ARTICLES

Spatial updating: how the brain keeps track of changing

© 2008 Nature Publishing Group http://www.nature.com/natureneuroscience

object locations during observer motion

Thomas Wolbers1,2, Mary Hegarty1, Christian Büchel2 & Jack M Loomis1

As you move through an environment, the positions of surrounding objects relative to your body constantly change. Updating these
locations is a central feature of situational awareness and readiness to act. Here, we used functional magnetic resonance imaging
and a virtual environment to test how the human brain uses optic flow to monitor changing object coordinates. Only activation
profiles in the precuneus and the dorsal premotor cortex (PMd) were indicative of an updating process operating on a memorized
egocentric map of space. A subsequent eye movement study argued against the alternative explanation that activation in PMd
could be driven by oculomotor signals. Finally, introducing a verbal response mode revealed a dissociation between the two
regions, with the PMd only showing updating-related responses when participants responded by pointing. We conclude that visual
spatial updating relies on the construction of updated representations in the precuneus and the context-dependent planning of
motor actions in PMd.

Knowing the positions of surrounding objects relative to one’s own
body is a central component of situational awareness and readiness to
act. Because these egocentric object locations constantly change as we
move through an environment, only continuous updating enables us to
effectively act on objects or to avoid getting lost. This process has been
termed spatial updating, and it is of major importance whenever
objects go out of view, when people walk with little vision in the
dark or when they operate in situations that are visually impoverished
and unreliable, such as the case with divers and firefighters. Moreover,
given that spatial updating operates not only in small-scale space, it is
also vital for learning about and navigating in complex environments.
Successful spatial updating requires an observer to perceive the initial
spatial positions of external objects and to create a corresponding
internal representation. Subdivisions of the posterior parietal cortex
code for spatial location in multiple body-based reference frames1.
Such locational cues form the basis of an egocentric map of the
surrounding space that critically depends on the precuneus and
connected inferior and superior parietal areas2–4. These representations
can be flexibly used, allowing not only for spatial judgments and
simulated navigation, but also for transforming object coordinates
into goal-directed motor actions. Dense connections between the
precuneus and premotor cortex5 can provide the latter with pivotal
spatial information needed to organize actions such as reaching
and pointing6–8.
When the observer starts moving around, many objects rapidly leave
the field of view. To mentally track their positions relative to the body,
the observer must monitor the extent of self motion and apply this
information to the object vectors stored in working memory. Humans
can accurately perceive self-motion purely on the basis of visual
feedback9, which has been shown to recruit the human motion
complex (hMT+), intraparietal areas and the precuneus10–14. However,
these experiments were not designed to investigate the simultaneous
tracking of external objects, and patient studies on spatial updating
during blindfolded navigation have yielded conflicting results15–17. As a
consequence and in sharp contrast to abundant findings on spatial
updating during saccadic eye movements18, it remains unknown how
the human brain continuously integrates the wealth of incoming
information during complete body displacements.
According to an elaborate neural model of spatial memory that
accommodates both human and animal findings2, short-term ego-
centric representations not only reside in the precuneus, but they are
hypothesized to also be updated there during observer motion. Here,
we tested this prediction using functional magnetic resonance imaging
(fMRI) and a parametric factorial design in which we manipulated the
amount of working memory load and the presence of self motion.
Participants initially encoded the positions of 1, 2, 3 or 4 geometric
objects presented at unpredictable positions in a virtual environment
(Fig. 1). Following encoding, the objects disappeared by sinking into
the ground, and, in the ensuing delay phase, subjects experienced a
simulated forward translation (updating trials), which was passive to
ensure identical travel duration across subjects and to avoid confound-
ing motor activation as a result of joystick manipulation. On reaching
the endpoint of the virtual movement, participants pointed to the
remembered location of one of the objects, taking into account the
extent of the forward translation. In contrast, static trials provided a
working memory condition without the need to update object posi-
tions. In these trials, subjects initially saw the same stimulus layouts as
during updating trials. In the subsequent delay phase, however, they

1Department of Psychology, University of California, UCen Road, Santa Barbara, California 93106, USA. 2Department of Systems Neuroscience, University Medical Center

Hamburg-Eppendorf, Martinistr. 52, 20246 Hamburg, Germany. Correspondence should be addressed to T.W. (wolbers@psych.ucsb.edu).
Received 2 May; accepted 22 July; published online 7 September 2008; doi:10.1038/nn.2189

