Balanced cortical microcircuitry for maintaining information in working memory

Abstract

Persistent neural activity in the absence of a stimulus has been identified as a neural correlate of working memory, but how such activity is maintained by neocortical circuits remains unknown. Here we show that the inhibitory and excitatory microcircuitry of neocortical memory-storing regions is sufficient to implement a corrective feedback mechanism that enables persistent activity to be maintained stably for prolonged durations. When recurrent excitatory and inhibitory inputs to memory neurons are balanced in strength, but offset in time, drifts in activity trigger a corrective signal that counteracts memory decay. Circuits containing this mechanism temporally integrate their inputs, generate the irregular neural firing observed during persistent activity, and are robust against common perturbations that severely disrupt previous models of short-term memory storage. This work reveals a mechanism for the accumulation and storage of memories in neocortical circuits based upon principles of corrective negative feedback widely used in engineering applications.