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Volume 17, Number 18,
Issue of September 15, 1997
pp. 7103-7110
Copyright ©1997 Society for Neuroscience
Recalling Routes around London: Activation of the Right
Hippocampus in Taxi Drivers
Eleanor A. Maguire,
Richard S. J. Frackowiak, and
Christopher D. Frith
Wellcome Department of Cognitive Neurology, Institute of Neurology,
London WC1N 3BG, United Kingdom
 ABSTRACT
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- DISCUSSION
- FOOTNOTES
- REFERENCES
ABSTRACT 
Functional imaging to date has examined the neural basis of
knowledge of spatial layouts of large-scale environments typically in
the context of episodic memory with specific spatiotemporal references.
Much human behavior, however, takes place in very familiar environments
in which knowledge of spatial layouts has entered the domain of general
facts often referred to as semantic memory. In this study, positron
emission tomography (PET) was used to examine the neural substrates of
topographical memory retrieval in licensed London taxi drivers of many
years experience while they recalled complex routes around the city.
Compared with baseline and other nontopographical memory tasks, this
resulted in activation of a network of brain regions, including the
right hippocampus. Recall of famous landmarks for which subjects had no
knowledge of their location within a spatial framework activated similar regions, except for the right hippocampus. This suggests that
the hippocampus is involved in the processing of spatial layouts
established over long time courses. The involvement of similar brain
areas in routes and landmarks memory indicates that the topographical
memory system may be primed to respond to any relevant topographical
stimulation; however, the right hippocampus is recruited specifically
for navigation in large-scale spatial environments. In contrast,
nontopographical semantic memory retrieval involved the left inferior
frontal gyrus, with no change in activity in medial temporal
regions.
Key words:
PET;
topographical memory;
landmarks;
taxi drivers;
semantic memory;
hippocampus
INTRODUCTION
Several functional imaging studies
document involvement of the human hippocampal formation/parahippocampal
gyrus in acquisition (Aguirre et al., 1996 ; Maguire et al., 1996a,
1997) and retrieval (Aguirre et al., 1996; Ghaem et al., 1996) of
knowledge of large-scale environmental space. These studies used tests
of episodic memory in which topographical learning had a specific
spatiotemporal reference (Tulving, 1983) and in which such memory
retrieval may still have involved a degree of active encoding of the
environment. Undoubtedly knowledge of environmental space has its basis
in distinct episodes of learning; however, much human behavior takes place in environments with which we are very familiar, and knowledge of
their spatial layout has entered the domain of general facts about the
world, often referred to as semantic memory. The neural substrates of
topographical memories of long standing (i.e., over several years) have
not yet been examined with functional imaging, although it is known
from case studies of patients with topographical disorientation in
familiar environments that such memories can be impaired (Landis et
al., 1986; Habib and Sirigu, 1987). Previous functional imaging work
indicates that there may be different anatomical substrates for verbal
episodic and semantic memory retrieval (Fletcher et al., 1995b; Tulving
et al., 1996). The aim of the present study was to examine semantic
topographical memory retrieval and to determine whether recall of well
established spatial layouts activates similar brain regions noted in
other studies to subserve episodic topographical memory, with reference in particular to the medial temporal region.
Topographical knowledge is thought to comprise information about both
landmarks and spatial relations between landmarks (Siegal and White,
1975; Thorndyke and Hayes, 1982). Evidence from patient studies of
different anatomical substrates for landmark and location knowledge is
inconsistent. Cases of topographical disorientation in which the main
deficit was spatial and not an agnosia for landmarks have been reported
after lesions to posterior parietal cortex (DeRenzi et al., 1977);
however, patients with topographical learning deficits of a similar
spatial character after circumscribed medial temporal lesions have also
been reported (Maguire et al., 1996b). The current study set out to
assess the neural instantiation of landmark knowledge, where such
knowledge was not confounded by location information about position
within a large-scale spatial layout. This was achieved by using a task
in which famous landmarks were known but their large-scale spatial
context was not. A final aim of the study was to examine topographical
memory (landmarks/spatial layouts) and also nontopographic semantic
memory retrieval to ascertain whether common brain regions subserve
semantic memory regardless of memory type.
