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Enhanced anticipatory biasing of visuospatial attention in deaf native-signing adults indexed by alpha-band (8-14 Hz) oscillatory neural activity

Ian A. DeAndrea-Lazarus, View ORCID ProfileEdward G. Freedman, Jiayi Xu, View ORCID ProfileKevin D. Prinsloo, Maeve M. Sargeant, View ORCID ProfileJohn J. Foxe
doi: https://doi.org/10.1101/2022.01.25.477746
Ian A. DeAndrea-Lazarus
1The Frederick J. and Marion A. Schindler Cognitive Neurophysiology Laboratory, The Del Monte Institute for Neuroscience
2Department of Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester, New York 14642, USA
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Edward G. Freedman
1The Frederick J. and Marion A. Schindler Cognitive Neurophysiology Laboratory, The Del Monte Institute for Neuroscience
2Department of Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester, New York 14642, USA
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  • ORCID record for Edward G. Freedman
Jiayi Xu
1The Frederick J. and Marion A. Schindler Cognitive Neurophysiology Laboratory, The Del Monte Institute for Neuroscience
2Department of Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester, New York 14642, USA
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Kevin D. Prinsloo
1The Frederick J. and Marion A. Schindler Cognitive Neurophysiology Laboratory, The Del Monte Institute for Neuroscience
2Department of Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester, New York 14642, USA
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Maeve M. Sargeant
1The Frederick J. and Marion A. Schindler Cognitive Neurophysiology Laboratory, The Del Monte Institute for Neuroscience
2Department of Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester, New York 14642, USA
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John J. Foxe
1The Frederick J. and Marion A. Schindler Cognitive Neurophysiology Laboratory, The Del Monte Institute for Neuroscience
2Department of Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester, New York 14642, USA
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  • ORCID record for John J. Foxe
  • For correspondence: john_foxe@urmc.rochester.edu
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Abstract

Deaf people show increased visuospatial attention abilities, especially towards peripheral inputs, but the neural mechanisms of these heightened abilities are not yet understood. In hearing individuals, topographically-specific alpha-band oscillatory activity (8-14 Hz) over parieto-occipital regions has been associated with active suppression of irrelevant locations. Here, we asked whether increases in this spatially-specific anticipatory oscillatory mechanism might underpin enhanced visuospatial attention abilities in deaf individuals, on the premise that deaf people might be more adept at transiently engaging and disengaging attentional processes involved in processing peripheral inputs. An alternative hypothesis was that deaf individuals might not produce lateralized alpha-band activity, because of the need to continuously monitor the periphery due to the absence of an auxiliary auditory spatial alerting system. High-density electroencephalography was recorded from 20 deaf native signers and 20 hearing non-signers performing a cued covert visuospatial attention task. Deaf participants responded significantly more rapidly and accurately and showed highly typical alpha-band lateralization during the cue-target interval of the task. Topographic analysis showed a greater extent of alpha-band anticipatory activity over right parietal scalp, suggesting sequestration of extra-visual attentional circuits (i.e., unused auditory regions), and post-hoc analysis pointed to substantially earlier onset of this activity during the cue-target interval. The presence of cue-evoked anticipatory alpha lateralization in deaf participants suggests that they are rapidly engaging and disengaging attentional processes involved in orienting attention to the periphery. The earlier and more extensive engagement of these anticipatory oscillatory processes may contribute to the improved visuospatial performance observed in these individuals.

Significance Statement Prior to this study, it was not known whether deaf people demonstrate lateralization of alpha-band oscillatory electroencephalographic (EEG) activity over the posterior region of the brain, which plays a role in the suppression of uncued regions of space during cued visuospatial attention tasks. We found that this lateralized pattern was observable in deaf participants and was not significantly different from that seen in hearing participants, except that alpha activity onsets earlier in deaf participants. However, when cue directions were collapsed, the scalp topographies of deaf participants showed a greater distribution of alpha activity, suggesting that they recruited a brain region typically reserved for audiospatial attentional control during the visuospatial attention task. Additionally, deaf participants responded significantly more quickly and accurately compared to hearing participants, demonstrating increased visuospatial attention abilities.

Competing Interest Statement

The authors have declared no competing interest.

  • Abbreviations List

    PPC
    Posterior Parietal Cortex
    ASL
    American Sign Language
    RT
    reaction time
    EEG
    electroencephalography
    TSE
    temporal spectral evolution
    CTI
    cue-target interval
    ROI
    region of interest
    DISS
    global dissimilarity
    GFP
    global field power
    GCE
    gaze-cueing effect
    ANOVA
    analysis of variance
    TANOVA
    topographical analysis of variance
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    Enhanced anticipatory biasing of visuospatial attention in deaf native-signing adults indexed by alpha-band (8-14 Hz) oscillatory neural activity
    Ian A. DeAndrea-Lazarus, Edward G. Freedman, Jiayi Xu, Kevin D. Prinsloo, Maeve M. Sargeant, John J. Foxe
    bioRxiv 2022.01.25.477746; doi: https://doi.org/10.1101/2022.01.25.477746
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    Enhanced anticipatory biasing of visuospatial attention in deaf native-signing adults indexed by alpha-band (8-14 Hz) oscillatory neural activity
    Ian A. DeAndrea-Lazarus, Edward G. Freedman, Jiayi Xu, Kevin D. Prinsloo, Maeve M. Sargeant, John J. Foxe
    bioRxiv 2022.01.25.477746; doi: https://doi.org/10.1101/2022.01.25.477746

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