HIPPOCAMPUS 19:1199–1211 (2009)
Sequential Egocentric Strategy is Acquired as Early as Allocentric
Strategy: Parallel Acquisition of These Two Navigation Strategies
Kinga Iglói, Mohamed Zaoui, Alain Berthoz, and Laure Rondi-Reig*
ABSTRACT: At least two main cognitive strategies can be used to
solve a complex navigation task: the allocentric or map-based strategy
and the sequential egocentric or route-based strategy. The sequential
egocentric strategy differs from a succession of independent simple ego-
centric responses as it requires a sequential ordering of events, possibly
sharing functional similarity with episodic memory in this regard. To
question the possible simultaneous encoding of sequential egocentric
and allocentric strategies, we developed a paradigm in which these two
strategies are spontaneously used or imposed. Our results evidenced
that sequential egocentric strategy can be spontaneously acquired at the
onset of the training as well as allocentric strategy. Allocentric and se-
quential egocentric strategies could be used together within a trial, and
bidirectional shifts (between trials) were spontaneously performed dur-
ing the training period by 30% of the participants. Regardless of the
strategy used spontaneously during the training, all participants could
execute immediate shifts to the opposite non previously used strategy
when this strategy was imposed. Altogether, our findings suggest that
subjects acquire different types of spatial knowledge in parallel, namely
knowledge permitting allocentric navigation as well as knowledge per-
mitting sequential egocentric navigation. V 2009 Wiley-Liss, Inc.
C
KEY WORDS: navigation; spatial memory; virtual reality; human;
strategies
INTRODUCTION
In animals as well as in humans, two main strategies have been
described for goal-oriented navigation: the allocentric strategy based on
a world centered representation and the egocentric strategy centered on
the navigator (Maguire et al., 1998; Berthoz, 2001; Bohbot et al., 2002;
Burgess et al., 2002). Allocentric strategy (also called map-based strat-
egy) is now well defined and requires encoding interrelationships among
environmental cues’ position, movements, and the location of the goal
(Tolman, 1948; O’Keefe and Nadel, 1978; Burgess et al., 2002). Ego-
centric strategy, by contrast is a less well-defined concept. For instance,
animals and humans are capable of estimating their current location rel-
ative to a starting point (i.e., homing vector) by integrating linear and
LPPA, UMR CNRS 7152, Collège de France, Paris, France
Grant sponsor: European grant Wayfinding; Grant number: FP6-2003-
NEST-PATH; Grant sponsors: Fondation pour la Recherche Médicale (FRM),
Fédération pour la Recherche sur le Cerveau (FRC), the UPMC, and ANR
young researcher program; Grant number: DLC20060206428 (to L.R.-R.).
*Correspondence to: Laure Rondi-Reig, NPA, ENMVI, UMR CNRS 7102,
UPMC, 9 quai St Bernard, case 01, Paris, France.
E-mail: laure.rondi@snv.jussieu.fr
Accepted for publication 2 February 2009
DOI 10.1002/hipo.20595
Published online 9 April 2009 in Wiley InterScience (www.interscience.
wiley.com).
C 2009
V WILEY-LISS, INC.
angular self-motion signals over time. This process,
termed path integration or dead reckoning (Mittel-
staedt and Mittelstaedt, 1980; Etienne et al., 1998),
relies upon idiothetic cues such as vestibular and kin-
aesthetic signals, motor command efferent copies, and
sensory (e.g., optic) flow information (Arleo and
Rondi-Reig, 2007). Since path integration does not
depend on external references, it allows a subject to
perform online self-localization during the navigation.
Egocentric strategy is called simple egocentric or
response strategy if the animal has to learn only one
body turn to find the goal, as defined in a rodents
study using a T-maze paradigm (Packard and
McGaugh, 1996). In human, egocentric strategy has
often been compared either with a response strategy
or with an ensemble of stimulus–response (S–R); it
has been called topokinetic, route-following, or non-
spatial strategy (Berthoz, 2001; Hartley et al., 2003;
Iaria et al., 2003). We recently introduced a distinc-
tion between a simple (response) and a sequential ego-
centric strategy (Rondi-Reig et al., 2006) when a tem-
poral sequence of body turns has to be learnt. What
we call sequential egocentric strategy in the present ar-
ticle refers to the memory of temporal relations
between specific environmental choice points. The se-
quential egocentric strategy differs from path integra-
tion in the sense that it does not allow online localiza-
tion but rather allows the memory of body turns asso-
ciated with specific choice points. Sequential
egocentric strategy also differs from a succession of in-
dependent simple egocentric responses [response strat-
egy described by Packard and McGaugh (1996); see
also O’Keefe and Nadel, (1978)] in requiring multiple
(n > 2) body turns to be associated with choice
points which are defined by their order in the
sequence of turns (sequence memory) (Arleo and
Rondi-Reig, 2007).That is, the sequential egocentric
strategy requires a sequential ordering of events, possi-
bly sharing a similarity with episodic memory in this
regard.
Separate neural networks have been shown to
underlie these navigation strategies. The use of an
allocentric strategy is proposed to depend on a mem-
ory system including the hippocampus, whereas the
simple egocentric strategy or S–R learning was shown
to depend on a memory system which includes the
striatum but not the hippocampus (Potegal, 1972;
Morris et al., 1982; Packard and McGaugh, 1996;
1200 IGLÓI ET AL.

