The neurobiology of consolidations, or, how stable is the engram?

Key Words memory, consolidation, persistence, retrieval, reconsolidation

* Abstract Consolidation is the progressive postacquisition stabilization of long-term memory. The term is commonly used to refer to two types of processes: synaptic consolidation, which is accomplished within the first minutes to hours after learning and occurs in all memory systems studied so far; and system consolidation, which takes much longer, and in which memories that are initially dependent upon the hippocampus undergo reorganization and may become hippocampal-independent. The textbook account of consolidation is that for any item in memory, consolidation starts and ends just once. Recently, a heated debate has been revitalized on whether this is indeed the case, or, alternatively, whether memories become labile and must undergo some form of renewed consolidation every time they are activated. This debate focuses attention on fundamental issues concerning the nature of the memory trace, its maturation, persistence, retrievability, and modifiability.

 
CONTENTS 
 
INTRODUCTION 
ON THE TERMINOLOGY OF CONSOLIDATION 
GENERIC CRITERIA FOR CONSOLIDATION 
SYNAPTIC CONSOLIDATION 
THE STANDARD MODEL OF SYNAPTIC CONSOLIDATION 
SYSTEM CONSOLIDATION 
THE STANDARD MODEL OF SYSTEM CONSOLIDATION 
DOES SYSTEM CONSOLIDATION OCCUR ONLY 
  IN DECLARATIVE SYSTEMS? 
WHY CONSOLIDATE? 
RESERVATIONS CONCERNING THE CONSOLIDATION THEORY 
SELECTED RESPONSES TO THE RESERVATIONS 
DO MEMORIES RECONSOLIDATE? 
DIFFERENCES BETWEEN SYNAPTIC CONSOLIDATION 
  AND POSTULATED RECONSOLIDATION 
THE POSSIBILITY OF SYSTEM RECONSOLIDATION 
ON THE MULTIPLE VERSIONS 
  OF THE RECONSOLIDATION HYPOTHESIS 
RESERVATIONS CONCERNING THE STRONGER VERSIONS OF 
  THE RECONSOLIDATION HYPOTHESIS 
SELECTED RESPONSES TO THE RESERVATIONS 
ON THE DISTINCTION BETWEEN RECONSOLIDATION 
  AND DECONSOLIDATION 
EPILOGUE 

INTRODUCTION

In the domain of memory research and theory, consolidation (Latin for "to make firm"), or memory consolidation, refers to the progressive postacquisition stabilization of long-term memory, as well as to the memory phase(s) during which such presumed stabilization takes place (Dudai 2002a). It has long been suggested that fresh memories need time to stabilize, and that often, such traces are prone to interference by distracting stimuli, injuries, or toxins, which, however, lose their effectiveness with the passage of time. The first documented reference to memory consolidation is in the writings of Quintillian, the noted Roman teacher of rhetoric, who tunas his readers' attention to the "curious fact ... that the interval of a single night will greatly increase the strength of the memory," and raises the possibility that "... the power of recollection ... undergoes a process of ripening and maturing during the time which intervenes" (Quintillian first century A.D.). That such posttraining, time-dependent maturation process takes place was therefore probably known in the Middle Ages to orators and mnemonists who were well versed in the writings and mnemonotechniques of their Roman predecessors. The idea resurfaced again occasionally in different versions before the birth of experimental psychology (e.g., Hartley 1810).

The term "consolidation" is attributed to Muller & Pilzecker, who rediscovered, in a series of studies carried out in Gottingen between 1892 and 1900, that memory takes time to fixate, of undergo Konsolidierung (Muller & Pilzecker 1900). Their evidence was based on systematic search for the laws that govern the acquisition and retrieval of verbal material, a la Ebbinghaus (1885). Muller & Pilzecker found that correct recall of the target material improved during the first few minutes after training, and that if presented during the first minutes after training, intervening new stimuli tend to impair recall of the target material (a phenomenon they termed "retroactive inhibition"). They suggested that this reflects a posttraining interval during which associations consolidate in memory. Interestingly, as aptly noted by Lechner et al. (1999), though the Muller & Pilzecker study is frequently cited and referred to as the beginning of the modern era in the prolific field of memory consolidation, it has never been translated in full from German, and non-German readers must rely on abstracts and extracts (Lechner et al. 1999, McDougall 1901). In spite of several reports of failure to replicate the aforementioned Muller & Pilzecker's findings (e.g., McGeoch 1933, reviewed and analyzed in Wixted 2004), their conclusion, that the trace is still uncompleted when training is over, has been overall well consolidated in the collective memory of memory research.

Shortly before Muller & Pilzecker introduced the term, the process of consolidation was also proposed based on clinical data. In "global," organic amnesia, memory of the recent past is commonly affected more than memory of the distant past; this observation is epitomized in Ribot's Law, or the Law of Regression: "Progressive destruction advances progressively from the unstable to the stable" (Ribot 1882). The idea was further elaborated a few years later by Burnham, who in a signal paper on amnesia integrated findings from experimental psychology and neurology, while at the same time emphasizing the dynamic nature of postexperience memory maturation: "There must be time for the processes of organization and assimilation (of memory) to take place. There must be time for nature to do her part.... Hurry defeats its own end" (Burnham 1903). It is noteworthy that Burnham's "time" actually refers to two different types of consolidation kinetics: fast, such as unveiled by the studies of Muller & Pilzecker, and slow, such as unveiled by the observations of residual premorbid memory in global amnesics. This temporal dichotomy suggests at the outset that the generic term "consolidation" conceals different types of processes and mechanisms. This is reflected in the title of this chapter and is further discussed below.