Opposing neural processing modes alternate rhythmically during sustained auditory attention

Abstract

Abstract During continuous tasks, humans show spontaneous fluctuations in performance, putatively caused by varying attentional resources allocated to process external information. If neural resources are used to process other, presumably “internal” information, sensory input can be missed and explain an apparent dichotomy of “internal” versus “external” attention. In the current study, we extract presumed neural signatures of these attentional modes in human electroencephalography (EEG): neural entrainment and α-oscillations (~10-Hz), linked to the processing and suppression of sensory information, respectively. We test whether they exhibit structured fluctuations over time, while listeners attend to an ecologically relevant stimulus, like speech, and complete a task that requires full and continuous attention. Results show an antagonistic relation between neural entrainment to speech and spontaneous α-oscillations in two distinct brain networks—one specialized in the processing of external information, the other reminiscent of the dorsal attention network. These opposing neural modes undergo slow, periodic fluctuations around ~0.07 Hz and are related to the detection of auditory targets. Our study might have tapped into a general attentional mechanism that is conserved across species and has important implications for situations in which sustained attention to sensory information is critical.