Mellet et al., 2000; Burgess et al., 2002; White and McDonald,

2002; Hartley et al., 2003; Iaria et al., 2003). Since the hippo-
campus mediates rapid encoding of information (O’Keefe and
Nadel, 1978), the allocentric strategy has been proposed to
appear early in the learning process. In contrast, the striatum is
involved in a slower learning process (Packard and McGaugh,
1996; Iaria et al., 2003) and thus the simple egocentric strategy
appears later in learning. Therefore, allocentric and simple ego-
centric strategies are proposed to be used successively depend-
ing on the early or late phase of the training (Iaria et al.,
2003). Nevertheless, an intact hippocampal function seems also
required in the acquisition of a sequential egocentric strategy
(Ghaem et al., 1997; Maguire et al., 1998; Lambrey and Ber-
thoz, 2003; Rondi-Reig et al., 2006) possibly in cooperation
with the caudate nucleus (Voermans et al., 2004). Previous
studies in humans proposed that the hippocampus could be
involved when a combination between visuospatial (allothetic)
and body position (idiothetic) information is required (Berthoz,
1997; Ghaem et al., 1997). In animals, sequence memory also
involves the hippocampus, in particular for learning new spatial
sequences (Rolls and Kesner, 2006). Our recent study of mice
lacking N-methyl D-aspartate (NMDA) receptors in the CA1 of
the hippocampus showed a deficit in the sequential egocentric
strategy, suggesting a role of the CA1 in the acquisition of this
sequential memory (Rondi-Reig et al., 2006). Since the hippo-
campus mediates rapid encoding of information, the sequential
egocentric strategy could therefore also be used early in
training.
In our task, two main types of spatial knowledge can be
acquired when people engage in spatial learning: route knowl-
edge (sequential egocentric) and map knowledge (allocentric).
Our aim was to investigate in which phases of the training allo-
centric and sequential egocentric strategies were acquired. We
also studied spontaneous shifts between strategies to question
the possibility of bidirectional shifts between allocentric and se-
quential egocentric strategies. To that purpose, we developed a
virtual reality version of the Starmaze—this particular spatial
navigation design allows a rapid and efficient learning of the
task using either allocentric and/or sequential egocentric strat-
egies. We could define the strategy(ies) spontaneously used dur-
ing learning through probe tests in which participants were
placed at a different departure point. Finally, by imposing the
allocentric or sequential egocentric strategy on the participants,
we tested their ability to immediately use both navigation strat-
egies, hence testing whether simultaneous encoding of the dif-
ferent strategies spontaneously occurred.
Our results indicate that participants used either an allocen-
tric or a sequential egocentric strategy, or a combination of
both of them within a trial, even during the early phase of the
training. Along the learning process, participants shifted from
allocentric to sequential egocentric strategy but also from se-
quential egocentric to allocentric strategy. By imposing the
strategy, we showed that participants performed above chance
level on both strategies. These results suggest that participants
have acquired these two strategies simultaneously.
MATERIALS AND METHODS
The entire paradigm consisted in two experiments: the Star-
maze task (containing Task 1 and Task 2) and the control
experiment.
Participants
Fifty healthy right-handed volunteers (19 females and 31
males) between 19 and 32 years old [mean age: 23.1 6 0.87
(mean 6 standard error mean)] participated in Task 1 (‘‘multi-
ple strategy version’’) and Task 2 (imposed strategy). Two par-
ticipants out of 50 only participated in Task 1 and did not par-
ticipate in Task 2. Participants first performed Task 1 and then,
in Task 2, the same participants were imposed to use the allo-
centric strategy (allocentric version, four trials) and the sequen-
tial egocentric one (egocentric version, three trials). The order
of the egocentric and the allocentric versions of the task were
counterbalanced among the participants (see Table 1 for the
succession of trials) and assessed randomly to all participants.
Twenty-three other right-handed volunteer participants (12
females and 11 males) participated in the control experiment.
None of the participants had any history of neurological dis-
orders and all volunteers gave informed consent. All partici-
pants had normal or corrected to normal vision.
Virtual Environment
The Virtual Starmaze paradigm was designed with 3D Stu-
dioMax and made interactive with Virtools (v3.5). The Star-
maze was composed of 10 alleys, five central ones forming a
pentagon and five alleys radiating from the angles of the central
pentagon (Fig. 1). Participants could move around and perform
rotations freely in all the alleys. They could see environmental
cues surrounding the maze. These landmarks consisted in two
different mountains, two distinct forests, and two antennas,
which were located between the ends of two adjacent alleys. To
encourage the participants to encode the relationships between
TABLE 1.
Succession of Trials During the Virtual Starmaze Task
Task 2: Allocentric and
Task 1: Multiple egocentric versions
strategy version (counterbalanced)
Training trial 1–5 Allocentric trial 1–4
Probe test 1 Egocentric trial 1–3
Training trial 6–8 OR
Probe test 2 Egocentric trial 1–3
Training trial 9–11 Allocentric trial 1–4
Probe test 3
Training trial 12–13
Probe test 4
Training trial 14–16
Probe test 5

