Introduction
The mammalian brain has developed a remarkable capacity to create an internal map
of space and keep track of current heading direction. Evidence of a cognitive map
comes from the spatially localized firing of hippocampal “place cells” and entorhinal
“grid cells,” which code for an animal’s current position in an environment [1, 2].
“Head direction cells” in companion structures [3] provide a signal for orientation.
Despite substantive gains in understanding how these cells support spatial cognition,
we know surprisingly little about how the brain uses such information to guide navigation.
While numerous functional MRI (fMRI) studies have explored the neural correlates of
navigation [4–16], few have tested predictions from computational models. Such models
have mainly used one of two mechanisms for guidance: (1) the straight-line Euclidean
distance to the goal is computed as part of a heading vector, allowing shortcuts to
be detected [17–21]; and (2) the path to the goal is computed, enabling optimal routes
to be selected and dead ends to be avoided [22–27]. These two mechanisms provide divergent
predictions about how neural activity will be modulated by the distance to the goal
during navigation, but both implicate medial temporal lobe (MTL) structures. Path-processing
models can be interpreted as predicting that MTL activity will reflect the distance
along the intended path to the goal (path distance) because computational demands
will vary with the path distance. By contrast, vector models argue that neurons provide
a firing-rate population vector proportional to the Euclidean distance to the goal.
Recently, it has been argued that the anterior hippocampus provides a global representation
of the environment, whereas the posterior hippocampus contains a fine-grained representation
[15, 28]. Thus, it is possible that the anterior and posterior hippocampus contain
different representations of the distance to the goal such that the posterior codes
the specific regions of space forming the path and the anterior codes more global
Euclidean distance information.
To test these predictions, we used fMRI and a novel real-world navigation task in
which the Euclidean distance and the path distance to the goal had separable values
over time. We found that MTL activity was correlated with both the path distance and
the Euclidean distance during navigation and that the relationship between MTL activity
and these spatial metrics depended on the task demands at different stages of navigation.
Results
Prior to scanning, subjects learned, via studying maps and an intensive walking tour,
the layout of a previously unfamiliar environment: the Soho district in London (Figures
1 and 2; Figure S1, available online). The day after the tour, subjects were scanned
while watching ten first-person-view movies of novel routes through the environment.
Five of the movies required subjects to make navigational decisions about how to reach
goal locations (navigation routes), and the other five required no navigational decision
making (control routes). Movies and tasks were counterbalanced across subjects. At
the start of each navigation route, subjects were oriented as to where they were,
and then shortly after (a period temporally jittered to be between 5 and 13 s), they
were shown a goal destination (New Goal Event) and asked to indicate via a button
press whether they thought the goal was to their left or right. They then viewed footage
in which their viewpoint traversed the street (travel period) until arriving near
the junction (Figure 2). At this time point, subjects pressed a button to indicate
which direction at the upcoming junction provided the shortest path to the goal (Decision
Point), after which the movie continued along the route. Varying the distance between
the Decision Point and the junction allowed for a temporal jitter (3–9 s) between
the Decision Point and outcome (crossing junction). Subjects were told they could
not choose to turn around or walk backward at any point. At the beginning of each
new street section, subjects were told which street they were on and the direction
they were facing (north, south, east, or west). Routes were predetermined such that
they generally followed the optimal route but occasionally required a forced detour
(Detours) where the movie traveled along a suboptimal path. Subjects were informed
that Detours were only temporary obstructions and would not affect the same junction
in the future. The goal being navigated to changed several times (four or five) during
each route at additional New Goal Events. In control routes (alternating in order
with navigation routes), subjects were instructed to not navigate and to avoid thinking
about the locations of goals or the directions to them. Control routes had the identical
format to navigation routes, except that at New Goal Events, subjects were asked to
indicate by a button press whether or not a drink could be purchased from that goal
and were instructed which button to press at Decision Points. The button to press
at each Decision Point was based on the optimal answer in the navigation version of
that route. All routes ended when the current goal was reached and the text “final
destination reached” was displayed with a photograph of the goal. Between routes,
a gray screen with a fixation cross appeared for 17 s. See Figures 1 and 2 and the
Supplemental Experimental Procedures for further details.
