Attention-related sampling of targets rhythmically alternates with increased susceptibility to co-occurring distractors
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The Rhythmic Theory of Attention proposes that visual spatial attention is characterized by alternating states that promote either sampling at the present focus of attention or a higher likelihood of shifting attentional resources to another location. While theta-rhythmically (4–8 Hz) occurring windows of opportunity for shifting attentional resources might provide cognitive flexibility, these windows might also make us more susceptible to distractors. Here, we used EEG in humans to test how frequency-specific neural activity phasically influences behavioral performance and visual processing when high-contrast distractors co-occur with low-contrast targets. For trials with and without distractors, perceptual sensitivity at the cued target location depended on pre-stimulus theta phase (∼7 Hz) recorded at central electrodes. For trials with distractors, there was a greater increase in false alarm rates at the same theta phase associated with lower hit rates (i.e., during the proposed ‘shifting state’), confirming theta-rhythmically occurring windows of increased susceptibility to distractors. In addition to these phase-behavior effects at central electrodes, we observed phase-behavior effects at frontocentral and occipital electrodes that (i) only occurred on trials with distractors, (ii) peaked in the alpha-frequency range (∼9– 10 Hz) and (iii) were strongest at occipital electrodes that were contralateral to distractors. Alpha phase at these electrodes was also associated with fluctuations in the amplitude of distractor-evoked visual responses, consistent with an alpha-mediated gating of distractors. The present findings thus provide evidence for distinct theta- and alpha-mediated mechanisms of spatial attention that phasically modulate the influence of distractors on task performance.
Significance
The Rhythmic Theory of Attention proposes that spatial attention is characterized by alternating states that promote either sampling at the present focus of attention or a higher likelihood of shifting attentional resources to another location. These alternating attentional states are associated with dynamic changes in attention-related neural and behavioral effects, occurring on a timescale in the theta-frequency range (4–8 Hz). Although interdigitated windows for shifting attentional resources might provide critical cognitive flexibility, they might also lead to an increased susceptibility to distractors. Here, we demonstrate such rhythmic fluctuations in susceptibility to high-contrast distractors that co-occur with low-contrast visual targets. Rhythmic attention-related sampling—while perhaps preventing us from becoming overly focused on any single location—can lead to behavioral disadvantages.