To examine well established topographical memory, we used subjects who
were all licensed London taxi drivers of many years experience.
Official London taxi drivers must train for ~3 years and pass
stringent examinations of spatial knowledge before receiving a license.
Their extensive knowledge of London meant that all subjects could be
tested on the same stimuli, with high levels of retrieval success and
with no encoding of new environmental information during task
performance. Studies from environmental psychology indicate that
experienced taxi drivers differ with respect to novices and the general
public in their increased knowledge of shortcuts and minor streets, but
not in the cognitive strategies used in way-finding (Chase, 1983;
Pailhous, 1984; Peruch et al., 1989; Giraudo and Peruch, 1988).
MATERIALS AND METHODS
Subjects. Eleven right-handed qualified and licensed
male London taxi drivers (mean age 45 ± 7 years) participated in
the study. None had a previous history of psychiatric or neurological illness. The average time spent working as a licensed London taxi driver was 14.55 ± 12 years, with the shortest time being 3 years. All subjects gave informed written consent, and the study was approved by the local hospital ethics committee and conducted under
certification from the Administration of Radioactive Substances Advisory Committee (Department of Health, London, UK).
Scanning techniques. PET scans were obtained using a
Siemens/CPS ECAT EXACT HR+ (model 962) PET scanner. Scanning was
performed with septa retracted, in three-dimension (3-D) mode. The
field of view of 15.5 cm in the axial extent allowed the whole brain to
be studied simultaneously. Volunteers received an
H215O intravenous bolus (330 MBq)
infused over 20 sec followed by a 20 sec saline flush through a forearm
cannula. The scan protocol included a delay frame of 15 sec to monitor
the average radioactivity counts in the scanner. The system allows the
activation frame to be triggered automatically, depending on the
physiology of the individual subject. Data were acquired in a 90 sec
scan frame. There were 12 successive administrations of
H215O, each separated by 8 min. The
integrated radioactivity counts accumulated over the 90 sec acquisition
period, corrected for background, were used as an index of regional
cerebral blood flow (rCBF). Attenuation correction was computed using a
transmission scan before emission scan acquisition. Images were
reconstructed into 128 × 128 pixels in 63 planes, with an
in-plane resolution of 6.5 mm. In addition, high resolution magnetic
resonance imaging (MRI) scans were obtained with a 2.0 Tesla Vision
system (Siemens GmbH, Erlangen, Germany) using a T1-weighted 3-D
gradient echo sequence. The image dimensions were 256 × 256 × 256 voxels. The voxel size was 1 × 1 × 3 mm.
Data analysis. Images were analyzed using Statistical
Parametric Mapping (SPM96; Wellcome Department of Cognitive Neurology, London, UK: http://www.fil.ion.ucl.ac.uk/SPM) executed in MATLAB
(Mathworks Inc., Sherborn MA). This approach combines the general
linear model and the theory of Gaussian fields to make statistical
inferences about regional blood flow effects (Friston et al., 1991,
1994; Worsley et al., 1992). All scans were automatically realigned to
the first scan and then normalized using a nonlinear deformation
(Friston et al., 1995) into standard stereotactic space (Talairach and
Tournoux, 1988) using a template from the Montreal Neurological
Institute (Evans et al., 1993). The structural MRI scans were
normalized into the same space to allow for the superimposition of PET
activations onto an averaged structural image. Images were smoothed
using an isotropic Gaussian kernel of 16 mm (full width half maximum)
to optimize the signal-to-noise ratio and to adjust for intersubject
differences in gyral anatomy. Global variance between conditions was
removed using analysis of covariance. For each pixel in stereotactic
space, condition-specific adjusted rCBF values with an associated
adjusted error variance were generated. Areas of significant change in
brain activity were then determined using appropriately weighted
contrasts between the task-specific scans and the t
statistic. The resulting sets of t values constituted the
statistical parametric map. Significance levels were set at
p < 0.001 (uncorrected).
Experimental tasks. There were six tasks, each performed
twice, with task order counterbalanced within and between subjects; five of the tasks are relevant to this discussion. The study had a
factorial design with two factors of interest. Figure
1 illustrates the experimental design.
