Remembering to Forget: A Dual Role for Sleep Oscillations in Memory Consolidation and Forgetting.

Abstract

It has been known since the time of patient H. M. and Karl Lashley’s equipotentiality studies that the hippocampus and cortex serve mnestic functions. Current memory models maintain that these two brain structures accomplish unique, but interactive, memory functions. Specifically, most modeling suggests that memories are rapidly acquired during waking experience by the hippocampus, before being later consolidated into the cortex for long-term storage. Sleep has been shown to be critical for the transfer and consolidation of memories in the cortex. Like memory consolidation, a role for sleep in adaptive forgetting has both historical precedent, as Francis Crick suggested in 1983 that sleep was for “reverse-learning,” and recent empirical support. In this article I review the evidence indicating that the same brain activity involved in sleep replay associated memory consolidation is responsible for sleep-dependent forgetting. In reviewing the literature, it became clear that both a cellular mechanism for systems consolidation and an agreed upon general, as well as cellular, mechanism for sleep-dependent forgetting is seldom discussed or is lacking. I advocate here for a candidate cellular systems consolidation mechanism wherein changes in calcium kinetics and the activation of consolidative signaling cascades arise from the triple phase locking of non-rapid eye movement sleep (NREMS) slow oscillation, sleep spindle and sharp-wave ripple rhythms. I go on to speculatively consider several sleep stage specific forgetting mechanisms and conclude by discussing a notional function of NREM-rapid eye movement sleep (REMS) cycling. The discussed model argues that the cyclical organization of sleep functions to first lay down and edit and then stabilize and integrate engrams. All things considered, it is increasingly clear that hallmark sleep stage rhythms, including several NREMS oscillations and the REMS hippocampal theta rhythm, serve the dual function of enabling simultaneous memory consolidation and adaptive forgetting. Specifically, the same sleep rhythms that consolidate new memories, in the cortex and hippocampus, simultaneously organize the adaptive forgetting of older memories in these brain regions.