Zhang 2012

r Human Brain Mapping 00:000–000 (2012) r
Human Neural Systems Underlying Rigid and

Flexible Forms of Allocentric Spatial
Representation
Hui Zhang and Arne Ekstrom*

Department of Psychology, Center for Neuroscience, University of California, Davis, California
r r
Abstract: Previous studies suggest the importance of medial temporal lobe, areas of parietal cortex,
and retrosplenial cortex in human spatial navigation, though the exact role of these structures in repre-
senting the relations of elements within a spatial layout (‘‘allocentric’’ representation) remains unre-
solved. Hippocampal involvement, in particular, during memory processing is affected by whether a
previously formed representation is employed in a novel fashion (‘‘flexible’’ usage) or in a manner
comparable with how it was encoded originally (‘‘rigid’’ usage). To address whether brain systems are
differentially involved during flexible vs. rigid utilization of a pre-existing allocentric representation,
subjects encoded the position of six different target buildings relative to a centrally located landmark
building in a virtual city seen from an aerial view. They then actively searched for the locations of
these target buildings using the landmark (rigid retrieval) or using a previously shown target building
in a novel fashion (flexible retrieval) while undergoing fMRI. Activations in posterior superior parietal
cortex and precuneus were greater during more rigid than flexible forms of allocentric retrieval while
activation in the hippocampus decreased linearly over blocks during flexible allocentric retrieval. A
functional connectivity analysis further revealed significant interactions between hippocampus and
these parietal areas during flexible compared with rigid allocentric retrieval. These results extend pre-
vious models of the neural basis of spatial navigation by suggesting that while the posterior superior
parietal cortex/precuneus play an important role in allocentric representation, the hippocampus, and
interactions between hippocampus and these parietal areas, are important for flexible utilization of
these representations. Hum Brain Mapp 00:000–000, 2012. VC 2012 Wiley Periodicals, Inc.
Key words: hippocampus; parahippocampus; retrosplenial; posterior superior parietal cortex; spatial
navigation; spatial memory; partial learning paradigm
r r
INTRODUCTION
Additional Supporting Information may be found in the online Navigation is a central component of our daily lives and
version of this article. the ability to locate ourselves in space is important to our
Contract grant sponsors: Alfred Sloan Foundation; The Hellman
survival. Navigation, particularly successful way-finding,
Young Investigator Award. has been hypothesized to rely in part on ‘‘cognitive
*Correspondence to: Dr. Arne Ekstrom, Center for Neuroscience,
maps,’’ which refer to spatial representations referenced to
UCDavis, 1544 Newton Ct., Davis, CA 95618. external coordinate systems. Repeated trajectories through
E-mail: adekstrom@ucdavis.edu an environment allow us to build up a representation in-
Received for publication 20 August 2011; Revised 15 September dependent of our heading that becomes referenced to
2011; Accepted 6 October 2011 external landmarks (‘‘allocentric’’) rather than our body
DOI: 10.1002/hbm.21494 position (‘‘egocentric’’), thus providing one means of form-
Published online in Wiley Online Library (wileyonlinelibrary. ing a cognitive map [Klatzky, 1998; O’Keefe and Nadel,
com). 1978; Sholl, 1987; Tolman, 1948]. An example of this would
V
C 2012 Wiley Periodicals, Inc.
r Zhang and Ekstrom r
be remembering the location of a restaurant you enjoy the importance of cortical rather than direct hippocampal
based on the fact that it is located 1/3 of the way between involvement in allocentric representation.
a street corner and a supermarket you frequent. Another In contrast, several fMRI studies involving free naviga-
means of extracting the relations between landmarks in a tion of a spatial environment provided evidence for hippo-
spatial layout is by viewing or learning their interrelations campal and parahippocampal involvement in forming ‘‘on-
from an aerial perspective or cartographic map [Siegel and the-fly’’ spatial representations of the environment. In a
White, 1975; Thorndyke and Hayes-Roth, 1982; Moeser, study by Hartley et al. [2003], subjects freely navigated in a
1988; Taylor and Tversky, 1992]. The processes of building virtual environment and then explored the environment
allocentric representations has been suggested to depend again while undergoing fMRI. When subjects employed
on brain regions such as the hippocampus [Brown et al., novel paths to get around obstacles, path accuracy within
2010; Goodrich-Hunsaker and Hopkins, 2010; Goodrich- and between subjects was associated with greater hippo-
Hunsaker et al., 2010; Hartley et al., 2003; Igloi et al., 2010; campal activation. Similarly, when subjects used a spatial
Maguire et al., 1998b; O’Keefe and Nadel, 1978; Parslow strategy (remembering the locations of landmarks in a vir-
et al., 2004, 2005; Suthana et al., 2009], retrosplenial/supe- tual maze), Iaria et al [2003] found greater hippocampal
rior posterior parietal cortex [Burgess et al., 2002; Epstein, activation compared with randomly searching for objects
2008; Rosenbaum et al., 2004; Shelton and Gabrieli, 2002; placed around the maze [see also: Aguirre et al., 1996; Par-
Shelton and Pippitt, 2007; Wolbers and Buchel, 2005], parslow et al., 2004; Shipman and Astur, 2008; Suthana et al.,
ahippocampal cortex [Committeri et al., 2004; Galati et al., 2009; Brown et al., 2010]. Similar results have also been
2010; Jordan et al., 2004; Maguire et al., 1998a; Shipman obtained for ‘‘free’’ mental navigation of recently learned
and Astur, 2008], and precuneus [Committeri et al., 2004; spatial environments, although the inferences of these stud-
Galati et al., 2010]. These previous studies have employed ies are necessarily limited by the fact that it is impossible to
environments with which subjects have had varying precisely monitor subjects’ actual movements during imagi-
degrees of familiarity (e.g., a well-learned environment vs. nation [Ghaem et al., 1997; Mellet et al., 2000]. As a whole,
a novel environment) and have utilized different degrees the inference from these studies is that subjects with better
of first-person vs. map-based learning (e.g., subjects topographical representations formed ‘‘on-the-fly’’ during
directly navigating or subjects viewing layouts from an free navigation utilized their hippocampus to a greater
aerial perspective and/or attempting to draw maps), all of degree [see also Voss et al., 2010].
which could potentially influence the relevant brain Consistent with the idea that map-learning and free navi-
regions involved reported. Thus, the extent to which first- gation possibly induce different types of representations,
person vs. aerial perspectives and familiar vs. novel spatial previous cognitive work suggests differences between in-
environments influence regional brain involvement in allo- formation learned from route-based navigation vs. learning
centric representation remains an open question. and retrieving information from maps. Evans and Pezdek
Previous fMRI studies demonstrating the involvement of [1980], in a finding subsequently replicated in several stud-
retrosplenial and superior posterior parietal cortex in allo- ies, found that recalling the positions of elements within
centric coding often, explicitly or implicitly, involved some both familiar maps (United states) and maps of recently
degree of reliance on cartographic maps. Wolbers and learned layouts (an unfamiliar campus) showed a strong
Buchel [2005] had subjects view videos of navigation degree of dependence on the original learned perspective,
through a virtual environment and then draw aerial maps such as north vs. south orientation [Evans and Pezdek,
of the environment following their fMRI session, providing 1980; Levine et al., 1984; Presson et al., 1989; Richardson
a putative measure of the geometric relation of landmarks et al., 1999; Shelton and McNamara, 2004]. In contrast,
to each other (‘‘survey knowledge’’). Following each recalling information following free navigation showed less
encoding session, subjects also indicated the relative loca- perspective dependence [McNamara et al., 2003; Sholl,
tion of a building that appeared next to a landmark (right, 1987]. These findings argue for the idea that map-learning
left, or behind). Retrosplenial activation correlated with may result in view-dependent representations that are com-
improvements in performance across sessions, leading the paratively inflexible to manipulation in contrast to route
authors to infer a greater involvement of retrosplenial cor- learning. Together, these studies suggests that map-learn-
tex in map representation compared with hippocampus. In ing and route learning could have differential effects on
a similar vein, Rosenbaum et al [2004] looked at relative how we structure our spatial representations [Thorndyke
and absolute distance judgments (as well as other meas- and Hayes-Roth, 1982].
ures) of experienced Toronto navigators. Participants, who Because the degree of map-learning and route learning
had extensive experience navigating Toronto (and likely may differentially affect spatial representations, this could,
