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

Rhythmic sampling of multiple decision alternatives in the human brain

“…Our approach differs from previous psychophysical and neurophysiological studies of rhythmic perception (or attention) by directly estimating the dynamics of the focus (i.e., strength and direction) of covert attention from neural data. Previous studies have either quantified temporal fluctuations of behavioral performance 18,24,26–28,65 and/or of cortical population activity 15,17,18,20,23,24,27,30,31,65 , without assessing the information content of the latter. By contrast, we here constructed content-specific decoders from patterns of cortical population activity (trained on independent localizer data) that enabled us to directly track the attentional focus, as it was expressed in selective patterns of cortical dynamics unfolding during the main decision-making task.…”

“…Recent literature has quantified temporal fluctuations in behavioral performance 14,26,28,29,46 and/or in cortical population activity [12][13][14][15]26,27,29,36,47 , without explicating the information content of the latter. By contrast, we here constructed content-specific decoders from patterns of cortical population activity (trained on independent localizer data).…”

“…In particular, it is expected that when attention is stronger, the tendency to maintain attention on one alternative is also strong (locus stability). When attention is weaker, the tendency to switch to a different alternative increases (locus instability) 17,28,29 , with attentional switches occurring swiftly analogously to covert 'attentional saccades' 16,30,31 .…”

Concurrent attention to hetero‐depth surfaces in 3‐D visual space is governed by theta rhythm

“…Attention, a fundamental determinant of visual perception, leads to enhanced neural activities and improved behavioral performance corresponding to the target information. Intriguingly, when the visual system is confronted with more than one attentional target, it employs a time‐multiplexing approach in which attentional resources are dynamically and periodically navigated between each target over time, a mechanism broadly known as rhythmic attentional sampling (Buschman & Kastner, 2015; Fiebelkorn & Kastner, 2019; Raposo et al., 2023; VanRullen, 2016). For the past decade, rhythmic attentional sampling has received mounting support from converging behavioral and neural findings.…”