Two of the tasks involved topographical knowledge: in one, taxi drivers
were given a starting and destination points in the greater London
area. They had to describe overtly during scan acquisition the shortest
legal route between the start and destinations (assuming normal traffic
flow outside rush hour). The other topographical task involved
recalling and describing the appearance of individual world-famous
landmarks (not in London) that subjects had never visited. An important
feature of navigation involves recalling information in a set sequence,
whereas landmark knowledge can be recalled in any order. Another factor
of interest in the design, therefore, was the requirement or notfor
sequencing. Two nontopographic tasks were also included to engage
subjects in semantic memory retrieval in a manner similar to the
topographical tasks, but without involving the recall of environmental
spatial information. The nontopographical tasks concerned memory for
films: recalling and describing the plots of familiar famous films
between given points in the story line, which like the recall of routes involves a set sequence of information retrieval; and recalling and
describing individual frames from famous films, not the plot of the
film, which does not involve any necessary sequence of information.
Tasks, therefore, involved either topographical or nontopographical
knowledge and had either a sequential component or not. A baseline task
to control for speech output was included in which subjects repeated
two four-digit numbers during scanning. Comparison with this baseline
facilitated examination of the network of brain regions involved in
each task by indicating whether changes of activity were relative or
absolute in relation to it. Subjects were blindfolded throughout, and
speech output was digitally recorded.
Fig. 1.
Experimental design, two factors of interest:
T, topographical memory; S, sequencing. A
baseline task was also included.
[View Larger Version of this Image (32K GIF file)]
Before they arrived for scanning, subjects completed and returned
questionnaires that inquired about the following: (1) areas of London
with which they were most familiar; (2) films they would rate as very
familiar, from a list of 150 color films made between 1939 and the
present day; and (3) individual landmarks from a list of 20 world-famous ones they had visited in person and could visualize in
their mind's eye. Routes from areas of London with which all subjects
were familiar were chosen as stimuli in the routes recall task. Those
films that all subjects selected in common as being very well known
were used as stimuli in the film plots and film frames tasks. These
were films that subjects were thoroughly familiar with and had
generally seen five or more times, with no memory for where, when, or
with whom they had seen the film (thus no spatiotemporal reference and
therefore semantic memories). Famous landmarks selected in common
across subjects as those they could visualize but had not
visited in person were selected. Landmarks that had not been visited by
any subject were selected to prevent subjects from recalling landmark
locations within a spatially extended environment, thus assessing the
neural basis of the landmarks per se as the most primary elements of topographical knowledge. During each scan, one stimulus item was presented (i.e., one route/film plot/film frame/landmark) for subjects
to respond to; this was determined by a pilot study with nonparticipating taxi drivers. Thus, during scanning, subjects engaged
in the retrieval tasks throughout the critical window in the rising
phase of brain radioactivity. A pilot study outside the scanner using
healthy normal volunteers performing the same tasks indicated no
differences in electro-oculography across the different tasks. The
tasks in this study were designed to examine those processes normally
engaged in in the real world; as a result, the tasks naturally are
complex, with many components. The current stimuli and study design
were selected as those best suited to answer the questions posed and to
minimize the effect of factors others than those of interest, although
there may be other differences between the tasks in addition to those
of primary concern.
RESULTS
Behavioral data
Table 1 shows the mean duration of
speech for each of the tasks that occurred over the 90 sec duration of
scan acquisition. Statistical analyses showed no significant
differences in speech duration between any of the main tasks. Not
surprisingly, given the repetitive nature of the task, significantly
more speech occurred during the baseline number repetition task
compared with each of the main tasks. The content of speech was also
examined. Before arrival for scanning it had been established by
questionnaire which stimuli subjects were familiar with, and this was
reflected in the high accuracy of subjects' recall. The goal of the
study was to engage subjects in the relevant task for the duration of each scan. All subjects performed the tasks fluently, without stopping.
Table 1.
Duration (seconds) of speech across the five tasks
| Task |
Mean |
SD |
Range
|
|
| Routes |
55.62 |
11.08 |
36 -75
|
| Landmarks |
58.23 |
7.76 |
43 -70 |
| Film
plots |
58.14 |
7.92 |
43 -70 |
| Film
frames |
56.36 |
8.78 |
36 -68 |
| Baseline number
repetition |
63.86 |
6.23 |
53 -76 |
|
|
Means were calculated across the 22 scan acquisitions (two per
subject) for each of the five tasks after data were digitally analyzed.
