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

C 2009
V WILEY-LISS, INC.
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- MATERIALS AND METHODS
campus mediates rapid encoding of information (O’Keefe and
Nadel, 1978), the allocentric strategy has been proposed to The entire paradigm consisted in two experiments: the Star-
appear early in the learning process. In contrast, the striatum is maze task (containing Task 1 and Task 2) and the control
involved in a slower learning process (Packard and McGaugh, experiment.
1996; Iaria et al., 2003) and thus the simple egocentric strategy
appears later in learning. Therefore, allocentric and simple ego- Participants
centric strategies are proposed to be used successively depend-
Fifty healthy right-handed volunteers (19 females and 31
ing on the early or late phase of the training (Iaria et al.,
males) between 19 and 32 years old [mean age: 23.1 6 0.87
2003). Nevertheless, an intact hippocampal function seems also
(mean 6 standard error mean)] participated in Task 1 (‘‘multi-
required in the acquisition of a sequential egocentric strategy
ple strategy version’’) and Task 2 (imposed strategy). Two par-
(Ghaem et al., 1997; Maguire et al., 1998; Lambrey and Ber-
ticipants out of 50 only participated in Task 1 and did not par-
thoz, 2003; Rondi-Reig et al., 2006) possibly in cooperation
ticipate in Task 2. Participants first performed Task 1 and then,
with the caudate nucleus (Voermans et al., 2004). Previous
in Task 2, the same participants were imposed to use the allo-
studies in humans proposed that the hippocampus could be
centric strategy (allocentric version, four trials) and the sequen-
involved when a combination between visuospatial (allothetic)
tial egocentric one (egocentric version, three trials). The order
and body position (idiothetic) information is required (Berthoz,
of the egocentric and the allocentric versions of the task were
1997; Ghaem et al., 1997). In animals, sequence memory also
counterbalanced among the participants (see Table 1 for the
involves the hippocampus, in particular for learning new spatial
succession of trials) and assessed randomly to all participants.
sequences (Rolls and Kesner, 2006). Our recent study of mice
Twenty-three other right-handed volunteer participants (12
lacking N-methyl D-aspartate (NMDA) receptors in the CA1 of
females and 11 males) participated in the control experiment.
the hippocampus showed a deficit in the sequential egocentric
None of the participants had any history of neurological dis-
strategy, suggesting a role of the CA1 in the acquisition of this
orders and all volunteers gave informed consent. All partici-
sequential memory (Rondi-Reig et al., 2006). Since the hippo-
pants had normal or corrected to normal vision.
campus mediates rapid encoding of information, the sequential
egocentric strategy could therefore also be used early in
training. Virtual Environment
In our task, two main types of spatial knowledge can be The Virtual Starmaze paradigm was designed with 3D Stu-
acquired when people engage in spatial learning: route knowl- dioMax and made interactive with Virtools (v3.5). The Star-
edge (sequential egocentric) and map knowledge (allocentric). maze was composed of 10 alleys, five central ones forming a
Our aim was to investigate in which phases of the training allo- pentagon and five alleys radiating from the angles of the central
centric and sequential egocentric strategies were acquired. We pentagon (Fig. 1). Participants could move around and perform
also studied spontaneous shifts between strategies to question rotations freely in all the alleys. They could see environmental
the possibility of bidirectional shifts between allocentric and se- cues surrounding the maze. These landmarks consisted in two
quential egocentric strategies. To that purpose, we developed a different mountains, two distinct forests, and two antennas,
virtual reality version of the Starmaze—this particular spatial which were located between the ends of two adjacent alleys. To
navigation design allows a rapid and efficient learning of the encourage the participants to encode the relationships between
task using either allocentric and/or sequential egocentric strat-
TABLE 1.
egies. We could define the strategy(ies) spontaneously used dur-
ing learning through probe tests in which participants were
Succession of Trials During the Virtual Starmaze Task
placed at a different departure point. Finally, by imposing the
allocentric or sequential egocentric strategy on the participants, Task 2: Allocentric and
we tested their ability to immediately use both navigation strat- Task 1: Multiple egocentric versions
egies, hence testing whether simultaneous encoding of the dif- strategy version (counterbalanced)
ferent strategies spontaneously occurred.
Training trial 1–5 Allocentric trial 1–4
Our results indicate that participants used either an allocen-
Probe test 1 Egocentric trial 1–3
tric or a sequential egocentric strategy, or a combination of
Training trial 6–8 OR
both of them within a trial, even during the early phase of the Probe test 2 Egocentric trial 1–3
training. Along the learning process, participants shifted from Training trial 9–11 Allocentric trial 1–4
allocentric to sequential egocentric strategy but also from se- Probe test 3
quential egocentric to allocentric strategy. By imposing the Training trial 12–13
strategy, we showed that participants performed above chance Probe test 4
Training trial 14–16
level on both strategies. These results suggest that participants
Probe test 5
have acquired these two strategies simultaneously.

