Opposing neural processing modes alternate rhythmically during sustained auditory attention

Kasten, Florian H.; Busson, Quentin; Zoefel, Benedikt · 2023 · Crossref

DOI: 10.1101/2023.10.04.560684

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Summary

This study investigates the neural mechanisms underlying spontaneous fluctuations in sustained auditory attention, specifically addressing the dichotomy between "external" attention to sensory input and "internal" attention. While previous research in non-human primates suggested that attentional states alternate rhythmically, it remained unclear whether humans exhibit similar rhythmic neural signatures during ecologically relevant tasks like speech perception. The authors hypothesized that neural entrainment to speech (reflecting external processing) and spontaneous alpha oscillations (~10 Hz, reflecting sensory suppression) would show slow, anti-phase fluctuations during sustained attention. To test this, the researchers recorded electroencephalography (EEG) data from participants listening to continuous 5-minute streams of rhythmic, monosyllabic French words presented at 3 Hz. Participants were instructed to detect words presented off-rhythm, a task requiring continuous attention. The study compared conditions with eyes open versus eyes closed. Using a sliding window approach, the authors extracted time-series data for inter-trial coherence (ITC) at 3 Hz to quantify auditory entrainment and alpha-band power to quantify alpha oscillations. They then performed spectral analysis on these time-series to identify slow fluctuations and assessed the phase coupling between the two neural markers. The results revealed that both neural entrainment and alpha oscillations exhibited slow, regular fluctuations with a dominant frequency of approximately 0.07 Hz (~14 seconds), consistent with findings in macaques. Crucially, these fluctuations were coupled in an anti-phase relationship: periods of high entrainment coincided with low alpha power, and vice versa. This antagonistic coupling was significant in fronto-central channels during the eyes-open condition but disappeared when participants closed their eyes. Source localization identified distinct cortical networks driving these modes: entrainment fluctuations originated in speech-processing regions (e.g., superior temporal gyrus, inferior frontal gyrus), while alpha fluctuations emerged from regions associated with the dorsal attention and default mode networks (e.g., posterior cingulate, superior parietal lobe). Furthermore, the phase of these fluctuations predicted behavioral performance; targets were more likely to be detected during phases of high entrainment and low alpha power. Control analyses ruled out that these rhythms were artifacts of stimulus timing. The study concludes that sustained auditory attention is not static but involves rhythmic alternations between opposing neural processing modes. These modes, governed by distinct cortical networks, fluctuate at an ultra-slow frequency of ~0.07 Hz. The findings suggest a conserved mechanism across species where attentional resources are rhythmically allocated between external sensory processing and internal states. This has significant implications for understanding attentional lapses and designing systems or interventions that account for the temporal dynamics of human attention.

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