Hippocampus
 SEQUENTIAL EGOCENTRIC AND ALLOCENTRIC STRATEGIES
FIGURE 1. Tasks performed in the virtual Starmaze paradigm.
A: Task 1, the multiple strategy version. B: Task 2 and control experi-
ment. A1. The training trial: The virtual maze figured a central pen-
tagonal ring (alleys 2, 4, 6, 8, and 10) from which five centrally sym-
metric alleys (1, 3, 5, 7, and 9) radiate. Departure point for training
trials was located in alley 1 and participants had to navigate to the
goal located at the end of the alley 7. When reaching the arrival point
a rewarding ‘‘Bravo’’ signal appeared ending the trial. The ideal path
is represented with a red arrow. To learn this trajectory, participants
could use allocentric or sequential egocentric strategies (the view
from the departure point is represented below the maze) A2. The
probe test. To identify which strategy the participants used to solve
the task, we changed the departure point to alley 5. The participant
could use: (i) the distal environmental cues corresponding to an allo-
centric strategy and reach the goal located in alley 7 (ideal path repre-
sented with the blue arrow); or (ii) the same sequence of body move-
environmental landmarks, these landmarks were presented in
sets of two.
The virtual environment was projected on a large screen
(height: 1.75 m; width: 2 m) and the participants were sitting
in an armchair located 1.5 m from this screen. In order to nav-
igate in the virtual world, they had to use a joystick allowing
going forwards or backwards and left or right. The experiment
took place in total darkness, so participants could only see the
scene projected on the screen. Before actual testing started, the
participants practiced the motor aspects of the task moving
freely in alley 1. The practice lasted for less than 90 seconds.
As soon as participants stated to be comfortable with the joy-
stick and with performing displacements in the virtual environ-
ment, the experiment started.
The Starmaze Paradigm
In Task 1, we investigated in which phase of the learning
process allocentric and sequential egocentric strategies were
spontaneously acquired (Fig. 1). In Task 2, by imposing the
allocentric (‘‘allocentric version’’) or the sequential egocentric
strategy (‘‘egocentric version’’) on the participants, we tested
their ability to immediately use the strategy they had not spon-
taneously chosen during the learning process.
1201
ments as during training trials (right-left-right body rotations) using
a sequential egocentric strategy leading to the goal in alley 1 (ideal
path represented with the green arrow). Both goals were rewarded for
probe tests. Below, the view from the departure point of a probe test.
B1. The imposed allocentric version. Participants started from the
ends of the alleys of the maze they had not been departed from before
(alleys 3 and 9) and had to navigate to a unique goal localized at the
end of alley 7 (ideal paths represented with green and purple arrows).
Below, the views from the departure alleys of the allocentric version.
B2. The imposed sequential egocentric version. All environmental
cues were removed; the virtual environment only consisted of the
walls boarding the alleys. Participants were departed from alley 1 and
the goal is located in alley 7 (ideal path represented by the red
arrow). Below the view from the departure alley of the egocentric ver-
sion with no environmental cues.
The rationale for the control experiment was to test whether
all subjects can use either allocentric or sequential egocentric
strategy right from the beginning of the training period.
Instructions given to participants
Participants were told to make displacements in the environ-
ment in order to find a goal which would always be at the
same place. Furthermore, they were told that the goal had no
visible distinction but when reaching it, a sparkling ‘‘bravo’’
would appear which indicated the end of the trial. They were
also told that the environment would not change during the
experiment. For each trial a maximal time of 120 seconds was
allowed. If participants failed to reach the goal within 120 sec-
onds the next trial was started. One exception was the first
training trial: if participants failed to reach the goal within 120
seconds, they were placed in the goal alley and were told to
reach the goal by going straight ahead.
Task 1, Spontaneous choice among strategies: The
multiple strategy version of the Starmaze task
The task consisted in 16 training trials and five probe
tests regularly inserted between training trials (Table 1). It is
Hippocampus
1202 IGLÓI ET AL.
important to note that participants were not informed about
the existence of probe tests.
During a training trial, participants were always placed in
alley 1 and had to find the goal located in alley 7 (Fig. 1A1).
Participants could navigate using the configuration of environ-
mental or allothetic cues (allocentric strategy) or a sequence of
successive body turns leading to the goal using idiothetic infor-
mation coming from the hand movement with the joystick and
optic flow during virtual displacement (sequential egocentric
strategy) or a combination of both (will be called mixed strat-
egy) as revealed by the probe test.
During a probe test (Fig. 1A2), participants had to find the
goal from a different departure point, i.e., alley 5; this depar-
ture point was defined to identify which strategy was spontane-
ously used by the participant during learning. The surrounding
views of the environment at the beginning of training trials
and probe tests were very similar (compare view from depar-
tures; Figs. 1A1,A2). Therefore, participants did not notice that
the departure point was different and in such way were trig-
gered to use the same strategy as during the training trials.
During probe tests, both strategies were considered as suitable
and participants were rewarded if they were using the allocen-
tric strategy based on environmental cues (leading to the end
of alley 7) as well as if they were using the sequential egocen-
tric strategy based on the sequence of body turns (right-left-
right body rotations leading to the end of alley 1).
Task 2, imposed strategy
The allocentric version of the Starmaze task is as follows:
two departure points, which had not been tested previously,
were used in the alleys 3 and 9 (Fig. 1B1). These departure
points were used twice each. Here, the task could only be
solved using environmental cues (allocentric strategy) as repro-
ducing the sequence of body turns (sequential egocentric strat-
egy) would not lead to the goal. We quantified the number of
successful trials for each participant, i.e., the number of direct
paths from the departure to the goal.
The egocentric version of the Starmaze task (Fig. 1B2) is as
follows: all environmental cues were removed to force the par-
ticipants to reproduce previously performed sequence of body-
turns, thus to navigate using a sequential egocentric strategy.
Participants had to do three trials in this egocentric version.
The order of the egocentric and the allocentric versions of
the task were counterbalanced among the subjects (see Table 1
for the succession of trials).
The control experiment
The task was realized in the same virtual environment as
described above. All participants first realized five training tri-
als and then received one imposed version of the task: 13
participants received the allocentric version and 10 partici-
pants received the egocentric version (see Fig. 6A for the
order of the trials). The maximum time for each trial was 90
seconds.
Hippocampus

Allocentric version of the control experiment (see Fig. 1B1)
is as follows: after the five training trials the participants
were told they would be in the same environment but start-
ing from a different departure point and that their task
would be to navigate to the goal as directly as possible. All
participants had to perform six trials in this task from two
different departure points (i.e., three trials from each).

