Shifting visuo-spatial attention in a virtual three

Cognitive Brain Research 10 (2001) 317–322
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Short communication
Shifting visuo-spatial attention in a virtual three-dimensional space
Francesco Maringelli a , John McCarthy b , Anthony Steed c , Mel Slater c , Carlo Umilta` d , *
a
Cognitive Neuroscience Sector, International School for Advanced Studies, Trieste, Italy
b
Department of Psychology, University College London, London, UK
c
Department of Computer Science, University College London, London, UK
d
Department of General Psychology, University of Padova, Padova, Italy
Accepted 13 June 2000
Abstract
The present investigation, with a virtual reality set-up, aimed to study attentional orienting within a three-dimensional visual world.
Near and far stimuli were used. Half of the subjects were provided with a virtual representation of their body, whereas half were not.
Results showed a different distribution of attentional resources in the two conditions, suggesting a dissociation between attentional
systems controlling the proximal and the distal visual space. In particular, attention was focused close to the subject’s body when a virtual
representation of it was present, whereas attention was focused away from the body when a virtual representation of the body was not
present.  2001 Elsevier Science B.V. All rights reserved.
Theme: Neural basis of behavior
Topic: Cognition
Keywords: Spatial attention; Orienting; Visual space; Space representation; Three-dimensional; Virtual reality
1. Introduction
During the last 50 years several paradigms were developed to examine the dynamics of visual attention. In
particular, Posner [16] showed that it is possible to pay
attention to a certain spatial location, independently of the
direction of gaze. Subjects were instructed to fixate a
central fixation point and to respond as quickly as possible
to the appearance of a simple target, a light, in the
periphery. Before the target was shown, a cue was
presented, which predicted with a high probability where
the subsequent target would be shown. There were three
experimental conditions: a valid condition (cue and target
were in the same spatial location), an invalid condition
(cue and target were in different spatial locations), and a
neutral condition (all target locations were cued). Posner
showed faster reaction time (RT) in the valid condition
than in the neutral condition (attentional ‘benefits’), and
slower RT in the invalid condition than in the neutral
*Corresponding author.
condition (attentional ‘costs’). Because subjects were not
allowed to move their eyes, he interpreted these differences
as a consequence of a correct / incorrect orienting of
attention.
Posner ([16]; see also Ref. [11]) also showed that
peripheral non-symbolic cues (e.g. flashing a light below a
given spatial location) elicited an automatic (involuntary)
orienting of attention, whereas centrally located symbolic
cues (e.g. an arrowhead pointing to a given spatial
location) elicited a controlled (voluntary) orienting of
attention.
What we know about spatial attention is mainly based
on experiments that were conducted within a two-dimensional visual world. Only a few studies addressed the
dynamics of attention in a three-dimensional (3D) space.
Downing and Pinker [8] asked their subjects to respond as
quickly as possible to a target, a light, which was shown at
one of eight possible locations. The lights were arranged in
two different depth planes, with the subjects’ fixation
directed between them. Before appearance of the target, a
centrally located cue was presented. They showed that
attentional benefits and costs for attentional shifts in both
the frontal plane and depth. Also, they found that, in depth,
0926-6410 / 01 / $ – see front matter  2001 Elsevier Science B.V. All rights reserved.
PII: S0926-6410( 00 )00039-2
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F. Maringelli et al. / Cognitive Brain Research 10 (2001) 317 – 322
attentional costs were greater when subjects were invalidly
cued to a near location then when they were invalidly cued
to a far location.
Similar results were obtained by Gawryszewski et al.
[9], who too found greater costs for shifting attention from
near to far locations than for shifting attention from far to
near locations. Gawryszewski et al. proposed that attentional resources are allocated in depth in a viewer-centred
fashion, with a peak close to the subject’s body.
Other studies addressing visual orienting in 3D space
were carried out by Andersen [1] and Andersen and
Kramer [2]. Andersen used a task in which subjects were
instructed to respond to a centrally located target while
ignoring the surrounding distractors. The distractors were
presented in seven different depth planes: three were
between the subject and the plane of the target, one was at
the plane of the target, and the other three were beyond the
plane of the target. The displays were random dot stereograms, viewed through a stereoscopic prism. The main
result was that the size of the interference effect was
directly related to the distance in depth between targets and
distractors. However, contrary to the result of Downing
and Pinker [8] and Gawryszewski et al. [9], the interference effect was greater for distant distractors than for close
distractors. Attention seemed to be allocated in a viewercentred fashion, as shown by previous investigations, but
with its peak concentrated at locations beyond fixation.
