Neural Mechanisms of Sustained Attention Are Rhythmic

• Published in: Neuron (Cambridge, Mass.) Vol. 99; no. 4; pp. 854 - 865.e5
• Main Authors: Helfrich, Randolph F., Fiebelkorn, Ian C., Szczepanski, Sara M., Lin, Jack J., Parvizi, Josef, Knight, Robert T., Kastner, Sabine
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 22.08.2018; Elsevier Limited
• Subjects: Accuracy; Adult; Attention; Attention - physiology; Behavior; Brain - physiology; discrete perception; electrocorticography; Electrodes, Implanted; Electroencephalography; Electroencephalography - instrumentation; Electroencephalography - methods; Excitability; Experiments; Female; frontoparietal attention network; functional network parcellation; high-frequency activity; Humans; intracranial EEG; Male; Middle Aged; perceptual cycles; Periodicity; phase-dependent behavior; Photic Stimulation - methods; Psychomotor Performance - physiology; Random Allocation; Reaction Time - physiology; Rhythm; rhythmic attention; Software; theta oscillations; Visual Perception - physiology; electrocorticography; rhythmic attention; high-frequency activity; phase-dependent behavior; frontoparietal attention network; functional network parcellation; discrete perception; theta oscillations; perceptual cycles; intracranial EEG
• ISSN: 0896-6273; 1097-4199; 1097-4199
• DOI: 10.1016/j.neuron.2018.07.032

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. •The functional architecture of attention is rhythmic•Frontoparietal theta activity predicts behavior on a rapid timescale•Theta activity controls cortical excitability and information flow•Rhythmic sampling is independent of task structure and context Helfrich et al. demonstrate that the neural basis of sustained attention is rhythmic. Using human intracranial recordings, they show that attentional allocation and overt behavior are modulated by a ∼4 Hz theta rhythm that predicts endogenous excitability fluctuations.