Egocentric version in the control experiment (see Fig. 1B2)
is as follows: after the five training trials subjects were told
that the environmental landmarks surrounding the maze
would be removed and that they would have to reproduce
the route previously learned to get to the goal. All partici-
pants had to perform six trials in this task.
The allocentric/egocentric versions of the control experiment
differed from the one realized in the main experiment on two
points. First, these tasks were performed after only five training
trials, so when the task was just learnt and no overtraining
could have occurred. Second, by the fact that participants were
informed that the departure point would be modified (allocen-
tric version) or that the environmental cues would be removed
(egocentric version).
We considered a trial as successful if the participant navi-
gated to the goal without entering any other peripheral alley
(i.e., direct path). If the participant entered another peripheral
alley but reached the goal within 90 seconds, this corresponded
to an indirect trial.
Data Collection
Every 200 ls, the exact position of the participant and his/
her moving direction was registered in a Cartesian coordinate
system. These records were analyzed with a Matlab program to
obtain the following parameters for each trial: number of vis-
ited alleys, accuracy of the traveled path (percentage of distance
error, DE), mean speed, and performed rotations parameter
(PR).
To define the number of visited alleys, we counted all the
alleys participants visited during each trial. Therefore, number
of visited alleys included departure alley, all visited central and
peripheral alleys (not containing the goal), and the goal alley.
DE was calculated by subtracting the length of the ideal
path (ideal path length, IPL) from the length of the traveled
path (traveled path length, TPL). We normalized this measure
by dividing it by IPL to allow the comparison of the accuracy
of different paths that do not have an identical ideal path
length (IPL), as it was the case in probe tests.
TPL  IPL
DEð%Þ ¼ 3100
IPL
Mean speed was calculated by dividing the TPL by the time to
reach the goal for each trial.
PR corresponded to the difference between the sum of abso-
lute angles made with the joystick during the navigation (per-
formed angle, PA) and the minimal amount of angles necessary
to reach the goal via the ideal path (minimum angle, MA) and
 SEQUENTIAL EGOCENTRIC AND ALLOCENTRIC STRATEGIES
FIGURE 2. Training trials. Performance parameters (number
of visited alleys, percentage of distance error, DE) and mean speed
(PR) for all participants (n 5 50). A. Learning curve for the num-
ber of visited alleys: plateau is reached after training trial four at
4.51 6 0.11 alleys (mean 6 SEM). Number of visited alleys
included departure, all visited central and peripheral alleys (not
containing the goal), and the goal alley. Therefore, 4 is the mini-
therefore corresponded to the visual scan performed by the par-
ticipants: the more the participants had looked around by mak-
ing turns with the joystick, the higher the rotation parameter,
thus this measure gave an indication of the visual exploring
activities of the participant.
In the Results section, all performed ANOVAs are (one- or
two-way) repeated measures ANOVAs.
Debriefing
After completion of the task, participants were debriefed.
They were asked to draw the environment and to indicate,
with arrows, the path they had used most to reach the goal.
We had not told the participants beforehand that they would
be asked to draw the environment in order not to influence
their memorizing during the task.
For the control experiment we additionally asked for the
imposed egocentric version if participants had imagined the
location of landmarks to solve the task.
RESULTS
Sex
We have performed parametric statistical analysis including
all participants for all experiments. Male (n 5 31) versus
female (n 5 19) comparison showed no significant differences
during the training phase of Task 1, neither on visited alleys
[analysis of variance (ANOVA) F(1,48) 5 0.03; P 5 0.866)]
distance error (F(1,48) 5 0.59; P 5 0.448) nor on speed
(ANOVA F(1,48) 5 0.325; P 5 0.571), nor on performed rota-
1203
mum number of alleys to visit to get to the goal (alleys 1-10-8-7).
B. Learning curve for the percentage of distance error, plateau is
reached after trial four at 20.00 6 5.2%. C. Evolution of mean
speed of navigation during training trials: a plateau is reached af-
ter four trials, at 128.58 6 2.06 virtual m 3 s21. D. Succession of
training trials (Tt) and probe trials (Pt): each participant per-
formed 16 training trials and five probe trials (see also Table 1).
tions (ANOVA F(1,48) 5 0.0051; P 5 0.943). Splitting the
strategy classification between male versus female gave similar
results (Chi square test: v2 5 1.843; df 5 3; P 5 0.606). Dur-
ing Task 2, when forced to use the allocentric or the sequential
egocentric strategy, males and females performed equally well
from the first trial (ANOVA, F(1,46) 5 0.801, P 5 0.376 for
the imposed allocentric version and ANOVA, F(1,46) 5 0.756;
P 5 0.39 for the imposed egocentric version). For all analysis
sex effect was included but showed no significant difference.
For the control experiment, we controlled for sex differences
in a two-way repeated measures ANOVA (with trial and sex as
factor) and report no differences between male and female par-
ticipants, F(1,11) 5 1.575 P 5 0.235 for the allocentric version
and F(1,8) 5 0, P 5 1 for the egocentric version.
Task 1: The Multiple Strategy Version of the
Starmaze Task
Participants learned the task rapidly, stability in performance
was reached after four trials (Fig. 2). This corresponds to 4.51
6 0.11 for the number of visited alleys (Fig. 2A), four being
the minimum number of alleys to visit to get to the goal (the
succession of alley for this ideal trajectory being 1–10–8–7),
20.0 6 5.2% [mean 6 standard error of mean (SEM)] for the
percentage of distance error (DE) (Fig. 2B) and 128.6 6 2.1
virtual m*s21 for the speed (Fig. 2C).
Participants used three different strategies:
Allocentric, sequential egocentric, and mixed
The first probe test took place after the fifth trial, i.e., after
participants reached stable performances. Testing for differences
between a training trial and a consecutive probe trial (training
Hippocampus
1204 IGLÓI ET AL.
FIGURE 3. A. Probe tests: three different strategies were spon-
taneously used by the participants. From left to right: (i) allocen-
tric paths performed during the probe test. The participants navi-
gate on behalf of environmental cues to the goal located in alley
7. (ii) sequential egocentric paths. The participants reproduce the
same sequence of body turns than during training trials and navi-
gate to the goal located in alley 1. (iii) mixed paths. The partici-
pants first reproduce the same sequence of body turns as for an
egocentric path and then correct the trajectory using environmen-
tal cues, to finally reach the goal that is reached by the allocentric
strategy users (at the end of alley 7). B. The amount of rotations
performed in each zone of the maze: allocentric strategy users per-
form a high amount of rotations at the start of the first alley. Ego-
centric strategy users perform few rotations along the path. Mixed
strategy users perform more rotations in the central zones of the
trial 5 and probe test 1) showed no difference for distance error
(P 5 0.36; Mann-Whitney rank sum test), indicating that par-
ticipants’ performance was not significantly different between
probe tests and training trials.
Participants performed five probe tests. We observed three
kinds of behavior and no other ones (Fig. 3A):
Hippocampus
maze. The asterisk represents a significant difference between allo-
centric and egocentric strategy users at the beginning of the trial
[ANOVA F(1,19) 5 9.91, P 5 0.005, post hoc test (P < 0.001)]. C.
Percentage of distance error (DE) to an ‘‘ideal path’’ to reach the
arrival point split by strategy used to navigate. D–E. Evolution of
mean speed and performed rotations (PR) with the joystick for
training trials. Within PR graph: mean speed vs. performed rota-
tions correlation for all trials. Linear regression showed high corre-
lation (Pearson product moment correlation R 5 20.88 P <
0.0001). There was no difference among the strategies for DE,
whereas allocentric strategy users navigated more slowly (ANOVA
F(2,33) 5 11.395, P < 0.001) and performed more rotations
(ANOVA F(2,33) 5 31.578, P < 0.001) during training trials than
egocentric or mixed strategy users.