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 ARTICLES
Encoding Delay
Variable error Mean reaction times
Updating 2,500 Updating
35
Static Static
© 2008 Nature Publishing Group http://www.nature.com/natureneuroscience
30
2,000
Time (ms)
Degrees
25
20
1,500
15
10 1,000
1 2 3 4 1 2
Number of objects Number of objects
remained stationary instead of moving forward, thus requiring them to
point toward the original location of the target object at retrieval.
RESULTS
Experiment I: behavioral performance
Mean reaction times were affected by working memory load and the
presence of self motion during the delay phase (Fig. 1). A repeated
measures analysis of variance (ANOVA) revealed significant main
effects of task (F ¼ 14.15, P ¼ 0.001) and the number of objects
(F ¼ 167.887, P o 0.001), but we found no interaction (F ¼ 0.186,
P ¼ 0.881). Notably, the main effect for number of objects was driven
by linear increases across both conditions (F ¼ 285.177, P o 0.001).
Similar results were obtained for variable pointing error, although
the main effect of task only showed a trend toward significance (task:
F ¼ 3.855, P ¼ 0.063; number of objects: F ¼ 8.82, P ¼ 0.001;
interaction: F ¼ 1.736, P ¼ 0.182). A planned contrast again revealed
linear increases with increasing number of objects (F ¼ 15.949,
P o 0.001). The marginal significance for the main effect of task was
caused by a single participant whose pointing errors for two conditions
(‘static one object’ and ‘static two objects’) were more than three
standard deviations above the sample means. Moreover, his pointing
errors for ‘static three objects’ and ‘static four objects’ were much
smaller, which contrasts with the general increase observed across all
three experiments. It appears likely that this participant used different
response strategies for different conditions, thereby greatly inflating the
mean pointing errors for the conditions ‘static one object’ and ‘static
two objects’. We re-analyzed the main effect of task while leaving out
this subject and found that the P value dropped to 0.018.
We tested for time-dependent changes in pointing performance and
found that less than 2% of the performance variability was related
to increasing familiarity with the tasks (static, r ¼ 0.025; updating,
r ¼ 0.126), which indicates that the extensive pre-training successfully
prevented learning and habituation effects from occurring over the
course of the experiment.
Altogether, increasing the number of objects increased the working
memory load during the delay phase, which resulted in linear increases
in reaction times and variable pointing error. In addition, the need to
compute changing object coordinates during spatial updating trials led
to longer reaction times and increases in pointing error.
1224
Figure 1 Experimental procedure, variable pointing error and reaction times
in Experiment I (mean ± s.e.m.). Top, experimental trials consisted of an
initial encoding phase, a delay phase and a subsequent retrieval phase. Each
trial started with a static presentation of the virtual environment during which
participants memorized the location and identity of 1, 2, 3 or 4 geometric
objects. Next, all objects gradually sank into the ground until they had
completely disappeared. In the delay phase, subjects either saw a virtual
Retrieval
forward movement (updating trials) or their point of view remained stationary
(static trials). In the retrieval phase, only one of the objects presented during
encoding was shown at the center of the screen, at a distance of 18 m, and
participants pointed toward that object’s remembered location. During
updating trials, subjects consequently had to take into account the extent of
forward motion to compute the new object position, whereas static trials
required them to point to the target’s initial position. Bottom, variable
pointing error represents the average circular s.d. of the signed pointing
errors. Note that conditions are directly comparable because target stimuli
were presented at identical positions in each of the eight conditions. Variable
error is large when pointing errors differ substantially from trial to trial,
indicating a high uncertainty when computing the response. Both behavioral
measures revealed that increasing the number of objects at encoding
produced an increase in working memory load. In addition, the need to
3 4
process self-motion and to compute changing object coordinates during
spatial updating trials posed additional processing demands, leading to
longer reaction times and increased pointing error.
Experiment I: fMRI results
BOLD responses during encoding of the stimulus layout did not differ
between updating and static trials, as we expected, given that both trial
types were indistinguishable in that phase. In contrast, activation in
numerous regions was tightly related to the number of objects that were
present in the scene (Table 1). These areas included the fusiform gyrus
and the lateral occipital complex, presumably reflecting the encoding of
object features such as color19 and shape20. Similar effects emerged in a
swath of tissue that encompassed the intraparietal sulcus (IPS), super-
ior parietal cortex and the precuneus. These activations confirm
previous findings on the perception of spatial positions in egocentric
reference frames21,22 and the construction of an internal representation
in the precuneus2,3. Finally, we observed parametric BOLD responses in
the dorsal precentral gyrus and the superior frontal gyrus.
In the delay phase, a widespread network of regions showed stronger
BOLD responses during updating as compared with static trials,
including the posterior parts of the IPS and the superior frontal
gyrus (Fig. 2 and Table 2). Notably, responses in both regions were
unaffected by working memory load, which contrasts with the linear
activation increase that we observed during encoding. Although close
inspection of the regression coefficients in the delay phase may suggest
a trend toward increasing activation during static trials that was absent
during updating trials, testing for a negative interaction between self-
motion and working memory load did not reveal any effects.
Across both updating and static conditions, activation in the super-
ior parietal cortex, the precuneus and the dorsal precentral gyrus
covaried with the number of objects whose locations had to be
memorized during the delay phase (Table 2). However, this pattern
does not inform about spatial updating, as a region that is crucial to the
updating process also needs to receive self-motion signals. Accordingly,
a cortical structure in which working memory representations of
objects are updated on the basis of incoming self-motion cues should
be sensitive to both working memory load and the presence of optic
flow. A conjunction analysis23 revealed that only the precuneus and the
left dorsal precentral gyrus were affected by both experimental manip-
ulations (Fig. 3 and Table 2): BOLD responses not only showed a linear
increase related to the number of objects, but were further elevated
during updating as compared with static trials. In other words,
activation profiles in both regions followed our experimental
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Table 1 Experiment I: encoding phase In the delay phase of updating trials, participants experienced an
expanding optic flow field. Optic flow is known to elicit fast saccades,
Spatial coordinates of the local maxima in the group analysis (P o 0.05 corrected) slow pursuit movements and involuntary reflexes24,25. Given that the
dorsal precentral gyrus has also been associated with oculomotor
Voxel level
control26,27, the precentral responses in the delay phase remain difficult
Region Coordinates (x, y, z, in mm) (t score)
to interpret. We therefore conducted an additional eye-tracking experi-
ment, using the same procedure as in Experiment I, to precisely assess
LH RH
Linear activation increase with increasing number of objects
the role of eye movements in relation to spatial updating.
Lateral occipital complex –38, –72, –10 14.88
© 2008 Nature Publishing Group http://www.nature.com/natureneuroscience