However, as Andersen pointed out, the prism stereoscope
and close viewing conditions (21 cm from the subject’s
eyes) might have led subjects to perceive the far distractors
as being larger. This difference in perceived size may
account for the greater interference from far distractors.
This hypothesis was investigated by Andersen and
Kramer [2]. They reported results consistent with those
reported by previous studies [8,9], that is greater costs
were observed for near than for far distractors. Because the
computer generated stereograms were perceived as being
at a greater distance than in the previous study (140 cm vs.
21 cm), and subjects might have mapped them on to
distant, extrapersonal space, Andersen and Kramer argued
that this factor was responsible for the inversion of the
attentional asymmetry.
The studies described above suggest a viewer-centred
(egocentric) system of co-ordinates for orienting attention
in visual space. However, whereas such a co-ordinate
system is needed to carry out some tasks, such as
movement towards a target, there are converging lines of
evidence in favour of another, probably parallel, co-ordinate system, based on an environment-centred (allocentric)
reference frame. The latter is thought to be necessary for
object identification. For example, a recent study [15]
showed that the luminance centroid of the display serves as
centre of gravity for attention allocation during pattern
recognition. The luminance centroid appears to serve, in
turn, as point of origin for the frame of reference within
which this process is carried out.
Several neurophysiological and neuropsychological ob-
servations (e.g. Refs. [3–7,10,13,14,17,18]) are in favour
of the existence of a functional and anatomical distinction
between mechanisms controlling the near and the far
space, and of the fact that information in near space might
be processed separately and independently from information in far space. Moreover, near and far space seem to
be characterised by different ‘attributes’. Near space is
mainly motoric, and is internally represented in egocentric
co-ordinates. In contrast, far space is mainly perceptual
and is internally represented through allocentric co-ordinates.
The present investigation aims to demonstrate in normal
subjects a dissociation between two attentional systems
operating in these two reference systems. To this purpose,
we made use of virtual reality (VR) scenarios.
2. Experiment
In this experiment the stimuli were presented at different
depth planes within the same display, using the binocular
disparity as an index of depth. The characteristics of the
cues and targets were kept constant at the two depth
planes. To use binocular disparity as an index of depth, the
stimuli were presented in the so-called ‘overlapping region’ of the visual field. In addition, we gave half of the
subjects a ‘virtual’ experience of their body, trunk and
hand, whereas the others were not provided with such a
virtual body. We thought that the group provided with the
virtual body would be aware of the relative distance of
near and far stimuli with respect to their body, whereas the
other group would be aware of the differences between the
two depth planes, but not (or less) aware of the relative
distance of the stimuli from their body. Although we did
not explicitly ask our subjects to map space and / or to
make any distance judgement about space, we invited them
to take a look at the virtual environment and to explore it
‘walking’ inside it for a while. It is conceivable that this
exploration produced an internal representation of virtual
space, based on distance evaluation among relevant spots.
Our prediction was that, in the body absent condition,
subjects would focus their attention further away than in
the body present condition, in which attention should be
naturally focused closer to the body. In particular, we
thought that the presence of the body should automatically
lead to a ‘normal’ distribution of attention to the virtual
limbs and trunk, whereas subjects not provided with the
virtual body would not be able to anchor their attention to
a representation of their body inside the virtual environment. This different allocation of attention to the visual
field should, in turn, lead to a difference in performance
between the two experimental groups.
2.1. Method
2.1.1. Subjects
Twenty students at the University College London
F. Maringelli et al. / Cognitive Brain Research 10 (2001) 317 – 322
319
Fig. 1. Display size and stimuli eccentricities in the Near space (A) and Far space (B) condition.
served as subjects in the experiment. They all had normal
¨ as to the
or corrected-to-normal vision and were naıve
purpose of the experiment. They were paid UK£4 for their
participation. Half of the subjects were randomly assigned
to the ‘body present’ condition, whereas the other half
were assigned to the ‘body absent’ condition.