viewed maps at some points as part of learning the city) in turn, possibly affect neural representations of spatial
showed significant retrosplenial and parahippocampal layouts [Shelton and Gabrieli, 2002; Shelton and Pippitt,
activation, but no hippocampal activation, during all three 2007]. In attempt to better understand how map-learning
types of judgment tasks relative to a perceptual baseline vs. free (first-person) navigation affect neural representa-
task [see also Epstein and Higgins, 2007; Epstein et al., tions, we wished to study the converse situation of what
2007; Shelton and Pippitt, 2007]. These findings argue for has often been studied previously [Rosenbaum et al., 2004;
r 2 r
r Different Forms of Spatial Representation r
Wolbers and Buchel, 2005]: how people navigate a spatial wall (40 virtual units in radius and 5 virtual units in height),
environment following learning a spatial layout using aerial- sky, and clouds. A landmark store was located at the center
view snap-shots. We reasoned that this manipulation could of the circle; the four sides of the landmark were different
potentially provide insight into how subjects utilize a novel colors (black, blue, pink, and green) and could easily be dis-
representation formed during simulated map-learning tinguished from both the aerial view and first-person navi-
(learning from an aerial perspective) when they subse- gation (see Fig. 1A–C). Surrounding the landmark were six
quently utilize these representations ‘‘on-the-fly’’ during stores, which were arranged irregularly on an invisible con-
free navigation. We did this by having subjects first study centric circle (30 virtual units in radius). The entire layout
aerial views of the spatial relations between buildings was contained within the circular wall (see Fig. 1C).
(‘‘stores’’) arranged around a centrally placed landmark The locations of the stores on the invisible circle relative
building (‘‘the landmark’’). We then employed fMRI to to the landmark store were the same every trial; however,
study neural activity while they freely searched for these a seventh store, used as part of our control condition,
stores during two critical searching conditions. A rigid re- appeared in a random location every encoding trial and
trieval condition involved finding the hidden target store therefore was not possible to represent relative to the land-
by referencing to its position relative to the landmark mark. The rules regarding the position of the randomly
learned previously from the aerial viewpoint. Thus, other located store were that (a) its location was randomized
than having to transfer knowledge from the aerial to first- each trial that it appeared in the scene during both the
person viewpoint, this condition closely matched how they encoding and retrieval session (b) its position never over-
had learned it from the previous aerial view. A flexible re- lapped with the position of other stores. Subjects learned
trieval condition also involved finding the hidden target the positions of stores relative to the central landmark
store but referenced to the location of a previously learned from an aerial view 78 virtual units above the center of the
store rather than the landmark. In this condition, subjects virtual city (Fig. 1A). We employed a partial learning para-
utilized their pre-existing spatial representation in a novel digm in which subjects viewed a set of configurations one
fashion, because, in addition to transferring their knowl- by one, comprised of a store seen in conjunction with the
edge from the aerial to first-person viewpoint, they had to centrally located landmark and a randomly located store
extrapolate between different encoding trials to derive the (see Fig. 1A). There were six configurations in each encod-
location of one store relative to the other. We additionally ing block with one configuration for each store. There
conducted two control conditions and a baseline task, were six encoding blocks in total; the order of configura-
which we describe in more detail in the methods. We ana- tions within each encoding block was randomized and
lyzed concurrently acquired fMRI data to determine brain each configuration appeared for 6 s.
regions active during flexible vs. rigid allocentric retrieval
and additionally employed a functional connectivity to
assess interactions between relevant brain regions. Retrieval During Active Navigation
After encoding, we tested knowledge of the spatial layout
MATERIALS AND METHODS of the virtual city by having subjects drive to the locations
Participants of the stores they had just encoded while they underwent
functional imaging. For each trial, the target store was ren-
Seventeen subjects (seven male, ten female) were dered invisible such that they had to reference to external
recruited from the general population in Davis, CA area. landmarks to find its location. Subjects drove to the target
Subjects were free of significant neurological deficits and store in four randomly interspersed conditions.
had no history of psychiatric disorders. All were right- The two primary conditions of interest were the land-
handed and had normal or corrected-to-normal vision and mark condition and store-reference conditions (Fig. 2B).
gave written informed consent to participate in the study, The landmark condition was designed to replicate, as
which was approved by the institutional review board at closely as possible, the conditions under which subjects
the University of California, Davis. One of the subjects had encoded this information from the aerial perspective.
was excluded in the further data analysis because of At the beginning of each trial, subjects were positioned to
excess head movement; another subject was excluded due face the landmark and then navigated to a hidden target
to technical issues with the scanner. The final data set was store using the landmark. The target store was hidden
comprised of fifteen subjects. until subjects were 14 virtual units from it; when they
were within this distance from the target store, it appeared
Experimental Stimuli on the screen and subjects drove directly to it. In the store-
reference condition, at the beginning of each trial, subjects
We used Panda3D software (Entertainment Technology were positioned to face one of the six stores (see Figs. 1C
Center, Carnegie Mellon University) to present a virtual and 2B). Subjects then navigated to the hidden target store
environment consisting of a set of rectangular stores (3.8 using the other store as a reference (the target store was
2.6 2.3 virtual units, length wide height), a circular again invisible until subjects were within 14 virtual units of
r 3 r
Figure 1.
Experimental design. A: Example layouts subjects experienced baseline task, which involved following arrows with the joystick.
during encoding. The red-box indicates the landmark, the blue C: Schematic of the layout of the city from an aerial view. The
box indicates the randomly located store used as part of one of store at the center of the circle was the landmark. The locations
the control conditions, and the yellow box indicates the store of stores on the dashed line were fixed relative to the landmark.
subjects were encoding on that trial. B: An example of a re- Zoomed inset shows actual view of the landmark from an aerial
trieval trial in the landmark condition. Subjects navigated to the view experienced by subjects. [Color figure can be viewed in
hidden target stores using the landmark; navigation occurred the online issue, which is available at wileyonlinelibrary.com.]
from a first-person perspective. Subjects then performed the
its location). Subjects had not previously experienced these (Fig. 1B) for 10 s while movement remained stopped; the
two stores in the same encoding configuration and had to arrow pointed randomly either left, right, up, and down
extract the location of the hidden target store from knowl- [Ekstrom et al., 2009; Stark and Squire, 2001]. The baseline
edge of the different encoding configurations (see Fig. 2A,B task was designed to control for movement unrelated to
for a schematic comparison of the two conditions). active navigation.
In the randomly located store control condition, which
involved finding the seventh randomly placed store they General Procedure
had seen during encoding trials, subjects searched as best
as they could for the randomly located hidden target. This We first placed subjects in a ‘‘mock’’ scanner to accus-
condition was designed to control for the use of an allocen- tom them to virtual navigation in the MRI environment.
tric representation because in this condition, subjects navi- They performed 20 min of practice driving in an unrelated
gated randomly and could not reference to other stores to virtual environment. Subjects then viewed three-dimen-
find the target store. This condition, however, still required sional images of all stores they would subsequently view
continuous updating of one’s bearing to avoid searching in on a gray background to familiarize them with store
the same locations they had previously visited. names and images. Each store appeared for eight seconds
In a second control condition, the visible target condi- and subjects read the name of the store outloud to make
tion, subjects navigated directly to the target store while it sure they could distinguish between the different stores.
was continuously visible to subject; this condition was Subjects then began the encoding session. After encoding,
