Opposing neural processing modes alternate rhythmically during sustained auditory attention

Kasten, Florian H.; Busson, Quentin; Zoefel, Benedikt · 2024 · Crossref

DOI: 10.1038/s42003-024-06834-x

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Summary

This study investigates the neural mechanisms underlying spontaneous fluctuations in sustained auditory attention, specifically addressing whether "internal" and "external" attentional modes alternate rhythmically. While previous research in non-human primates suggested that attentional lapses occur at regular intervals (~0.06 Hz), it remained unclear if humans exhibit similar rhythmicity during ecologically relevant tasks, such as listening to speech. The authors hypothesized that neural entrainment to speech (indicative of external attention) and spontaneous alpha oscillations (~10 Hz, indicative of sensory suppression or internal attention) would show slow, anti-phase fluctuations. To test this, the researchers recorded electroencephalography (EEG) data from 23 participants who listened to 5-minute streams of rhythmic, monosyllabic French words presented at 3 Hz. Participants were instructed to detect off-rhythm target words, a task requiring continuous attention. The study included both eyes-open and eyes-closed conditions to control for visual system influences on alpha power. The authors used a sliding window approach to quantify the time-varying evolution of auditory entrainment (measured via inter-trial coherence at 3 Hz) and alpha power. They then analyzed the spectral properties of these time series to identify slow fluctuations and assessed the phase coupling between the two neural markers. The results demonstrated that both alpha oscillations and neural entrainment exhibited slow, regular fluctuations with a dominant frequency of approximately 0.07 Hz (~14 seconds). Crucially, these fluctuations were coupled in an anti-phase relationship: periods of high alpha power coincided with reduced neural entrainment, and vice versa. This anti-phasic coupling was significant in fronto-central and parietal channels during the eyes-open condition but disappeared when participants closed their eyes, suggesting the effect is linked to active auditory processing rather than general arousal. Source localization revealed that these opposing modes emerge from interactions between distinct cortical networks: entrainment fluctuations originated in auditory and speech-processing regions (e.g., superior temporal gyrus), while alpha fluctuations arose from regions associated with the dorsal attention and default mode networks (e.g., posterior cingulate cortex, 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. The study concludes that sustained auditory attention is not static but involves rhythmic alternations between external and internal processing modes, conserved across species. These findings imply that attentional lapses are an inherent feature of sustained attention, driven by the competitive interaction between sensory processing networks and top-down attentional control networks. This rhythmicity has significant implications for understanding human error in critical tasks and may inform the design of systems that require sustained vigilance.

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