Interplay between persistent activity and activity-silent dynamics in the prefrontal cortex underlies serial biases in working memory.

Abstract

Persistent neuronal spiking has long been considered the mechanism underlying working memory, but recent proposals argue for alternative, “activity-silent” substrates. Using monkey and human electrophysiology, we show here that attractor dynamics that control neural spiking during mnemonic periods interact with activity-silent mechanisms in PFC. This interaction allows memory reactivations, which enhance serial biases in spatial working memory. Stimulus information was not decodable between trials, but remained present in activity-silent traces inferred from spiking synchrony in PFC. Just prior to the new stimulus, this latent trace was reignited into activity that recapitulated the previous stimulus representation. Importantly, the reactivation strength correlated with the strength of serial biases in both monkeys and humans, as predicted by a computational model integrating activity-based and activity-silent mechanisms. Finally, single-pulse TMS applied to the human prefrontal cortex between successive trials enhanced serial biases, demonstrating the causal role of prefrontal reactivations in determining working memory behavior.