Behavioral Results
Subjects acquired a detailed spatial knowledge and accurately performed the tasks
(Table S1). For navigation routes, mean accuracy was 84.82% (SD = 10.96) at New Goal
Events and 79.91% (SD = 13.28) at Decision Points. For control routes, mean accuracy
was 95.90% (SD = 5.77) at New Goal Events and 97.63% (SD = 5.74) at Decision Points.
Subjects made significantly fewer errors in the control task (F(1,23) = 40.27, p <
0.001). Subjects were both faster to respond and more accurate at Decision Points
when the goal was situated closer (in terms of the path distance) and more directly
ahead (Table S1). At New Goal Events, we found no relationship between subjects’ performance
(accuracy and response time) and the magnitude of the change in any of the spatial
parameters (Table S1).
fMRI Results
fMRI analyses revealed that retrosplenial, parietal, and frontal cortical regions
and the cerebellum were significantly more active (at an uncorrected threshold of
p < 0.001) during the navigation task blocks, New Goal Events, and Decision Points
than during the control task blocks and events (Figure S2; Table S2). Significantly
greater right posterior hippocampal activity was also observed during navigation task
blocks than during control task blocks (Table S2).
To gain leverage on the spatial computations performed by the brain during navigation,
we probed the fMRI data with measures of the Euclidean distance, path distance, and
egocentric direction to the goal. First, we explored our a priori predictions (see
Supplemental Experimental Procedures) during New Goal Events, Decision Points, Detours,
and Travel Period Events (events sampled during travel periods at the temporal midway
point between the time points of the other events, for both navigation and control
routes). Second, on finding significant effects, we examined whether similar responses
occurred in the control routes. Third, where responses were specific to navigation,
we tested whether there was a significantly greater effect in navigation routes than
in control routes. Finally, we examined whether these responses were significantly
greater during certain event types than others and whether responses were significantly
more correlated with one parameter than with others.
Both Euclidean and Path Distances Are Tracked by the Hippocampus during Travel
During Travel Period Events in the navigation routes, activity in the posterior hippocampus
was significantly positively correlated with the path distance to the goal (i.e.,
more active at larger distances, see Figures 3A and 3B; Table S2). However, at the
same time points, activity in the anterior hippocampus was significantly positively
correlated with the Euclidean distance to the goal (Figures 3A and 3B; Table S2).
Significant correlations were also present when we downsampled the Travel Period Events
to remove 25% of the events in which the Euclidean and path distances were most correlated
(Table S2). A region-of-interest (ROI)-based analysis of the hippocampal longitudinal
axis revealed that whereas the posterior and mid hippocampus were specifically correlated
with the path distance to the goal (but not the Euclidean distance), the anterior
hippocampus was not specific to the Euclidean distance (Figure 3F; Figure S3). This
was further confirmed by direct contrasts between parameters (Table S3).
Models assume that the guidance system is under volitional goal-directed control rather
than automatic control. Our data support this view. No significant correlation between
hippocampal activity and the distance (either Euclidean or path) to the goal was observed
during the Travel Period Events in the control routes. Furthermore, hippocampal activity
was also significantly more positively correlated with distance measures in these
events during navigation routes than during control routes (Figures 3C–3E; Table S2).
Because route (1–5 versus 6–10) and task (navigation versus control) were counterbalanced
across subjects, significant correlations could not have been purely stimulus driven.
Nor were the correlations with the distance to the goal confounded with the time elapsed
or distance traveled since the route began (Table S2).
Beyond the MTL, at a corrected threshold, the anterior cingulate was the only region
that showed a significant correlation with distance in any of our event types, specifically
(1) during navigation routes and (2) more in navigation routes than in control routes.
It was positively correlated with the path distance to the goal during Travel Period Events
in navigation routes and significantly more positively correlated in navigation routes
than in control routes (Figure S4; Table S2).
Egocentric Goal Direction Is Tracked by the Posterior Parietal Cortex during Travel
Activity in the MTL during travel periods was not correlated with egocentric direction
to the goal or the interaction between this directional measure and distance (either
Euclidean or path) to the goal. However, consistent with prior observations [10],
during navigation routes, activity in the superior posterior parietal cortex was significantly
positively correlated with the egocentric direction to the goal (i.e., the greater
the angle between the current heading and the heading directly to the goal, the greater
the activity [Figures S3 and S4; Table S2]). No such correlation was observed during
Travel Period Events in the control routes. However, although the correlation was
more positive during the Travel Period Events in navigation routes than in control
routes, it was not significantly more positive (Table S2). We also observed lateral
posterior parietal activity negatively correlated with the egocentric direction to
the goal (Figure S4; Table S2); however, this did not survive at corrected thresholds.