2.1.2. Apparatus and display
The scenarios were implemented using dVS / dVISE
4.01 software from Division Limited. This ran on a Silicon
Graphics Onyx with twin 196 MHz R10000 processors,
Infinite Reality Graphics and 64M main memory. The
tracking system was a Polhemus Fastrak, with two receivers. One receiver was attached to the head-mounted display
(HMD), and the second to a standard three-button mouse
that was held in the right hand. HMD was a Virtual
Research VR4 that has a resolution of 7423230 pixels for
each eye, 170 660 colour elements, and a field of view of
678 diagonal at 85% overlap. The scene consisted of a
garden of dimension 50390 m. The garden, comprising a
boundary wall, a path and some trees, was made by a few
hundred polygons, which rendered at 60 Hz, 30 Hz per
eye. Latency between the participant’s head movements
and the corresponding change inside the HMD was approximately 120 ms. Half of the subjects were provided
with a virtual body. The torso hung vertically under the
position of the neck, and rotated, in yaw only, to point
along the direction of gaze. The arm was modelled with a
simple inverse-kinematics procedure so that the elbow
flexed as the participants moved their hand.
Apart from the virtual garden and the virtual body, the
stimuli consisted of a classical spatial-attention experimental paradigm (e.g. Ref. [16]). The cues were yellow, bright
arrows (4.48 high31.58 wide) and were shown at 168 of
eccentricity (see Fig. 1). The target was a red, 3D modelled
ball (3.18 diameter), which appeared either just over the
cue or in the corresponding position in the opposite visual
field, depending on the type of trial. There was also a
fixation cross (2.932.98), which moved consistently with
the subject’s head. Subjects did not move through the
environment, but were free to turn around.
Half of the trials were presented in the near space, at a
distance of about 50 cm from the subject’s head, within
his / her reachable space. The remaining trials were shown
in the far space, at a distance of about 20 m far from the
subject’s head, well beyond his / her reachable space.
2.1.3. Procedure
In this experiment we used a 23232 factorial design.
One of the factors, namely the Body / No-Body condition,
was treated as a between-subjects factor, whereas Type of
Space (near / far), and Type of Trial (valid / invalid) were
manipulated within subjects. Within the main factor Type
of Trial, we manipulated both the ‘X’ dimension (Side)
and the ‘Z’ dimension (Depth). In other words, valid cued
trials were situations in which the target appeared on the
same side and at the same depth as the cue, whereas
invalid cued trials were situations in which the target was
shown at the diagonally opposite location with respect to
the cue. We also used two filling conditions in which we
showed valid side / invalid depth cued stimuli and vice
versa. This manipulation was intended to ensure that
subjects had a clear impression of both side and depth
main manipulations.
The Type of Space condition was manipulated using
different binocular disparity for the near and far cues /
targets. The Type of Trial manipulation was designed to
explore benefits / costs due to the correct / incorrect orient-
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F. Maringelli et al. / Cognitive Brain Research 10 (2001) 317 – 322
ing of attention.1 The proportion of valid / invalid trials was
2:1. Subjects responded to 60 valid trials and to 30 invalid
trials. About 10% of the trials (10) were ‘catch trials’, on
which no target was presented after the cue, and subjects
were instructed to refrain from responding. Valid, invalid
and catch trials were presented in random order.
The fixation crosses and the cues were turned on at the
beginning of the experiment and remained on until the end
of it. The sequence of the event for each trial was as
follows. First, either the left or the right cue was flashed
for 35 ms.2 After 90 ms, the target appeared either in the
same or in the opposite hemifield with respect to the cue,
depending on type of trial. The target was turned off after
300 ms and the next trial began after an interval randomly
distributed between 1500 and 2500 ms.
Subjects were instructed to fixate the central fixation
cross and to press as fast as possible one of the mouse keys
when they saw the target. There were four fixation crosses
in the environment, located on a circle centred at the
subjects position and separated by intervals of 908. Subjects completed a block of 100 trials at each of the four
positions.
When they were introduced into a silent room, they were
fitted with the HMD and given details about the environment in which they were to be immersed, and the task they
were asked to perform. The entire experiment consisted of
a unique session of 400 trials (240 valid, 120 invalid, and
40 catch trials) and lasted about 20 min. Most of the time
subjects remained unaware of their virtual body, virtual
arm and hand, because of the relatively limited field of
view.
3. Results and discussion
Errors were rare (less than 1%) and were not analysed.
RTs comprised between 200 ms and 750 ms, which
accounted for about 97% of the total number of responses,
were entered into a three-way repeated-measures MANOVA with Virtual Body (present vs. absent) as a betweensubjects factor, and Type of Space (near vs. far), and Type
of Trial (valid vs. invalid) as within-subjects factors. The
two filling conditions (i.e. valid side / invalid depth and
valid depth / invalid side) were not analysed.