32, –72, –10 10.26 Experiment II: behavioral performance and eye movements
Calcarine gyrus –10, –86, 4 12.69 Reaction times and variable pointing errors closely matched the
16, –78, 6 10.97 performance observed in Experiment I (Fig. 4). Mean reaction times
Superior occipital gyrus –20, –90, 22 12.88 were characterized by significant main effects of task (F ¼ 8.973,
24, –84, 24 9.12 P ¼ 0.007) and number of objects (F ¼ 104.823, P o 0.001), but we
Middle occipital gyrus –28, –78, 20 11.32 found no interaction (F ¼ 0.332, P ¼ 0.673). The main effect for
30, –78, 20 9.55 number of objects was driven by linear increases in both conditions
Lingual gyrus –22, –62, 2 9.20 (F ¼ 167.072, P o 0.001). Similar results were obtained for variable
24, –60, 6 10.70 pointing error (task: F ¼ 34.306, P o 0.001; number of objects:
Fusiform gyrus –34, –54, –14 9.85 F ¼ 16.336, P o 0.001; interaction: F ¼ 0.844, P ¼ 0.465), and a
–26, –70, –10 10.08 planned contrast again revealed linear increases with increasing num-
38, –50, –22 8.14 ber of objects (F ¼ 25.533, P o 0.001). Moreover, we failed to observe
30, –68, –10 8.78 learning and habituation effects, given that less than 1% of the
Precuneus –8, –52, 48 4.37 performance variability was related to increasing familiarity with the
8, –52, 50 5.97
tasks (static, r ¼ –0.005; updating, r ¼ 0.044).
IPS –16, –60, 50 8.64
Eye movement data were analyzed separately for encoding and delay
18, –62, 50 9.02
phases. As updating and static conditions were indistinguishable
Superior parietal lobe –24, –54, 52 12.04
during the initial encoding phase, we expected similar patterns of
–30, –60, 44 6.67
saccadic eye movements for both conditions. This prediction was
24, –56, 56 11.95
28, –64, 34 8.47
confirmed by a repeated measures ANOVA on the number of saccades
Supplementary motor area –6, 2, 62 14.12
per second (Fig. 4), which failed to reveal a main effect of task
Dorsal precentral gyrus –46, –2, 48 13.18 (F ¼ 3.133, P ¼ 0.091). In contrast, the saccade rate was clearly related
52, 0, 50 6.42 to the number of objects present in the scene (F ¼ 21.128, P o 0.001),
Superior frontal gyrus –26, –2, 52 5.90 but did not show an interaction between both factors (F ¼ 1.683,
30, –2, 50 7.07 P ¼ 0.191). Notably, the main effect for number of objects was driven
by linear increases in saccades per second in both conditions (static:
LH, left hemisphere; RH, right hemisphere.
F ¼ 41.814, P o 0.001; updating: F ¼ 14.516, P ¼ 0.001).
manipulations in the same way as the behavioral measures, thus In the delay phase, subjects produced fewer saccades in both
strongly suggesting their importance for the updating process. Further conditions compared with the encoding phase (Fig. 5). Moreover, in
analyses using an uncorrected threshold of P o 0.001 did not reveal any addition to the main effect for number of objects (F ¼ 3.991,
additional clusters of activation, thus sup-
porting the specificity of the results. Encoding Delay
Encoding activation at Delay activation at
x = 24, y = –2, z = 52 x = 24, y = –2, z = 52
0.7
Regression coefficients

Regression coefficients

0.2 0.6
Figure 2 Main effect of self motion during the
(arbitrary units)

(arbitrary units)

0.1 0.5
delay phase (Experiment I). In the delay phase, a 0.4
0
large network of areas showed stronger activation 0.3
–0.1
during updating as compared with static trials 0.2
(middle). The panels on the right indicate the –0.2 Updating 0.1 Updating
corresponding regression coefficients of the peak –0.3 Static 0 Static
voxels (mean ± s.e.m.) in the right superior frontal 1 2 3 4 1 2 3 4
gyrus and the right posterior IPS. Note that, Number of objects Number of objects
although both regions were sensitive to the Encoding activation at Delay activation at
presence of optic flow, they were unaffected by x = 14, y = –58, z = 58 x = 14, y = –58, z = 58
working memory load. In contrast, the number of 0.5
1.2
Regression coefficients

Regression coefficients

objects had a strong effect in both regions during 0.4

0.3 1.0
(arbitrary units)

(arbitrary units)

encoding of the spatial layout (left). The middle

0.2
panels show the results of the random effects 0.1
0.8
analysis that tested for overall differences 0 0.6
between updating and static trials during the –0.1 0.4
delay phase. Activations are projected onto the –0.2 Updating Updating
Montreal Neurological Institute (MNI) template –0.3 Static 0.2 Static
brain, using a statistical threshold of P o 0.05 1 2 3 4 1 2 3 4
corrected for the entire brain. Number of objects Number of objects

