Behavioural Brain Research 154 (2004) 345–352
Research report
Entorhinal cortex lesions impair the use of distal but not
proximal landmarks during place navigation in the rat
Carole Parron, Bruno Poucet, Etienne Save
∗
Laboratory of Neurobiology and Cognition UMR 6155, CNRS-University of Aix-Marseille I,
31 Chemin Joseph-Aiguier, 13402 Marseille, Cedex 20, France
Received 8 September 2003; received in revised form 2 March 2004; accepted 4 March 2004
Available online 24 April 2004
Abstract
Rats with entorhinal cortex lesions were trained in two versions of the place navigation task in the Morris water maze. In the distal
condition, they had to locate the hidden platform on the basis of remote landmarks, while in the proximal condition, they had to rely only
on a configuration of proximal objects, placed directly in the pool. Entorhinal rats were impaired in using distal landmarks but were able
to use proximal landmarks to navigate toward the platform. These results suggest that the use of distal and proximal landmarks during
navigation involves activation of different neural structures. They also suggest, in agreement with previous data, that there are two distinct
landmark-processing systems, one devoted to the processing of proximal landmarks and the other to the processing of distal landmarks.
© 2004 Elsevier B.V. All rights reserved.
Keywords: Entorhinal cortex; Place navigation; Water-maze; Rats
1. Introduction
There is a wealth of data showing the importance of en-
vironmental cues in guiding the animals’ spatial behavior.
In their early theoretical work, O’Keefe and Nadel [21]
proposed that perception of distal cues enables an animal
to use a mapping strategy during navigation, i.e. a strategy
based on a representation encoding spatial relations among
cues (allothetic relations). In support of this hypothesis, rats
have been repeatedly shown to be able to reach a hidden
platform in the Morris water maze from different starting
places by relying on the configuration of room cues [17,32].
Consistent with these results are also the findings that ma-
nipulation of distal cues disrupts the animals’ performance
during various spatial tasks [33]. The strong influence ex-
erted by distal cues over navigation and place learning may
be related to the fact that they provide a stable spatial frame
of reference in the sense that they do not change their rel-
ative positions as the animal moves in the environment. In
contrast, proximal cues are subject to changes in their rel-
ative positions as the animal locomotes. Thus, it may be a
∗
Corresponding author. Tel.: +33-491-16-43-64;
fax: +33-491-71-49-38.
E-mail address: save@lnf.cnrs-mrs.fr (E. Save).
priori more difficult for the animals to build a stable frame
of reference by using proximal cues than distal cues. In
general, distal landmarks are visual cues located beyond the
animal’s “working space” whereas proximal landmarks are
objects that can be directly approached during exploration.
Behavioral studies indicate that rodents nevertheless are
able to integrate proximal landmarks in their spatial repre-
sentation [2,5,11], therefore, confirming O’Keefe’s early as-
sumption that “spatially separated intramaze cues can also
serve as place cues” [20]. In addition, several experiments
show that active exploration of an environment allows the
animal to encode the spatial relationship among proximal
landmarks [28,35]. However, it is often reported that it is
difficult to train animals in spatial tasks requiring the use of
proximal cues [11,12,34]. Such difficulty contrasts with the
rapid learning commonly observed in rats trained in spatial
navigation based on distal cues (e.g. [14]). Thus, although
distal and proximal landmarks can both be used to support
mapping strategies, the data suggest that using these two
kinds of landmarks involves different mechanisms.
One way to demonstrate the existence of two landmark-
processing systems is to show that they are mediated by
different brain structures. It is abundantly documented that
navigation based on the use of distal landmarks is disrupted
by lesions of the hippocampus (e.g. [18]). In contrast, there
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doi:10.1016/j.bbr.2004.03.006