Posterior Hippocampal Activity Increases with Proximity and Orientation toward the
Goal at Decision Points
Hippocampal activity did not correlate with the Euclidean or path distance at Decision
Points. However, because subjects responded faster, and more accurately, when the
path distance was shorter and the goal was ahead of them (Table S1), we explored whether
hippocampal activity was related to an interaction between the path distance and the
egocentric goal direction by examining the response to the multiplication of these
two variables (Figure 4). We also included response time in our analysis. We found
that posterior hippocampal activity increased the closer, and more directly ahead,
the goal lay (Figures 4B–4D; Figures S3 and S4; Table S2). Activity increased such
that when subjects were close to and facing the goal, activity was similar to that
during the fixation period between routes. No significant correlation with the path
distance by egocentric goal direction was observed in the posterior hippocampus in
control routes, and the correlation between this parameter and posterior hippocampal
activity was significantly more negative in navigation routes than in control routes
(Figures 4E–4G; Table S2). The significant correlation in navigation routes was independent
of response time, which did not modulate MTL activity. The number of options at Decision
Points (two or three) also had no impact on MTL activity (the path distance did not
differ between these two types of Decision Points [t(51) = 0.04, p = 0.97]).
Entorhinal Activity Scales with the Change in the Euclidean Distance at New Goal Events
At New Goal Events, the distance to the goal changed abruptly (Figures 5A and 5C).
For navigation routes, we found that the greater the change in the Euclidean distance
(but not the path distance) at these time points, the greater the evoked response
in the right entorhinal cortex (Figure 5D; Figures S3 and S5; Table S2). At New Goal
Events, the goal could move to a location that was closer to or farther from the subject
(in terms of both path and Euclidean distances). We found no difference in MTL activity
associated with New Goal Events either when the new goal was located closer to the
subject or when it was located farther away (for both distance types). Notably, increases
and decreases in either the Euclidean or path distance for these two types of New
Goal Events were not significantly different in magnitude (Euclidean distance: t(41) =
0.54, p = 0.59; path distance: t(41) = 1.96, p = 0.056). No significant correlation
with the change in the Euclidean distance was observed in the entorhinal cortex in
control routes, and the correlation between entorhinal activity and this parameter
was significantly more positive in the New Goal Events in navigation routes than in
control routes (Figures 5E–5G; Table S2). The correlation between entorhinal activity
and the change in the Euclidean distance during New Goal Events in navigation routes
was also significantly more positive than the correlation with the change in the path
distance during New Goal Events in navigation routes (Table S3). Finally, we also
explored the MTL response to the distance (path and Euclidean) to the new goal at
New Goal Events and found no significant correlation between MTL activity and either
type of distance (Figure S3).
Right Posterior Hippocampal Activity Reflects the Amount of Change in the Path Distance
at Detours
At Detours, subjects were unable to proceed along the optimal path and thus had to
derive an alternative route to the goal. At these events, the path distance to the
goal increased abruptly and by varying amounts (Figures 5B and 5C). Our data show
a dissociation between prefrontal and MTL responses at Detours. Consistent with prior
studies [6, 29], prefrontal regions, but not MTL regions, were significantly more
active at Detours than during optimal route progression at junctions or events in control
routes (Figure S2; Table S2). However, we found that right posterior hippocampal,
but not prefrontal, activity was positively correlated with the magnitude of change
in the path distance during Detours (i.e., Detours that added a large amount of distance
evoked more posterior hippocampal activity than did Detours that added a small distance
[Figures 5D and 5H; Figures S3 and S5; Table S2]). No equivalent significant correlation
was present at corresponding Detour events in the control movies. Although the correlation
between the change in the path distance and hippocampal activity at Detours was greater
in navigation routes than in control routes, this difference did not reach significance
(Figures 5E–5G; Table S2). See Table 1 for a summary of these and other results.
