Strong long-range temporal correlations of beta/gamma oscillations are associated with poor sustained visual attention performance

Neuronal oscillations exhibit complex amplitude fluctuations with autocorrelations that persist over thousands of oscillatory cycles. Such long-range temporal correlations (LRTC) are thought to reflect neuronal systems poised near a critical state, which would render them capable of quick reorganization and responsive to changing processing demands. When we concentrate, however, the influence of internal and external sources of distraction is better reduced, suggesting that neuronal systems involved with sustained attention could benefit from a shift toward the less volatile sub-critical state. To test these ideas, we recorded electroencephalography (EEG) from healthy volunteers during eyes-closed rest and during a sustained attention task requiring a speeded response to images deviating in their presentation duration. We show that for oscillations recorded during rest, high levels of alpha-band LRTC in the sensorimotor region predicted good reaction-time performance in the attention task. During task execution, however, fast reaction times were associated with high-amplitude beta and gamma oscillations with low LRTC. Finally, we show that reduced LRTC during the attention task compared to the rest condition correlates with better performance, while increased LRTC of oscillations from rest to attention is associated with reduced performance. To our knowledge, this is the first empirical evidence that ‘resting-state criticality’ of neuronal networks predicts swift behavioral responses in a sensorimotor task, and that steady attentive processing of visual stimuli requires brain dynamics with suppressed temporal complexity.