Opposing neural processing modes alternate rhythmically during sustained auditory attention

Abstract

AbstractWhen confronted with 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.Each of these opposing attentional modes might have their own distinct neural signature. For instance, α-oscillations (∼10-Hz) have been linked to a suppression of sensory information and might therefore reflect a state of internal attention. In the current study, we extracted neural signatures of internal and external attention in human electroencephalography (EEG) - α-oscillations and neural entrainment, respectively. We then tested whether they exhibit structured fluctuations over time, when listeners attended to an ecologically relevant stimulus like speech and completed a task that required full and continuous attention.Results showed an antagonistic relation between neural activity synchronized to speech and spontaneous α-oscillations in two distinct brain networks – one specialized in the processing of external information (i.e., entrainment to speech), the other entailing fronto-parietal brain regions reminiscent of the dorsal attention network. These opposing neural modes underwent slow, periodic fluctuations around ∼0.07 Hz that were strikingly similar to previous observations in in non-human primates and related to the successful 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.Graphical Abstract