Means represent the number of seconds when speech output occurred
during the total 90 sec of scan acquisition.
|
|
It was notable that the routes chosen by subjects during the navigation
task were all very similar, with small differences in the minor roads
selected. Street names were recalled accurately, as were relevant
landmarks, and traffic restrictions were adhered to. Figure
2 presents an example of the speech
output of a taxi driver during one of the navigation scans; the map is
included to help illustrate the route taken. Subjects did not actually see maps at any time during the study. In some cases, the names of
streets were not recalled, although their spatial location was (e.g.,
"... take the second street on the left... "); in such cases,
this was regarded as correct topographical information. Indeed, even if
no street names had been provided in the presence of correct location
information this would have been acceptable; accurate verbal labeling
was not a prerequisite for accurate topographical knowledge. Subjects
were debriefed after scanning and reported visualizing actual travel
along the routes, including "seeing" salient landmarks as they were
passed. During the tasks describing film plots and frames and famous
world landmarks, subjects reported that they recalled the
films/frames/landmarks from memory as if they were looking at them. The
film frames were described as if in "freeze frame," with no mention
of sequential plot action but merely descriptions of who was in the
scene and other visual information. Rich descriptions of landmarks were
provided, with many details recalled. Overall, subjects denied
recalling any specific spatiotemporal context related to any of the
information retrieved.
Fig. 2.
Map illustrating the complex route recalled by a
taxi driver during a route scan. Subjects did not see any maps; they
were blindfolded throughout. His speech output for this task follows: Pick up on Grosvenor Square in Mayfair, drop off at Bank Underground Station, then at the Oval Cricket Ground... "Grosvenor square,
I'd leave that by Upper Grosvenor Street and turn left into Park Lane. I would eh enter Hyde Park Corner, a one-way system and turn second left into Constitution Hill. I'd enter Queen Victoria Memorial one-way
system and eh leave by the Mall. Turn right Birdcage Walk, sorry right
Horse Guards Parade, left Birdcage Walk, left forward Great George
Street, forward into Parliament Square, forward Bridge Street. I would
then go left into the eh the Victoria Embankment, forward the Victoria
Embankment under the Blackfriars underpass and turn immediate left into
Puddledock, right into Queen Victoria Street, left into Friday Street,
right into Queen Victoria Street eh and drop the passenger at the Bank
where I would then leave the Bank by Lombard Street, forward King
William Street eh and forward London Bridge. I would cross the River
Thames and London Bridge and go forward into Borough High Street. I
would go down Borough High Street into Newington Causeway and then I
would reach the Elephant and Castle where I would go around the one-way
system... . " (end of scan).
[View Larger Version of this Image (103K GIF file)]
PET results
Overview
The design of this experiment had two major features: (1)
factorial, with two factors of interest (memory type:
topographical/nontopographical; sequencing: with or
without), and (2) an additional baseline condition. Analyses based on
the factorial design and those based on comparison with the baseline
offer complementary insights into the data. Only those analyses germane
to the outlined research questions are presented. Comparison with the
baseline gave an overall picture of the neural systems supporting each
task individually. From this, one can also observe brain regions that
tasks activate in common or differently. More direct comparisons
between tasks were made within the framework of the factorial design:
to determine (1) simple main effects within memory type, (2)
compound main effects across memory type and across the
sequencing factor, and also to examine (3) the interaction
between memory type and sequencing.
