Elsevier

Neuropsychologia

Volume 47, Issue 3, February 2009, Pages 938-941
Neuropsychologia

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Recall of remote episodic memories can appear deficient because of a gist-based retrieval orientation

https://doi.org/10.1016/j.neuropsychologia.2008.12.006Get rights and content

Abstract

Determining whether patients with amnesia can succeed in remembering their distant past has pivotal implications for theories of memory storage. However, various factors influence recall. We speculated that some patients with anterograde amnesia adopt a gist-based retrieval orientation for memories from all time periods, thereby exaggerating remote recall deficits. We tested whether an experimentally induced gist-based retrieval orientation could indeed hinder remote recall. Healthy individuals described photographs of complex scenes (e.g., of a cluttered desk) either with many words or few words (detail- or gist-based manipulation, respectively). They subsequently recalled autobiographical events and produced less episodic information after engaging the gist-based compared to the detail-based orientation. These results demonstrate the ease with which a gist-based orientation can produce apparent recall impairments. Deficits in remote episodic recall, and in future-event imagining, must thus be interpreted in light of habitual tendencies toward gist-based retrieval that some amnesic patients may exhibit.

Introduction

Patients with extensive hippocampal damage tend to exhibit profound impairments when retrieving memories for recent events (Scoville & Milner, 1957; Squire, Clark, & Bayley, 2004; Stefanacci, Buffalo, Schmolck, & Squire, 2000). In contrast, these same patients can exhibit normal memory when they recall events from decades ago. A standard explanation for this pattern of impaired recent memory with preserved remote memory is that episodic memories are subject to a hippocampal-dependent consolidation process. Memory storage and retrieval are initially dependent on both hippocampal and cortical networks. As consolidation proceeds, storage comes to depend mostly on distributed cortical networks and less on the hippocampus (Paller, 2009; Squire, Cohen, & Nadel, 1984). If the hippocampus is damaged, recent memories still dependent on the hippocampus become difficult to retrieve whereas most remote memories can be retrieved normally (Kirwan, Bayley, Galvan, & Squire, 2008; Stefanacci et al., 2000).

This view is at odds with several recent findings. In one study, patients with unilateral temporal lobe damage due to epilepsy or epilepsy surgery exhibited impaired recall of specific episodic information from remote personal events, though recall of general facts about the events was intact (Viskontas, McAndrews, & Moscovitch, 2000). In two other studies, patients with hippocampal damage exhibited impaired episodic recall regardless of the time period of the past event (Nadel, Samsonovich, Ryan, & Moscovitch, 2000; Steinvorth, Levine, & Corkin, 2005). In addition, a patient with extensive hippocampal damage and relatively intact temporal neocortex displayed more severe remote episodic memory deficits than patients with extensive temporal neocortical damage and little hippocampal damage (Rosenbaum et al., 2008). This evidence suggests that the episodic components of declarative memories retained their dependence on the hippocampus, such that all memories for episodic details are lost when the hippocampus is damaged, in keeping with a memory theory known as Multiple Trace Theory (Cipolotti & Moscovitch, 2005; Moscovitch, Nadel, Winocur, Gilboa, & Rosenbaum, 2006; Nadel & Moscovitch, 1997).

A novel way to explain these inconsistent findings in the literature on the neuropsychology of remote episodic memory is to invoke retrieval factors, as follows. For patients with significant anterograde amnesia, recent events are very difficult to remember in detail, whereas it typically remains easy to bring to mind general information about common experiences. A habit may thus be acquired in coping with difficulties in remembering recent events, such that producing generic or gist information comes to dominate the cognitive strategies engaged at retrieval. In this manner, a severe anterograde amnesic deficit could have an indirect influence on the presentation of retrograde amnesia. We propose that a pervasive gist-based retrieval orientation may contribute to the poor performance in retrieving details of remote events in some amnesic patients. To the extent that such a mechanism is operative, it would be incorrect to infer an actual loss of remote memories on the basis of apparent remote deficits. Rather, these deficits could in part reflect a maladaptive retrieval tendency.

To what extent can recall of decades-old episodic memories be hindered by a gist-based retrieval orientation? To investigate this question, we implemented a retrieval-orientation manipulation to induce either a gist-based or a detail-based retrieval orientation in healthy subjects with no known cognitive impairments. We focus on remote recall, as this is the essence of the primary divergence between Multiple Trace Theory and Standard Consolidation Theory, whereas both predict similar patterns of recall of recently acquired information (Paller, 2009). Our manipulation was designed to simulate, in a mild and temporary manner, the alterations in retrieval orientation potentially caused by severe anterograde amnesia. Demonstrating that retrieval orientation can systematically bias remote episodic recall (even without showing whether anterograde amnesia leads to a pervasive bias of this sort) could lend plausibility to our hypothesis concerning the interpretation of remote memory impairments.

Section snippets

Subjects

We tested remote memory in 12 adults (seven females and five males) 67–78 years of age. All provided informed consent.

Procedure

The procedure is illustrated in Fig. 1. Subjects completed two recall sessions at least 24 h apart. First, subjects produced the titles of four distinct autobiographical events that they could later recall in detail. They were instructed that acceptable events consisted of a single, discrete episode that occurred between the ages of 18 and 30 years old. The order of recall from

Results

Episodic recall counts are shown in Fig. 2A. As predicted, the type of task undertaken in Phase 2 influenced Phase 3 recall, as more episodic information was produced in the detail condition than in the gist condition [t(11) = 4.69, p < .001]. Recall in Phase 1 did not differ across the two conditions [t(11) = .54]. Recall differences between conditions did not differ as a function of whether the gist or detail session occurred first [t(10) = .08 in Phase 1 and t(10) = 1.12 in Phase 3].

Given the

Discussion

Retrieval orientation systematically influenced episodic recall in people with no known cognitive impairments. The number of episodic details was reduced when a gist-based orientation was operative at the time of recall compared to when a detail-based orientation was operative. On the other hand, the number of semantic details was unaffected by retrieval orientation. The specificity of the influence of the retrieval-orientation manipulation can be understood by considering a hierarchical model

Acknowledgments

Support was provided by NSF (BCS-0518800 and a graduate research fellowship to JDR). We thank Courtney Clark for analysis assistance and the Northwestern Cognitive Neurology and Alzheimer's Disease Center (NIH P30-AG13854) for assistance with recruiting participants.

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