Sleep-dependent memory consolidation and reconsolidation
Introduction
The question of “sleep-dependent memory consolidation” is a complex one. Each term in the phrase – sleep, dependent, memory, and consolidation – begs for clarification. For a start, the term “memory” covers a wide range of memory types, which differ in the kinds of information stored, the brain structures mediating this storage, and, in humans, whether the information is accessible to conscious awareness. There is no clear consensus at this time on how many such memory systems there are, and how they should be defined, either in terms of information content or brain structures involved in their storage [1]. The most widely accepted taxonomy divides human memories first into declarative and non-declarative, based on their accessibility to conscious recall, and then into finer and finer subdivisions of these basic categories (Fig. 1A) [2].
Similarly, the term “memory consolidation” refers to a poorly defined set of processes which take an initial, unstable memory representation and convert it into a form that is both more stable and more effective. At this time, it is unclear how memories are altered after initial encoding, and no consensus as to which of the processes contributing to this alteration should be included under the umbrella of memory consolidation. When the term was first introduced, it referred to as yet unknown processes which, over a period of minutes to hours, made learning resistant to degradation by, for example, electroconvulsive shock [3], [4], [5], but this notion of a single, relatively rapid process of memory consolidation has yielded to one including phases of stabilization, enhancement, and integration, extending over hours to years.
More recently, the concept “memory reconsolidation” has resurfaced to describe yet another aspect of post-encoding memory modification [6]. There is now evidence that when previously stabilized memories are reactivated, either by returning an animal to an earlier learning environment or by having humans briefly perform a previously learned task, the memory is destabilized and returns to a labile state in which it is again susceptible to destructive interference. Thus, the terms “consolidated” and “stabilized” must take on a more nuanced meaning, reflecting the relative consolidation and stabilization of the memory.
Many of the steps in this consolidation cascade occur preferentially or even exclusively during periods of sleep. Researchers are now focusing on identifying those types of memory, and, for each, the individual steps that show strong sleep-dependent activation. However, again, sleep does not refer to a simple unitary phenomenon, instead representing a complex array of brain states that differ in their physiology, chemistry, and phenomenological experiences. Sleep has been broadly divided into rapid eye movement (REM) sleep and non-REM (NREM) sleep, which alternate across the night, in humans in a 90-min cycle (Fig. 1B). NREM sleep is further subdivided into NREM stages 1–4 [7], which appear to differ in their contribution to sleep-dependent memory consolidation [8].
Before describing these systems of memory consolidation in greater detail, we would like to offer an overview of our perspective on memory consolidation and reconsolidation. First, all of these processes occur over time automatically, outside of awareness and without intent. Thus, they are specifically different from changes that result from conscious reminiscing or intentional rehearsal. In this respect, they are no different from molecular cascades triggered by an initial biochemical event, but while molecular cascades are normally restricted to a single cell, the cascade of events characterizing memory consolidation range from intracellular gene inductions to brain-wide, system-level reorganizations of memories representations.
Second, while these processes occur automatically, they are, nevertheless, modulated by other factors. Again, this is not different from what is seen with intracellular molecular cascades, but the greatly extended time course allows for different forms of modulation. As a result, the multiple components of memory consolidation and reconsolidation form a coherent whole, which functions to optimally integrate initially encoded memories into an organism’s existing informational networks, and which continues to refine and remodel these memories following reactivation, during wake and sleep. In short, memories do not simply form in the brain; they evolve.
For the purposes of this review, we use the term memory consolidation to refer to all post-encoding memory processing that is automatic and which occurs without intent or awareness under the rubric of “memory consolidation,” while those that require either conscious or behavioral rehearsal are excluded. Thus, the development of hippocampal independence as described by McClelland and colleagues [9] would be included, but improvement through actual or imagined rehearsal would not. Similarly, all post-recall memory processing that is automatic and which occurs without intent or awareness is placed under the rubric of “memory reconsolidation.”
Section snippets
Stages of memory consolidation and reconsolidation
The evolution of a memory can be a long and complex process, occurring in several distinct stages (Fig. 2). While the initial encoding of a memory is a rapid (milliseconds) process, its long-term maintenance requires processes that continue to modify it over hours to years, processes that are collectively referred to as memory consolidation [10].
Even the original view of consolidation as stabilization is now in flux. When originally proposed in 1900 [10], consolidation was defined by resistance
Sleep-dependent memory consolidation
Over the last 10 years, a large body of evidence has been reported supporting a role for sleep in the offline (re)processing of memories. We have recently reviewed the evidence for the critical role of sleep in memory consolidation [38] and only briefly summarize the behavioral literature here ([for an opposing viewpoint, see 39]).
Specific stages of sleep appear to be critical for discrete steps in the consolidation of various forms of memory, while for other steps sleep appears unnecessary
Sleep and brain plasticity
Memory formation depends on brain “plasticity”–lasting structural and/or functional neural changes in response to stimuli (such as experiences). If sleep is to be considered a critical mediator of memory consolidation, then evidence of sleep-dependent plasticity would greatly strengthen this claim. Indeed, there is now a wealth of data describing sleep-dependent brain plasticity at a variety of different levels in both animals and humans, complementing evidence of sleep-dependent changes in
Conclusions
Learning and memory are dependent on processes of brain plasticity, and sleep-dependent learning and memory consolidation must be mediated by such processes. Many examples of such plasticity during sleep have now been reported, with several of them specifically induced by waking experiences. What remains to be demonstrated is that these specific components of brain plasticity, aside from the overall requirement for protein synthesis, specifically mediate sleep-dependent learning and memory
Acknowledgement
This work was supported by grants from the National Institutes of Health (MH48,832, MH65,292, MH67,754, and MH69,985).
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