Comparisons with baseline
The relative rCBF increases associated with the main memory
tasks in comparison with the baseline task are presented in Table 2. Comparison of the activity during the
routes task with the baseline revealed bilateral activity in
extrastriate regions, the medial parietal lobe, the posterior cingulate
cortex, and parahippocampal gyrus, and also activation of the right
hippocampus. There was no significant activation of frontal regions
associated with this comparison. The landmarks task compared with
baseline also resulted in activation of the posterior cingulate cortex, the medial parietal lobe, and occipito-temporal regions, including the
parahippocampal gyrus. In this case, however, there was no activation
of the hippocampus, but there was significant activation of left
inferior and middle frontal gyri. In comparison with the baseline, the
film tasks (both plots and frames) activated left frontal regions,
middle temporal gyrus (plots left, frames right), and left angular
gyrus but not medial temporal areas. The cerebellum was activated by
all task comparisons with the baseline as was the left temporal pole
(subthreshold for the routes comparison). In summary, the answer to our
first question is that the network of brain regions, including the
right hippocampus, that supports semantic topographical memory
retrieval is similar to that noted in a previous study (Maguire et al.,
1996a): it supports both the learning of new complex spatial layouts as
well as the retrieval of recently acquired topographical memories. The
answer to our second question, specifically inquiring about the neural
instantiation of landmarks, is that both retrieval of landmark
knowledge and retrieval of complex route information activate many
similar brain regions, but the right hippocampus is activated only
during routes recall.
Table 2.
Increases in rCBF associated with comparison of each task
with the baseline task
|
Routes (coordinates/z
score) |
Landmarks (coordinates/z score) |
Film
plots (coordinates/z score) |
Film frames
(coordinates/z score) |
|
| R H |
16,
 38, 0/3.66 |
| L PHG |
28, 42, 6/4.92 |
28, 42, 6/4.24
|
| R PHG |
18, 38, 6/3.97 |
(8, 42, 0/2.90) |
| L O-T (BA
37) |
|
22, 42, 12/4.63 |
| L PCG (BA 31) |
14, 60,
26/5.90 |
| R PCG (BA 30/31) |
|
14, 52, 20/4.48 |
| L SPL (BA
7) |
20, 70, 56/5.40 |
| L AG (BA 39) |
|
|
54, 62,
18/4.03 |
54, 62, 18/3.65 |
| R MP |
6, 66, 62/5.00 |
| L
MP |
10, 66, 40/4.60 |
2, 64, 58/3.86 |
| L TP (BA
38) |
(40, 18, 26/3.00) |
32, 22, 34/3.68 |
36, 22, 32/4.18 |
34, 24, 28/3.89 |
| L ITG (BA 20) |
|
40, 30,
22/4.55 |
| L MTG (BA 21) |
|
|
46, 44, 4/3.54 |
50, 0, 26/3.54 |
| L IFG (BA 44) |
|
50, 18, 22/4.70 |
56, 24, 16/3.40 |
| L MFG (BA 11) |
|
24, 30, 18/4.22 |
| L SFG (BA
6) |
|
18, 12, 52/4.08 |
|
12, 10, 64/3.35 |
| R SOG (BA
19) |
40, 80, 28/7.05 |
| L SOG (BA 19) |
32, 82,
36/6.70 |
30, 88, 32/4.11 |
| L C |
48, 78,
24/3.87 |
14, 42, 16/4.38 |
8, 86, 40/3.52 |
| R
C |
|
34, 76, 40/4.50 |
36, 78, 50/4.55 |
34, 76,
50/4.46 |
|
|
Coordinates in stereotactic space (Talairach and Tournoux, 1988)
refer to local maxima. BA, Brodmann's area; R, right; L, left; H,
hippocampus; PHG, parahippocampal gyrus; O-T, occipito-temporal; PCG,
posterior cingulate gyrus; SPL, superior parietal lobe; AG, angular
gyrus; MP, medial parietal (precuneus); TP, temporal pole; ITG,
inferior temporal gyrus; MTG, middle temporal gyrus; IFG, inferior
frontal gyrus; MFG, middle frontal gyrus; SFG, superior frontal gyrus;
SOG, superior occipital gyrus; C, cerebellum. P < 0.001 (uncorrected) except for those in parentheses, which just failed
to reach significance at this level but are included for the sake of
completeness.
|
|
Simple main effects
Comparison of the activity during routes recall with
activity during any of the other conditions revealed significantly
increased activation of the right hippocampus. The two topographical
tasks, routes and landmarks, were compared; the activity during the
landmarks task was subtracted from the activity during the routes task. This comparison revealed increased activation of medial parietal cortex, posterior cingulate cortex, and the right hippocampus for
routes relative to landmarks. Figure 3
shows this comparison where the activation is superimposed at the level
of the hippocampal activation onto the averaged MRI scan of the 11 taxi
drivers normalized to the same stereotactic space. This confirms that
activity in the right hippocampus is increased during routes recall, as
in topographical encoding (Maguire et al., 1996a), but is not increased during the recall of landmarks. The opposite comparison (landmarks vs
routes) showed activation in the left inferior frontal gyrus for
landmarks compared with routes. Film plots compared with film frames
showed no significant changes in rCBF.