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Table 2 Experiments I and III: delay phase measures ANOVAs confirmed these observations, failing to reveal
significant differences on any of the four parameters that we
Spatial coordinates of the local maxima in the group analysis (P o 0.05 corrected) computed to characterize each subject’s distributions (mean:
F ¼ 2.332, P ¼ 0.103; s.d.: F ¼ 1.467, P ¼ 0.234; skewness:
Coordinates Voxel level
F ¼ 1.209, P ¼ 0.309; kurtosis: F ¼ 1.365, P ¼ 0.266).
Region (x, y, z, in mm) (t score)
In sum, subjects produced more saccades in the encoding phase
when the number of objects increased. During the delay phase, we
LH RH
Experiment I
observed fewer saccades for updating trials, which was related to the
Spatial updating versus static
additional presence of slow-phase velocity movements. Notably,
© 2008 Nature Publishing Group http://www.nature.com/natureneuroscience

Calcarine gyrus 10, –80, 8 6.23 neither saccadic nor slow-phase velocity eye movements were affected
Superior occipital gyrus –20, –84, 24 7.67 by the number of objects subjects needed to update.
22, –84, 26 7.89 Eye movements during spatial updating were not affected by work-
Cuneus –18, –76, 40 9.80 ing memory load, suggesting that the linearly increasing precentral
20, –72, 40 10.36 responses in Experiment I were rather related to spatial updating. Given
Precuneus –10, –48, 56 8.31 that we had observed similar responses in the precentral gyrus and in
10, –44, 52 11.17 the precuneus, both regions may use incoming self-motion cues to
hMT+ complex –44, –68, 10 6.63 either update spatial locations or prepare potential pointing move-
44, –62, 6 6.58 ments. Alternatively, the precuneus may provide and update a spatial
IPS –14, –60, 56 7.12 representation of the objects that is converted into motor plans for
14, –58, 58 11.76 pointing movements only at the level of the precentral gyrus. To better
32, –46, 48 6.30 characterize the roles of both structures, we conducted an fMRI study
Supplementary motor area 6, 16, 48 5.11 in which we replaced the static condition of Experiments I and II by a
Dorsal precentral gyrus –40, –2, 50 4.61 verbal condition that was identical to updating trials except for the
44, 4, 42 5.70
response mode. Instead of pointing toward the target object, subjects
Superior frontal gyrus –24, –2, 56 6.75
gave numerical estimates of the direction with a virtual scale (see Sup-
24, –2, 52 11.57
plementary Methods online for details). A region mediating spatial
Middle frontal gyrus 34, 20, 4 6.96
representations during the delay phase should be unaffected by this
30, 26, 38 5.97
manipulation, as both conditions required the observer to update
Inferior frontal gyrus 54, 10, 16 6.60
Linear activation increase with increasing number of objects
spatial positions. In contrast, preparing potential pointing movements
Precuneus –8, –54, 46 3.40 (n.s.)
would not be beneficial for verbal trials; therefore, BOLD responses in a
6, –58, 46 3.97 structure concerned with the planning of movement vectors should
Superior parietal lobe –30, –60, 44 3.78 only covary with the number of objects when the task required a
32, –60, 42 2.89 (n.s.) pointing response.
Dorsal precentral gyrus –46, 0, 50 4.89
Conjunction between linear activation increase and spatial updating versus static Experiment III: behavioral performance
Precuneus 6, –58, 48 3.97 Variable pointing error increased with increasing working memory
Dorsal precentral gyrus –40, 0, 50 4.06 load, but did not differ between the two responses modes (number of
objects: F ¼ 7.099, P ¼ 0.002; response mode: F ¼ 0.004, P ¼ 0.951;
Experiment III interaction: F ¼ 1.362, P ¼ 0.278; see Supplementary Fig. 1 online). As
Linear activation increase with increasing number of objects in the previous experiments, the main effect for number of objects was
Precuneus 0, –56, 44 4.09 driven by a linear increase (F ¼ 14.701, P ¼ 0.003). In contrast, mean
2, –58, 44 3.92 reaction times were longer for verbal than for pointing trials
Interaction between number of objects and response mode (F ¼ 228.257, P o 0.001) and were further affected by the number
Dorsal precentral gyrus –38, 2, 46 2.47 of objects (F ¼ 139.121, P o 0.001; interaction: F ¼ 0.874, P ¼ 0.443).
n.s., nonsignificant. The main effect for number of objects was again driven by linear
increases across conditions (pointing: F ¼ 288.251, P o 0.001). Finally,
P ¼ 0.021), the difference in perceptual stimulation (moving versus we failed to observe learning and habituation effects, given that less
stationary dots) led to a higher number of saccades for static trials than 1% of the performance variability was related to increasing
(F ¼ 26.445, P o 0.001), but no interaction between both factors was familiarity with the tasks (verbal, r ¼ –0.086; pointing, r ¼ –0.033).
observed (F ¼ 0.59, P ¼ 0.57). Notably, the main effect of number of Altogether, the need to convert directional estimates into numeric
objects was driven by a slight linear increase from 1.58 to 1.96 saccades labels for the verbal trials did not affect variable pointing error, which
s–1 in the static condition (F ¼ 11.808, P ¼ 0.003) that was absent in the argues against differential processing demands during the delay phase.
updating condition (F ¼ 2.231, P ¼ 0.15). Rather, the isolated increase in reaction times indicates that subjects
Participants experienced optic flow only in the delay phase of only generated these labels at retrieval.
updating trials. Therefore, eye movements in this condition should
also include slow velocity components. To elucidate the pattern of slow- Experiment III: fMRI results
phase velocity eye movements, we computed the velocity at each time A region that updates spatial representations during the delay phase
point after removing saccade periods. When averaging the resulting should be sensitive to working memory load while being unaffected by
frequency distributions for each of the four updating trial types across our manipulation of response mode. A bilateral cluster in the precuneus
participants, we obtained markedly similar distributions with peaks showed linear activation increases across both response modes (Fig. 6
around 2 deg s–1 and a sharp skewness (Fig. 5). Separate repeated and Table 2); during the delay phase, BOLD responses covaried linearly

