Theta coupled replay in working memory

Working memory allows information from transient events to persist in the brain as active representations. This enables goal-directed behaviours such as decision making and learning to utilize information even beyond its transient sensory availability. Computational modelling based on neuronal firing patterns in animals suggests that one putative neural mechanism enabling working memory is periodic reactivation (henceforth termed “replay”) of the maintained information and that the periodicity of replay is coordinated by neural oscillations at theta (4-8 Hz) and gamma (30-80 Hz) frequency. This possibility has remained largely theoretical because its investigation requires decoding replayed neural activity at high temporal resolution. We trained multivariate pattern classifier (MVPC) decoding algorithms on the oscillatory brain response to the visual presentation of images depicting natural scenes, recorded with high temporal resolution using magneto-encephalography (MEG). These classifiers were applied to brain activity associated with subsequent maintenance of the scenes over an interval of five seconds. We detected replay during the entire maintenance interval. Replay was specific to whether the maintained image depicted an indoor or an outdoor scene and whether maintenance centred on configural associations of scene elements or just single scene elements. The periodicity of replay events was coordinated by the phase of theta oscillations and the amount of theta- coordination was correlated with the accuracy of working memory performance. By confirming the predictions of a mechanistic model and linking these to behavioural performance in humans, these findings identify theta coupled replay as a mechanism of working memory maintenance