Behavioural Brain Research 123 (2001) 37–48
Research report
Spatial problem solving and hippocampal place cell firing in rats:
control by an internal sense of direction carried across
environments
John R. Huxter
a,
*, Christina M. Thorpe
b
, Gerard M. Martin
c
, Carolyn W. Harley
c
a
Department of Anatomy and De6elopmental Biology, Uni6ersity College London,
4
th
Floor, Gower Street, London WC
1
E
6
BT, UK
b
Department of Psychology, Uni6ersity of British Columbia,
2136
West Mall, Vancou6er, BC, Canada V
6
T
1
Z
4
c
Department of Psychology, Memorial Uni6ersity of Newfoundland, St. John
’
s, Nfld, Canada A
1
B
3
X
9
Received 28 July 2000; received in revised form 16 February 2001; accepted 16 February 2001
Abstract
Rats learned to find the baited corner of a box surrounded by a curtain, regardless of whether they had a fixed or random point
of entry (POE) through the curtain. On probe trials, rats used an internal direction sense carried from outside the curtain to solve
the problem, and only used the visual cue inside the curtain if disoriented and denied access to a view of the room en route.
Similar disorientation procedures were required to obtain cue control of hippocampal place fields. The results suggest that: (1)
POE effects previously found in the water maze may be task-specific; (2) an undisrupted internal sense of direction carried from
one environment to another may provide the preferred solution to spatial problems in the second environment, even when this
second environment is a familiar one with stable visual cues; and (3) choice behaviour is sometimes, but not always, representative
of the hippocampal representation of space. © 2001 Elsevier Science B.V. All rights reserved.
Keywords
:
Spatial learning; Direction sense; Place cell; Hippocampus; Rat
www.elsevier.com/locate/bbr
1. Introduction
Animals appear to automatically create internal rep-
resentations of their environments — i.e. spatial or
cognitive maps (see [9], for a review) — using informa-
tion from multiple sensory modalities [25], and with the
particular involvement of the hippocampus and related
structures [17,20,23]. To make correct choices on a
spatial learning task, an animal must recognise the
environment in order to call up the correct cognitive
map, confer an orientation onto the map appropriate to
the direction from which it entered the environment,
and track its own movement (path integrate) through
the environment in order to continually update its
internal representation of direction and position. The
control of map orientation has been the subject of
considerable debate in the past, and is the focus of the
current experiment.
Salient visual features of an environment can control
the angular orientation of an animal’s cognitive map, as
measured by spatially directed behaviour [29] and the
spatially selective firing of pyramidal neurons in the
hippocampus (‘place cells’, [22]). However, there is evi-
dence that control of place field orientation by visual
cues may only develop over time, and only if animals
are not disoriented during training [14], but see also [6].
Recent theory based on such findings posits that the
stability of visual cues, relative to a reference frame
defined by path integration (from an arbitrary starting
point), needs to be established before such cues can
exert control over spatial map orientation [16]. The
geometric shape of an environment has been shown to
override control by other visual cues following disorien-
tation [4,11,18], but in the absence of disorientation,
* Corresponding author. Tel.: +44-171-4193388; fax: + 44-171-
3911306.
E-mail address
:
jhuxter@maze.ucl.ac.uk (J.R. Huxter).
0166-4328/01/$ - see front matter © 2001 Elsevier Science B.V. All rights reserved.
PII: S0166-4328(01)00194-2