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Encoding Delay Figure 3 Conjunction analysis: main effect of self

Encoding activation at Delay activation at motion and a linear activation increase during the
x = 6, y = –58, z = 48 x = 6, y = –58, z = 48 delay phase (Experiment I). A conjunction analysis
0.6 1.5 revealed that only the precuneus and the left

Regression coefficients
Regression coefficients

0.5 dorsal precentral gyrus showed a combination of

0.4

(arbitrary units)
(arbitrary units)

0.3 both main effects in the delay phase (middle);

0.2 1.0 not only were BOLD responses elevated during
0.1 updating as compared with static trials, but they
0
–0.1 also showed a linear increase related to the
Updating Updating
–0.2 Static 0.5 Static number of objects. This indicates that both
–0.3 regions are sensitive to working memory load and
© 2008 Nature Publishing Group http://www.nature.com/natureneuroscience

1 2 3 4 1 2 3 4
the presence of optic flow, suggesting a prominent
Number of objects Number of objects
role for spatial updating. The panels on the right
Encoding activation at Delay activation at show regression coefficients of the peak voxels
x = –40, y = 0, z = 50 x = – 40, y = 0, z = 50 (mean ± s.e.m.) in the right precuneus and the

Regression coefficients
0.5 left dorsal precentral gyrus. The panels on the left
Regression coefficients

0.4 0.6 show the corresponding regression coefficients

(arbitrary units)
0.3
(arbitrary units)

0.2 0.5 observed during encoding of the spatial layout.

0.1 0.4 The panels in the middle indicate the results of
0 the random effects analysis (upper panel at x ¼ 6)
–0.1 0.3
–0.2 Updating Updating that tested for the conjunction between working
0.2
–0.3 Static Static memory load and the effect of self-motion in the
–0.4 0.1
1 2 3 4 1 2 3 4 delay phase. To show the subthreshold extent of
Number of objects Number of objects the activated regions, results of the random
effects analysis are displayed with a threshold of
P o 0.01 (uncorrected) on the MNI template brain.

with the number of objects whose locations had to be updated. Notably, updating-related responses when the task required a pointing response.
we failed to observe differential activation between pointing and verbal We therefore conclude that visual spatial updating is tightly linked
trials; therefore, spatial updating in the precuneus was independent of to the dynamic interplay of self-motion processing with the aut-
the upcoming action. In contrast, activation in the dorsal precentral omatic construction of updated representations in the precuneus
gyrus showed a significant interaction between number of objects and and the context-dependent planning of potential motor actions in
response mode (Fig. 6 and Table 2); BOLD responses increased with dorsal precentral gyrus.
increasing working memory load only during pointing trials, whereas a When navigating in familiar environments or over longer durations,
flat response curve was observed when participants gave verbal esti- humans predominantly monitor changes in orientation and position
mates. This pattern of activation differed from the precuneus, demon- using path integration and later reconstruct object locations from
strating that working memory load only affected precentral responses enduring allocentric representations28. In contrast, spatial updating
when the task required a pointing response. Elsewhere in the brain, we over short time scales in novel environments operates on transient,
did not observe any additional voxels showing an interaction. egocentric representations, in which the relationship between each
object and the observer must be constantly updated as the observer
DISCUSSION moves28,29. In the present study, we did not observe effects in medial
In these three experiments, we found that humans can update up to four
spatial positions during simulated self-motion. Pointing errors and Behavioral performance
Variable error Mean reaction times
reaction times increased with increasing working memory load Updating
2,500
Updating
35
and were further elevated when self-motion cues were present. In Static Static
Experiment I, only activation in the precuneus and the dorsal precentral 30
2,000
gyrus closely followed both experimental manipulations, thus suggesting
Time (ms)
Degrees

25
their importance for the updating process. Experiment II revealed that
eye movements during spatial updating were unaffected by working 20
1,500
memory load, which suggests that activation in the dorsal precentral
15
gyrus was not driven by oculomotor signals. Finally, introducing a verbal
response mode in Experiment III revealed a dissociation between the 10 1,000
1 2 3 4 1 2 3 4
precuneus and the precentral gyrus, with the latter only showing Number of objects Number of objects

Figure 4 Behavioral performance and saccadic eye movements in Saccadic eye movements
Encoding Delay
Experiment II (mean ± s.e.m.). Top, behavioral performance in the 4.0 4.0
Updating Updating
eye-movement study confirmed the results from Experiment I. Both measures 3.5 Static 3.5 Static
indicated that increasing the number of objects at encoding produced 3.0 3.0
increasing working memory load. In addition, the need to process self-motion
Saccades s –1

Saccades s–1

2.5 2.5
and to compute changing object coordinates during spatial updating trials
2.0 2.0
posed additional processing demands, leading to longer reaction times and
increased pointing error. Bottom, saccadic eye movements during encoding 1.5 1.5
(left) did not differ between static and updating trials, but were clearly 1.0 1.0
affected by the number of objects present in the scene. In the subsequent 0.5 0.5
delay phase (right), participants produced fewer saccades in both conditions. 0 0
Notably, during updating trials, the number of saccades per second did not 1 2 3 4 1 2 3 4
Number of objects Number of objects
covary with the number of objects.