designed to control for the presence of visually salient subjects were placed in the scanner for the retrieval task.
objects in our task. Subjects started each trial in a random position in the
Finally, in a baseline task, subjects moved the joystick virtual city. This was done to avoid alignment in facing
following the direction of an arrow shown on the screen direction between learning and test phases, which might
r 4 r
Figure 2.
Example subject paths and schematic of store-reference and landmark vs. store-reference conditions. As an example, in the
landmark conditions. A: Examples of paths taken in each condi- landmark condition, subjects navigated to 1st Bank using the
tion of one representative subject. The colored squares were landmark. In contrast, in the store-reference condition, subjects
the positions of each store on the invisible circle (dashed line in needed to use Toy Store as a reference to find the 1st Bank.
Fig. 1c.) while the colored lines were routes the subject Thus, in the store reference conditions, subjects inferred the
employed to find the target store. VT, the visible target condi- position of Toy Store based on their knowledge of its location
tion (control condition); L, the landmark condition; SR, the relative to 1st Bank on the circle (dashed white line). [Color fig-
store-reference condition; RLT, the randomly located target ure can be viewed in the online issue, which is available at
store condition (control condition). B: Schematic illustrating the wileyonlinelibrary.com.]
inadvertently serve as an implicit egocentric retrieval cue block with six test blocks in total. The order of trials in
[McNamara et al., 2003]. We determined the subjects start- each test block was randomized.
ing position on each trial according to the following crite-
ria: (1) the location was randomly generated for each trial, Behavioral Data Acquisition and Analysis
(2) the initial position was at least six virtual units from all
the stores in the scene, (3) the initial position was a mini- During active navigation (the retrieval session in which
mum of 15 virtual units from the target store, (4) subjects we scanned brain activity), we recorded the position and fac-
always faced the landmark at the beginning of the trial in ing direction of subjects every 20 ms into a log file. We ana-
the landmark and two control conditions and faced the lyzed the response accuracy, latency and excess path length
reference-store in the store-reference condition. While for each of the four conditions. The response accuracy was
searching for the target store, subjects were encouraged to the number of trials that subjects successfully found the tar-
take a path as direct as possible and to find a target store get store within the allotted time (30 s) for each condition.
as quickly as possible. Each trial during the retrieval phase Latency was the time interval between the onset of the trial
lasted 40 seconds in total. Subjects searched for the target and the onset of the baseline task following that trial (for cor-
store for 30 s and then performed the baseline task for 10 rect trials only). The excess path length was computed by
s. In cases in which subjects found the target store before taking the deviation of the subject’s actual path from the
expiration of the allotted time, they performed the baseline straightest path to the target, based on the idea that a better
task for the remaining period. There were three trials for representation of the position of the target would lead to
each condition in a block resulting in 12 trials in each test lower excess path length [Newman et al., 2007].
r 5 r
MRI Acquisition large cluster might fail to reveal smaller clusters of signifi-
cant activity within that larger cluster, we additionally
Scanning was performed at the Imaging Research Center conducted voxelwise post hoc t-tests within clusters of
at the University of California, Davis on a 3T Siemens activation revealed by the ANOVA.
(Erlangen, Germany) Trio equipped with a thirty-two-chan-
nel head coil. Forty-three contiguous axial slices were
acquired using a gradient-echo echo-planar T2*-sensitive fMRI Linear BOLD Signal Analysis
sequence [repetition time (TR), 3000 ms; echo time (TE), 29
ms; voxel size, 2.5 2.5 2.5 mm3; matrix size, 88 88 We searched for linear decreases in BOLD across each
43]. Structural T1-weighted images for anatomical localiza- of the four conditions based on previous work suggesting
tion were acquired using a three-dimensional magnetiza- decreases in hippocampal activation over learning blocks
tion-prepared rapid-acquisition gradient echo pulse in particular during navigation [Wolbers and Buchel,
sequence [TR, 1,900 ms; TE, 2.88 ms; inversion time (TI), 2005]. We did this by convolving the HRF with a decreas-
1,100 ms; voxel size, 1 1 1 mm3; matrix size, 256 256 ing linear function over trials.
208]. Visual stimuli were projected onto a screen at the
end of the scanner with an Digital Projection Mercury fMRI Functional Connectivity Analysis
5000HD projector equipped with a three-chip DLP technol-
ogy (Edmund Optics, Barrington, NJ 08007-1380) and We used the beta-series correlation method [Rissman
viewed through a custom in-bore screen (Mag Design and et al., 2004] to analyze whole brain functional connectivity
Engineering, Inc. Sunnyvale, CA 94086) mounted to the relative to seed ROIs. For this analysis, a new GLM matrix
head coil. Responses were recorded using a MR-compatible was constructed to model each trial individually for each
joystick (Current Design, Philadelphia, PA). The linear and subject. Whole brain maps of functional connectivity were
turning acceleration of the joystick were 28 virtual units/s2 generated for each subject by extracting beta values for
and 22 deg/s2, respectively; the full linear and turning each trial from each seed ROI and correlating the mean
speed were 28 virtual units/s and 100 deg/s, respectively. beta values across trials with every other voxel in the
brain [Rissman et al., 2004]. Four seed ROIs were chosen:
parahippocampus, precuneus, retrosplenial, and superior
fMRI Data Analysis parietal lobe. To avoid the possibility of selection bias
Image processing and statistical analysis were per- (‘‘double dipping’’) [Kriegeskorte et al., 2009], we selected
formed using Statistical Parametric Mapping (SPM8, The clusters of activation with our ROIs based on three previ-
Wellcome Department of Imaging Neuroscience, Institute ous studies of navigation using fMRI. No single previous
of Neurology, London, UK). Functional images were cor- study reported clusters of activation in all four ROIs so we
rected for differences in slice timing by resampling slices selected clusters from most relevant papers that contained
in time to match the first slice of each volume, realigned activations in these areas, all of which we have mentioned
with respect to the first image of the scan, and high-pass previously in the Introduction. A study by Wolbers and
filtered to remove baseline drifts. After resampling the Buchel [2005] found activation in retrosplenial cortex [clus-
functional data at 1 x 1 x 1 mm3 and normalizing to the ter centered at (18 -68 60)] and superior parietal cortex
MNI template, the functional data were resliced to their (cluster centered at [-14 -54 58)], a study by Hartley et al.
original 2.5 2.5 2.5 mm3 resolution and smoothed [2003] found activation in precuneus [cluster centered at (6
with a 6 mm full-width at half-maximum (FWHM) iso- -66 33)], and a study by Epstein and Higgins [2007]
tropic Gaussian kernel. Data were first modeled for each reported activation in parahippocampal cortex [cluster
subject individually using a general linear model (GLM) with maximum activation centered in parahippocampal
[Friston et al., 1995]; only correct trials were modeled. This cortex at (20 -36 -6)]. We then created seeds of activation
first-level analysis provided parameter estimates for each by averaging mean signal change based on a sphere of ra-
condition and each subject. These parameter estimates dius 20 mm centered on these coordinates and intersected
were then entered into a repeated-measures, whole brain, with our anatomical regions of interest.
random-effects 1 4 condition (landmark, store reference,
randomly located, and visually guided conditions) Correction For Multiple Comparisons
ANOVA to determine activation patterns across the group.
We extracted the mean signal based on the intersection of For all whole brain analyses (ANOVA and post hoc
clusters revealed by the whole brain ANOVA and specific voxel-wise t-tests), we used a threshold of PFWE < 0.05,
brain areas of interest. We then conducted post hoc t-tests i.e., corrected for family-wise error (FWE). We did this by
comparing the percent signal change within these large calculating the cluster size needed for a threshold of PFWE
clusters between individual conditions. We also conducted < 0.05 using Monte Carlo simulations [Forman et al., 1995]
an additional ANOVA on these signals to see how relative with alphaSim software based on an uncorrected, voxel-
activations between regions might change due to our task. wise P < 0.005. These simulations showed that our thresh-
Because statistical tests on signal change extracted from a old of PFWE < 0.05 corresponded to P < 0.005 with a voxel
r 6 r
TABLE I. The mean (standard deviation) response latency, accuracy, and excess path length of the behavioral data
during test phase
Visible target Landmark Store reference Randomly located

