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Periodic neglect after frontoparietal lesions provides causal evidence for rhythmic attention sampling

Isabel Raposo, Sara M. Szczepanski, Kathleen Haaland, Tor Endestad, Anne-Kristin Solbakk, Robert T. Knight, Randolph F. Helfrich
doi: https://doi.org/10.1101/2022.11.07.515418
Isabel Raposo
1Hertie Institute for Clinical Brain Research, University Medical Center Tübingen, Tübingen, Germany
2International Max Planck Research School for the Mechanisms of Mental Function and Dysfunction, University of Tübingen, Tübingen, Germany
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Sara M. Szczepanski
3Department of Psychology and the Helen Wills Neuroscience Institute, UC Berkeley, Berkeley, CA, USA
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Kathleen Haaland
4Dept. of Psychiatry and Behavioral Sciences, University of New Mexico Health Sciences, Albuquerque, NM, USA
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Tor Endestad
5Department of Psychology, University of Oslo, Oslo, Norway
6RITMO Centre for Interdisciplinary Studies in Rhythm, Time, and Motion, University of Oslo, Oslo, Norway
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Anne-Kristin Solbakk
5Department of Psychology, University of Oslo, Oslo, Norway
6RITMO Centre for Interdisciplinary Studies in Rhythm, Time, and Motion, University of Oslo, Oslo, Norway
7Department of Neurosurgery, Oslo University Hospital, Oslo, Norway
8Department of Neuropsychology, Helgeland Hospital, Mosjøen, Norway
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Robert T. Knight
3Department of Psychology and the Helen Wills Neuroscience Institute, UC Berkeley, Berkeley, CA, USA
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Randolph F. Helfrich
1Hertie Institute for Clinical Brain Research, University Medical Center Tübingen, Tübingen, Germany
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  • For correspondence: randolph.helfrich@gmail.com
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Summary

Contemporary models conceptualize spatial attention as a blinking spotlight that sequentially samples visual space. Hence, behavior fluctuates over time even in states of presumed ‘sustained’ attention. Recent evidence suggested that rhythmic neural activity in the frontoparietal network constitutes the functional basis of rhythmic attentional sampling. However, causal evidence to support this notion remains absent. Using a lateralized spatial attention task, we addressed this issue in patients with focal lesions in the frontoparietal attention network. Our results uncovered that frontoparietal lesions introduce periodic neglect, i.e., temporally-specific behavioral deficits that were aligned with the underlying neural oscillations. Attention-guided perceptual sensitivity was on par with healthy controls during optimal phases but attenuated during the less excitable sub-cycles. Theta-dependent sampling (3 – 8 Hz) was causally dependent on prefrontal cortex, while alpha-band sampling (8 – 14 Hz) emerged from parietal areas. Collectively, our findings reveal that lesion-induced high amplitude, low frequency brain activity is not epiphenomenal, but has immediate behavioral consequences. More generally, these results provide causal evidence for the hypothesis that the functional architecture of attention is inherently rhythmic.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted November 07, 2022.
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Periodic neglect after frontoparietal lesions provides causal evidence for rhythmic attention sampling
Isabel Raposo, Sara M. Szczepanski, Kathleen Haaland, Tor Endestad, Anne-Kristin Solbakk, Robert T. Knight, Randolph F. Helfrich
bioRxiv 2022.11.07.515418; doi: https://doi.org/10.1101/2022.11.07.515418
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Periodic neglect after frontoparietal lesions provides causal evidence for rhythmic attention sampling
Isabel Raposo, Sara M. Szczepanski, Kathleen Haaland, Tor Endestad, Anne-Kristin Solbakk, Robert T. Knight, Randolph F. Helfrich
bioRxiv 2022.11.07.515418; doi: https://doi.org/10.1101/2022.11.07.515418

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