New views on old memories: re-evaluating the role of the hippocampal complex

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Abstract

Evidence of temporally graded retrograde amnesia (RA) following hippocampal damage has fuelled the long-standing belief that memory undergoes a consolidation process, whereby memories are progressively modified in neocortical regions until they are independent of the hippocampal (HPC) complex. Support for this position derives from both the animal and human RA literature, although the results are not consistent. Specifically, consolidation theory does not account for loss of episodic (detail) information in humans and context-dependent information in animals, which often extend back for much of the life span. We discuss an alternative approach, the Multiple Trace Theory, which suggests that the HPC complex contributes to the retrieval of recent and remote episodic and context-dependent memories. According to this view, such memory traces are represented as spatially distributed interactions between the HPC and neocortex that persist for as long as those memories exist. On the other hand, semantic, or context-free, memories can become independent of the HPC as consolidation theory predicts. In support of this view, we report recent accounts of relatively flat RA gradients in autobiographical and spatial detail loss in patients and animal models with extensive bilateral HPC lesions. By comparison, temporally graded RA was observed in tests of semantic and context-free memory. We also report neuroimaging studies in which hippocampal activity, elicited during recollection of autobiographical memories, did not distinguish recent from remote episodes. Our discussion suggests ways to reconcile discrepancies in the literature and guide predictions of the occurrence of flat versus temporally limited gradients of remote episodic and semantic memory loss following lesions to HPC.

Introduction

In 1957, Scoville and Milner [66] discovered that bilateral damage to the hippocampal (HPC) complex1 and adjacent regions within the medial temporal lobe (MTL) produces an amnesic syndrome characterized by a profound loss of long-term memory for events occurring subsequent to the damage (anterograde amnesia, AA). Since then, a great deal has been learned about the nature of AA, in particular, that memory loss is not uniform for all types of information. For example, we now know that the loss is most pronounced for information that can be recalled only with conscious awareness as part of explicit or declarative memory [42], [75]. Although it is clear that memory for personal experiences is impaired, there is some debate as to whether other types of declarative knowledge such as that which comprises semantic memory, are equally affected [76], [84], [85], [86]. Memory without awareness (implicit memory), whether perceptual, conceptual, or procedural, is relatively well preserved even in profoundly amnesic patients (for reviews, see [65], [74]). Likewise, various types of premorbid memories appear to be well retained except for a short period of retrograde amnesia (RA) for events immediately preceding the onset of the lesion (e.g. [39], [40], [74]).

Despite the widely held view that RA is relatively brief and temporally graded, not all evidence is consistent with this pattern [17], [25], [44], [48]. A recent revival of interest in remote memory has yielded additional contradictory evidence, which combined with previous findings, has forced investigators to reconsider the state of premorbid memories following HPC damage. In this paper, we examine evidence deriving from human and animal models and argue that the pattern of RA, like that of AA, varies with the type of memory under investigation and probably with the location of the lesion. Specifically, we propose that, to understand the varied pattern of RA following HPC damage, an important distinction must be drawn between semantic and episodic memories in humans and between context-free and context-dependent memories in animals. Our review suggests that temporally graded RA is observed on tests of semantic and context-free memory, whereas measures of episodic or context-dependent memory are likely to yield extensive memory loss with a flatter gradient. If confirmed, these views challenge traditional consolidation theory and argue in favor of Multiple Trace Theory that, (1) attributes to the HPC formation a unique role in retention and retrieval of episodic, context-dependent memories for as long as they exist; and (2) describes the interaction between HPC and neocortex in forming semantic, context-free memories [37], [44], [48].

Section snippets

Episodic versus semantic memory

Scoville and Milner's [66] observations of temporally graded RA in the well-studied bitemporal amnesic, HM, were consistent with the prevailing view that remote memories are relatively spared in amnesia. In the following year, similar anecdotal evidence of limited RA was found in two left temporal lobectomy patients [58], one with suspected, and the other with confirmed, damage to the right HPC [57]. Formal testing corroborated these findings in a host of amnesic patients with known or presumed

Retrograde amnesia: animal studies

For many years, research into the behavioural effects of HPC damage in animals focused almost exclusively on new learning and anterograde memory function. While these studies revealed patterns of AA that paralleled those seen in MTL/HPC amnesia, there was virtually no attempt to determine if RA accompanied this effect for pre-operatively experienced events. Undoubtedly, the development of animal models of RA was hampered by the lack of suitable paradigms. In particular, it was difficult to

Summary and conclusions

A re-examination of the early literature on retrograde memory loss as well as consideration of new data have forced a re-evaluation of the standard consolidation hypothesis and promotion of an alternative theoretical model. With regard to human memory, the duration of RA sometimes is short, but more often RA for details of autobiographical events after large MTL lesions can extend for decades, or even a lifetime, far longer than would be biologically plausible for a consolidation process to

Acknowledgements

Research reported in this paper and the preparation of this manuscript were supported by a Natural Sciences and Engineering Research Council (NSERC) grant to GW, a Canadian Institutes of Health Research (CIHR) grant to GW and MM, and a NSERC postgraduate scholarship and CIHR doctoral award to RSR. The authors wish to thank Doug Caruana and Kimberly Oxbro for their technical assistance.

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