condition condition condition Target Store Condition
Response Latency (s) 14.22 (1.96) 18.49 (1.75) 18.89 (2.47) 16.01 (1.43)
Accuracy 0.91 (0.12) 0.68 (0.18) 0.63 (0.18) 0.78 (0.16)
Excess path length 6.78 (3.87) 8.10 (3.91) 10.07 (4.46) 15.67 (7.76)
extent (k) of 38. For behavioral analyses and post hoc com- as the target, which was significantly higher than a chance
parisons on percent signal change extracted from ROIs, we level of 25% (time: t(14)¼4.42, P < 0.001; path length:
employed an uncorrected P-value of 0.05. t(14)¼5.43, P < 0.001). Similarly, in the store-reference con-
dition, subjects spent 33% of their total searching time and
traveled 33% of their total path in the same quadrant as
RESULTS the target, which was significantly greater than chance
Behavioral Results (time: t(14)¼2.98, P < 0.01; path length: t(14) ¼ 2.97, P <
0.05). Because one possibility is that subjects simply
For all the behavioral indices, there were no differences avoided the most distant quadrant rather than searching
between the landmark and store-reference conditions in the target quadrant, we directly compared searching
(response latency: [t(14) ¼ 0.74, P ¼ 0.47]; accuracy: [t(14) time and total distance traveled in the target quadrant
¼ 1.20, P ¼ 0.25]; excess path length: [t(14) ¼ 1.08, P ¼ compared with the two adjacent quadrants. We found that
0.30]; see Table I; sample paths shown in Fig. 2A,B). Speed subjects searched in the target quadrant at significantly
and accuracy were highly negatively correlated across sub- higher levels than the adjacent quadrants (landmark condi-
jects (r ¼ 0.99, df ¼ 14), indicating that the higher the action: time: t(14) ¼ 3.53, P < 0.005, path length: t(14) ¼ 4.27,
curacy in finding a hidden target store, the faster the P < 0.001; store-reference condition: time: t(14) ¼ 2.19, P <
subject found the target. This indicates there was no 0.05, path length: t(14)¼2.30, P < 0.05). These findings sup-
speed-accuracy trade-off in our data [Fitts, 1954], justifying port the idea that in both the landmark and store-reference
analysis of our reaction time data. As might be expected condition, subjects transferred knowledge from the aerial
for the two control conditions, we found differences in view to the first-person perspective to successfully locate
performance in the randomly located and visually guided target stores. We discuss possible explanations for their
condition. Performance was significantly different in both relatively low accuracy levels on the first blocks of finding
conditions compared with the experimental conditions, the target in the discussion.
which was likely due to the fact that both experimental We then looked at whether performance improved over
conditions required retrieving and manipulating a learned trials during navigation and whether this changed differ-
representation while the control conditions did not neces- entially between the landmark and store-reference condi-
sitate these. We discuss differences in performance, excess tion as a function of retrieval trial. Both conditions showed
path, and latency in the control conditions in detail in the a significant linear increase in accuracy over blocks [see
Supporting Information. We accounted for the differences Supporting Information Figure 1S, F(1,14) ¼ 14.49, P <
in performance in terms of functional activation patterns 0.005 in the store-reference condition; F(1,14) ¼ 4.48, P <
by including only correct trials in each condition; includ- 0.05 in the landmark condition], consistent with the idea
ing subject performance as covariates separately for each that the retrieval conditions involved some degree of new
condition led to identical results. Thus, we include only learning as subjects repeatedly navigated to target stores
analyses using correct trials for further consideration. over blocks. Degrees of learning over blocks did not differ
To ensure that subjects transferred knowledge from the between the two conditions [no interaction effect between
aerial to the first-person perspective, as hypothesized, we conditions and blocks, F(5,70) ¼ 0.903, P ¼ 0.484], suggest-
analyzed their performance on the first trial in which they ing equivalent degrees of new learning in both conditions.
navigated to each target store. We divided their trajectories
for each trial into four different quadrants (the target
quadrant, two adjacent quadrants, and the opposite quad- fMRI Analysis: Involvement of Precuneus and
rant) to assess whether they searched the target quadrant Superior Posterior Parietal Cortex in Rigid
at a level that would be expected to exceed a chance level Allocentric Representation
of searching [Morris et al., 1982]. We averaged the time
spent and distance traveled in each quadrant over all trials Our whole brain ANOVA analysis revealed a large clus-
separately for each subject. We found that in the landmark ter of activation centered in the precuneus and medial
condition, subjects spent 39% of their total searching time temporal gyrus (Fig. 3E and Table 1S). We did not find
and traveled 42% of their total path in the same quadrant significant activation in the hippocampus with our
r 7 r
Figure 3.
ROI analyses illustrating brain regions involved in experimental of activation identified by ANOVA (Table 1S) (PFWE < 0.05). F:
manipulations. VT, the visible target condition; L, the landmark Interaction effect between parahippocampus and retrosplenial
condition; SR, the store-reference condition; RLT, the randomly cortex in the visible target and landmark condition. [Color fig-
located target store condition. A–D: Region of interest analysis ure can be viewed in the online issue, which is available at
for (A) parahippocampal cortex, (B) retrosplenial cortex, (C) wileyonlinelibrary.com.]
precuneus, and (D) superior posterior parietal lobe. E: Clusters
ANOVA comparison. Using these clusters, we then con- [t(14) ¼ 2.01, P ¼ 0.06] in superior posterior parietal cor-
ducted post hoc tests on clusters identified with our tex. Voxelwise post hoc t-tests again confirmed the signifi-
ANOVA analysis in parahippocampus, retrosplenial, pre- cance of activation in superior posterior parietal cortex (30,
cuneus, and superior posterior parietal lobe. -60, 45) and additionally revealed smaller clusters of acti-
Mean percent signal change within all clusters within vation in precuneus (-23, -62, 38) during the landmark vs.
regions of interest (Fig. 3) showed greater activity in the store-reference contrast (see Fig. 4B and Table II). Activa-
landmark condition to be higher than the randomly tion for the visible target control condition was higher
located store control condition [t(14) ¼ 2.86, 2.29, 2.77, and than the randomly located store control condition in para-
2.85, respectively; P < 0.05]. Activation during the store- hippocampus, precuneus, retrosplenial, and superior pari-
reference compared with the randomly located store con- etal lobe [t(14) ¼3.42, 2.66, 3.26, and 3.41, P < 0.05 for all
trol was significantly higher [t(14) ¼ 2.96, P < 0.05] in pre- the comparisons]. In the parahippocampal cortex activa-
cuneus and marginally significantly higher [t(14) ¼ 2.05, P tion in the visible target control condition was also higher
¼ 0.059] in superior posterior parietal lobe. Voxelwise post than the store-reference condition [t(14) ¼ 2.92, P < 0.05];
hoc t-tests (conducted at PFWE < 0.05; see Methods) con- this was not the case in any other brain regions.
firmed the significance of the effect in superior posterior Although the absolute magnitude of activations may be
parietal lobe (-24, -70, 42) and additionally revealed problematic to compare between different brain regions
smaller clusters of activation in retrosplenial cortex (-11, - because areas may differ in terms of raw signal strength
65, 9) during the store-reference vs. randomly located store (e.g., a main effect of ROI), the presence of an interaction
control condition (Fig. 4A and Table II). Activation during effect indicates a relative difference in terms of activations
the landmark compared with the store-reference condition produced by different conditions [Ekstrom and Book-
was significantly higher [t(14) ¼ 2.63, P < 0.05] in the par- heimer, 2007; Epstein and Higgins, 2007; Epstein et al.,
ahippocampal cortex and marginally significantly higher 2007]. We found a significant interaction effect in the
r 8 r
Figure 4.
Post hoc voxel-wise t-tests between conditions of interest. A: Store-reference vs. control con-
trast showing significant activation in retrosplenial cortex (PFWE < 0.05). B: Landmark vs. store-
reference contrast showing precuneus and superior posterior parietal activation (PFWE < 0.05).
[Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
visible target control and landmark condition between par- retrieval compared with the flexible form, implicating these
ahippocampal and retrosplenial cortex (Fig. 3F, F(1,14) ¼ regions specifically in rigid forms of allocentric retrieval (3)
5.177, MSE ¼ 0.004, P < 0.05]); this interaction effect was greater activation in parahippocampal cortex for the rigid
also present between parahippocampal cortex and precu- form of retrieval compared with the randomly located store
neus (F(1,14)¼18.8, P < 0.001) and parahippocampal cortex control condition and the flexible condition, coupled with
and superior posterior parietal cortex (F(1,14)¼42.8, P < greater relative activation in parahippocampal cortex during
0.001). This indicated that retrosplenial, precuneus, and the visible target control condition compared with the land-
posterior parietal cortex activated to a higher degree in the mark condition, implicating parahippocampal cortex more
landmark condition than the visible target control condi- specifically in rigid scene processing compared with the
tion, while the parahippocampal cortex activated to a other three areas we investigated.
higher degree in the visible target control condition than
the landmark condition. We conclude from this that the
two conditions resulted in a different pattern of relative Linear-Effects Analysis Showing Involvement of
activation in the parahippocampal cortex compared with the Hippocampus in Flexible-Allocentric
the other three regions, with parahippocampal cortex Retrieval
showing a greater relative involvement in the visible target
control condition compared with the landmark condition. As described in the methods, we modeled a linear
To summarize the principle results from these analyses, change in activation over blocks to assess whether there
we found (1) greater activation in retrosplenial cortex, poste- was a systematic decrease in brain activation that paral-
rior superior parietal cortex, and precuneus in the two allo- leled retrieval in the different conditions [Wolbers and
centric conditions compared with the randomly located Buchel, 2005]. Activations are described in Table 2S. As
control condition, implicating these regions specifically in shown in Figure 5A,B, we found a negative linear correla-
allocentric retrieval (2) greater activation in superior posterior tion with learning blocks in the hippocampus and parahip-
parietal cortex and precuneus for the rigid form of allocentric pocampal cortex across trials in the store-reference
r 9 r
TABLE II. Spatial coordinates of brain regions of