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Slow-phase eye movements In the delay phase of Experiment I, static and updating trials differed
Updating one object Updating two objects on a purely perceptual level (moving versus stationary dots). Many areas
700 700
Skewness = 2.40 Skewness = 2.46
600 Kurtosis = 7.91 600 Kurtosis = 8.23
responded to the presence of motion, including the hMT+ complex, the
Number of samples

Number of samples
500 500 posterior IPS and the caudal part of the superior frontal sulcus. The
400 400 latter region contains the human homolog of the monkey frontal eye
300 300 fields (FEF)30–32, and the coordinates of our superior frontal activation
200 200 were similar to those of previous reports on the human FEF6,27. Both
100 100 FEF and the posterior IPS have been associated with spatial attention,
0 0 spatial working memory and spatial updating across saccadic eye
0 2 4 6 8 10 12 14 0 2 4 6 8 10 12 14
© 2008 Nature Publishing Group http://www.nature.com/natureneuroscience

–1
Velocity (deg s ) Velocity (deg s–1)
movements18,33–35. During encoding, BOLD responses increased when
more objects were presented, which could reflect increasing attentional
Updating three objects Updating four objects
700 700 demands. However, presenting more objects also increased the number
Skewness = 2.47 Skewness = 2.39
600 600 of saccades in Experiment II, and a tight correlation between FEF
Number of samples

Kurtosis = 8.24 Kurtosis = 7.82

Number of samples

500
400
300
200
100
0
0 2 4 6 8 10 12 14
Velocity (deg s–1)
Figure 5 Slow-phase velocity eye movements during the delay phase of
updating trials (Experiment II). Frequency distributions for slow-phase
velocity eye movements averaged across participants. Shaded areas represent
the 95% confidence interval of the mean (dotted lines). Similar distributions
were observed for each of the four updating trial types, with peaks around
2 deg s–1 and a sharp skewness. Analogous the pattern of saccades (Fig. 4),
slow-phase velocity eye movements were independent of the number of
objects subjects needed to update.
prefrontal cortex and the hippocampus, two regions that are known to
be involved in visual path integration13. Moreover, in the precuneus
and the dorsal precentral gyrus, activation during the delay phase was
clearly affected by both working memory load and optic flow. This
response profile argues against a mere updating of the observer’s
position, which should only evoke an overall response to optic flow
independent of working memory load. Given that the characteristics of
our task also correspond well with the conditions associated with
egocentric updating, it is reasonable to assume that self motion cues
were used online to update the stored egocentric object representations.
500 activation and saccade rate has been established previously36. Moreover,
400 in the delay phase, activation in both regions did not covary with the
300 number of objects, which argues against a role in maintaining or
200 updating the stimulus layout in working memory or in directing spatial
100 attention to memorized locations. Conversely, this response profile
0
0 2 4 6 8 10 12 14
resembles the pattern of eye movements that was observed during
Velocity (deg s–1)
spatial updating in Experiment II, as neither slow velocity movements
nor fast saccades were affected by working memory load. Given that
expanding optic-flow fields are known to elicit voluntary and reflexive
eye movements24,25,37 and that the role of the FEF and the posterior IPS
in the control of saccades and smooth pursuit movements is well
established30,32, the overall pattern of activation in both regions appears
to be most consistent with the planning and initiation of eye movements
to keep track of the optic flow field.
A cortical structure that combines memorized object positions with
incoming self-motion cues to construct an up-to-date representation
needs to be sensitive to both working memory load and the presence of
optic flow. In Experiment I, only two regions fulfilled this criterion;
BOLD responses in the precuneus and the dorsal precentral gyrus were
not only stronger during updating trials, but they also showed a linear
increase related to the number of objects. In the precuneus, the
increasing activation during static trials would be consistent with
maintaining the egocentric map of the surrounding space in working
memory. In support of this interpretation, topographically organized
activation has been observed when humans memorize spatial positions
across short delay periods38, thus lending strong support for the
existence of transient spatial maps in medial parietal cortex.

Figure 6 Linear activation increase and interaction with response mode during Delay activation at
x = 0, y = –58, z = 48
the delay phase (Experiment III). Top, in the delay phase of Experiment III,
2.6
only BOLD responses in the precuneus showed a linear increase that closely
Regression coefficients

2.4
followed the number of objects in both conditions. Activation did not differ
2.2
(arbitrary units)

between the two response modes (pointing versus verbal), suggesting that the 2.0
precuneus updated spatial representations independent of the upcoming 1.8
action. Top right, regression coefficients of the peak voxel (mean ± s.e.m.) in 1.6
the precuneus. Top left, results of the random effects analysis (at x ¼ –4) that 1.4
Pointing
tested for linear activation increases in the delay phase. Bottom, in contrast 1.2
Verbal
with the precuneus, dorsal precentral activation showed an interaction 1.0
between working memory load and response mode. BOLD responses only 1 2 3 4
Number of objects
increased with increasing number of objects when subjects gave a subsequent
Delay activation at
pointing response. Conversely, when the task called for converting directional 1.3
x = –38, y = 2, z = 46
1.2
Regression coefficients

estimates into verbal labels, BOLD responses were unaffected by working

1.1
memory load. This pattern indicates a context-dependent planning and
(arbitrary units)

