Gamma and beta bursts during working memory readout suggest roles in its volitional control

Mikael Lundqvist,Scott L Brincat,Pawel Herman,Melissa R Warden,Earl K Miller

doi:10.1038/s41467-017-02791-8

Mikael Lundqvist, Scott L Brincat + Show 3 more

Open Access

https://doi.org/10.1038/s41467-017-02791-8

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Abstract

Working memory (WM) activity is not as stationary or sustained as previously thought. There are brief bursts of gamma (~50–120 Hz) and beta (~20–35 Hz) oscillations, the former linked to stimulus information in spiking. We examined these dynamics in relation to readout and control mechanisms of WM. Monkeys held sequences of two objects in WM to match to subsequent sequences. Changes in beta and gamma bursting suggested their distinct roles. In anticipation of having to use an object for the match decision, there was an increase in gamma and spiking information about that object and reduced beta bursting. This readout signal was only seen before relevant test objects, and was related to premotor activity. When the objects were no longer needed, beta increased and gamma decreased together with object spiking information. Deviations from these dynamics predicted behavioral errors. Thus, beta could regulate gamma and the information in WM.

Highlights

Working memory (WM) activity is not as stationary or sustained as previously thought
As in prior work[6], we found that local field potentials (LFPs), (n = 188 electrodes with at least one spiking neuron) recorded in prefrontal cortex (PFC; Supplementary Fig. 1) showed bursts of gamma and beta oscillations (Fig. 2)
We found that information on a single-neuron level was positively correlated with gamma bursting across time (r = 0.23 in both delays, p < 0.00001, t-test, including neurons with significant delay information, n = 146) and uncorrelated with beta bursting (r = −0.07 in first delay, p = 0.06, r = 0.01 in second delay, p = 0.73, n = 146) during delays

Summary

Introduction

Working memory (WM) activity is not as stationary or sustained as previously thought. The use of a test sequence revealed that these readout dynamics only occurred when test objects were behaviorally relevant, suggesting volitional control Consistent with this view, gamma and beta showed different dynamics for different types of match/nonmatch decisions (identity, order) and did so in a way that predicted different types of errors the animals could make. This lends support for the hypothesis that discrete oscillatory dynamics underlie maintenance, readout, and control of working memory

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