Fig. 3.
Comparison of routes recall with landmarks recall.
The activations are superimposed onto the averaged MRI scan of the 11 taxi drivers normalized to the same stereotactic space. The voxel of peak activation in the right hippocampus has been located here on
relevant transverse sections. Other areas of significant activation in
this comparison included the medial parietal region and the posterior
cingulate gyrus.
[View Larger Version of this Image (60K GIF file)]
Compound main effects
Comparison of each task with the baseline (Table 2) suggests that
very different networks of brain regions were involved in the routes
and landmarks tasks on the one hand and the film tasks on the other.
The main effect of memory type (topographical vs nontopographical) was
determined directly by comparing the activity during topographical
tasks (routes and landmarks) with activity during nontopographical
tasks (film plots and film frames). This comparison is shown in Figure
4a. There was increased
activation of the bilateral medial parietal regions, the posterior
cingulate cortices, fusiform gyri, and parahippocampal gyri during
topographical relative to nontopographical memory retrieval. In
summary, the answer to our third question is that the network of brain
regions showing increased activation during semantic topographical
memory retrieval are entirely different from those activated during
retrieval of nontopographical semantic memory. The main effect of
sequencing was determined by comparing the activity during tasks
involving sequencing (routes and film plots) with activity during
nonsequencing tasks (landmarks and film frames). This comparison is
shown in Figure 4b. The effect of sequencing was shown to be
in bilateral medial parietal regions. There was no change of
hippocampal activity in relation to sequencing.
Fig. 4.
A, Main effect of memory type
displayed on a glass brain to show all areas of significant activation.
Areas of increased rCBF during topographical memory compared with
nontopographical memory. B, Main effect of sequencing
displayed on a glass brain. Areas of increased activity when sequencing
was required for correct memory recall are compared with memory recall
for which no particular sequence of information was necessary.
[View Larger Version of this Image (49K GIF file)]
Interaction
Examination of the interaction between memory type (topographical
vs nontopographical) and sequencing reveals an interaction in the
medial parietal region and in the right inferior parietal cortex (BA
40), where activation is greatest in topographical memory that involves
sequencing, as in the recall of routes (Fig. 5).
Fig. 5.
Brain areas in which the effects of memory type
and sequencing interacted are shown here on relevant transverse
sections of the averaged MRI scan of the 11 taxi drivers. The
interaction was determined by the following comparison
[(routes-landmarks) (film plots-film frames)]. The
arrow indicates the voxel of peak activation in the
medial parietal region; the graph
(bottom) shows the adjusted blood flow values at this
voxel, revealing that the increased activity in this area is
attributable primarily to sequencing in topographical memory (the two
histogram bars for each task represent the two scans of the total 12 scans during which this task was performed).
[View Larger Version of this Image (70K GIF file)]
DISCUSSION
Retrieval of route knowledge
The aim of the present study was to examine semantic topographical
memory retrieval and to determine whether recall of well established
spatial layouts activates similar brain regions noted in other studies
to subserve episodic topographical memory, with reference in particular
to the medial temporal region. Activation of the parahippocampal gyrus,
posterior cingulate cortex, precuneus, and cerebellum has been
associated with episodic topographical memory retrieval (Aguirre et
al., 1996; Ghaem et al., 1996) and learning of spatially extended
environments (Maguire et al., 1996a, 1997). Recall of routes around
London by taxi drivers in the present study activated the same brain
regions compared with a baseline task. Therefore, it seems that both
learning and recall from topographical episodic or semantic
memory have broadly the same network of brain regions as their neural
substrate. Thus, for topographical memory at least, the distinction
between episodic and semantic memory seems to have no anatomical
basis.
