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Fast and Slow Rhythms of Naturalistic Reading Revealed by Combined Eye-Tracking and Electroencephalography

Neural oscillations are thought to support speech and language processing. They may not only inherit acoustic rhythms, but might also impose endogenous rhythms onto processing. In support of this, we here report that human (both male and female) eye movements during naturalistic reading exhibit rhyt...

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Autores principales: Henke, Lena, Lewis, Ashley G., Meyer, Lars
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10278671/
https://www.ncbi.nlm.nih.gov/pubmed/37208175
http://dx.doi.org/10.1523/JNEUROSCI.1849-22.2023
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author Henke, Lena
Lewis, Ashley G.
Meyer, Lars
author_facet Henke, Lena
Lewis, Ashley G.
Meyer, Lars
author_sort Henke, Lena
collection PubMed
description Neural oscillations are thought to support speech and language processing. They may not only inherit acoustic rhythms, but might also impose endogenous rhythms onto processing. In support of this, we here report that human (both male and female) eye movements during naturalistic reading exhibit rhythmic patterns that show frequency-selective coherence with the EEG, in the absence of any stimulation rhythm. Periodicity was observed in two distinct frequency bands: First, word-locked saccades at 4-5 Hz display coherence with whole-head theta-band activity. Second, fixation durations fluctuate rhythmically at ∼1 Hz, in coherence with occipital delta-band activity. This latter effect was additionally phase-locked to sentence endings, suggesting a relationship with the formation of multi-word chunks. Together, eye movements during reading contain rhythmic patterns that occur in synchrony with oscillatory brain activity. This suggests that linguistic processing imposes preferred processing time scales onto reading, largely independent of actual physical rhythms in the stimulus. SIGNIFICANCE STATEMENT The sampling, grouping, and transmission of information are supported by rhythmic brain activity, so-called neural oscillations. In addition to sampling external stimuli, such rhythms may also be endogenous, affecting processing from the inside out. In particular, endogenous rhythms may impose their pace onto language processing. Studying this is challenging because speech contains physical rhythms that mask endogenous activity. To overcome this challenge, we turned to naturalistic reading, where text does not require the reader to sample in a specific rhythm. We observed rhythmic patterns of eye movements that are synchronized to brain activity as recorded with EEG. This rhythmicity is not imposed by the external stimulus, which indicates that rhythmic brain activity may serve as a pacemaker for language processing.
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spelling pubmed-102786712023-06-20 Fast and Slow Rhythms of Naturalistic Reading Revealed by Combined Eye-Tracking and Electroencephalography Henke, Lena Lewis, Ashley G. Meyer, Lars J Neurosci Research Articles Neural oscillations are thought to support speech and language processing. They may not only inherit acoustic rhythms, but might also impose endogenous rhythms onto processing. In support of this, we here report that human (both male and female) eye movements during naturalistic reading exhibit rhythmic patterns that show frequency-selective coherence with the EEG, in the absence of any stimulation rhythm. Periodicity was observed in two distinct frequency bands: First, word-locked saccades at 4-5 Hz display coherence with whole-head theta-band activity. Second, fixation durations fluctuate rhythmically at ∼1 Hz, in coherence with occipital delta-band activity. This latter effect was additionally phase-locked to sentence endings, suggesting a relationship with the formation of multi-word chunks. Together, eye movements during reading contain rhythmic patterns that occur in synchrony with oscillatory brain activity. This suggests that linguistic processing imposes preferred processing time scales onto reading, largely independent of actual physical rhythms in the stimulus. SIGNIFICANCE STATEMENT The sampling, grouping, and transmission of information are supported by rhythmic brain activity, so-called neural oscillations. In addition to sampling external stimuli, such rhythms may also be endogenous, affecting processing from the inside out. In particular, endogenous rhythms may impose their pace onto language processing. Studying this is challenging because speech contains physical rhythms that mask endogenous activity. To overcome this challenge, we turned to naturalistic reading, where text does not require the reader to sample in a specific rhythm. We observed rhythmic patterns of eye movements that are synchronized to brain activity as recorded with EEG. This rhythmicity is not imposed by the external stimulus, which indicates that rhythmic brain activity may serve as a pacemaker for language processing. Society for Neuroscience 2023-06-14 /pmc/articles/PMC10278671/ /pubmed/37208175 http://dx.doi.org/10.1523/JNEUROSCI.1849-22.2023 Text en Copyright © 2023 Henke et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (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
Henke, Lena
Lewis, Ashley G.
Meyer, Lars
Fast and Slow Rhythms of Naturalistic Reading Revealed by Combined Eye-Tracking and Electroencephalography
title Fast and Slow Rhythms of Naturalistic Reading Revealed by Combined Eye-Tracking and Electroencephalography
title_full Fast and Slow Rhythms of Naturalistic Reading Revealed by Combined Eye-Tracking and Electroencephalography
title_fullStr Fast and Slow Rhythms of Naturalistic Reading Revealed by Combined Eye-Tracking and Electroencephalography
title_full_unstemmed Fast and Slow Rhythms of Naturalistic Reading Revealed by Combined Eye-Tracking and Electroencephalography
title_short Fast and Slow Rhythms of Naturalistic Reading Revealed by Combined Eye-Tracking and Electroencephalography
title_sort fast and slow rhythms of naturalistic reading revealed by combined eye-tracking and electroencephalography
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10278671/
https://www.ncbi.nlm.nih.gov/pubmed/37208175
http://dx.doi.org/10.1523/JNEUROSCI.1849-22.2023
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