Comparison of Correlations with Spatial Parameters across Different Event Types
We found that all correlations between MTL activity and the distance to the goal were
specific to each event type (Table S4). For example, the correlation between posterior
hippocampal activity and the path distance during Travel Period Events was significantly
more positive during Travel Period Events than during Decision Points or New Goal
Events. The posterior parietal response to egocentric goal direction was not significantly
more positive during Travel Period Events than during other events (Table S4).
Analysis of the Mean Response in ROIs
When we used an alternative approach of examining the mean response in our ROIs, we
found a small number of differences from our statistical parametric mapping (SPM)
analysis (Figure S3; Table S6). Examining the Euclidean distance to the goal during
Travel Period Events, we found that although there was no significant cluster in the
right entorhinal cortex in SPM, our ROI analysis revealed a significant correlation.
A similar pattern was found in the left posterior parietal cortex for the egocentric
goal direction to the new goal at New Goal Events.
Discussion
Using a novel real-world task, we explored how the brain dynamically encodes the distance
to goals during navigation. Our results provide support for both vector- and path-processing
accounts of navigational guidance [17–26] and give insight into the precise navigation
stages during which the different regions of the MTL process the distance to future
goals. In summary, we found that whereas posterior hippocampal activity was related
to the path distance to the goal (during travel, decision making, and forced detours),
anterior hippocampal activity (during travel) and entorhinal activity (during the
processing of new goals) reflected the Euclidean distance to the goal. These responses
were relatively specific to these time periods, and with the exception of anterior
hippocampal activity, responses were relatively selective to one type of distance.
Our study provides a number of advances over previous fMRI studies exploring representations
of distance in the MTL [10, 16, 30, 31]. First, the absence of significant effects
in our control routes, and the observation of significantly stronger activity during
navigation routes than during control routes in the majority of analyses, indicates
that simply being led along a path to a goal is insufficient to engage the MTL in
processing the distance. Rather, our data are consistent with the view that distance-to-goal
coding requires active navigation based on long-term memory of the environment. Second,
while the visual properties of the stimuli and their temporal dynamics might have
driven the effects in prior studies [10, 16, 30, 31], we show that this was not the
case in our study because task and route were counterbalanced. Finally, the fact that
we altered the distance to the goal sporadically at time points (Detours and New Goal
Events) along the route shows that the MTL activity correlated with the distance was not
simply a function of the time elapsed or distance traveled.
These findings advance our understanding of navigational guidance systems in several
ways. Whereas many models propose that the brain processes either the path [24–27]
or the Euclidean [17–21] distance component of a vector to the goal, we reveal that
both representations are actively deployed during different time windows and by different
MTL regions. While it is important to acknowledge that the responses we observed show
modulation over time rather than categorical on and off responses, our results are
consistent with the following explanation: during the initiation of navigation, when
the spatial relationship to the goal must be established, information related to the
Euclidean distance along the vector is processed, and when path choice is required
at Decision Points or a detour along a new route is required, information related
to the path distance is represented. Although such results are consistent with models
in which both vector and path search mechanisms are used [23], no current model captures
the dynamic pattern of distance representations we observed. Thus, we provide much
needed empirical data for the development of future models.
Previous studies reporting MTL activity correlated with the distance to goal have
provided apparently contradictory reports. While some studies have found that activity
increases as the goal becomes farther away [10, 31], others have reported that activity
increases as the goal becomes closer [16, 30, 32]. These prior studies did not dissect
the operational stages during navigation, nor did they isolate the type of distance
that might have been represented. By doing so, we found that both profiles of response
can occur at different stages of a single journey and that different types of distances
can be represented in different time windows. A possible determinant of the activity
profile may be whether subjects had to update their spatial position or decide which
path to take. In our study, and others [10, 31], activity increased as the distance
during periods of spatial updating (e.g., Travel Period Events) became longer. By
contrast, in other studies [16, 30], hippocampal activity increased as the distance
to the goal became shorter during decision making about which path or direction to
take. Our findings extend prior work by revealing that the proximity to the goal along
the path (but not the Euclidean) distance, combined with the direction to the goal,
modulates hippocampal activity at Decision Points. Previous studies reporting that
hippocampal activity increased with proximity to the goal did not include goal direction
in their analysis [16, 30]; thus, it is possible that an interaction between distance
and direction was present, but not detected. While several models predict that the
path to the goal is represented in the hippocampal population activity [22, 24–27]
or that activity changes with goal proximity [17, 18, 20], none argue that activity
reflects both distance and direction. Given that estimates of the distance along a
path have been found to be biased by the number of junctions and turns along the path
[33], it is possible that facing away from the goal might increase the subject’s internal
estimate of the distance. If so, our combined measure of distance and direction may
more accurately reflect the subjects’ estimate of the distance than the distance we
measured from geospatial data. Exploring this will require further research.