post hoc t-test between conditions of interested (PFWE < 0.05)
Coordinate (x, y, z; in mm)

Voxel level
Region LH RH (z-score)
Paired t-test between the landmark and the store-reference condition

Inferior Frontal Gyrus 38, 3, 30 3.66
Superior Parietal Lobule 30, 60, 48 2.92
Inferior Parietal Lobule 33, 54, 45 3.99
Middle Occipital Gyrus 37, 77, 2 4.21
30, 80, 20 3.71
36, 87, 5 3.66
Inferior Occipital Gyrus 33, 77, 8 3.67
Parahippocampal Gyrus 28, 44, 8 4.15
Fusiform Gyrus 38, 70, 15 4.49
37, 44, 18 3.84
42, 64, 12 3.78
Angular Gyrus 30, 64, 32 3.17
Paired t-test between the landmark and the randomly located target condition
Inferior Frontal Gyrus 40, 3, 30 5.23
38 10 28 4.76
40, 8, 30 3.56
54, 36, 15 3.00
Middle Frontal Gyrus 42, 28, 18 3.56
Medial Frontal Gyrus 8, 16, 52 3.81
Superior Parietal Lobule 28, 64, 40 5.76
32, 60, 48 4.72
Precentral Gyrus 40, 10, 42 3.57
Precuneus 33, 54, 45 5.65
Posterior Cingulate 14, 57, 22 4.44
Paired t-test between the store-reference and the randomly located target condition
Precentral Gyrus 43, 3, 35 3.28
Precuneus 6, 74, 50 4.38
7, 62, 45 3.97
40, 70, 35 3.33
22, 57, 22 3.48
Superior parietal Lobe 37, 57, 52 3.67
Middle Temporal Gyrus 40, 70, 25 3.38
RH, right hemisphere; LH, left hemisphere.
condition but not in the other three conditions. To explore campus and parahippocampal cortex are involved early in
the extent to which these changes over blocks correlated learning in the store-reference condition. We note that
with behavioral performance, we extracted the percent sig- because we did not find differences in learning rate
nal change in these two clusters and calculated the correla- between the landmark and store reference conditions, this
tion with response accuracy in each corresponding block argues that the linear decrease we observed in the store
in the store-reference condition. As shown in the Figure reference but not landmark condition was not due to dif-
5C, in the store-reference condition, hippocampal activa- ferences in performance but likely related to differential
tion and accuracy were significantly correlated (r ¼ involvement of these two brain regions over trials.
0.937, P < 0.01), an effect we also observed in the para-
hippocampus (r ¼ 0.875, P < 0.05). To ensure that this Functional Connectivity Analyses Showing
effect did not generalize to the landmark condition, we Significant Connectivity Between Hippocampus
applied the same cluster mask to the pattern of activations and Extrahippocampal Cortical Areas During the
in the landmark condition; we did not find a significant Store-Reference Condition
correlation with accuracy in either the hippocampus (r ¼
0.299, P ¼ 0.565) or parahippocampal cortex (r ¼ 0.562, P We additionally performed a beta-series correlation
¼ 0.246). These data thus support the idea that the hippo- analysis to assess functional connectivity between regions
r 10 r
Figure 5.
Decreasing linear activation in hippocampus during store-refer- between accuracy and activation in the hippocampus and para-
ence condition. A: Brain areas that had a negative linear correla- hippocampal cortex over testing blocks. We observed a signifi-
tion with trials in the store-reference condition. The cant negative correlation between accuracy and activation in
hippocampus (17.7 15,9 18) and parahippocampus (10.1 both hippocampus and parahippocampal cortex. [Color figure
46.8 6.66) showed significant clusters of activation in the can be viewed in the online issue, which is available at
whole brain analysis (PFWE < 0.05). B: The model used to per- wileyonlinelibrary.com.]
form the negative linear correlation analysis. C: Correlation
in the landmark and store-reference conditions [Rissman mary of functional connectivity during the landmark >
et al., 2004]. Because hippocampal activation was present store-reference contrast. No other seed regions showed sig-
only transiently over blocks, we used the extrahippocam- nificant functional interactions in the landmark > store-ref-
pal regions (parahippocampus, retrosplenial, precuneus, erence contrast. These findings argue for the involvement
and superior posterior parietal cortical clusters; see Meth- of functional interactions between the retrosplenial cortex
ods for details) as seeds in our connectivity analysis. The and superior posterior parietal cortex with other cortical
retrosplenial cortex had significantly higher connectivity areas in rigid-forms of spatial representation.
with the inferior parietal lobe and the superior temporal We then looked for brain areas that showed higher func-
gyrus in the landmark compared with the store-reference tional connectivity during the store-reference vs. landmark
condition (Table III). We also found significant connectiv- condition. Both precuneus and superior posterior parietal
ity between superior posterior parietal cortex and medial cortex had significantly higher connectivity with the poste-
frontal gyrus and the precentral gyrus during the land- rior hippocampus in this contrast (Fig. 6A,B). We did not
mark > store-reference contrast. See Table III for a sum- find any significant connectivity between parahippocampal
r 11 r
TABLE III. Spatial coordinates of brain regions showing resentations prior to navigation, our contrasts allowed us to
higher functional connectivity for landmark vs. directly compare utilization of a spatial representation allo-
store-reference condition with seed region indicated centrically in a more rigid compared with more flexible
(PFWE < 0.05) fashion. Our behavioral results indicated that subjects per-
formed above chance on the first trial of retrieval for find-
Coordinate ing a specific store in both the landmark and store-
(x, y, z; in mm)
Voxel level reference conditions, both when we compared the time
Region LH RH (z-score) spent in a quadrant and the distance traveled within a
quadrant. We note, though, that the time spent and dis-
Seed ¼ retrosplenial cortex tance traveled within the target quadrant on the first trial of
Superior temporal gyrus 37, 40, 5 4.07 searching for the target store, particularly in the store-refer-
Inferior parietal lobule 14, 8, 22 3.40 ence condition, was numerically low (Landmark: 39%;
Sublobar 44, 37, 28 3.44
Store-reference: 33%). Transferring knowledge from the
Seed ¼ superior posterior parietal cortex
Medial Frontal Gyrus 20, 14, 52 3.70
aerial perspective to a first-person view-point involved
Paracentral Lobule 14, 27, 52 3.42 inferring information from one perspective to a different
Precentral Gyrus 27, 20, 45 3.13 one and could be expected to be challenging [Hartley et al.,
37, 20, 58 3.24 2007] and previous studies have noted that allocentric rep-
32, 32, 52 3.13 resentations may be less precise and less readily employed
than egocentric representations [Wang and Spelke, 2000;
RH, right hemisphere; LH, left hemisphere Waller and Hodgson, 2006]. Thus, because our paradigm
involved subjects inferring information from one perspec-
cortex and hippocampus nor retrosplenial cortex and hip- tive to another while simultaneously employing an allocen-
pocampus (Table IV). Retrosplenial cortex, however, tric representation, subject performance, at least initially,
showed significant functional connectivity with prefrontal could be expected to be numerically low.
cortex during the store-reference > landmark contrast. We In addition to transferring from one perspective to
summarize areas showing significantly greater connectivity another, the store-reference condition involved an addi-
in the store-reference vs. landmark contrast in Table IV. tional inference in that subjects had to extrapolate the loca-
Our findings indicate that precuneus and superior poste- tion of one store relative to another by inferring this
rior parietal cortex interacted functionally with the poste- information across different encoding trials. Despite this
rior hippocampus during retrieval in the store-reference important and critical difference between these conditions,
condition. Our functional connectivity results thus support the store-reference and landmark conditions did not differ
the involvement of the hippocampus in the flexible store- on any of our behavioral measures (accuracy, latency, and
reference condition via interactions with cortical areas excess path). Furthermore, improvements in performance
involved in more rigid forms of scene representation. over trials during first-person navigation did not differ
between the two conditions. Thus, although a challenging
DISCUSSION
The goals of this paper were to (1) to investigate the
effects of prior learning from an aerial perspective on the
neural systems underlying active navigation; (2) to compare
flexible and rigid implementations of allocentric representa-
tions acquired from an aerial view during first-person navi-
gation. Our two primary contrasts of interest involved
subjects finding a target store in which they utilized a land-
mark to navigate to a hidden store (the ‘‘rigid’’ landmark
condition) or utilized a store in a flexible fashion to find the
hidden target (the ‘‘flexible’’ store-reference condition).
Both conditions necessitated computing the position of the Figure 6.
hidden target based on its relative direction and position to Functional connectivity analyses. Connectivity between hippo-
the landmark or another store, therefore involving an allo- campus and extrahippocampal brain areas during the store-refer-
centric computation [Klatzky, 1998; O’Keefe and Nadel, ence condition (Tables III and IV). A: Significantly greater
1978; Tolman, 1948]. Furthermore, because subjects had to connectivity in hippocampus with precuneus for store-reference
transfer knowledge from the aerial to first-person perspec- > landmark (PFWE < 0.05). B: Significantly greater connectivity
tive, they could not rely on previously learned viewpoint in hippocampus with superior posterior parietal cortex for
(egocentric) knowledge and instead required an allocentric store-reference > landmark (PFWE < 0.05). [Color figure can be
strategy to find target stores. Thus, what is particularly viewed in the online issue, which is available at
novel in our approach is that because subjects learned rep- wileyonlinelibrary.com.]
r 12 r
TABLE IV. Spatial coordinates of brain regions showing higher functional

connectivity for store-reference vs. landmark condition with seed region indicated
(PFWE < 0.05)
Coordinate (x, y, z; in mm)