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SEQUENTIAL EGOCENTRIC AND ALLOCENTRIC STRATEGIES 1201

FIGURE 1. Tasks performed in the virtual Starmaze paradigm. ments as during training trials (right-left-right body rotations) using
A: Task 1, the multiple strategy version. B: Task 2 and control experi- a sequential egocentric strategy leading to the goal in alley 1 (ideal
ment. A1. The training trial: The virtual maze figured a central pen- path represented with the green arrow). Both goals were rewarded for
tagonal ring (alleys 2, 4, 6, 8, and 10) from which five centrally sym- probe tests. Below, the view from the departure point of a probe test.
metric alleys (1, 3, 5, 7, and 9) radiate. Departure point for training B1. The imposed allocentric version. Participants started from the
trials was located in alley 1 and participants had to navigate to the ends of the alleys of the maze they had not been departed from before
goal located at the end of the alley 7. When reaching the arrival point (alleys 3 and 9) and had to navigate to a unique goal localized at the
a rewarding ‘‘Bravo’’ signal appeared ending the trial. The ideal path end of alley 7 (ideal paths represented with green and purple arrows).
is represented with a red arrow. To learn this trajectory, participants Below, the views from the departure alleys of the allocentric version.
could use allocentric or sequential egocentric strategies (the view B2. The imposed sequential egocentric version. All environmental
from the departure point is represented below the maze) A2. The cues were removed; the virtual environment only consisted of the
probe test. To identify which strategy the participants used to solve walls boarding the alleys. Participants were departed from alley 1 and
the task, we changed the departure point to alley 5. The participant the goal is located in alley 7 (ideal path represented by the red
could use: (i) the distal environmental cues corresponding to an allo- arrow). Below the view from the departure alley of the egocentric ver-
centric strategy and reach the goal located in alley 7 (ideal path repre- sion with no environmental cues.
sented with the blue arrow); or (ii) the same sequence of body move-

environmental landmarks, these landmarks were presented in The rationale for the control experiment was to test whether
sets of two. all subjects can use either allocentric or sequential egocentric
The virtual environment was projected on a large screen strategy right from the beginning of the training period.
(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-
Instructions given to participants
igate in the virtual world, they had to use a joystick allowing
going forwards or backwards and left or right. The experiment Participants were told to make displacements in the environ-
took place in total darkness, so participants could only see the ment in order to find a goal which would always be at the
scene projected on the screen. Before actual testing started, the same place. Furthermore, they were told that the goal had no
participants practiced the motor aspects of the task moving visible distinction but when reaching it, a sparkling ‘‘bravo’’
freely in alley 1. The practice lasted for less than 90 seconds. would appear which indicated the end of the trial. They were
As soon as participants stated to be comfortable with the joy- also told that the environment would not change during the
stick and with performing displacements in the virtual environ- experiment. For each trial a maximal time of 120 seconds was
ment, the experiment started. 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
The Starmaze Paradigm
seconds, they were placed in the goal alley and were told to
In Task 1, we investigated in which phase of the learning reach the goal by going straight ahead.
process allocentric and sequential egocentric strategies were
spontaneously acquired (Fig. 1). In Task 2, by imposing the
Task 1, Spontaneous choice among strategies: The
allocentric (‘‘allocentric version’’) or the sequential egocentric
multiple strategy version of the Starmaze task
strategy (‘‘egocentric version’’) on the participants, we tested
their ability to immediately use the strategy they had not spon- The task consisted in 16 training trials and five probe
taneously chosen during the learning process. tests regularly inserted between training trials (Table 1). It is

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1202 IGLÓI ET AL.