The analysis showed significant main effects of Type of
1
Although the classical paradigm consists of valid trials, invalid trials, and
neutral trials, in this experiment we used only valid and invalid trials to
shorten the experiment. This was due to an intrinsic characteristic of VR
scenarios, namely that subjects may feel a sense of sickness when they
spend more than half an hour in a virtual environment. Therefore, our
benefits / costs analysis does not correspond to the classical one, in which
benefits are estimated by the RT difference between valid and neutral
conditions and costs are estimated by the RT difference between invalid
and neutral conditions.
2
All timing had a variation of 65 ms, because of general characteristics
of computer’s and keyboard / mouse updating frequencies.
Fig. 2. Mean reaction time in ms for the Body present condition (group
1) and the Body absent condition (group 2).
Space (F(1,18)57.64, P,0.013), and Type of Trial
(F(1,18)523.69, P,0.0001). Subjects were about 8 ms
faster to respond to far than to near targets (453 vs. 461
ms), and about 24 ms faster to respond to validly cued
targets than to invalidly cued targets (445 vs. 469 ms). The
between-subjects factor (Virtual Body) did not reach
significance.
Two interactions were significant, namely that between
Virtual Body and Type of Space (F(1,18)57.29, P,
0.015), and that between Virtual Body, Type of Space, and
Type of Trial (F(1,18)58.4, P,0.01). Because of the
significant three-way interaction, we split our group into
two sub-groups (simple main effect analysis; see Ref.
[12]), on the basis of the Body / No-Body manipulation.
Then two separate repeated-measures MANOVAs were run
(see Fig. 2).
3.1. Group 1: Virtual Body present
The MANOVA run on this condition (see Table 1)
showed a significant main effect of Validity (F(1,9)5
12.47, P,0.006), and the interaction between Type of
Space and Validity (F(1,9)55.72, P,0.04), indicating that,
when the Virtual Body was provided, RTs were only
marginally affected by orienting of attention in the near
space in comparison to the far space. A Newman–Keuls
post hoc analysis showed significant differences (P,0.01)
between valid and invalid trials in both near and far space,
but the difference in the far space was almost twice as big
as the difference in near space.
Table 1
Mean reaction time in ms for the Body present condition
Invalid trials
Valid trials
Near space
Far space
482
462
491
453
F. Maringelli et al. / Cognitive Brain Research 10 (2001) 317 – 322
Table 2
Mean reaction time in ms for the Body absent condition (group 2)
Invalid trials
Valid trials
Near space
Far space
462
436
440
429
These subjects seem to allocate attention more densely
to the near space than to the far one. That is attested by the
fact that smaller attentional benefits due to attentional
orienting were present when targets were shown in the
near space, in comparison to the far space. Note that this
asymmetry in attentional allocation is congruent with the
asymmetry found by Andersen and Kramer [2], Downing
and Pinker [8], and Gawryszewski et al. [9].
3.2. Group 2: Virtual Body absent
The MANOVA run on data from this condition (see
Table 2) showed significant main effects of Type of Space
(F(1,9)512.31, P,0.007) and Type of Trial (F(1,9)5
12.27, P,0.007), whereas the interaction was not significant. Subjects were about 15 ms faster to respond to targets
shown in the far space (434 vs. 449 ms), and about 18 ms
faster to respond to validly cued targets (433 vs. 451 ms).
In addition, attentional benefits in near space were more
than twice greater than attentional benefits in far space.
This asymmetry is opposite to the one found in the body
present condition and is in accord with Andersen’s [1]
results.
4. General discussion
Our investigation has shown that VR is not only an
efficient way of controlling input variables, but may
provide unique information. In particular, we found that
having a virtual body framed our subjects’ central representation in a viewer-centred way, leading to a dense
distribution of attentional resources in the near space, close
to the subject’s body. In contrast, when the representation
of the body was lacking, attention was allocated in a rather
different way.
It is interesting to note that, although the level of
‘immersion’ 3 rendered by the VR set-up is rather high,
subjects were directly exposed to their virtual body for a
few minutes only at the beginning of the experiment.
Because of the relatively limited field of view, during the
experiment subjects remained mostly unaware of their
virtual body. Nevertheless, our results clearly showed an
effect of the virtual body on the distribution of attention:
attention was largely focused on the representation of the
3
Immersion refers to the extent to which a system generates streams of
sensory output that deliver an extensive, surrounding, vivid, and inclusive
virtual environment to a participant.
