Periodic attention deficits after frontoparietal lesions provide causal evidence for rhythmic attentional sampling

Isabel Raposo; Sara M Szczepanski; Kathleen Haaland; Tor Endestad; Anne-Kristin Solbakk; Robert T Knight; Randolph F Helfrich

doi:10.1016/j.cub.2023.09.065

Periodic attention deficits after frontoparietal lesions provide causal evidence for rhythmic attentional sampling

Curr Biol. 2023 Nov 20;33(22):4893-4904.e3. doi: 10.1016/j.cub.2023.09.065. Epub 2023 Oct 17.

Authors

Isabel Raposo¹, Sara M Szczepanski², Kathleen Haaland³, Tor Endestad⁴, Anne-Kristin Solbakk⁵, Robert T Knight², Randolph F Helfrich⁶

Affiliations

¹ Hertie Institute for Clinical Brain Research, University Medical Center Tübingen, 72076 Tübingen, Germany; International Max Planck Research School for the Mechanisms of Mental Function and Dysfunction, University of Tübingen, Tübingen, Germany.
² Department of Psychology and the Helen Wills Neuroscience Institute, UC Berkeley, Berkeley, CA 94720, USA.
³ Department of Psychiatry and Behavioral Sciences, University of New Mexico Health Sciences, Albuquerque, NM 87102, USA.
⁴ Department of Psychology, University of Oslo, 0373 Oslo, Norway; RITMO Centre for Interdisciplinary Studies in Rhythm, Time, and Motion, University of Oslo, 0371 Oslo, Norway.
⁵ Department of Psychology, University of Oslo, 0373 Oslo, Norway; RITMO Centre for Interdisciplinary Studies in Rhythm, Time, and Motion, University of Oslo, 0371 Oslo, Norway; Department of Neurosurgery, Oslo University Hospital, 0372 Oslo, Norway; Department of Neuropsychology, Helgeland Hospital, 8656 Mosjøen, Norway.
⁶ Hertie Institute for Clinical Brain Research, University Medical Center Tübingen, 72076 Tübingen, Germany. Electronic address: randolph.helfrich@gmail.com.

PMID: 37852264
PMCID: PMC10842514 (available on 2024-11-20)
DOI: 10.1016/j.cub.2023.09.065

Abstract

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 has 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 revealed that frontoparietal lesions introduce periodic attention deficits, i.e., temporally specific behavioral deficits that are aligned with the underlying neural oscillations. Attention-guided perceptual sensitivity was on par with that of healthy controls during optimal phases but was attenuated during the less excitable sub-cycles. Theta-dependent sampling (3-8 Hz) was causally dependent on the prefrontal cortex, while high-alpha/low-beta 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.

Keywords: EEG; electroencephalography; frontoparietal network; rhythmic sampling; spatial attention; stroke.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Electroencephalography
Humans
Periodicity*
Photic Stimulation / methods
Visual Perception*

Abstract

Publication types

MeSH terms

Grants and funding