Participants navigating based on environmental cues reached directly
the goal in alley 7. This corresponds to the allocentric strategy.

Participants reproducing the same sequence of body turns
during the probe test than during training trials reached the
goal in alley 1. This corresponds to the sequential egocentric
strategy.
 SEQUENTIAL EGOCENTRIC AND ALLOCENTRIC STRATEGIES
FIGURE 4. A. Percentage of participants using an allocentric, se-
quential egocentric or mixed strategy for each probe test (from 1 to
5). Each strategy is used all along the task from the first to the last
probe test. B. Classification of participants according to the paths they
performed during the five probe tests: participants who performed five
allocentric, sequential egocentric, or mixed paths were classified
respectively as allocentric (n 5 7, 14%), sequential egocentric (n 5
21, 42%), and mixed (n 5 7, 14%) strategy users. Participants who

Other participants started the trial by performing the previ-
ously realized body turns (corresponding to the sequential
egocentric strategy), but reoriented themselves during the
navigation using environmental cues (corresponding to the
allocentric strategy) and reached alley 7. We named this
strategy the ‘‘mixed’’ strategy.
The allocentric strategy was characterized by an increase in
rotation performed at the beginning of the trial (t-test allocen-
tric vs. egocentric for the first zone of the trial: t(1,27) 5 5.56,
P < 0.001) (Fig. 3B, left column) and correlated with a
decrease in the execution speed of the task (two-way ANOVA
with trial and strategy as factors: F(2,33) 5 11.395, P < 0.001,
post hoc test allocentric vs. egocentric: P < 0.001) (Figs.
3D,E). By contrast, sequential egocentric strategy was character-
ized by a rapid execution of the sequence of body movements
leading to the goal (Fig. 3D) with no specific observations of
the landmarks (Fig. 3B, middle column). The mixed strategy
was characterized by an intermediate profile between allocentric
and sequential egocentric strategy: participants observed envi-
ronmental landmarks at the beginning of the probe trial (how-
ever, less than allocentric but more than egocentric learners)
(Fig. 3B, right column) and speed is equivalent to the egocen-
tric speed [same ANOVA as above, post hoc test (egocentric vs.
1205
performed more than one type of path during probe tests are shifters
(n 5 15, 30%). C. Classification of the shifts performed by ‘‘shifters’’:
type and number of spontaneously performed shifts during the ‘‘mul-
tiple strategies’’ version of the task. We evaluated the direction of the
performed shifts, considering that mixed paths involved more allo-
thetic information than an egocentric path, and more idiothetic infor-
mation than an allocentric path. [Color figure can be viewed in the
online issue, which is available at www.interscience.wiley.com.]
mixed): P 5 0.665] (Fig. 3D). To assess for any differences
between learning performance of the strategies we have per-
formed a two-way repeated measures ANOVA on % of dis-
tance error with trial and strategy as factors on results presented
in Figure 3C (F(2,33) 5 1.76, P 5 0.19). We conclude that
there is no difference among egocentric, allocentric, and mixed
strategy users during the training trials. The three strategies
were therefore equally performing in solving the task.
Allocentric and Sequential Egocentric Strategies
Were Both Used During the Early Phase of the
Learning Process and Shifts Between Strategies
Were Bidirectional
Allocentric, sequential egocentric, and mixed strategies were
used from the first probe test. A majority of participants used
the sequential egocentric strategy (Fig. 4). The three strategies
were also all used by participants during the four other probe
tests (Fig. 4A).
Participants who had performed five egocentric, five allocen-
tric, or five mixed paths during the five probe tests were named
egocentric, allocentric, or mixed strategy users, respectively. The
participants who had performed more than one kind of trajec-
tory during the five probe tests were classified as shifters.
Hippocampus
1206 IGLÓI ET AL.

TABLE 2.

Details of Shifts Performed During Task 1

Probe Probe Probe Probe Probe Number

Participants Type test 1 test 2 test 3 test 4 test 5 of shifts

35 Shifter Egocentric Egocentric Egocentric Allocentric Allocentric 1

15 Shifter Egocentric Egocentric Egocentric Allocentric Mixed 2
23 Shifter Egocentric Egocentric Egocentric Allocentric Egocentric 2
9 Shifter Egocentric Failed Mixed Mixed Mixed 1
17 Shifter Egocentric Mixed Allocentric Allocentric Allocentric 2
50 Shifter Egocentric Egocentric Mixed Egocentric Egocentric 2
22 Shifter Egocentric Mixed Mixed Mixed Mixed 1
28 Shifter Egocentric Egocentric Mixed Mixed Mixed 1
7 Shifter Egocentric Egocentric Egocentric Mixed Egocentric 2
30 Shifter Mixed Allocentric Allocentric Allocentric Mixed 2
16 Shifter Mixed Mixed Mixed Allocentric Allocentric 1
39 Shifter Mixed Mixed Mixed Egocentric Egocentric 1
40 Shifter Mixed Mixed Egocentric Egocentric Egocentric 1
43 Shifter Mixed Egocentric Egocentric Egocentric Egocentric 1
48 Shifter Allocentric Egocentric Egocentric Egocentric Egocentric 1

Among the 35 nonshifters participants, 21 (42%) were pure
egocentric strategy users, 7 (14%) were pure allocentric strategy
users, and 7 (14%) were mixed strategy users. Fifteen partici-
pants (30%) were shifting from one strategy to another during
the five probe tests (Fig. 4B).
All types of shifts between strategies were observed. Shifts
occurred from the use of more environmental cues (allocentric
strategy) to the use of more body-related cues (sequential ego-
centric strategy) or vice versa. We report 15 shifter participants,
(see Table 2 for a detail of the shifts):

Three participants shifted once from a more allocentric to a
more egocentric strategy.

Six participants shifted twice (one time from a more allocen-
tric to a more egocentric strategy and one time from a more
egocentric to a more allocentric strategy).