1.0
updating of movement vectors for impending motor actions in the dorsal 0.9
precentral gyrus. Bottom right, regression coefficients of the peak voxel (mean 0.8
0.7
± s.e.m.) in the left dorsal precentral gyrus. Bottom left, results of the random
0.6
effects analysis that tested for an interaction between working memory load 0.5 Pointing
and response mode in the delay phase. To show the subthreshold extent of the 0.4 Verbal
activated regions, results of the random effects analysis are shown with a 0.3
1 2 3 4
threshold of P o 0.01 (uncorrected) on the MNI template brain. See Number of objects
Supplementary Table 1 online for results from the encoding phase.

1228 VOLUME 11 [ NUMBER 10 [ OCTOBER 2008 NATURE NEUROSCIENCE


During updating trials, the egocentric representation needed to be
continuously modified to keep track of the changing object locations.
Electrocortical stimulation in the precuneus can induce the sensation of
translational self-motion39 and BOLD responses in this structure
correlate with the subjective experience of self-motion12. As hypothe-
sized previously2, we therefore conclude that it is exactly the updating
of the stored egocentric object vectors, which was based on incoming
self-motion cues, that led to an additional activation increase in the
precuneus during updating trials. In our purely visual protocol, this
© 2008 Nature Publishing Group http://www.nature.com/natureneuroscience
process could be mediated by dense connections between area MSTand
the precuneus5, providing the latter with crucial information about
translational self motion as derived from optic flow.
In Experiment I, participants responded by pointing at the end of the
delay phase. Therefore, the precuneus could also contribute directly to
preparing upcoming pointing responses, given that it may contain a
human homolog of the monkey parietal reach region6,40. However,
recent evidence suggests that the human parietal reach region codes for
spatial positions in coordinates that are independent of upcoming
motor commands41, and the precuneus is also recruited when subjects
make linguistic judgments about spatial positions42. In Experiment III,
precuneus activation in the delay phase always followed the number of
positions subjects needed to monitor, even when they responded with a
verbal label. Stated differently, we observed hemodynamic responses
that were indicative of spatial updating not only when participants
pointed toward the updated target position, but also when they
converted their estimates into a numerical label. As a consequence,
the storing and updating of egocentric representations of space,
independent of potential actions, constitutes the most parsimonious
interpretation of the activation in the precuneus.
In contrast to the precuneus, the role of the premotor cortex in
planning arm or hand movements is well established. In nonhuman
primates, neurons in PMd show preparatory activity that facilitates the
initiation of arm movements according to predetermined motor para-
meters43–45. When monkeys are presented with multiple potential
targets, directional signals reflecting all corresponding movement direc-
tions arise in PMd44. Notably, these signals are maintained until the
target object is identified, thus suggesting a form of prospective code for
impending actions44. Premotor involvement in movement preparation
has also been demonstrated in humans6,46,47 and the location of our
dorsal precentral effects closely matches previous activations classified as
dorsal premotor cortex6,47. The combined results of Experiments I and
III strongly suggest that whenever subjects responded by pointing, the
egocentric spatial map in the precuneus was transformed into corre-
sponding vectors for pointing movements in PMd, which could be
accomplished via direct connections between both regions5,7,48. The
greater the number of objects presented at encoding, the more motor
plans were generated in PMd. During the static trials of Experiment I, all
potential movement vectors were then maintained across the delay
phase, as participants were not informed about the target object until
retrieval. Conversely, given that object locations changed during updat-
ing trials, these motor programs were continuously modified, which
further augmented BOLD responses. In other words, the constant
updating of premotor codes pre-activated the appropriate movement
vectors at any given moment in time, which would be an important
mechanism for readiness to act throughout the delay phase.
A continuous updating of motor plans toward invisible objects has
also been described for saccadic eye movements49, suggesting that it
may constitute a ubiquitous mechanism for transforming dynamic
representations of space into goal-directed motor actions. However,
Experiment III provides clear evidence that spatial updating in PMd is
highly context sensitive. In the verbal condition, we did not observe
NATURE NEUROSCIENCE VOLUME 11 [ NUMBER 10 [ OCTOBER 2008
ARTICLES
activation indicative of spatial updating, demonstrating that the PMd
only codes for potential pointing movements when the task requires a
pointing response. As a consequence, the updating of movement
vectors does not appear to be an automatic process, but instead
depends on how we plan to interact with our environment.
In closing, our results provide the first evidence, to the best of our
knowledge, for spatial updating of egocentric representations in the
precuneus and corresponding motor plans in dorsal premotor cortex.
These findings constitute an important step toward comprehensive
theories of human spatial memory, imagery and navigation. The
network that we have identified is presumably specific to egocentric
online updating, as partially distinct circuits should be recruited when
the task involves allocentric representations. Future studies are there-
fore needed to further characterize the cortical structures that subserve
spatial updating during complete body displacements in humans.
METHODS
Subjects. All three experiments used healthy male volunteers with normal or
corrected-to-normal vision. Subjects gave written informed consent to parti-
cipate in this study, which was approved by the Ethics Board of the Board of
Physicians in Hamburg, Germany, and by the Human Subjects Committee of
the University of California, Santa Barbara. All subjects understood the
instructions without difficulty and none were aware of the hypotheses at the
time of testing. See Supplementary Methods for further details.
Experimental stimuli and procedure. We used Vizard 2.53 (WorldViz) to
animate a desktop virtual environment that participants viewed from a first-
person perspective (eye height, 180 cm). The environment contained a ground
floor consisting of white dots that covered the entire field of view laterally. In
Experiments I and II, we employed a 2
4 factorial parametric design with
factors task (static versus updating) and number of objects (1–4). Each trial
consisted of an initial encoding phase, a delay phase and a subsequent retrieval
phase. During encoding, participants saw geometric objects positioned in front
of the observer at random distances (Fig. 1). Participants memorized the
location and identity of each object as precisely as possible. Next, all objects
gradually sank into the ground until they had completely disappeared. In the
following delay phase, subjects either saw a forward translation (updating
trials) or remained still at their initial location (static trials). In the final
retrieval phase, only one of the objects the subject had seen during encoding
was presented at the center of the screen. Participants pointed toward that
object’s remembered location by deflecting a joystick. During updating trials,
they consequently had to take into account the extent of forward motion to
compute the new object position. In Experiment III, we replaced the static
condition by a verbal condition that also required subjects to perform spatial
updating during the delay phase. Verbal trials were identical to updating trials
except for the response mode. At retrieval, subjects gave a numerical estimate
(in degrees) of the direction toward the retrieval object by manipulating a
virtual scale with the joystick. See Supplementary Methods for further details.
Magnetic resonance imaging acquisition. Magnetic resonance scanning was
carried out on a 3T MRI Scanner (Siemens Trio) with a standard head coil. We
acquired 34 axial slices (slice thickness, 3 mm; gap, 0.5 mm) using a gradient
echo echo-planar T2*-sensitive sequence (matrix, 64
64; field of view, 192

