Elsevier

NeuroImage

Volume 25, Issue 3, 15 April 2005, Pages 993-1001
NeuroImage

Dissociable brain activations during the retrieval of different kinds of spatial context memory

https://doi.org/10.1016/j.neuroimage.2004.12.021Get rights and content

Abstract

Although memory for spatial information has often been regarded as unitary, it may be divided into two distinct types: memory for the place where an individual experienced an event and memory for the location of an experienced event within a specific reference object. We used functional magnetic resonance imaging (fMRI) to elucidate the distinctions between the retrieval of these two types of spatial context memory. During scanning, subjects judged the room (Place task) in which a photograph had been presented or the location of the photograph on the computer display (R–L task) during the encoding phase. In a control task, subjects were asked to judge whether the photograph had been presented or not. The left middle frontal gyrus, lateral parietal and occipital regions, and bilateral precunei were found to be active during both the Place task and the R–L task compared with the control task. Critically, the place task, compared with the R–L task, was associated with activations in the right lateral prefrontal gyri, the posterior part of the left parahippocampal gyrus, bilateral retrosplenial and lateral parieto-occipital areas, whereas the R–L task, relative to the place task, with activation only in the right lateral parietal cortex. These findings indicate that the retrieval processes of spatial context memory are not associated with a single network, but may vary and recruit different neural networks depending on the type of spatial information to be retrieved.

Introduction

Episodic memory is defined as memory of personal experiences of events and includes information about temporal and spatial circumstances in which an individual experienced the events. There are various kinds of information attached to the content of the event, but memory related to information about when and where an individual experienced it is one of the most important features of episodic memory (Tulving, 2002). There is a growing body of evidence from neuroimaging studies concerning the neural networks associated with the retrieval of temporal and/or spatial context memory attached to content memory (temporal: Cabeza et al., 1997, Fujii et al., 2002, Konishi et al., 2002, Suzuki et al., 2002, Zorrilla et al., 1996; spatial: Burgess et al., 2001, Cansino et al., 2002, Johnsrude et al., 1999, Kohler et al., 1998, Moscovitch et al., 1995, Owen et al., 1996, Rugg et al., 1999, Slotnick et al., 2003; both: Fujii et al., 2004, Henson et al., 1999, Nyberg et al., 1996).

As for spatial context memory, several neuroimaging studies have examined it by presenting a set of stimuli on a computer display and then asking subjects to retrieve their spatial location during the encoding phase (Cansino et al., 2002, Henson et al., 1999, Johnsrude et al., 1999, Kohler et al., 1998, Moscovitch et al., 1995, Nyberg et al., 1996, Owen et al., 1996, Rugg et al., 1999, Slotnick et al., 2003). As Burgess et al. (2001) pointed out, most of these studies have shown brain activities in the lateral prefrontal and parietal areas without concurrent activities in the medial temporal or retrosplenial areas, which have been reported as important regions in studies of spatial memory or navigation in humans (Aguirre et al., 1996, Alsaadi et al., 2000, Epstein and Kanwisher, 1998, Gron et al., 1999, Katayama et al., 1999, Maguire et al., 1996, Maguire et al., 1998, Suzuki et al., 1998, Takahashi et al., 1997; for a review, see Maguire, 2001), as well as in animals (Malkova and Mishkin, 2003, O'Keefe and Nadel, 1978, Rolls, 1999). Two neuroimaging studies have investigated the retrieval processes of spatial context memory attached to a lifelike event, one using a virtual reality setting (Burgess et al., 2001) and the other a real-world event (Fujii et al., 2004), and found brain activities in the medial temporal or retrosplenial areas. Given that different types of spatial context memory have been associated with activities in different brain areas, the neural network associated with the retrieval processes of spatial context memory may vary according to the type of spatial contextual information to be retrieved.

We previously focused on the dissociation of two different types of temporal contextual information and showed that each retrieval process was associated with a distinct prefrontal network: the right prefrontal region for judging the temporal order of items in two lists and the left prefrontal region for items within a single list (Suzuki et al., 2002). We speculated that this dissociation reflects different cognitive processes for retrieving temporal context memory attached with content in separate episodes and within a single episode. Based on previous neuroimaging data regarding spatial context memory mentioned above and by analogy with our previous findings concerning temporal context memory, we can divide spatial context memory into (at least) two different types, i.e., large-scale spatial context memory (memory for the place where an individual experienced an event: town, building, room, and other places as an environment) and small-scale spatial context memory (memory for the location of an experienced event within a specific reference object: location within a room, location on a desk, location on a computer display, and other locations within a certain object). It is worthwhile confirming the validity of this idea in the understanding of episodic memory, especially in the theoretical categorization of context memory and the relationship between context memory and content memory. However, none of the previous neuroimaging studies compared the retrieval processes of these two types of spatial context memory in a single experimental paradigm.

In the present study, we used functional magnetic resonance imaging (fMRI) to examine whether or not distinct neural networks were associated with the two types of spatial context memory. Before fMRI scanning, each stimulus was shown in one of two different locations on a computer display in one of two different rooms. During fMRI scanning, subjects judged the room in which a stimulus had been presented (Place task) or the location (the right side or the left side) of the stimulus on the computer display during the encoding phase (R–L task). In a control task, subjects were asked to judge whether the stimulus had been presented or not (Item task). We compared the Place task and the R–L task with the Item task, and the Place task with the R–L task and vice versa.

Section snippets

Subjects

Eighteen right-handed volunteers participated in this study (seven females and eleven males; mean age 21.1 years; age range 20–23 years). All of the subjects were healthy, with no history of psychiatric or neurological illness. None had pathological findings on brain magnetic resonance imaging. Written informed consent was obtained from all subjects according to the Declaration of Helsinki. One subject was excluded from all analyses because of loss of functional imaging data due to technical

Behavioral data

A one-way ANOVA on the proportion of correct responses for the three tasks (the Place task, mean ± SD, 0.64 ± 0.06; the R–L task, 0.68 ± 0.05; the Item task, 0.89 ± 0.07) yielded a significant effect [F(2, 32) = 146.98, P < 0.0001]. Post hoc analysis using Scheffe test showed significant differences between the Place task and the Item task (P < 0.0001), and between the R–L task and the Item task (P < 0.0001), but no significant difference between the Place task and the R–L task (P = 0.11). The

Discussion

The purpose of this study was to provide evidence that there are, at least, two different types of spatial context memory and to elucidate the differences between the neural networks associated with them: large-scale spatial context memory (memory for the place where an individual experienced an event) and small-scale spatial context memory (memory for the location of an experienced event within a specific reference object). The results provide strong evidence that the two different types of

Acknowledgments

This study was supported by a grant from the Japan Society for the Promotion of Science (JSPS-RFTF97L00202) for A.Y. and by grants for scientific research from the Japanese Ministry of Education, Culture, Sports, Science and Technology (08279103) for A.Y.

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