Six participants shifted once from a more egocentric to a
more allocentric strategy.
This means that 3 1 6, i.e., 9 participants out of 50 (18%)
shifted from more allocentric to more egocentric strategies and
6 1 6 participants out of 50 (24%) shifted from more egocen-
tric to more allocentric strategies (Fig. 4C).
Task 2: Imposing the Strategy to Use
Allocentric and Egocentric Versions of
the Virtual ‘‘Starmaze’’ Task
Above chance performances were reported from the first trial
of these imposed strategy tasks in both allocentric and egocen-
tric versions (Figs. 5A,B) (one-way ANOVAs compared with
chance-level for allocentric version F(4,47) 5 37.399, P <
0.001, for egocentric version F(4,47) 5 39.699, P < 0.001). All
participants, whatever the strategy they were using in the multi-
ple strategy version of the Starmaze task, performed above
chance level when they were challenged to use either only the
allocentric or only the egocentric strategy of the task (Fig. 5B).
Imposed allocentric version is as follows: trial-by-trial analy-
sis (one-way ANOVA) showed that there was no significant dif-
ference between the four groups (egocentric, allocentric, mixer,
and shifters) for neither of the trials (Trial 1: F(3,46) 5 2.999,
P 5 0.041, post hoc tests (Holm-Siddack method) showed no
significant differences; Trial 2: F(3,46) 5 1.43, P 5 0.23; Trial
3: F(3,46) 5 0.889, P 5 0.454; Trial 4: F(3,46) 5 0.951, P 5
0.424).
Imposed egocentric version is as follows: trial by trial analysis
showed that there was no significant difference between the
four groups (egocentric, allocentric, mixer, and shifters) for nei-
ther of the trials (Trial 1: F(3,46) 5 0.869, P 5 0.467; Trial 2:
F(3,46) 5 0.466, P 5 0.71; Trial 3: F(3,46) 5 1.660, P 5
0.193).
There was no order effect on the allocentric and egocentric
versions of the task. Testing for the difference between imposed
egocentric performance if realized first versus imposed egocen-
tric performance if realized after imposed allocentric perform-
ance showed no difference (Mann-Whitney rank sum test, P 5
0.985). There was no order effect of imposed allocentric per-
formance either (Mann-Whitney rank sum test, P 5 0.869).
The Control Experiment
We analyzed the percentage of successful (direct) and unsuc-
cessful (indirect and failed) trials for each task (Figs. 6B,C). All
performances were above chance level (i.e., 25%). For the allo-
centric version mean performance was 89.7,436 6 3.457%
(one-way ANOVA F(5,12) 5 14.072 , P < 0.001) (Fig. 6B).
For the egocentric version (Fig. 6C) mean was 93.333 6

Hippocampus
 SEQUENTIAL EGOCENTRIC AND ALLOCENTRIC STRATEGIES 1207

FIGURE 5. Allocentric and egocentric versions of the virtual
Starmaze. A. Schematic representation of the allocentric and ego-
centric versions of the virtual Starmaze with the surrounding views
of the maze. B. Left percentage of success for each allocentric and
sequential egocentric trial. A successful trial consists of a direct
path to the goal location and chance-level is to enter randomly
one of the four open alleys (25%). Performances are high above
chance level from the first trial of the allocentric and the egocen-
tric versions. Right percentage of successful trials (mean 6 SEM)
during the allocentric and egocentric version of the Starmaze, split
by strategy. ANOVA and all pair-wise post hoc comparison showed
sequential egocentric strategy users perform poorer than correcting
strategy users (P < 0.05). Chance-level being to enter randomly
one of the four peripheral alleys, all performances were above
chance level (P < 0.05).

FIGURE 6. The control experiment. A. Arrangement of the trials in the control experiment.
The departure alley for trials of the allocentric version is indicated between brackets. B. Percentage
of successful, indirect, and failed trials in the allocentric version of the experiment (n 5 13). C. Per-
centage of successful, indirect, and failed trials in the egocentric version of the experiment (n 5 10).