While our primary focus was the MTL, we found responses in other regions thought to
be important for navigation. Consistent with prior research [5, 11, 16, 34], we observed
greater activity in parietal and retrosplenial cortices during navigation tasks (route
blocks, New Goal Events, and Decision Points) than during control tasks. Of these
regions, the posterior parietal cortex showed a correlation with the egocentric direction
to the goal, consistent with a similar previous report [10] and a role in egocentric
processing [35]. It is not clear why parietal activity increases the more the goal
lies behind the subject. It is possible that landmarks and geometry in the current
field of view make it easier to determine the direction to a goal ahead of the subject,
and thus by comparison, make it more demanding to track goals located behind. Alternatively,
increased parietal activity may suggest that subjects pay greater attention to direction
the more the goal lies behind them.
Our results inform the debated specialization of function in the anterior and posterior
hippocampus [28, 36, 37]. Posterior hippocampal activity was consistently correlated
with the path distance to the goal. This region is the homolog of the rodent hippocampal
dorsal (septal) pole, which contains place cells, representing small regions of space
with their “place fields” [38], and is thus suited to the fine-grain coding of space
along precise paths [28]. Moreover, such cells can exhibit “forward sweeps” during
travel [39] and “replay” of locations along the path ahead prior to travel [40], plausibly
recruiting more cells the longer the future path, leading to a predicted positive
correlation between the length of the path and hippocampal activity. While responses
during Travel Period Events and Detours are consistent with this prediction, our response
at Decision Points is the opposite of this prediction. Thus, while our data consistently
indicate that the posterior hippocampus processes information about the path, it does
not appear to do so in a manner directly predicted from “preplay.” Greater integration
of rodent and human neural recording methods would be useful for gaining traction
on this issue.
Our observed anterior hippocampal activity tracking the distance to the goal during
travel periods is consistent with a role in spatial updating [13, 31, 41–43]. If human
anterior hippocampal cells, like those of rodents [38], have broad spatial tuning,
it would make them suited to extracting global environmental information rather than
precise paths [28]. Similarly, the spatially extensive repeating grid-like firing
of entorhinal grid cells may make them ideal for computing vectors rather than paths
[19, 21, 23]. Our observation of a Euclidean-based code in the right entorhinal cortex
is consistent with the finding that the same region codes the Euclidean distance to
the goal in London taxi drivers navigating a simulation of London [10]. We found that
the entorhinal cortex was equally active for increases and decreases in the Euclidean
distance, indicating that resetting the distance rather than purely extending it may
drive the response. It is possible that the entorhinal cortex is driven by resetting
because it may be more computationally demanding to make large alterations in the
representation of the distance than to make small changes. Alternatively, another
explanation, provided by Morgan et al. [31], is that this response is driven by a
repetition-suppression effect. According to this view, the activity is maximal when
the change in the distance is large because it provides the least overlap in the regional
representation of the distance.
In this study, we separated path and Euclidean distances. Future studies will be required
for dissecting the path distance from other variables. Two such variables are “time
to reach the goal” and “reward expectation.” While our analysis revealed that time
elapsed was not correlated with hippocampal activity, it is possible that correlates
of the path distance rather than purely the distance relate to the estimated time
to the goal. Similarly, because reaching a goal is rewarding and the likelihood of
this increases with proximity along the path, the path distance and reward expectation
are related. Manipulating travel speed, travel costs, and reward outcomes may help
separate distance, time, and reward expectation. This would help clarify whether the
anterior cingulate activity observed to correlate with the path distance is related
to reward expectation. Such a prediction is based on evidence that this region processes
progress toward goals [44] and the probability of obtaining a reward [45].
Here, we examined navigation in a recently learned environment. In future research,
it will be useful to compare how distance is represented in recently learned and remotely
learned environments. It is possible that in remotely learned environments, the distance
to the goal is represented by cortical regions rather than the hippocampus [46, 47]
and that the type of distance represented changes with familiarity of the environment.