Voxel level
Region LH RH (z-score)
Seed ¼ parahippocampal cortex

Medial frontal gyrus 14, 33, 48 3.74
6, 26, 42 3.24
2, 48, 42 3.72
Middle frontal gyrus 22, 30, 45 3.28
Superior frontal gyrus 14, 50, 40 2.95
Seed ¼ precuneus
Insula 36, 40, 20 4.14
Superior temporal gyrus 43, 24, 2 3.73
Middle temporal gyrus 40, 54, 8 3.18
58, 57, 10 3.18
50, 27, 10 3.46
2, 50, 35 3.49
37, 28, 48 3.37
28, 20, 38 3.54
Parahippocampal gyrus 23, 37, 5 3.21
23, 42, 5 2.75
Hippocampus 23, 34, 5 3.14
Seed ¼ retrosplenial cortex
30, 20, 40 3.44
36, 28, 40 3.32
Cingulate gyrus 20, 10, 38 3.42
Precentral gyrus 40, 13, 40 3.33
Seed¼ superior posterior parietal cortex
Insula 36, 44, 20 3.73
38, 24, 28 3.71
Hippocampus 23, 42, 2 3.04
RH, right hemisphere; LH, left hemisphere.
task, our data indicate that subjects did indeed utilize in- rigid and flexible allocentric retrieval conditions, navigat-
formation from the aerial perspective to find their way ing to a randomly located target store (randomly located
during active navigation, and, despite the differences in store control condition), and finding a the target store
transferring knowledge during the rigid and flexible con- when it appeared at the beginning of the trial (visible tar-
ditions, these two conditions did not differ overall in per- get control condition). We then performed post hoc tests
formance. Our approach and behavioral findings thus to identify specific differences within conditions based on
positioned us to explore the neural correlates of rigid vs. these activation clusters. Retrosplenial cortex, superior pa-
flexible allocentric retrieval. rietal lobe, and precuneus activated in both the landmark
vs. control and store-reference vs. control contrasts, indi-
cating their general importance to allocentric retrieval.
Roles of Superior Posterior Parietal, These findings are broadly consistent with previous stud-
Retrosplenial Cortex, and Precuneus During ies demonstrating the involvement of retrosplenial cortex,
Allocentric Representation precuneus, and superior posterior parietal cortex in allo-
centric representation [Committeri et al., 2004; Galati et al.,
We first identified broad areas of activation related to 2010; Jordan et al., 2004; Rosenbaum et al., 2004; Shelton
our task using a whole brain ANOVA by comparing acti- and Gabrieli, 2002; Shelton and Pippitt, 2007; Wolbers and
vation patterns across our four conditions of interest: the Buchel, 2005). These findings are further consistent with
r 13 r
the proposal of Galati et al. [2010] that the precuneus and condition involved some retrieval of a previously learned
retrosplenial cortex form a network of brain regions sub- representation. Broadly speaking, though, the visible-target
serving retrieval of object locations within the context of a condition provided an index into the neural systems
stable reference frame. Previous studies though have also involved in visually guided navigation without the need
implicated parts of posterior parietal cortex in egocentric for direct use of an internal representation [Hartley et al.,
representation [Galati et al., 2000, 2010; Neggers et al., 2003; Iaria et al., 2003]. Thus, the presence of greater rela-
2006]. In our study, we looked specifically at an area of tive activation in the parahippocampal cortex in the visibly
posterior parietal cortex, superior posterior parietal cortex, guided condition, compared with the three other regions,
implicated in previous studies in contrasts of aerial view indicates greater involvement for parahippocampal cortex
vs. first-person encoding of spatial layouts and hypothe- in visually guided scene-based navigation. The parahippo-
sized to play a role in translation from multiple view campal cortex also showed greater activation in the land-
points into a holistic object representation supporting an mark vs. control contrast but not the store-reference vs.
allocentric representation [Shelton and Gabrieli, 2002; Shel- control contrast, suggesting its specificity to more rigid
ton and Pippitt, 2007]. Thus, it is possible that the activa- forms of scene representation. These findings are broadly
tions we reported in superior posterior parietal cortex consistent with data showing greater parahippocampal
could potentially differ from those classically associated activation during viewing of visual scenes from specific
with egocentric representation in posterior parietal cortex. view-points [Epstein et al., 2003] and together suggest the
possibility of less direct parahippocampal involvement
during retrieval of recently learned spatial representations
Roles of Precuneus, Superior Parietal, and and a more direct involvement in active scene processing
Retrosplenial Cortex in Rigid Forms of Spatial [Aguirre et al., 1996; Epstein and Kanwisher, 1998; Epstein
Representation et al., 2007; Janzen and van Turennout, 2004].
Because the landmark condition involved utilizing a
spatial representation based on similar conditions to which
Role of Hippocampus, and Interactions Between
it had been encoded while the store-reference condition
additionally involved reference to another store by infer- Hippocampus and Cortical Areas, in Flexible
ring across encoding trials, the two conditions allowed us Allocentric Retrieval of Recently Learned Spatial
to directly contrast a more rigid form of spatial representa- Layouts
tion with a more flexible version. We observed that activa-
We found greater functional connectivity between precu-
tion was higher in the rigid landmark condition compared
neus and posterior hippocampus and between superior
with the flexible store-reference condition in two key
posterior parietal cortex and posterior hippocampus during
regions: precuneus and superior posterior parietal cortex.
the store-reference compared with the landmark condition.
We also observed significantly higher connectivity
These findings indicate the potential importance of the hip-
between superior posterior parietal cortex/retrosplenial
pocampus in the store-reference condition and thus a role
cortex with parts of temporal and parietal cortex during
in extracting new spatial relations based on previously
rigid compared with flexible allocentric retrieval (Table
learned metric information residing in extrahippocampal
III). These data thus extend the model of Galati et al.
regions. We also found hippocampal activation in the store-
[2010] to suggest the specific involvement of precuneus,
reference condition but not landmark condition, which
superior posterior parietal cortex, and retrosplenial cortex
decreased linearly over blocks. This demonstrates that the
in more rigid forms compared with more flexible forms of
hippocampus was engaged early in trials during the store-
allocentric spatial representation.
reference condition but that it was less involved in later
learning blocks, consistent with previous findings on both
Parahippocampal Cortex in Rigid Scene navigation [Wolbers and Buchel, 2005] and paired-associate
Representation learning [Poldrack et al., 2001; Zeineh et al., 2003]. One pos-
sible explanation for the presence of significant functional
We also observed a significant interaction between the connectivity in the store-reference vs. landmark condition
landmark and visible target conditions and their respective over blocks in the absence of continuing activation during
activation levels in parahippocampal cortex compared later blocks could be due to the presence of coupled rather
with the other three regions we investigated, with parahip- than significantly increased activity later in learning [Riss-
pocampal cortex showing relatively more activation in the man et al., 2004]. Finally, we noted that the degree of hip-
visible-target control compared with the landmark condi- pocampal activation early in learning trials correlated
tion. The visible-target condition differed from the other positively with overall performance on the store-reference
control condition in that it involved navigating directly to task. These findings all suggest the importance of hippo-
a visible store. A subject could potentially use the visible- campal involvement in the store-reference condition.
target condition to update the existing representation of In both the landmark and the store-reference condition,
the target locations and thus we cannot rule out that this subjects needed to retrieve the encoded knowledge of the
r 14 r
position of each store relative to the landmark. However, over all learning trials. Our findings are consistent with
compared with the landmark condition, the store-reference the idea that hippocampal activation is strongest when a
condition involved inferring the spatial relationship of the spatial representation might be expected to be employed
target and based on the reference store despite the fact most flexibly, and similar to Wolbers and Buchel, the first
that they had never seen these two stores on the same block of retrieval was also the period when learning was
trial. From this perspective, both the rigid and flexible con- the most pronounced in our task (see Supporting Informa-
ditions involved similar processes supporting the retrieval tion Figure 1S). Our results, though, extend the findings of
of relationships between stores and the static landmark Wolbers and Buchel to include (1) utilization of previously
except that the flexible condition involved an additional learned representation during active navigation (as
relational inference task across encoding trials [Konkel and opposed to the Wolbers and Buchel study, where the test
Cohen, 2009]. Our findings showed brain areas involved phase involved a paired-associate comparison of land-
in rigid representation retrieval (precuneus and superior marks) (2) utilization of a representation specific to the
parietal lobe) were highly connected to hippocampus in flexible-store condition rather than generally to learning
the flexible retrieval condition. Our findings regarding hip- the distance of landmarks in a layout (3) continued inter-
pocampal involvement in the flexible but not rigid reaction of hippocampus and extrahippocampal areas dur-
trieval condition are thus consistent with rodent and ing retrieval requiring a flexible representation, as
human studies showing a critical role for the hippocampus indicated by our functional connectivity analysis (which
in flexible and relational coding of information [Eichen- Wolbers and Buchel did not perform).
baum et al., 1992; Eichenbaum and Cohen, 2001; Konkel In contrast to our results and those of Wolbers and
et al., 2008; Konkel and Cohen, 2009]. Our findings, how- Buchel [2005], Rosenbaum et al. found little hippocampal
ever, potentially extend the results from these studies by and primarily retrosplenial and parahippocampal activa-
emphasizing the importance of functional interactions tion in navigators highly familiar with a spatial environ-
between hippocampus and extrahippocampal regions dur- ment they had navigated for several years. Because this
ing flexible retrieval of spatial information, suggesting not study looked at a highly familiar environment, which likely
just the importance of the hippocampus to this process but would benefit little from relearning and on-line manipula-
rather its active interactions with extrahippocampal tion, it is possible they did not see hippocampal activation
