Human Beta Oscillations Reflect Magnitude and Fidelity of Priority Shifts in Working Memory

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Abstract

Flexible prioritisation in working memory (WM) is supported by neural oscillations in frontal and sensory brain areas, but the roles of different oscillations remain poorly understood. Recordings in humans suggest an interplay between prefrontal slow frequency (2-8Hz) and posterior alpha-band (10Hz) oscillations regulating top-down control and retrieval of WM representations, respectively. Complementary work, primarily in non-human primates, suggests an additional role for beta (15-30Hz) oscillations in clearing or inhibiting stimuli from entering WM. Here we investigated the role of neural oscillations in prioritising WM content using electroencephalography (EEG) as participants (humans of any sex) performed a task requiring frequent priority switches between two memorized oriented bars. Behavioral performance revealed switch costs, which scaled with the angular distance between the two items, suggesting that priority shifts are modulated by shift magnitude. Time-frequency analyses revealed increased frontal theta (4–8Hz) and decreased central-parietal beta (15–25Hz) power during switches. Crucially, only beta desynchronization scaled with the magnitude of the priority shift and predicted the fidelity of neural decoding of the newly prioritized item during subsequent recall. Theta power, by contrast, was elevated on switch trials but did not vary with update magnitude or decoding strength, suggesting a more general role in signaling control demands. Our findings highlight a particular and previously overlooked role for beta-band desynchronization in the flexible prioritisation of WM content.

Significance statement

Working memory permits flexible switching between mental representations, so we can focus on what is most relevant at the moment. Different brain rhythms in frontal control and sensory memory storage areas orchestrate switches but their respective roles remain unclear. Here, using EEG, we show that desynchronization of ∼20Hz oscillations over central-parietal regions, usually associated with the motor system, closely tracks the magnitude of the required switch and the fidelity of the prioritized memory. In contrast, slower 4-8Hz (theta-band) activity over frontal regions increases during priority switches but tracks neither magnitude nor fidelity. Our findings suggest a unique function for central-parietal beta oscillations in the flexible control of working memory.

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