Sara M. Szczepanski

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

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.

Authors:

  • Isabel Raposo

  • Sara M. Szczepanski

  • Kathleen Haaland

  • Tor Endestad

  • Anne-Kristin Solbakk

  • Robert T. Knight

  • Randolph F. Helfrich

Date: 2023

DOI: https://doi.org/10.1016/j.cub.2023.09.065

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Neural mechanisms of sustained attention are rhythmic

ABSTRACT

Classic models of attention suggest that sustained neural firing constitutes a neural correlate of sustained attention. However, recent evidence indicates that behavioral performance fluctuates over time, exhibiting temporal dynamics that closely resemble the spectral features of ongoing, oscillatory brain activity. Therefore, it has been proposed that periodic neuronal excitability fluctuations might shape attentional allocation and overt behavior. However, empirical evidence to support this notion is sparse. Here, we address this issue by examining data from large-scale subdural recordings, using two different attention tasks that track perceptual ability at high temporal resolution. Our results reveal that perceptual outcome varies as a function of the theta phase even in states of sustained spatial attention. These effects were robust at the single-subject level, suggesting that rhythmic perceptual sampling is an inherent property of the frontoparietal attention network. Collectively, these findings support the notion that the functional architecture of top-down attention is intrinsically rhythmic.





AUTHORS

  • Randolph F. Helfrich

  • Ian C. Fiebelkorn

  • Sara M. Szczepanski

  • Jack J. Lin

  • Josef Parvizi

  • Robert T. Knight

  • Sabine Kastner

Date: 2018

DOI: 10.1016/j.neuron.2018.07.032

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