regions involved in representing spatial layouts. because little flexible usage of the spatial representation
Comparable with our results, Hartley et al. and Iaria was required. Another possibility is that spatial layout rep-
et al. also found greater hippocampal activation when sub- resentations were consolidated to cortical areas in the flexi-
jects used existing allocentric representations in a novel ble condition, thus obviating the need for hippocampal
fashion, although these studies did not systematically com- involvement [McClelland et al., 1995; Rosenbaum et al.,
pare rigid and flexible forms of representations as we did 2004; Tse et al., 2007]. This would also explain why, in our
in our study, instead relying on inferences based on navi- study, the hippocampus was not involved in the landmark
gation strategies post hoc. One possible implication of our condition, as perhaps, by the time of retrieval, it was suffi-
results, in light of those by Hartley et al and Iaria et al, is ciently consolidated to no longer require hippocampal
that hippocampal involvement is not specific to allocentric involvement. Unfortunately, we can only speculate on
retrieval but rather specific to utilizing that representation issues related to consolidation as our paradigm was not set-
in a flexible manner [Cohen and Eichenbaum, 1991; Kon- up to address this idea directly. Future studies will need to
kel and Cohen, 2009]. This interpretation provides possible address the importance of consolidation in the context of
additional insight into why hippocampal lesions often human allocentric representation.
affect some forms of allocentric memory [Goodrich-Hun-
saker et al., 2010; Goodrich-Hunsaker and Hopkins, 2010;
Hartley et al., 2007; Parslow et al., 2005] but not others Encoding vs. Retrieval During Navigation
[Bohbot and Corkin, 2007; Bohbot et al., 1998; Ploner et al.,
1999, 2000]. Namely, conditions requiring utilization of In the current study, subjects were shown the spatial
previously learned spatial information flexibly invoke the relation of each store relative to the landmark during
hippocampus [Eichenbaum et al., 1992] while utilizing an encoding and had no direct view of the relationship
allocentric representation on its own, particularly when between any two stores on the invisible circle (Fig. 1c). Af-
consistent with how it was originally encoded, may not ter the encoding session, subjects were immediately put
involve or require the hippocampus directly. into the scanner for the retrieval task. Thus, they had no
Wolbers and Buchel [2005] also showed hippocampal chance to learn the relationship of any two stores on the
involvement as subjects learned the distance between land- invisible circle before the task. During the navigation task
marks in a virtual environment. Hippocampal activation in the store-reference condition, subjects thus had to calcu-
in their study correlated most strongly with periods of late the spatial relations of stores on the invisible circle.
high-learning, which were most pronounced during early During this retrieval procedure, subjects possibly encoded
testing blocks; retrosplenial activation, in contrast, corre- new information of the relation between stores on the in-
lated with performance on the landmark-distance task visible circle, especially during earlier trials in the store-
r 15 r
reference condition (see also the discussion about the role neus and superior posterior parietal cortex, and greater
of hippocampus above). Early reports suggested that there functional connectivity between superior posterior parie-
might be differences in hippocampal activation during tal/retrosplenial cortex and other cortical areas (e.g., supe-
encoding and retrieval (Lepage et al., 1998); however, rior temporal and medial frontal gyrus) during rigid
more recent reports demonstrate hippocampal activation compared with flexible allocentric representation. Our
during both encoding (Cansino et al., 2002; Davachi et al., results also confirmed the importance of parahippocampal
2003; Uncapher et al., 2006; Diana et al., 2009; Staresina cortex to more rigid forms of scene representation. In con-
and Davachi, 2009) and retrieval (Hayes et al., 2004; Dase- trast, we found greater connectivity between precuneus/
laar et al., 2006; Ekstrom and Bookheimer, 2007; Mugikura superior posterior parietal and the hippocampus during
et al., 2010) of item and general contextual information. flexible utilization of an existing representation, suggesting
These data, in addition to others, suggest that encoding the hippocampus as a possible mediator of accessing previ-
and retrieval likely tap into largely intersecting brain ously stored rigid scene information to permit its flexible
regions, including areas such as the hippocampus (see: engagement. We also found a linear decrease in hippocam-
Rugg et al., 2008 for a review). Baumann et al. 2010 also pal involvement in the flexible allocentric condition over
found hippocampal activation in a navigation task involv- trials, suggesting its initial more direct involvement in this
ing encoding of landmark locations and subsequently find- process early in trials. Finally, the degree of hippocampal
ing hidden versions of these landmarks during retrieval activation on early trials correlated significantly with per-
[Baumann et al., 2010]. formance during flexible retrieval. Our results are consist-
It should be noted though that during active navigation, ent with previous models of human spatial navigation
the line between encoding and retrieval is necessarily less suggesting the importance of superior posterior parietal
defined than verbal memory paradigms because active cortex and precuneus in allocentric spatial representation
navigation involves a continual updating of representa- and extend these findings to suggest their specific involve-
tions based on available sensory input and the current ment in more rigid forms of representations. Our results
navigational goal. While some paradigms explicitly also highlight the role of the hippocampus in flexible forms
attempted to separate encoding and retrieval during navi- of retrieval, extending these findings to human spatial navi-
gation [Baumann et al., 2010; Shelton and Pippitt, 2007], gation following learning from an aerial perspective.
landmarks may serve as a potential cues to recollect and
update spatial representations [Sturz et al., 2009], even
during retrieval. Thus, while it may be possible to separate ACKNOWLEDGMENTS
encoding and retrieval components for navigation, as has The authors wish to thank Weimin Mou, Dan Ragland,
been done in previous verbal memory paradigms, it is not Andrew Watrous, and the UC-Davis Memory Group for
clear that this distinction holds as strongly during naviga- helpful comments on the manuscript.
tion as it might for verbal memory paradigms. Further-
more, previous findings from verbal memory paradigms
and navigation studies suggest the involvement of several
REFERENCES
key brain regions, such as the hippocampus, during both Aguirre GK, Detre JA, Alsop DC, D’Esposito M (1996): The para-
encoding and retrieval, as part of forming and utilizing a hippocampus subserves topographical learning in man. Cereb
spatial representation. Importantly, because our behavioral Cortex 6:823–829.
results indicated that subjects transferred knowledge from Baumann O, Chan E, Mattingley JB (2010): Dissociable neural cir-
the aerial to active navigation condition, while learning cuits for encoding and retrieval of object locations during
occurred during both encoding and retrieval in our para- active navigation in humans. Neuroimage 49:2816–2825.
Bohbot VD, Corkin S (2007): Posterior parahippocampal place
digm, there can be little doubt that subjects did in fact uti-
learning in H.M. Hippocampus 17:863–872.
lize information during retrieval they had acquired during Bohbot VD, Kalina M, Stepankova K, Spackova N, Petrides M,
encoding, albeit with some modification. These findings Nadel L (1998): Spatial memory deficits in patients with
thus argue for the validity of our brain activation patterns lesions to the right hippocampus and to the right parahippo-
regarding rigid vs. flexible forms of spatial representation. campal cortex. Neuropsychologia 36:1217–1238.
Brown TI, Ross RS, Keller JB, Hasselmo ME, Stern CE (2010):
Which way was I going? Contextual retrieval supports the dis-
ambiguation of well learned overlapping navigational routes.
CONCLUSION J Neurosci 30:7414–7422.
Burgess N, Maguire EA, O’Keefe J (2002): The human hippocam-
Our results provide an important extension to previous
pus and spatial and episodic memory. Neuron 35:625–641.
work on human allocentric representation. Our findings
Cansino S, Maquet P, Dolan RJ, Rugg MD (2002): Brain activity
demonstrate increased activation during allocentric re- underlying encoding and retrieval of source memory. Cereb
trieval in retrosplenial, superior posterior parietal cortex, Cortex 12:1048–1056.
and precuneus, particularly during retrieval that relies pri- Cohen NJ, Eichenbaum H (1991): The theory that wouldn’t die: A
marily on utilizing an existing representation with little critical look at the spatial mapping theory of hippocampal
modifications. We also found greater activation in precu- function. Hippocampus 1:265–268.
r 16 r
Committeri G, Galati G, Paradis AL, Pizzamiglio L, Berthoz A, Goodrich-Hunsaker NJ, Hopkins RO (2010): Spatial memory defi-
LeBihan D (2004): Reference frames for spatial cognition: dif- cits in a virtual radial arm maze in amnesic participants with
ferent brain areas are involved in viewer-, object-, and land- hippocampal damage. Behav Neurosci 124:405–413.
mark-centered judgments about object location. J Cogn Goodrich-Hunsaker NJ, Livingstone SA, Skelton RW, Hopkins
Neurosci 16:1517–1535. RO (2010): Spatial deficits in a virtual water maze in amne-
Daselaar SM, Fleck MS, Cabeza R (2006): Triple dissociation in the sic participants with hippocampal damage. Hippocampus
medial temporal lobes: recollection, familiarity, and novelty. 20:481–491.
J Neurophysiol 96:1902–1911. Hartley T, Maguire EA, Spiers HJ, Burgess N (2003): The well-worn
Davachi L, Mitchell JP, Wagner AD (2003): Multiple routes to route and the path less traveled: Distinct neural bases of route
memory: Distinct medial temporal lobe processes build item following and wayfinding in humans. Neuron 37:877–888.
and source memories. Proc Natl Acad Sci USA 100:2157–2162. Hartley T, Bird CM, Chan D, Cipolotti L, Husain M, Vargha-Kha-
Diana RA, Yonelinas AP, Ranganath C (2009): Medial temporal dem F, Burgess N (2007): The hippocampus is required for
lobe activity during source retrieval reflects information type, short-term topographical memory in humans. Hippocampus
not memory strength. J Cogn Neurosci 22:1808–1822. 17:34–48.
Eichenbaum H, Cohen NJ (2001): From Conditioning to Conscious Hayes SM, Ryan L, Schnyer DM, Nadel L (2004): An fMRI study
Recollection: Memory Systems of the Brain. New York: Oxford of episodic memory: Retrieval of object, spatial, and temporal
University Press. information. Behav Neurosci 118:885–896.
Eichenbaum H, Otto T, Cohen NJ (1992): The hippocampus— Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD (2003): Cogni-
What does it do? Behav Neural Biol 57:2–36. tive strategies dependent on the hippocampus and caudate nu-
Ekstrom A, Suthana N, Millett D, Fried I, Bookheimer S (2009): Corre- cleus in human navigation: Variability and change with
