www.scopus.com/inward/record.url?scp=85032929862&partnerID=8YFLogxK
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U2 - 10.1523/JNEUROSCI.1704-17.2017
DO - 10.1523/JNEUROSCI.1704-17.2017
M3 - Article
C2 - 28972130
AN - SCOPUS:85032929862
SN - 0270-6474
VL - 37
SP - 10636
EP - 10644
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 44
ER -