192 mm). An LCD projector back-projected the virtual environment on a
screen positioned behind the head coil. Subjects lay on their backs in the bore
of the magnet and viewed the stimuli binocularly via a 451 mirror that reflected
the images displayed on the screen. To minimize head movement, subjects were
stabilized with tightly packed foam padding surrounding the head.
Statistical analysis of behavioral, eye movement and neuroimaging data. For
each trial, we measured reaction time and variable pointing error, quantified as
the s.d. of the signed pointing error across all responses in a given condition.
Variable error is large when pointing errors differ substantially from trial to trial,
indicating a high uncertainty when computing the response. To assess the effects
of our experimental manipulations across subjects, we performed two-way
1229
 ARTICLES
repeated measures ANOVAs with number of objects and task (Experiments I
and II) or response mode (Experiment III) as within-group factors.
In Experiment II, eye velocity was computed by linearly interpolating the
250-Hz eye-position traces to a sampling rate of 1 kHz, filtering with a
symmetrical Gaussian low-pass with a cutoff frequency of 30 Hz, and
subsequent three-point differentiation. To identify saccades and slow-phase
components, we used a one-dimensional median filter (length, 500 ms) to
estimate the two-dimensional slow-phase velocity. Next, the vector difference
between the eye-velocity trace and the slow-phase velocity estimate was
computed and served as a two-dimensional estimate of the fast-phase velocity.
© 2008 Nature Publishing Group http://www.nature.com/natureneuroscience
Saccades were detected when the fast-phase velocity estimate exceeded a
velocity threshold of 10 deg s–1. The beginning and end of each saccade were
defined by the points in time before and after peak velocity when the fast-phase
velocity vector either became zero or the sign of its acceleration changed.
Image processing and statistical analysis of fMRI data were carried out using
SPM5 (Wellcome Department of Imaging Neuroscience). All volumes were
realigned to the first volume, spatially normalized to an EPI template in a
standard coordinate system and finally smoothed using a 9-mm full-width at
half-maximum isotropic Gaussian kernel. Encoding, delay and retrieval inter-
vals were modeled as boxcar functions convolved with a hemodynamic
response function; however, trials in which participants failed to respond in
the response interval were modeled as separate regressors and were discarded
during statistical analysis. Specific effects were tested with appropriate linear
contrasts of the parameter estimates, and the corresponding contrast images
were subsequently entered into a random effects analysis. To account for non-
sphericity as a result of our repeated-measures design, we explicitly modeled
dependent error terms. See Supplementary Methods for further details.
Note: Supplementary information is available on the Nature Neuroscience website.
ACKNOWLEDGMENTS
We thank T. Sommer for helpful comments on an earlier draft of this manuscript
and S. Glasauer for help with the eye-movement analysis. This work was
supported by the European Commission (Marie Curie Outgoing International
Fellowship 022072 awarded to T.W.), the Volkswagenstiftung and the German
Ministry of Education and Research (BMBF).
AUTHOR CONTRIBUTIONS
T.W. designed the experiments, conducted data acquisition and analyses, and
wrote the manuscript. M.H. and J.M.L. designed the experiments and wrote the
manuscript. C.B. wrote the manuscript.
Published online at http://www.nature.com/natureneuroscience/
Reprints and permissions information is available online at http://npg.nature.com/
reprintsandpermissions/
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