important to note that participants were not informed about  Allocentric version of the control experiment (see Fig. 1B1)
the existence of probe tests. is as follows: after the five training trials the participants
During a training trial, participants were always placed in were told they would be in the same environment but start-
alley 1 and had to find the goal located in alley 7 (Fig. 1A1). ing from a different departure point and that their task
Participants could navigate using the configuration of environ- would be to navigate to the goal as directly as possible. All
mental or allothetic cues (allocentric strategy) or a sequence of participants had to perform six trials in this task from two
successive body turns leading to the goal using idiothetic infor- different departure points (i.e., three trials from each).
mation coming from the hand movement with the joystick and  Egocentric version in the control experiment (see Fig. 1B2)
optic flow during virtual displacement (sequential egocentric is as follows: after the five training trials subjects were told
strategy) or a combination of both (will be called mixed strat- that the environmental landmarks surrounding the maze
egy) as revealed by the probe test. would be removed and that they would have to reproduce
During a probe test (Fig. 1A2), participants had to find the the route previously learned to get to the goal. All partici-
goal from a different departure point, i.e., alley 5; this depar- pants had to perform six trials in this task.
ture point was defined to identify which strategy was spontane-
The allocentric/egocentric versions of the control experiment
ously used by the participant during learning. The surrounding
differed from the one realized in the main experiment on two
views of the environment at the beginning of training trials
points. First, these tasks were performed after only five training
and probe tests were very similar (compare view from depar-
trials, so when the task was just learnt and no overtraining
tures; Figs. 1A1,A2). Therefore, participants did not notice that
could have occurred. Second, by the fact that participants were
the departure point was different and in such way were trig-
informed that the departure point would be modified (allocen-
gered to use the same strategy as during the training trials.
tric version) or that the environmental cues would be removed
During probe tests, both strategies were considered as suitable
(egocentric version).
and participants were rewarded if they were using the allocen-
We considered a trial as successful if the participant navi-
tric strategy based on environmental cues (leading to the end
gated to the goal without entering any other peripheral alley
of alley 7) as well as if they were using the sequential egocen-
(i.e., direct path). If the participant entered another peripheral
tric strategy based on the sequence of body turns (right-left-
alley but reached the goal within 90 seconds, this corresponded
right body rotations leading to the end of alley 1).
to an indirect trial.

Task 2, imposed strategy Data Collection


The allocentric version of the Starmaze task is as follows: Every 200 ls, the exact position of the participant and his/
two departure points, which had not been tested previously, her moving direction was registered in a Cartesian coordinate
were used in the alleys 3 and 9 (Fig. 1B1). These departure system. These records were analyzed with a Matlab program to
points were used twice each. Here, the task could only be obtain the following parameters for each trial: number of vis-
solved using environmental cues (allocentric strategy) as repro- ited alleys, accuracy of the traveled path (percentage of distance
ducing the sequence of body turns (sequential egocentric strat- error, DE), mean speed, and performed rotations parameter
egy) would not lead to the goal. We quantified the number of (PR).
successful trials for each participant, i.e., the number of direct To define the number of visited alleys, we counted all the
paths from the departure to the goal. alleys participants visited during each trial. Therefore, number
The egocentric version of the Starmaze task (Fig. 1B2) is as of visited alleys included departure alley, all visited central and
follows: all environmental cues were removed to force the par- peripheral alleys (not containing the goal), and the goal alley.
ticipants to reproduce previously performed sequence of body- DE was calculated by subtracting the length of the ideal
turns, thus to navigate using a sequential egocentric strategy. path (ideal path length, IPL) from the length of the traveled
Participants had to do three trials in this egocentric version. path (traveled path length, TPL). We normalized this measure
The order of the egocentric and the allocentric versions of by dividing it by IPL to allow the comparison of the accuracy
the task were counterbalanced among the subjects (see Table 1 of different paths that do not have an identical ideal path
for the succession of trials). length (IPL), as it was the case in probe tests.

TPL  IPL
The control experiment DEð%Þ ¼ 3100
IPL
The task was realized in the same virtual environment as
described above. All participants first realized five training tri- Mean speed was calculated by dividing the TPL by the time to
als and then received one imposed version of the task: 13 reach the goal for each trial.
participants received the allocentric version and 10 partici- PR corresponded to the difference between the sum of abso-
pants received the egocentric version (see Fig. 6A for the lute angles made with the joystick during the navigation (per-
order of the trials). The maximum time for each trial was 90 formed angle, PA) and the minimal amount of angles necessary
seconds. to reach the goal via the ideal path (minimum angle, MA) and

Hippocampus
SEQUENTIAL EGOCENTRIC AND ALLOCENTRIC STRATEGIES 1203

FIGURE 2. Training trials. Performance parameters (number mum number of alleys to visit to get to the goal (alleys 1-10-8-7).
of visited alleys, percentage of distance error, DE) and mean speed B. Learning curve for the percentage of distance error, plateau is
(PR) for all participants (n 5 50). A. Learning curve for the num- reached after trial four at 20.00 6 5.2%. C. Evolution of mean
ber of visited alleys: plateau is reached after training trial four at speed of navigation during training trials: a plateau is reached af-
4.51 6 0.11 alleys (mean 6 SEM). Number of visited alleys ter four trials, at 128.58 6 2.06 virtual m 3 s21. D. Succession of
included departure, all visited central and peripheral alleys (not training trials (Tt) and probe trials (Pt): each participant per-
containing the goal), and the goal alley. Therefore, 4 is the mini- formed 16 training trials and five probe trials (see also Table 1).

