Retrieval failure versus memory loss in experimental amnesia: Definitions and processes

Abstract

For at least 40 years, there has been a recurring argument concerning the nature of experimental amnesia, with one side arguing that amnesic treatments interfere with the formation of enduring memories and the other side arguing that these treatments interfere with the expression of memories that were effectively encoded. The argument appears to stem from a combination of (1) unclear definitions and (2) real differences in the theoretical vantages that underlie the interpretation of relevant data. Here we speak to how the field might avoid arguments that are definitional in nature and how various hypotheses fare in light of published data. Existing but often overlooked data favor very rapid (milliseconds) synaptic consolidation, with experimental amnesia reflecting, at least in part, deficits in retrieval rather than in the initial storage of information.As most commonly conceived, "memory consolidation" refers uniquely to the processes by which newly acquired information, which is initially represented in ongoing synaptic transmission, comes over time to be encoded in a format that was independent of ongoing activity (and thus sensory stimulation) (Müller and Pilzecker 1900;McGaugh 1966). Fundamental to consolidation theory as it was originally formulated is that there were dual representational systems, one dependent upon ongoing neural transmission and the other dependent on enduring (i.e., structural/molecular) changes in the nervous system (e.g., pathway synthesis, facilitation of transmitter release, potentiation of sensitivity to transmitter binding, enhancement of membrane excitability) (for a review, see Matzel et al. 1998). Presumably there was a sequential dependence of the latter process (consolidation) on the former process (see Hebb 1949). Today it is widely recognized that there are a number of different molecular-structural representations that may be formed during memory storage, and that these representations become stable (i.e., "encoded") at very different rates and are dependent on different neuroanatomical sites (see Gibbs and Ng 1977;McGaugh 2000). This conceptualization of the consolidation process is often referred to as "system consolidation," although it should be noted that these different structural-molecular representations need not be sequentially linked (see Tully et al. 1994). Much recent attention has been devoted to system consolidation, which is relatively slow and measured in hours, days, or even months (see Kim and Fanselow 1992), as opposed to the earlier but still not fully answered questions of initial consolidation, which is generally assumed to occur in seconds or minutes. Although careless use of language has resulted in some confusion between these two related but different types of consolidation, some researchers distinguish them by using the expression "synaptic consolidation" (or "short-term molecular consolidation") for initial consolidation, which they differentiate from system consolidation (Nadel and Moscovitch 1997; Nader et al. 2000b;Dudai 2004). The focus of...

Persistence and plasticity in the human memory system: An empirical investigation of the overwriting hypothesis

“…Below we examine a number of similar recovery e ects that have been observed in studies where amnesia is induced through brain injury or invasive interventions such as ECS and PSIs (for review see Lewis & Maher, 1965;R. R. Miller & Springer, 1973;R. R. Miller & Matzel, 2006;Riccio & Richardson, 1984;Spear, 1973 Brown, 2002;Squire & Alvarez, 1995).…”

Antiretroviral Adherence and the Nature of HIV-Associated Verbal Memory Impairment

“…Also, as in other areas of memory research (e.g., experimental amnesia 35 ), studies of HIV-related memory impairment have varied significantly in the operational definitions and semantic labels used for various memory-process deficits. To reduce any potential confusion in this regard, in the present study and discussion, we used a three-stage/process model of episodic memory: 36 the first process being encoding, where information is taken in and transformed into a format that can be stored in the brain; the second stage is consolidation, where the transformed information is stored in the brain for later use; the third is retrieval, or extraction of the stored information for use.…”

Postretrieval new learning does not reliably induce human memory updating via reconsolidation

“…However, from the perspective of the aforementioned storage-retrieval debate (18), this interpretation should be viewed with caution, especially as retrieval deficit explanations were not explored. For example, it was not clear whether the effect endured beyond the 3-day study period, or showed propensity for recovery under favorable retrieval conditions (26), effects that have been observed in several investigations of reconsolidation with nonhuman animals (e.g., refs.…”

“…It is worth noting that the reconsolidation controversy is only the latest chapter in an enduring historical debate about the locus of interference and forgetting effects (18). On the one hand, amnesia for previously recallable information has been attributed to storage deficits: the permanent physical modification of memory traces by postencoding and postretrieval interventions [e.g., "consolidation" (19); "unlearning" (20); "destructive updating" (21); "reconsolidation" (2)].…”