Hippocampus
1208 IGLÓI ET AL.
3.25% (one-way ANOVA F(6,9) 5 14.080, P < 0.001). There
is no trial effect for the egocentric version of the task (ANOVA
F(5,8) 5 0.649 P 5 0.664); there is a trial effect for the allo-
centric version (repeated measures ANOVA F(5,11) 5 2.631, P
5 0.02) though all pair-wise post hoc tests gave insignificant
results.
Debriefing Analysis
Participants had to draw on a blank paper sheet the environ-
ment after the experiment. The analysis of the drawings
revealed that 84% (42 participants out of 50) drew landmarks
positioned in correct order. Hundred percentage of allocentric
and 86% of mixed strategy users, 81% of sequential egocentric
strategy users, and 80% of shifters did so. Participants were
also asked to draw the path they had most often performed.
Ninety percentage (45 participants out of 50) drew the correct
path. 100% of allocentric and mixed strategy users, 81% of se-
quential egocentric strategy users, and 93% of shifters drew the
correct path. Therefore, we showed that all participants have
encoded information about the landmarks of the environment.
Results also indicated that participants had memorized the
sequence of turns they had to do in the maze whatever the
strategy they used.
For the control experiment all participants who had to per-
form the egocentric version of the task (n 5 11) gave negative
answer when asked if they had imagined the location of land-
marks to solve the task.
DISCUSSION
The current study was based on the starmaze paradigm that
allows spontaneous choice between allocentric (or map-based)
and/or sequential egocentric (or route-based) strategies. Two
major points emerge from this study. First, sequential egocen-
tric and allocentric strategies were used from the onset of the
training period and subjects using either strategy solved the
navigation task with equal performance. The second main find-
ing of the present study is the existence of bidirectional shifts
between the two strategies independently of the training phase.
In particular, we observed shifts from sequential egocentric to
allocentric strategy as often as allocentric to sequential egocen-
tric shifts. Overall, these results suggest that subjects acquired
different types of spatial knowledge in parallel.
Spontaneous Strategy Preference
to Solve the Task
Maze tasks that involve navigating along alleys (and not in
an open space) such as the cross maze, the radial arm maze, or
the starmaze, have been proven reliable in identifying the strat-
egy used relying on the path chosen both in animals (Packard
and McGaugh, 1996; Rondi-Reig et al., 2006) and in humans
(Iaria et al., 2003; Astur et al., 2004; Etchamendy and Bohbot,
Hippocampus
2007). Previous navigation studies in humans, focusing on
spontaneous choice when multiple spatial strategies were avail-
able during the learning of a navigation task, distinguished
between response (simple egocentric) and allocentric strategies
(Iaria et al., 2003) but not between sequential egocentric and
allocentric strategies. In the current study, we specifically
focused on spontaneous choice when sequential egocentric and
allocentric strategies were both available. We designed the test
to have a range of clearly definable navigation strategies, repro-
ducible by all participants. This was done to maximize the
interpretability of the navigation trajectories. Therefore we
deliberately chose starting positions and one goal locations
identical for all the participants. Participants learned the task
using three distinct strategies: the allocentric, the sequential
egocentric, and a mixed strategy (Fig. 3A).
Allocentric Strategy Relies on the
Representation of the Relationships
Between Environmental Landmarks
Our results on the rotations performed by the subjects
showed that allocentric strategy users performed rotations at
the beginning of the start alley and not at the entrance of the
goal alley (see Fig. 3B, left column), indicating that they ori-
ent themselves at the beginning of the trials and do not locate
the arrival according to the view of the arrival arm. This
behavior appears consistent with the position of the land-
marks, which are never placed at the end of the alleys but
always projected between two adjacent alleys. In addition, the
‘‘bird’s eye view’’ maps drawn by the subjects present a correct
configuration of the landmarks in 84% of the cases. These
results suggest that more than two adjacent landmarks were
memorized by the participants and that the allocentric repre-
sentation encoded by participants relies on the representation
of the relationships between environmental landmarks.
Sequential Egocentric Strategy Requires
Memorizing a Temporal Sequence of
Context-Response Associations
To get from one peripheral alley to the goal alley in the Star-
maze, sequential egocentric behavior involves remembering
three successive body turns associated with three spatially dis-
tinct but successive choice points. Indeed, the participant had
to associate a specific body direction at each choice point and
then to organize these three movements sequentially. Impor-
tantly, we introduced a distinction between simple (stimulus–
response S–R) egocentric strategies [defined in O’Keefe and
Nadel (1978)] and sequential egocentric strategies in which a
temporal sequence of body turns has to be learnt. This notion
of temporal organization of multiple S–R is here the key point
differentiating the sequential egocentric strategy from a simple
response strategy as defined by Packard and Mc Gaugh (1996).
That is, the sequential egocentric strategy requires a sequential
ordering of events, possibly sharing a similarity with episodic
memory in this regard. The difference in the nature of the ego-
centric strategy described in the starmaze (i.e., sequence mem-
 SEQUENTIAL EGOCENTRIC AND ALLOCENTRIC STRATEGIES
ory rather than simple S–R associations) might well account
for its parallel encoding with the allocentric strategy.
A Coexistence Between Allocentric and
Sequential Egocentric Strategies?
Several results suggest a possible coexistence of allocentric
and sequential egocentric strategies. First, the existence of the
mixed strategy favors the hypothesis of parallel information
processing during a given trial as mixer participants do first use
an egocentric knowledge to go directly to the egocentric goal
and then correct their trajectory according to allocentric knowl-
edge to reach the allocentric goal. Second, by asking the partic-
ipants to draw the environment, we probed the ability to recall
information needed for allocentric behavior, whereas asking
participants to draw their sequence of movements, we probed
the memory of the route necessary to perform the sequential
egocentric strategy. Third, performances on the imposed allo-
centric and imposed egocentric versions of the task informed
on parallel learning of both strategies.
When forced to use a strategy that was not used during the
training (Task 2), nonshifter participants immediately suc-
ceeded above chance level (Fig. 5B) in using a previously not
used strategy. As participants were not informed of the switch
to the imposed allocentric or the imposed egocentric task, the
first trial served as the trial informing participants of the task
switch. Focusing on Trial 2 of imposed allocentric or imposed
egocentric protocol, we showed no significant difference
between the four groups (egocentric, allocentric, mixer, and
shifters). This therefore suggests that the egocentric group did
learn the allocentric strategy in parallel to the sequential ego-
centric strategy and the allocentric group did learn the sequen-
tial egocentric strategy in parallel to the allocentric strategy.
We also performed the control experiment on two groups of
participants at the very beginning of the training period to
assess whether both strategies are learnt after the initial learn-
ing. Following five training trials, the first group of participants
performed a test in which we removed all the environmental
cues to assess the ability of participants to reproduce previously
performed sequence of body turns. As shown on Figure 6B,
89.7 6 3.5 of the participants were able to reproduce the cor-
rect and direct sequence of movements, therefore using route
knowledge to perform the task. Similarly, we performed a test
of cue rotation with another group of subjects at the very be-
ginning of the training. We also observed that 93.3% of sub-
jects are perfectly able to use the interrelationships between
environmental cues as they are perfectly able to find the loca-
tion of the goal whatever the performed rotation (departure
from alley 9 or departure from alley 3).