therefore corresponded to the visual scan performed by the par- tions (ANOVA F(1,48) 5 0.0051; P 5 0.943). Splitting the
ticipants: the more the participants had looked around by mak- strategy classification between male versus female gave similar
ing turns with the joystick, the higher the rotation parameter, results (Chi square test: v2 5 1.843; df 5 3; P 5 0.606). Dur-
thus this measure gave an indication of the visual exploring ing Task 2, when forced to use the allocentric or the sequential
activities of the participant. egocentric strategy, males and females performed equally well
In the Results section, all performed ANOVAs are (one- or from the first trial (ANOVA, F(1,46) 5 0.801, P 5 0.376 for
two-way) repeated measures ANOVAs. 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.
Debriefing For the control experiment, we controlled for sex differences
After completion of the task, participants were debriefed. in a two-way repeated measures ANOVA (with trial and sex as
They were asked to draw the environment and to indicate, factor) and report no differences between male and female par-
with arrows, the path they had used most to reach the goal. ticipants, F(1,11) 5 1.575 P 5 0.235 for the allocentric version
We had not told the participants beforehand that they would and F(1,8) 5 0, P 5 1 for the egocentric version.
be asked to draw the environment in order not to influence
their memorizing during the task. Task 1: The Multiple Strategy Version of the
For the control experiment we additionally asked for the Starmaze Task
imposed egocentric version if participants had imagined the
location of landmarks to solve the 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
RESULTS 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
Sex percentage of distance error (DE) (Fig. 2B) and 128.6 6 2.1
virtual m*s21 for the speed (Fig. 2C).
We have performed parametric statistical analysis including
all participants for all experiments. Male (n 5 31) versus
Participants used three different strategies:
female (n 5 19) comparison showed no significant differences
Allocentric, sequential egocentric, and mixed
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)] The first probe test took place after the fifth trial, i.e., after
distance error (F(1,48) 5 0.59; P 5 0.448) nor on speed participants reached stable performances. Testing for differences
(ANOVA F(1,48) 5 0.325; P 5 0.571), nor on performed rota- between a training trial and a consecutive probe trial (training

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1204 IGLÓI ET AL.

FIGURE 3. A. Probe tests: three different strategies were spon- maze. The asterisk represents a significant difference between allo-
taneously used by the participants. From left to right: (i) allocen- centric and egocentric strategy users at the beginning of the trial
tric paths performed during the probe test. The participants navi- [ANOVA F(1,19) 5 9.91, P 5 0.005, post hoc test (P < 0.001)]. C.
gate on behalf of environmental cues to the goal located in alley Percentage of distance error (DE) to an ‘‘ideal path’’ to reach the
7. (ii) sequential egocentric paths. The participants reproduce the arrival point split by strategy used to navigate. D–E. Evolution of
same sequence of body turns than during training trials and navi- mean speed and performed rotations (PR) with the joystick for
gate to the goal located in alley 1. (iii) mixed paths. The partici- training trials. Within PR graph: mean speed vs. performed rota-
pants first reproduce the same sequence of body turns as for an tions correlation for all trials. Linear regression showed high corre-
egocentric path and then correct the trajectory using environmen- lation (Pearson product moment correlation R 5 20.88 P <
tal cues, to finally reach the goal that is reached by the allocentric 0.0001). There was no difference among the strategies for DE,
strategy users (at the end of alley 7). B. The amount of rotations whereas allocentric strategy users navigated more slowly (ANOVA
performed in each zone of the maze: allocentric strategy users per- F(2,33) 5 11.395, P < 0.001) and performed more rotations
form a high amount of rotations at the start of the first alley. Ego- (ANOVA F(2,33) 5 31.578, P < 0.001) during training trials than
centric strategy users perform few rotations along the path. Mixed egocentric or mixed strategy users.
strategy users perform more rotations in the central zones of the

trial 5 and probe test 1) showed no difference for distance error  Participants navigating based on environmental cues reached directly
(P 5 0.36; Mann-Whitney rank sum test), indicating that par- the goal in alley 7. This corresponds to the allocentric strategy.
ticipants’ performance was not significantly different between  Participants reproducing the same sequence of body turns
probe tests and training trials. during the probe test than during training trials reached the
Participants performed five probe tests. We observed three goal in alley 1. This corresponds to the sequential egocentric
kinds of behavior and no other ones (Fig. 3A): strategy.

