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lesion studies (7) in the rodent, the hippocampus has been offered (1) as the site of a “cognitive map” responsible for the flexible representation of exocentric position. The specificity of the role played by the hippocampus (i.e., Ammon’s horn, the dentate gyrus, and the subiculum) in spatial representation subsequently has been debated at length (see, e.g., ref. 20). At the very least, it is clear that selective (neurotoxic), bilateral lesions of this structure in the rodent greatly impair performance on “place” learning tasks such as the water maze (21, 22).

The importance of the hippocampus for exocentric spatial representation in the human has been more difficult to demonstrate. Spatial memory tests that present fixed stimulus arrays to a stationary patient (see, e.g., refs. 23 and 24) are not strictly relevant because the cognitive map theory proposes a flexible, map-like representational role for the hippocampus. In contrast to other sites (described below), unilateral lesions of the hippocampus do not produce any appreciable real world way-finding impairments in humans (25). The existence of anterograde way-finding deficits in patients with general anterograde amnesia after bilateral lesions of the hippocampus (and adjacent structures) (2628) has not been commented on explicitly. However, if present, any topographical difficulties obviously would be accompanied by memory impairments in other areas. Retrograde loss of way-finding knowledge in these patients is not apparently disproportionate to losses in other areas (27) and can be preserved (29). Based on these findings, if the hippocampus is indeed necessary for the representation of topographical space in humans, then it must be said (i) that way-finding in previously learned places can be accomplished in its absence (29) and (ii) that place learning is but one of many kinds of knowledge for which it is necessary [i.e., place learning is a type of declarative memory (30)].

fMRI Studies of Topographical Learning. We have attempted to examine the neural correlates of exocentric spatial learning in the human by using fMRI (11). The purpose of this study was to create conditions under which neuroanatomical structures that increase their activity during the acquisition of place knowledge could be identified. This information could then be used to either support or question assertions regarding the role of different medial-temporal lobe structures for these kinds of memory tasks. Nine subjects were studied with fMRI during their free exploration of a “virtual reality” maze (Fig. 1A and B). The signal obtained during these periods was compared with that obtained while subjects repetitively traversed a simple corridor. Subjects were tested both on their ability to produce sketch maps of the maze (Fig. 1C) and to perform way-finding tasks within the environment from novel start points. The ability of our subjects to perform these tasks strongly suggests, but does not absolutely prove (31), the acquisition of exocentric representations. The interpretation of this experiment relied on two assumptions. The first was that the navigation of a virtual reality environment engages the same cognitive processes used during real world way-finding (32). The second was the “cognitive subtraction” assumption, which allows one to attribute differences in signal between the two conditions to the putatively isolated cognitive process of exocentric learning (33).

The primary finding of the study was that, within the medial-temporal lobes, activity was confined to the parahippocampal gyrus (Fig. 2A). The laterality of this activity varied among the nine subjects, with three each demonstrating left, right, and bilateral signal changes. Differences in signal between the two conditions also were noted in several other areas of the brain, including (bilaterally) the posterior-parietal cortex, retrosplenial cortex, and medial-occipital cortex. No


The parahippocampal gyrus is comprised of several, distinct cortical fields, including the entorhinal cortex, the parahippocampal cortex (areas TH and TF) and perirhinal cortex (34). Our use of the specific term “parahippocampal cortex” and the general term “parahippocampal gyrus” (when more specific anatomical statements cannot be made) is deliberate.

FIG. 1. Stimuli from an fMRI study of topographical learning. (A) Subject view. Actual stimuli were in full color and were several times wider in the horizontal plane than pictured. (B) Aerial view of maze. (C) Representative subject rendition of maze.

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