Our study reveals activation of the hippocampus proper in topographical
memory retrieval. This is consistent with animal work that documents
the importance of the hippocampus in allocentric mapping of space
(O'Keefe and Nadel, 1978). This observation indicates a role for the
right hippocampus in processing spatial layouts over long time courses
not assessed by the short time scales of previous studies. This study
and that of Maguire et al. (1996a), in which activation of the
hippocampus proper during topographical learning was also recorded,
contrast with the two other topographical memory studies (Aguirre et
al., 1996; Maguire et al., 1997) in which hippocampal activation was
not found. These studies used computer-simulated environments, whereas
the present study and that of Maguire et al. (1996a) involved memory
for real-world environments. Real environments are more complex than
the simulations used to date and involve the potential for using many
routes to navigate to a goal, as reflected in the task put before the
taxi drivers to find the shortest route to a destination. The
recruitment of the hippocampus when real-world environments are
involved may reflect its role in higher level spatial manipulation and
decision making. The absence of activation of the hippocampus in the
two simulation studies that used novel stimuli (Aguirre et al., 1996; Maguire et al., 1997) and the fact that taxi drivers were familiar with
the routes in the present study make it unlikely that hippocampus activation in topographical memory tasks is attributable to novelty of
stimuli (Tulving et al., 1994).
Retrieval of landmark knowledge
The current study also set out to assess the neural instantiation
of landmark knowledge where such knowledge was not confounded by
location information about position within a large-scale spatial layout. Both landmarks and routes activated occipitotemporal regions, posterior cingulate gyrus, medial parietal area, and the
parahippocampal gyrus in comparison with the baseline. The involvement
of many of the same brain regions, both dorsal and ventral, in routes and landmarks memory indicates that the topographical memory system is
primed for relevant topographical information even when the landmarks,
as in this case, have no spatial connotation. Farrell (1996), in a
recent review of topographical disorientation, concluded from the
literature that there was no evidence for distinct mechanisms for the
identification of environmental features on the one hand and their
location on the other. Rather, he concludes that these are two aspects
of the same allocentric system located in the ventral stream. Our
findings support this view. The main difference between activation
patterns for routes and landmarks was that the right hippocampus was
activated only in the routes task but not during recall of landmarks.
The landmarks lacked a location within a large-scale spatial framework
and thoughts of navigation between them were not possible, again
suggesting a role for the right hippocampus in the crucial complex
stage of facilitating navigation in large-scale space.
The recall of landmarks, but not the recall of routes, was associated
with activation of the left lateral prefrontal cortex. Activation of
left frontal regions has been noted in many PET studies of memory, most
often with verbal episodic memory encoding (Kapur et al., 1994;
Shallice et al., 1994). Perhaps the recall of landmarks from semantic
memory involves, as Nyberg et al. (1996) suggest, the encoding of such
material into (verbal) episodic memory; however, it is not clear why
this would be the case for landmarks specifically, but not for recall
of routes from semantic memory. Fletcher et al. (1996) suggest that the
activation of the left prefrontal cortex associated with cued recall of
nonimageable words may reflect an attempt by subjects to form
alternative semantic links between cue and response not necessary when
words are highly imageable. Landmarks are usually very important anchor
points in the representation of spatially extended environments. One might speculate that recall of landmarks that are devoid of position within a spatial layout may invoke functions and areas not normally concerned with the representation of space when it is within a coherent
framework.
Semantic memory type
A final aim of the study was to examine topographical memory
(landmarks/spatial layouts) and also nontopographic semantic memory
retrieval to ascertain whether common brain regions subserve semantic
memory regardless of memory type. The use of familiar film plots as
stimuli engaged subjects in memory recall at a similar level and with
broadly similar characteristics as in the routes task, such as the
recall of information in a specific temporal sequence (i.e.,
progression along a route or progression of a story line). Except for
cerebellar activity, recall of film plots was associated with brain
regions different from those activated during the routes task. Most
activity was left-sided, and there was no activation of
occipitotemporal or medial temporal regions when compared with the
baseline. The recall of film plots and frames, however, resulted in
activation of the left inferior frontal gyrus. All of the semantic
memory recall tasks activated the left inferior frontal region, except
for the routes recall task. Therefore, it may be the case that this
activation is associated, as Nyberg et al. (1996) suggest, with the
encoding of semantic knowledge (including spatially devoid landmarks)
back into episodic memory, or perhaps this area houses a mechanism
common to both episodic memory encoding and semantic memory retrieval.