lation Between BOLD fMRI and theta-band local field potentials practice. J Neurosci 23:5945–5952.
in the human hippocampal area. J Neurophysiol 101:2668–2678. Igloi K, Doeller CF, Berthoz A, Rondi-Reig L, Burgess N (2010):
Ekstrom AD, Bookheimer SY (2007): Spatial and temporal episodic Lateralized human hippocampal activity predicts navigation
memory retrieval recruit dissociable functional networks in the based on sequence or place memory. Proc Natl Acad Sci USA
human brain. Learn Mem 14:645–654. 107:14466–14471.
Epstein R, Kanwisher N (1998): A cortical representation of the Janzen G, van Turennout M (2004): Selective neural representation
local visual environment. Nature 392:598–601. of objects relevant for navigation. Nat Neurosci 7:673–677.
Epstein R, Graham KS, Downing PE (2003): Viewpoint-specific Jordan K, Schadow J, Wuestenberg T, Heinze HJ, Jancke L (2004):
scene representations in human parahippocampal cortex. Neu- Different cortical activations for subjects using allocentric or
ron 37:865–876. egocentric strategies in a virtual navigation task. Neuroreport
Epstein RA (2008): Parahippocampal and retrosplenial contribu- 15:135–140.
tions to human spatial navigation. Trends Cogn Sci 12:388–396. Klatzky R (1998) Allocentric and egocentric spatial representa-
Epstein RA, Higgins JS (2007): Differential parahippocampal and tions: Definitions, distinctions, and interconnections. In: Freksa
retrosplenial involvement in three types of visual scene recog- C, Habel C, Wender CF, editors. Spatial cognition: An Interdis-
nition. Cereb Cortex 17:1680–1693. ciplinary Approach to Representation and Processing of Spatial
Epstein RA, Parker WE, Feiler AM (2007): Where am I now? Dis- Knowledge. Berlin: Springer-Verlag. pp 1–17.
tinct roles for parahippocampal and retrosplenial cortices in Konkel A, Cohen NJ (2009): Relational memory and the hippo-
place recognition. J Neurosci 27:6141–6149. campus: Representations and methods. Front Neurosci 3:166–
Evans GW, Pezdek K (1980): Cognitive mapping: knowledge of 174.
real-world distance and location information. J Exp Psychol Konkel A, Warren DE, Duff MC, Tranel DN, Cohen NJ (2008):
Hum Learn 6:13–24. Hippocampal amnesia impairs all manner of relational mem-
Fitts PM (1954): The information capacity of the human motor sys- ory. Front Hum Neurosci 2:15.
tem in controlling the amplitude of movement. J Exp Psychol Kriegeskorte N, Simmons WK, Bellgowan PS, Baker CI (2009): Cir-
47:381–391. cular analysis in systems neuroscience: The dangers of double
Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll dipping. Nat Neurosci 12:535–540.
DC (1995): Improved assessment of significant activation in Lepage M, Habib R, Tulving E (1998): Hippocampal PET activa-
functional magnetic resonance imaging (fMRI): Use of a clus- tions of memory encoding and retrieval: The HIPER model.
ter-size threshold. Magn Reson Med 33:636–647. Hippocampus 8:313–322.
Friston KJ, Frith CD, Frackowiak RS, Turner R (1995): Characteriz- Levine M, Marchon I, Hanley G (1984): The placement and mis-
ing dynamic brain responses with fMRI: A multivariate placement of you-are-here maps. Environ Behav 16:139.
approach. Neuroimage 2:166–172. Maguire EA, Frith CD, Burgess N, Donnett JG, O’Keefe J (1998a)
Galati G, Pelle G, Berthoz A, Committeri G (2010): Multiple refer- Knowing where things are parahippocampal involvement in
ence frames used by the human brain for spatial perception encoding object locations in virtual large-scale space. J Cogn
and memory. Exp Brain Res 206:109–120. Neurosci 10:61–76.
Galati G, Lobel E, Vallar G, Berthoz A, Pizzamiglio L, Le Bihan D Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD,
(2000): The neural basis of egocentric and allocentric coding of O’Keefe J (1998b) Knowing where and getting there: a human
space in humans: A functional magnetic resonance study. Exp navigation network. Science 280:921–924.
Brain Res 133:156–164. McClelland JL, McNaughton BL, O’Reilly RC (1995): Why there
Ghaem O, Mellet E, Crivello F, Tzourio N, Mazoyer B, Berthoz A, are complementary learning systems in the hippocampus and
Denis M (1997): Mental navigation along memorized routes neocortex: Insights from the successes and failures of connec-
activates the hippocampus, precuneus, and insula. Neurore- tionist models of learning and memory. Psychol Rev 102:419–
port 8:739–744. 457.
r 17 r
McNamara TP, Rump B, Werner S (2003): Egocentric and geocen- Shelton AL, Gabrieli JD (2002): Neural correlates of encoding space
tric frames of reference in memory of large-scale space. Psy- from route and survey perspectives. J Neurosci 22:2711–2717.
chon Bull Rev 10:589–595. Shelton AL, McNamara TP (2004): Orientation and perspective de-
Mellet E, Briscogne S, Tzourio-Mazoyer N, Ghaem O, Petit L, Zago pendence in route and survey learning. J Exp Psychol Learn
L, Etard O, Berthoz A, Mazoyer B, Denis M (2000): Neural cor- Mem Cogn 30:158–170.
relates of topographic mental exploration: The impact of route Shelton AL, Pippitt HA (2007): Fixed versus dynamic orientations
versus survey perspective learning. Neuroimage 12:588–600. in environmental learning from ground-level and aerial per-
Moeser S (1988) Cognitive mapping in a complex building. Envi- spectives. Psychol Res 71:333–346.
ron Behav 20:21–48. Shipman SL, Astur RS (2008): Factors affecting the hippocampal
Morris RGM, Garrud P, Rawlins JNP, O’Keefe J (1982): Place navi- BOLD response during spatial memory. Behav Brain Res
gation impaired in rats with hippocampal lesions. Nature 187:433–441.
297:681–683. Sholl MJ (1987): Cognitive maps as orienting schemata. J Exp Psy-
Mugikura S, Abe N, Suzuki M, Ueno A, Higano S, Takahashi S, chol Learn Mem Cogn 13:615–628.
Fujii T (2010): Hippocampal activation associated with success- Siegel AW, White SH (1975): The development of spatial represen-
ful external source monitoring. Neuropsychologia 48:1543–1550. tations of large-scale environments. In Reese HW, editor.
Neggers SF, Van der Lubbe RH, Ramsey NF, Postma A (2006): Advances in Child Development and Behavior. New York:
Interactions between ego- and allocentric neuronal representa- Academic.
tions of space. Neuroimage 31:320–331. Staresina BP, Davachi L (2009): Mind the gap: Binding experiences
Newman EL, Caplan JB, Kirschen MP, Korolev IO, Sekuler R, across space and time in the human hippocampus. Neuron
Kahana MJ (2007): Learning your way around town: How vir- 63:267–276.
tual taxicab drivers learn to use both layout and landmark in- Stark CE, Squire LR (2001) When zero is not zero: The problem of
formation. Cognition 104:231–253. ambiguous baseline conditions in fMRI. Proc Natl Acad Sci
O’Keefe J, Nadel L (1978): The Hippocampus as a Cognitive Map. USA 98:12760–12766.
Oxford: Clarendon Press. Sturz BR, Brown MF, Kelly DM (2009): Facilitation of learning
Parslow DM, Morris RG, Fleminger S, Rahman Q, Abrahams S, spatial relations among locations by visual cues: Implications
Recce M (2005): Allocentric spatial memory in humans with for theoretical accounts of spatial learning. Psychon Bull Rev
hippocampal lesions. Acta Psychol (Amst) 118:123–147. 16:306–312.
Parslow DM, Rose D, Brooks B, Fleminger S, Gray JA, Giampietro Suthana NA, Ekstrom AD, Moshirvaziri S, Knowlton B, Book-
V, Brammer MJ, Williams S, Gasston D, Andrew C, Vythelin- heimer SY (2009): Human hippocampal CA1 involvement dur-
gum GN, Loannou G, Simmons A, Morris RG (2004): Allocen- ing allocentric encoding of spatial information. J Neurosci
tric spatial memory activation of the hippocampal formation 29:10512–10519.
measured with fMRI. Neuropsychology 18:450–461. Taylor HA, Tversky B (1992): Spatial mental models derived from
Ploner CJ, Gaymard BM, Rivaud-Pechoux S, Baulac M, Clemen- survey and route descriptions. J Mem Lang 31:261–292.
ceau S, Samson S, Pierrot-Deseilligny C (2000): Lesions affect- Thorndyke PW, Hayes-Roth B (1982): Differences in spatial
ing the parahippocampal cortex yield spatial memory deficits knowledge acquired from maps and navigation. Cogn Psychol
in humans. Cereb Cortex 10:1211–1216. 14:560–589.
Ploner CJ, Gaymard BM, Ehrle N, Rivaud-Pechoux S, Baulac M, Tolman EC (1948): Cognitive maps in rats and men. Psychol Rev
Brandt SA, Clemenceau S, Samson S, Pierrot-Deseilligny C 55:189–208.
(1999): Spatial memory deficits in patients with lesions affect- Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood
ing the medial temporal neocortex. Ann Neurol 45:312–319. ER, Witter MP, Morris RG (2007): Schemas and memory con-
Poldrack RA, Clark J, Pare-Blagoev EJ, Shohamy D, Creso Moyano solidation. Science 316:76–82.
J, Myers C, Gluck MA (2001): Interactive memory systems in Uncapher MR, Otten LJ, Rugg MD (2006): Episodic encoding is
the human brain. Nature 414:546–550. more than the sum of its parts: An fMRI investigation of multi-
Presson CC, DeLange N, Hazelrigg MD (1989): Orientation speci- featural contextual encoding. Neuron 52:547–556.
ficity in spatial memory: What makes a path different from a Voss JL, Gonsalves BD, Federmeier KD, Tranel D, Cohen NJ
map of the path? J Exp Psychol Learn Mem Cogn 15:887–897. (2010): Hippocampal brain-network coordination during voli-
Richardson AE, Montello DR, Hegarty M (1999): Spatial knowl- tional exploratory behavior enhances learning. Nat Neurosci
edge acquisition from maps and from navigation in real and 14:115–120.
virtual environments. Mem Cognit 27:741–750. Waller D, Hodgson E (2006): Transient and enduring spatial rep-
Rissman J, Gazzaley A, D’Esposito M (2004): Measuring functional resentations under disorientation and self-rotation. J Exp Psy-
connectivity during distinct stages of a cognitive task. Neuro- chol Learn Mem Cogn 32:867–882.
image 23:752–763. Wang RF, Spelke ES (2000): Updating egocentric representations
Rosenbaum RS, Ziegler M, Winocur G, Grady CL, Moscovitch M in human navigation. Cognition 77:215–250.
(2004): "I have often walked down this street before": fMRI Wolbers T, Buchel C (2005): Dissociable retrosplenial and hippo-
studies on the hippocampus and other structures during mental campal contributions to successful formation of survey repre-
navigation of an old environment. Hippocampus 14:826–835. sentations. J Neurosci 25:3333–3340.
Rugg MD, Johnson JD, Park H, Uncapher MR (2008): Encoding-re- Zeineh MM, Engel SA, Thompson PM, Bookheimer SY (2003): Dy-
trieval overlap in human episodic memory: A functional neu- namics of the hippocampus during encoding and retrieval of
roimaging perspective. Prog Brain Res 169:339–352. face-name pairs. Science 299:577–580.
r 18 r

Zhang 2012

Uploaded by

Copyright:

Available Formats

Zhang 2012

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Zhang 2012

Uploaded by

Copyright:

Available Formats

r Human Brain Mapping 00:000–000 (2012) r

Human Neural Systems Underlying Rigid and

Hui Zhang and Arne Ekstrom*

Visible target Landmark Store reference Randomly located

TABLE II. Spatial coordinates of brain regions of

Coordinate (x, y, z; in mm)

Paired t-test between the landmark and the store-reference condition

RH, right hemisphere; LH, left hemisphere.

TABLE IV. Spatial coordinates of brain regions showing higher functional

Coordinate (x, y, z; in mm)

Seed ¼ parahippocampal cortex

RH, right hemisphere; LH, left hemisphere.

You might also like

Pfad - The Proxy pFad of © 2024 Garber Painting. All rights reserved.