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SEQUENTIAL EGOCENTRIC AND ALLOCENTRIC STRATEGIES 1205

FIGURE 4. A. Percentage of participants using an allocentric, se- performed more than one type of path during probe tests are shifters
quential egocentric or mixed strategy for each probe test (from 1 to (n 5 15, 30%). C. Classification of the shifts performed by ‘‘shifters’’:
5). Each strategy is used all along the task from the first to the last type and number of spontaneously performed shifts during the ‘‘mul-
probe test. B. Classification of participants according to the paths they tiple strategies’’ version of the task. We evaluated the direction of the
performed during the five probe tests: participants who performed five performed shifts, considering that mixed paths involved more allo-
allocentric, sequential egocentric, or mixed paths were classified thetic information than an egocentric path, and more idiothetic infor-
respectively as allocentric (n 5 7, 14%), sequential egocentric (n 5 mation than an allocentric path. [Color figure can be viewed in the
21, 42%), and mixed (n 5 7, 14%) strategy users. Participants who online issue, which is available at www.interscience.wiley.com.]

 Other participants started the trial by performing the previ- mixed): P 5 0.665] (Fig. 3D). To assess for any differences
ously realized body turns (corresponding to the sequential between learning performance of the strategies we have per-
egocentric strategy), but reoriented themselves during the formed a two-way repeated measures ANOVA on % of dis-
navigation using environmental cues (corresponding to the tance error with trial and strategy as factors on results presented
allocentric strategy) and reached alley 7. We named this in Figure 3C (F(2,33) 5 1.76, P 5 0.19). We conclude that
strategy the ‘‘mixed’’ strategy. there is no difference among egocentric, allocentric, and mixed
strategy users during the training trials. The three strategies
The allocentric strategy was characterized by an increase in
were therefore equally performing in solving the task.
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,
Allocentric and Sequential Egocentric Strategies
P < 0.001) (Fig. 3B, left column) and correlated with a
Were Both Used During the Early Phase of the
decrease in the execution speed of the task (two-way ANOVA
Learning Process and Shifts Between Strategies
with trial and strategy as factors: F(2,33) 5 11.395, P < 0.001,
Were Bidirectional
post hoc test allocentric vs. egocentric: P < 0.001) (Figs.
3D,E). By contrast, sequential egocentric strategy was character- Allocentric, sequential egocentric, and mixed strategies were
ized by a rapid execution of the sequence of body movements used from the first probe test. A majority of participants used
leading to the goal (Fig. 3D) with no specific observations of the sequential egocentric strategy (Fig. 4). The three strategies
the landmarks (Fig. 3B, middle column). The mixed strategy were also all used by participants during the four other probe
was characterized by an intermediate profile between allocentric tests (Fig. 4A).
and sequential egocentric strategy: participants observed envi- Participants who had performed five egocentric, five allocen-
ronmental landmarks at the beginning of the probe trial (how- tric, or five mixed paths during the five probe tests were named
ever, less than allocentric but more than egocentric learners) egocentric, allocentric, or mixed strategy users, respectively. The
(Fig. 3B, right column) and speed is equivalent to the egocen- participants who had performed more than one kind of trajec-
tric speed [same ANOVA as above, post hoc test (egocentric vs. tory during the five probe tests were classified as shifters.

