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Fronto-medial theta coordinates posterior maintenance of working memory content

Oliver Ratcliffe, Kimron Shapiro, Bernhard P. Staresina
doi: https://doi.org/10.1101/2021.03.18.435966
Oliver Ratcliffe
School of Psychology and Centre for Human Brain Health, University of Birmingham, UK
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Kimron Shapiro
School of Psychology and Centre for Human Brain Health, University of Birmingham, UK
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Bernhard P. Staresina
School of Psychology and Centre for Human Brain Health, University of Birmingham, UK
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  • For correspondence: b.staresina@bham.ac.uk
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Abstract

How does the human brain manage multiple bits of information to guide goal-directed behaviour? Successful working memory (WM) functioning has consistently been linked to oscillatory power in the theta frequency band (4-8 Hz) over fronto-medial cortex (fronto-medial theta, FMT). Specifically, FMT is thought to reflect the mechanism of an executive sub-system that coordinates maintenance of memory contents in posterior regions. However, direct evidence for the role of FMT in controlling specific WM content is lacking. Here we collected high-density Electroencephalography (EEG) data whilst participants engaged in load-varying WM tasks and then used multivariate decoding methods to examine WM content during the maintenance period. Higher WM load elicited a focal increase in FMT. Importantly, decoding of WM content was driven by posterior/parietal sites, which in turn showed load-induced functional theta coupling with fronto-medial cortex. Finally, we observed a significant slowing of FMT frequency with increasing WM load, consistent with the hypothesised broadening of a theta ‘duty cycle’ to accommodate additional WM items. Together these findings demonstrate that frontal theta orchestrates posterior maintenance of WM content. Moreover, the observed frequency slowing elucidates the function of FMT oscillations by specifically supporting phase-coding accounts of WM.

Significance Statement How does the brain juggle the maintenance of multiple items in working memory (WM)? Here we show that increased WM demands increase theta power (4-8 Hz) in fronto-medial cortex. Interestingly, using a machine learning approach, we found that the content held in WM could be read out not from frontal, but from posterior areas. These areas were in turn functionally coupled with fronto-medial cortex, consistent with the idea that frontal cortex orchestrates WM representations in posterior regions. Finally, we observed that holding an additional item in WM leads to significant slowing of the frontal theta rhythm, supporting computational models that postulate longer ‘duty cycles’ to accommodate additional WM demands.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 18, 2021.
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Fronto-medial theta coordinates posterior maintenance of working memory content
Oliver Ratcliffe, Kimron Shapiro, Bernhard P. Staresina
bioRxiv 2021.03.18.435966; doi: https://doi.org/10.1101/2021.03.18.435966
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Fronto-medial theta coordinates posterior maintenance of working memory content
Oliver Ratcliffe, Kimron Shapiro, Bernhard P. Staresina
bioRxiv 2021.03.18.435966; doi: https://doi.org/10.1101/2021.03.18.435966

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