Research Article: Forgetting, Reminding, and Remembering: The Retrieval of Lost Spatial Memory

Date Published: August 17, 2004

Publisher: Public Library of Science

Author(s): Livia de Hoz, Stephen J Martin, Richard G. M Morris

Abstract: Retrograde amnesia can occur after brain damage because this disrupts sites of storage, interrupts memory consolidation, or interferes with memory retrieval. While the retrieval failure account has been considered in several animal studies, recent work has focused mainly on memory consolidation, and the neural mechanisms responsible for reactivating memory from stored traces remain poorly understood. We now describe a new retrieval phenomenon in which rats’ memory for a spatial location in a watermaze was first weakened by partial lesions of the hippocampus to a level at which it could not be detected. The animals were then reminded by the provision of incomplete and potentially misleading information—an escape platform in a novel location. Paradoxically, both incorrect and correct place information reactivated dormant memory traces equally, such that the previously trained spatial memory was now expressed. It was also established that the reminding procedure could not itself generate new learning in either the original environment, or in a new training situation. The key finding is the development of a protocol that definitively distinguishes reminding from new place learning and thereby reveals that a failure of memory during watermaze testing can arise, at least in part, from a disruption of memory retrieval.

Partial Text: For more than a century, the phenomenon of retrograde amnesia (RA)—the loss of memory for events that occur prior to a variety of precipitating brain insults—has provided the foundation for theories of memory consolidation and the locus of trace storage (McGaugh 1966; Davis and Squire 1984; Dudai and Morris 2000). However, RA may also reflect the inability of a memory system to access a trace—a failure of memory retrieval (Warrington and Weiskrantz 1968). This very dilemma was noted by Ribot (1883, p. 475) in his seminal discussion of RA:
“Two suppositions are equally warranted, viz., that either the registration of the prior states has been effaced; or that the retention of the anterior states persisting, their aptitude for being revived by associations with the present is destroyed. We are not in a position to decide between these two hypotheses.”

A summary of the experimental design is provided in Figure 1 (see Materials and Methods).

The key finding of this study is that rats with partial lesions of the hippocampus can be reminded of a preoperatively learned escape location in a watermaze by both correct and potentially misleading information. Whereas sham-lesioned rats showed new one-trial learning towards or away from the originally trained quadrant as a function of the type of reminder treatment to which they were exposed, partially lesioned animals were unable to learn. Instead, the first PT served only as a reminder of the original platform location irrespective of where in the pool the platform was raised at the end of this trial. Rats with complete hippocampal lesions showed neither new learning nor reminding.



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