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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 ple strategy version of the Starmaze task, performed above
egocentric strategy users, 7 (14%) were pure allocentric strategy chance level when they were challenged to use either only the
users, and 7 (14%) were mixed strategy users. Fifteen partici- allocentric or only the egocentric strategy of the task (Fig. 5B).
pants (30%) were shifting from one strategy to another during Imposed allocentric version is as follows: trial-by-trial analy-
the five probe tests (Fig. 4B). sis (one-way ANOVA) showed that there was no significant dif-
All types of shifts between strategies were observed. Shifts ference between the four groups (egocentric, allocentric, mixer,
occurred from the use of more environmental cues (allocentric and shifters) for neither of the trials (Trial 1: F(3,46) 5 2.999,
strategy) to the use of more body-related cues (sequential ego- P 5 0.041, post hoc tests (Holm-Siddack method) showed no
centric strategy) or vice versa. We report 15 shifter participants, significant differences; Trial 2: F(3,46) 5 1.43, P 5 0.23; Trial
(see Table 2 for a detail of the shifts): 3: F(3,46) 5 0.889, P 5 0.454; Trial 4: F(3,46) 5 0.951, P 5
0.424).
 Three participants shifted once from a more allocentric to a
Imposed egocentric version is as follows: trial by trial analysis
more egocentric strategy.
showed that there was no significant difference between the
 Six participants shifted twice (one time from a more allocen-
four groups (egocentric, allocentric, mixer, and shifters) for nei-
tric to a more egocentric strategy and one time from a more
ther of the trials (Trial 1: F(3,46) 5 0.869, P 5 0.467; Trial 2:
egocentric to a more allocentric strategy).
F(3,46) 5 0.466, P 5 0.71; Trial 3: F(3,46) 5 1.660, P 5
 Six participants shifted once from a more egocentric to a
0.193).
more allocentric strategy.
There was no order effect on the allocentric and egocentric
This means that 3 1 6, i.e., 9 participants out of 50 (18%) versions of the task. Testing for the difference between imposed
shifted from more allocentric to more egocentric strategies and egocentric performance if realized first versus imposed egocen-
6 1 6 participants out of 50 (24%) shifted from more egocen- tric performance if realized after imposed allocentric perform-
tric to more allocentric strategies (Fig. 4C). 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).
Task 2: Imposing the Strategy to Use
Allocentric and Egocentric Versions of
the Virtual ‘‘Starmaze’’ Task The Control Experiment
Above chance performances were reported from the first trial We analyzed the percentage of successful (direct) and unsuc-
of these imposed strategy tasks in both allocentric and egocen- cessful (indirect and failed) trials for each task (Figs. 6B,C). All
tric versions (Figs. 5A,B) (one-way ANOVAs compared with performances were above chance level (i.e., 25%). For the allo-
chance-level for allocentric version F(4,47) 5 37.399, P < centric version mean performance was 89.7,436 6 3.457%
0.001, for egocentric version F(4,47) 5 39.699, P < 0.001). All (one-way ANOVA F(5,12) 5 14.072 , P < 0.001) (Fig. 6B).
participants, whatever the strategy they were using in the multi- 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 tric versions. Right percentage of successful trials (mean 6 SEM)
Starmaze. A. Schematic representation of the allocentric and ego- during the allocentric and egocentric version of the Starmaze, split
centric versions of the virtual Starmaze with the surrounding views by strategy. ANOVA and all pair-wise post hoc comparison showed
of the maze. B. Left percentage of success for each allocentric and sequential egocentric strategy users perform poorer than correcting
sequential egocentric trial. A successful trial consists of a direct strategy users (P < 0.05). Chance-level being to enter randomly
path to the goal location and chance-level is to enter randomly one of the four peripheral alleys, all performances were above
one of the four open alleys (25%). Performances are high above chance level (P < 0.05).
chance level from the first trial of the allocentric and the egocen-

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 2007). Previous navigation studies in humans, focusing on
is no trial effect for the egocentric version of the task (ANOVA spontaneous choice when multiple spatial strategies were avail-
F(5,8) 5 0.649 P 5 0.664); there is a trial effect for the allo- able during the learning of a navigation task, distinguished
centric version (repeated measures ANOVA F(5,11) 5 2.631, P between response (simple egocentric) and allocentric strategies
5 0.02) though all pair-wise post hoc tests gave insignificant (Iaria et al., 2003) but not between sequential egocentric and
results. 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
Debriefing Analysis
to have a range of clearly definable navigation strategies, repro-
Participants had to draw on a blank paper sheet the environ- ducible by all participants. This was done to maximize the
ment after the experiment. The analysis of the drawings interpretability of the navigation trajectories. Therefore we
revealed that 84% (42 participants out of 50) drew landmarks deliberately chose starting positions and one goal locations
positioned in correct order. Hundred percentage of allocentric identical for all the participants. Participants learned the task
and 86% of mixed strategy users, 81% of sequential egocentric using three distinct strategies: the allocentric, the sequential
strategy users, and 80% of shifters did so. Participants were egocentric, and a mixed strategy (Fig. 3A).
also asked to draw the path they had most often performed.
Ninety percentage (45 participants out of 50) drew the correct Allocentric Strategy Relies on the
path. 100% of allocentric and mixed strategy users, 81% of se- Representation of the Relationships
quential egocentric strategy users, and 93% of shifters drew the Between Environmental Landmarks
correct path. Therefore, we showed that all participants have
Our results on the rotations performed by the subjects
encoded information about the landmarks of the environment.
showed that allocentric strategy users performed rotations at
Results also indicated that participants had memorized the
the beginning of the start alley and not at the entrance of the
sequence of turns they had to do in the maze whatever the
goal alley (see Fig. 3B, left column), indicating that they ori-
strategy they used.
ent themselves at the beginning of the trials and do not locate
For the control experiment all participants who had to per-
the arrival according to the view of the arrival arm. This
form the egocentric version of the task (n 5 11) gave negative
behavior appears consistent with the position of the land-
answer when asked if they had imagined the location of land-
marks, which are never placed at the end of the alleys but
marks to solve the task.
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
DISCUSSION
memorized by the participants and that the allocentric repre-
sentation encoded by participants relies on the representation
The current study was based on the starmaze paradigm that
of the relationships between environmental landmarks.
allows spontaneous choice between allocentric (or map-based)
and/or sequential egocentric (or route-based) strategies. Two
Sequential Egocentric Strategy Requires
major points emerge from this study. First, sequential egocen-
Memorizing a Temporal Sequence of
tric and allocentric strategies were used from the onset of the
Context-Response Associations
training period and subjects using either strategy solved the
navigation task with equal performance. The second main find- To get from one peripheral alley to the goal alley in the Star-
ing of the present study is the existence of bidirectional shifts maze, sequential egocentric behavior involves remembering
between the two strategies independently of the training phase. three successive body turns associated with three spatially dis-
In particular, we observed shifts from sequential egocentric to tinct but successive choice points. Indeed, the participant had
allocentric strategy as often as allocentric to sequential egocen- to associate a specific body direction at each choice point and
tric shifts. Overall, these results suggest that subjects acquired then to organize these three movements sequentially. Impor-
different types of spatial knowledge in parallel. 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
Spontaneous Strategy Preference
temporal sequence of body turns has to be learnt. This notion
to Solve the Task
of temporal organization of multiple S–R is here the key point
Maze tasks that involve navigating along alleys (and not in differentiating the sequential egocentric strategy from a simple
an open space) such as the cross maze, the radial arm maze, or response strategy as defined by Packard and Mc Gaugh (1996).
the starmaze, have been proven reliable in identifying the strat- That is, the sequential egocentric strategy requires a sequential
egy used relying on the path chosen both in animals (Packard ordering of events, possibly sharing a similarity with episodic
and McGaugh, 1996; Rondi-Reig et al., 2006) and in humans memory in this regard. The difference in the nature of the ego-
(Iaria et al., 2003; Astur et al., 2004; Etchamendy and Bohbot, centric strategy described in the starmaze (i.e., sequence mem-

