Coordinated memory trace reactivation across distributed neural ensembles in the primate neocortex

Abstract

The process of forming a long-lasting memory may involve the selective linking together of neural representations stored widely throughout neocortex. The successful binding together of these disparate representations may require their coordinated reactivation while the cortex is 'offline' i.e., not engaged in processing external stimuli. This hypothesis was tested through simultaneous extracellular recording of 28-99 cells over four sites in the macaque neocortex. The recordings were conducted as the monkey performed repetitive reaching tasks, and in rest periods immediately preceding and following the task. In motor, somatosensory and parietal cortex (but not prefrontal cortex), the task-related neural activity patterns within and across regions were similar to the activity patterns seen afterwards, during the rest epoch. Moreover, the temporal sequences of neural ensemble activity that occurred during task performance were preserved in subsequent rest. The preservation of correlation structure and temporal sequencing are consistent with the reactivation of a memory trace and not merely the persistence of a fixed activity pattern. The observed memory trace reactivation was coordinated over large expanses of neocortex, confirming a fundamental tenet of the trace replay theory of memory consolidation.