Topographical memory for large-scale space, however, is clearly not
recalled via this mechanism, and seems to remain a function of the
posterior brain. It might be argued that the taxi drivers, who were
very knowledgeable about the spatial layout of London, were so
practiced that their responses were automatic and so required no
increased activation of frontal regions; however, the task required
them to plan the shortest routes between start and destination points,
and analysis of verbal output clearly demonstrated that subjects
reflected on their responses in a considered and nonautomatic
manner.
Case reports in which topographical disorientation is the primary
deficit are most consistently reported after posterior brain lesions.
The ability to navigate in large-scale space is one that humans share
with a multitude of other species. Many species with a smaller relative
area of prefrontal cortex than that of humans are able to navigate
successfully, suggesting that perhaps other more posterior brain areas
are most involved in such abilities. Other work has found that it is
the size of the hippocampus relative to the size of the telencephalon
that varies according to whether spatial skills are critical to
survival. For example, in food-storing birds, the hippocampus is larger
than in species who cache food to a lesser extent (Sherry et al., 1992;
Hampton et al., 1995). Topographical memory is a phylogenetically old
ability and perhaps depends less on frontal regions, the hippocampal
region being sufficient for its support. Of course, it is possible that
frontal regions are recruited into topographical memory processing
under circumstances that have not yet been examined in functional
imaging studies, although notably, frontal regions were not activated in two previous PET studies of topographical learning (Maguire et al.,
1996a, 1997).
The medial parietal region (precuneus) has been activated in many
PET memory studies and is often held to be associated with visual
imagery (Fletcher et al., 1995a). This is a function noted previously
(Maguire et al., 1997) to be compatible with the requirements of a
topographical memory system. The findings of the present study,
however, throw more light on the function of the parietal region in the
context of topographical memory. A significant feature of both film
story lines and navigation is their inherent sequential nature; for
example, to go from a to b one might have to go via x, y, and z. It
would seem that the medial and right inferior parietal cortex, and not
the hippocampal region, are particularly involved in such sequencing,
with the interaction analysis showing that this is particularly the
case in the context of topographical memory. A significant feature of
person-centered or egocentric spatial processing is its sequential
nature; this compares to the greater flexibility of more map-like
object-centered or allocentric spatial representations. The parietal
cortex has been proposed to be involved in egocentric aspects of
topographical orientation (O'Keefe and Nadel, 1978; Gross and
Graziano, 1995). Our finding that medial and inferior parietal cortex
activation is specifically modulated by sequencing requirements in
topographical memory is further support for this view.
In summary, the network of brain regions subserving topographical
memory in humans, whether during encoding or retrieval of recent or
well established topographical knowledge, includes occipitotemporal areas, medial parietal cortex, posterior cingulate cortex, and the
parahippocampal gyrus. The right hippocampus is recruited, over long
and short time courses, when the environments involved are complex, as
they are in the real world, offering multiple routes to a destination.
The brain system for topographic representation is undiscriminating and
flexible, activating in the presence of any kind of topographic
stimulation. In contrast, semantic memory for nontopographic
information involves increased activity in the left inferior frontal
gyrus but not in the hippocampus. Topographical memory retrieval does
not engage this frontal region and seems to remain a function of the
posterior brain.
FOOTNOTES
Received April 10, 1997; revised July 7, 1997; accepted July 9, 1997.
This work was supported by The Wellcome Trust.
Correspondence should be addressed to Dr. Eleanor A. Maguire, Wellcome
Department of Cognitive Neurology, Institute of Neurology, 12 Queen
Square, London WC1N 3BG, UK.
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[Abstract]
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E. A. Maguire, D. G. Gadian, I. S. Johnsrude, C. D. Good, J. Ashburner, R. S. J. Frackowiak, and C. D. Frith
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PNAS,
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[Abstract]
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