Hippocampus
SEQUENTIAL EGOCENTRIC AND ALLOCENTRIC STRATEGIES 1209

ory rather than simple S–R associations) might well account drive the flexible behavior required when rotations of the de-
for its parallel encoding with the allocentric strategy. 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
A Coexistence Between Allocentric and
thought that allocentric knowledge may drive both the allocen-
Sequential Egocentric Strategies?
tric and the egocentric response if people had imagined the
Several results suggest a possible coexistence of allocentric removed cues when performing the cue elimination control
and sequential egocentric strategies. First, the existence of the tests. We debriefed the participants and nobody mentioned
mixed strategy favors the hypothesis of parallel information having imagined environmental features during the cue removal
processing during a given trial as mixer participants do first use task but all reported to reproduce the sequence of learned
an egocentric knowledge to go directly to the egocentric goal movements.
and then correct their trajectory according to allocentric knowl- In addition, a very large majority of the participants (84%;
edge to reach the allocentric goal. Second, by asking the partic- more specifically 81% of spontaneous egocentric strategy users)
ipants to draw the environment, we probed the ability to recall spontaneously positioned landmarks on their drawings, demon-
information needed for allocentric behavior, whereas asking strating that allothetic information was indeed encoded. Ninety
participants to draw their sequence of movements, we probed percentage of the participants were able to retrieve correct idi-
the memory of the route necessary to perform the sequential othetic information about their navigation, as evidenced by
egocentric strategy. Third, performances on the imposed allo- their ability to draw the correct path. Interestingly, 100% of
centric and imposed egocentric versions of the task informed allocentric strategy users drew the correct path. On the whole,
on parallel learning of both strategies. drawing analyses comfort our hypothesis of coexisting naviga-
When forced to use a strategy that was not used during the tion strategies.
training (Task 2), nonshifter participants immediately suc- These different results therefore suggest that participants did
ceeded above chance level (Fig. 5B) in using a previously not acquire both allocentric and egocentric knowledge from the be-
used strategy. As participants were not informed of the switch ginning of the training period and that they could flexibly use
to the imposed allocentric or the imposed egocentric task, the them depending on the requirement of the task.
first trial served as the trial informing participants of the task
switch. Focusing on Trial 2 of imposed allocentric or imposed
Bidirectional Shifts Between Sequential
egocentric protocol, we showed no significant difference
Egocentric and Allocentric Strategies
between the four groups (egocentric, allocentric, mixer, and
shifters). This therefore suggests that the egocentric group did All strategies were spontaneously used from the beginning of
learn the allocentric strategy in parallel to the sequential ego- the practice. Therefore, egocentric paths were observed from
centric strategy and the allocentric group did learn the sequen- the first probe trial as well as allocentric and mixed strategies.
tial egocentric strategy in parallel to the allocentric strategy. With practice, 30% of the participants shifted from one strat-
We also performed the control experiment on two groups of egy to another. In our task a shifter participant corresponded
participants at the very beginning of the training period to to a participant who changed strategy between the different
assess whether both strategies are learnt after the initial learn- probe tests, thus did not use the same strategy throughout the
ing. Following five training trials, the first group of participants whole task. As it was the case in Iaria et al. (2003) using the
performed a test in which we removed all the environmental eight-arm radial maze, we showed that normal participants
cues to assess the ability of participants to reproduce previously spontaneously adopted different navigational strategies and we
performed sequence of body turns. As shown on Figure 6B, also observed the traditional shift from allocentric to egocentric
89.7 6 3.5 of the participants were able to reproduce the cor- strategy [18% in our case vs. 39% in Iaria et al. (2003)]. This
rect and direct sequence of movements, therefore using route also corroborates what had been first demonstrated in rats using
knowledge to perform the task. Similarly, we performed a test a T-maze paradigm, i.e., a shift from allocentric to response
of cue rotation with another group of subjects at the very be- strategy with increasing practice of the task (Packard and
ginning of the training. We also observed that 93.3% of sub- McGaugh, 1996). However, no participants shifted from ego-
jects are perfectly able to use the interrelationships between centric to allocentric strategy in Iaria et al. (2003), whereas
environmental cues as they are perfectly able to find the loca- 24% of our subjects shifted from sequential egocentric to allo-
tion of the goal whatever the performed rotation (departure centric strategy in our case. Shifts toward a more procedural
from alley 9 or departure from alley 3). strategy may occur as a result of habit formation, which gener-
These two experiments strongly suggest conjunct learning of ally refers to a great number of automatic and unconscious rep-
both allocentric and sequential egocentric strategies from the etitions of a given S–R behavior over time (Mishkin et al.,
beginning of the training and do not result of overtraining. 1984; White and McDonald, 2002). In our study, the shifter
This raises the question whether the same knowledge could participants did not repeat the same strategy throughout the
drive the allocentric and the egocentric strategies. We actually task; during the five probe tests they used at least two different
doubt that the egocentric knowledge only (i.e., the memory of strategies. Further, shifts were reported in both directions (Fig.
temporal relations between specific environmental choices) may 4C). These results strongly suggest no hierarchy or practice-