These two experiments strongly suggest conjunct learning of
both allocentric and sequential egocentric strategies from the
beginning of the training and do not result of overtraining.
This raises the question whether the same knowledge could
drive the allocentric and the egocentric strategies. We actually
doubt that the egocentric knowledge only (i.e., the memory of
temporal relations between specific environmental choices) may
1209
drive the flexible behavior required when rotations of the de-
parture points are performed. Indeed, the temporal relations
needed in this particular cue rotation experiment are totally dif-
ferent from the learned sequence. We could however have
thought that allocentric knowledge may drive both the allocen-
tric and the egocentric response if people had imagined the
removed cues when performing the cue elimination control
tests. We debriefed the participants and nobody mentioned
having imagined environmental features during the cue removal
task but all reported to reproduce the sequence of learned
movements.
In addition, a very large majority of the participants (84%;
more specifically 81% of spontaneous egocentric strategy users)
spontaneously positioned landmarks on their drawings, demon-
strating that allothetic information was indeed encoded. Ninety
percentage of the participants were able to retrieve correct idi-
othetic information about their navigation, as evidenced by
their ability to draw the correct path. Interestingly, 100% of
allocentric strategy users drew the correct path. On the whole,
drawing analyses comfort our hypothesis of coexisting naviga-
tion strategies.
These different results therefore suggest that participants did
acquire both allocentric and egocentric knowledge from the be-
ginning of the training period and that they could flexibly use
them depending on the requirement of the task.
Bidirectional Shifts Between Sequential
Egocentric and Allocentric Strategies
All strategies were spontaneously used from the beginning of
the practice. Therefore, egocentric paths were observed from
the first probe trial as well as allocentric and mixed strategies.
With practice, 30% of the participants shifted from one strat-
egy to another. In our task a shifter participant corresponded
to a participant who changed strategy between the different
probe tests, thus did not use the same strategy throughout the
whole task. As it was the case in Iaria et al. (2003) using the
eight-arm radial maze, we showed that normal participants
spontaneously adopted different navigational strategies and we
also observed the traditional shift from allocentric to egocentric
strategy [18% in our case vs. 39% in Iaria et al. (2003)]. This
also corroborates what had been first demonstrated in rats using
a T-maze paradigm, i.e., a shift from allocentric to response
strategy with increasing practice of the task (Packard and
McGaugh, 1996). However, no participants shifted from ego-
centric to allocentric strategy in Iaria et al. (2003), whereas
24% of our subjects shifted from sequential egocentric to allo-
centric strategy in our case. Shifts toward a more procedural
strategy may occur as a result of habit formation, which gener-
ally refers to a great number of automatic and unconscious rep-
etitions of a given S–R behavior over time (Mishkin et al.,
1984; White and McDonald, 2002). In our study, the shifter
participants did not repeat the same strategy throughout the
task; during the five probe tests they used at least two different
strategies. Further, shifts were reported in both directions (Fig.
4C). These results strongly suggest no hierarchy or practice-
Hippocampus
1210 IGLÓI ET AL.
dependant development of strategies and indicate that sequen-
tial egocentric learning did not result from habit formation or
response learning. In addition, equal learning performance of
all strategies and the variability in the shifts performed by the
participants further comforts that in the Starmaze task one
strategy is not more efficient than the other one.
Bidirectional spontaneous shifts between sequential egocen-
tric and allocentric strategies support the idea of noncompeti-
tive encoding between these two strategies and suggests comple-
mentary processing and parallel encoding of information in
multiple memory systems, as it was previously suggested by
Burgess (2006).
This is also consistent with Voermans et al.’s study (2004)
reporting psychophysiological interaction between the anterior
caudate nucleus and the medial temporal lobe related to the
route recognition versus visuomotor control condition in con-
trol subjects. As mentioned by the authors, ‘‘this effect reflects
a stronger correlation of activity in the control group between
the right caudate nucleus and the anterior hippocampus in
route recognition compared to visuo-motor control.’’ Parallel
activation of the two memory systems, i.e., the one dependent
on the hippocampus and the one dependent on the caudate
nucleus could support a possible generalization of our finding.
These different results do not question the involvement of
the hippocampus in the allocentric learning neither the role of
the striatum in response (simple egocentric strategy) learning.
These two points have been clearly stated in the literature
(Hartley et al., 2003; Iaria et al., 2003; Bohbot et al., 2004).
However, the recent distinction (as defined above) between
response learning and sequential egocentric learning questions
the possibility that different neural bases may sustain these two
learning processes. In particular, we recently proposed (Rondi-
Reig et al., 2006) that a cooperation between hippocampal and
striatal systems might be required during sequential egocentric
learning, the striatum being involved in the S–R associations
and the hippocampus in the sequential (temporal) organization
of the multiple S–R. Our aim was not to prove this point in
this study. Already existing findings give credit to part of this
hypothesis and comfort the possible importance of providing
detailed description of the route-memory system. This task has
been proven to involve the CA1 of the hippocampus in mice
(Rondi-Reig et al., 2006) and previous fMRI study mentioned
the implication of the hippocampus in route-based learning
(Ghaem et al., 1997; Hartley et al., 2003). The possible impli-
cation of the hippocampus in both allocentric and sequential
egocentric strategies is in agreement with the theoretical propo-
sition of its role in episodic memory and more precisely in its
role in spatiotemporal organization of events (Mizumori et al.,
1999; Eichenbaum, 2001; Hassabis et al., 2007). Increasing
evidences tend to show that the hippocampal formation
(wherein place, head direction, and grid cells) plays a role in
spatiotemporal representation of places, routes, and associated
experiences in events composing episodic memory system
(Lipton and Eichenbaum, 2008; Moser et al., 2008). Our
study adds another argument, here in a human study, to the di-
chotomy of multiple memories that might be considered in
Hippocampus
term of spatiotemporal organization independently on the na-
ture of the memorized information rather than in terms of spa-
tial versus nonspatial memories (Eichenbaum and Cohen,
2001). With such a former dichotomy sequential egocentric
strategy might be considered as sharing some functional proper-
ties of the episodic memory system.
CONCLUSION
In conclusion, this study demonstrates that subjects acquire
different types of spatial knowledge in parallel, i.e., knowledge
permitting allocentric navigation as well as knowledge permit-
ting sequential egocentric navigation. The results show the im-
portance of providing detailed description of the route-memory
system, in particular to distinguish between a simple egocentric
(response) and a sequential egocentric strategy, the second one
being used early during training as the allocentric one. This
suggests that the distinction between navigation strategies might
be larger than between response strategy and allocentric strategy
and may include the distinction between simple and sequential
egocentric strategy. Inside this latest distinction, the simple ego-
centric (response) strategy would be dependant of the proce-
dural memory system whereas the sequential egocentric strategy
would also involve the episodic memory system.
Acknowledgments
The authors thank Dr. Catherine Thinus-Blanc for critical
reading of the manuscript. The authors also thank Céline Pous-
sineau and Tristan Moreau for their help designing the Matlab
analysis software, Safi Saada and Philippe Barbot for the virtual
environment.
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