Theta-Coupled Periodic Replay in Working Memory

Abstract

SummaryWorking memory allows information from transient events to persist as active neural representations [1] that can be used for goal-directed behaviors such as decision making and learning [2, 3]. Computational modeling based on neuronal firing patterns in animals suggests that one putative mechanism enabling working memory is periodic reactivation (henceforth termed “replay”) of the maintained information coordinated by neural oscillations at theta (4–8 Hz) and gamma (30–80 Hz) frequency [4–6]. To investigate this possibility, we trained multivariate pattern classifier decoding algorithms on oscillatory brain responses to images depicting natural scenes, recorded with high temporal resolution via magnetoencephalography. These classifiers were applied to brain activity recorded during the subsequent five second maintenance of the scenes. This decoding revealed replay during the entire maintenance interval. Replay was specific to whether an indoor or an outdoor scene was maintained and whether maintenance centered on configural associations of scene elements or just single scene elements. Replay was coordinated by the phase of theta and the amount of theta coordination was correlated with working memory performance. By confirming the predictions of a mechanistic model and linking these to behavioral performance in humans, these findings identify theta-coupled replay as a mechanism of working memory maintenance.

Hippocampal Theta-Phase Modulation of Replay Correlates with Configural-Relational Short-Term Memory Performance: Figure 1.

“…The data were taken from Fuentemilla et al (2010). Hence, information about participants, stimuli, task, data acquisition, and multivariate pattern classification analysis is as in Fuentemilla et al (2010).…”

“…Hence, information about participants, stimuli, task, data acquisition, and multivariate pattern classification analysis is as in Fuentemilla et al (2010). These aspects of the methods will be briefly summarized here.…”

“…Eight right-handed healthy subjects (six males; mean age, 21 years; SD, 1.3 years) participated in the experiment after giving written informed consent (Fuentemilla et al, 2010). The study was approved by the University College London Research Ethics Committee for humanbased research.…”

“…In agreement with this model, theta/ gamma coupling has been observed in relation to sequential (Axmacher et al, 2010) and spatial (Tort et al, 2009) shortterm memory. Fuentemilla et al (2010) investigated theta-coupled periodic replay during short-term memory maintenance using wholehead magnetoencephalographic (MEG) recordings. They trained a multivariate pattern classification (MVPC) algorithm on highfrequency (beta and gamma frequency range) oscillatory responses during the encoding phase of a visual delay match-tosample (DMS) task.…”

“…In the current study, we explored which brain regions were involved in generating the theta oscillations that coordinated the periodic replay of configural-relational information in the study of Fuentemilla et al (2010). We predicted that a hippocampal theta generator would phase couple to instances of replay in the delay interval of configural-relational maintenance and that interindividual variability in the degree of phase coupling of the hippocampal theta generator would correlate with memory performance.…”