Hippocampus
1210 IGLÓI ET AL.

dependant development of strategies and indicate that sequen- term of spatiotemporal organization independently on the na-
tial egocentric learning did not result from habit formation or ture of the memorized information rather than in terms of spa-
response learning. In addition, equal learning performance of tial versus nonspatial memories (Eichenbaum and Cohen,
all strategies and the variability in the shifts performed by the 2001). With such a former dichotomy sequential egocentric
participants further comforts that in the Starmaze task one strategy might be considered as sharing some functional proper-
strategy is not more efficient than the other one. ties of the episodic memory system.
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 CONCLUSION
multiple memory systems, as it was previously suggested by
Burgess (2006). In conclusion, this study demonstrates that subjects acquire
This is also consistent with Voermans et al.’s study (2004) different types of spatial knowledge in parallel, i.e., knowledge
reporting psychophysiological interaction between the anterior permitting allocentric navigation as well as knowledge permit-
caudate nucleus and the medial temporal lobe related to the ting sequential egocentric navigation. The results show the im-
route recognition versus visuomotor control condition in con- portance of providing detailed description of the route-memory
trol subjects. As mentioned by the authors, ‘‘this effect reflects system, in particular to distinguish between a simple egocentric
a stronger correlation of activity in the control group between (response) and a sequential egocentric strategy, the second one
the right caudate nucleus and the anterior hippocampus in being used early during training as the allocentric one. This
route recognition compared to visuo-motor control.’’ Parallel suggests that the distinction between navigation strategies might
activation of the two memory systems, i.e., the one dependent be larger than between response strategy and allocentric strategy
on the hippocampus and the one dependent on the caudate and may include the distinction between simple and sequential
nucleus could support a possible generalization of our finding. egocentric strategy. Inside this latest distinction, the simple ego-
These different results do not question the involvement of centric (response) strategy would be dependant of the proce-
the hippocampus in the allocentric learning neither the role of dural memory system whereas the sequential egocentric strategy
the striatum in response (simple egocentric strategy) learning. would also involve the episodic memory system.
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 Acknowledgments
response learning and sequential egocentric learning questions The authors thank Dr. Catherine Thinus-Blanc for critical
the possibility that different neural bases may sustain these two reading of the manuscript. The authors also thank Céline Pous-
learning processes. In particular, we recently proposed (Rondi- sineau and Tristan Moreau for their help designing the Matlab
Reig et al., 2006) that a cooperation between hippocampal and analysis software, Safi Saada and Philippe Barbot for the virtual
striatal systems might be required during sequential egocentric environment.
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
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