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.