321
body, leading to an asymmetry. Conversely, the presence
in a virtual environment without a representation of the
body may have led to a relatively passive attitude toward
the experimental set-up. In this condition, subjects may
have felt as if they were observers rather than actors.
Pavlovskaya et al. [15] proposed that object recognition
is a dual-step process, in which the selection of the frame
of reference precedes identification / discrimination. In their
view, under simple conditions (i.e. single object analysis),
attention is allocated to the centroid of the display. In
contrast, when more complex visual configurations are
shown, the point of origin of the reference frame is chosen
separately for each discrete object. This process implies
frequent shifts of attention on the visual display. Their
results are in accord with those we reported here. Our
subjects seem to centre their attention at different locations
in relation to the way the depth plane and the body are
defined.
Our results are also in accord with those of previous
studies of 3D attentional orienting. The group provided
with a virtual body showed an attentional asymmetry in
depth that is similar to the one found by Andersen and
Kramer [2], Downing and Pinker [8], and Gawryszewski et
al. [9]. This asymmetry indicates that attention was
allocated in a viewer-centred fashion, with its resource
peak close to the subject’s body. In this condition, it was
more difficult to disengage attention from the near position, and to engage it on the far position, than the other
way round. Conversely, when subjects were not provided
with a virtual body, the attention asymmetry in depth
favoured far stimuli. As reported by Andersen [1], the
resource peak was further from the subject’s body, leading
to higher costs to switch from far to near positions.
Andersen [1] proposed that the direction of the
asymmetry he found was not congruent with the one
reported by Downing and Pinker [8] and by Gawryszewski
et al. [9] because of differences in the experimental
procedures. Later, Andersen and Kramer [2] pointed out
that showing stimuli at different depth planes through a
prism stereoscope may have led to a systematic overestimation of the size of the far distractors, and, in turn, to a
greater interference due to far distractors than to near ones.
They proposed that, when viewing the stereo images
through such a device, the optical axis of the eyes are
aligned in parallel and the convergence angle is zero.
Under this viewing condition, small variations in apparent
distance would have a relatively large effect on the
perceived size of the stimuli.
Although this explanation may be applicable to the
Andersen [1] study, our results suggest a different interpretation of the asymmetry he reported. In our experiment, the
viewing conditions were the same in either group: subjects
viewed the virtual world through a direct projection of it in
their eyes. The distance between the HMD and the
subject’s eyes was about 3 cm, actually much less than the
one employed by Andersen [1]. That is to say, in both the
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F. Maringelli et al. / Cognitive Brain Research 10 (2001) 317 – 322
body present and the body absent conditions the subject’s
eyes were aligned in parallel and information about
distance had to be derived from binocular disparity only. It
is worth noting that, in both conditions, subjects were
generally faster in responding to far targets than to near
targets. That may have been due to the perceptual factor
identified by Andersen. However, we showed that both
attentional asymmetries manifested themselves, depending
on the presence / absence of the virtual body.
Our results also support and extend several neuropsychological observations in favour of a dissociation
between representations of the visual world. It has been
proposed that different areas of the brain are involved in
processing the near, egocentric space and the far, allocentric space. Rizzolatti et al. [17], for example, showed a
double dissociation between impairment of near and far
visual information processing in monkeys, due respectively
to posterior or anterior brain damages. Observations on
human neglect (e.g. Refs. [3,6,7,10]) favour a functional
and anatomical specialisation of the human brain in
processing either near (personal and peripersonal) or far
(extrapersonal) stimuli. We reported similar asymmetry in
healthy subjects: the distribution of attentional resources is
related to the ‘suggested’ co-ordinates frame. In addition,
our results seem to favour a parallel organisation of two
largely independent attentional systems. Information falling within a near, reachable space seems to be represented
in terms of egocentric co-ordinates and selected by an
attentional system devoted to the analysis of this portion of
the visual space. Conversely, when information falls
outside the reachable space, its representation appears to be
largely allocentric and selection is carried on by a second
attentional system, working mainly on the far portion of
the visual space.
Finally, it is worth noting that our results are consistent
with a parallel organisation of two largely independent
attentional systems, although we did not provide direct
evidence about the neural organisation. That means that
the alternative hypothesis of a single neural system with
attention being placed at varying depth planes depending
on the display cannot be ruled out. However, because we
showed a different distribution of attentional resources in
the two experimental conditions, it would seem likely that
two mechanisms rather than a single mechanism are
involved. Information falling within a near, reachable
space seems to be represented in terms of egocentric
coordinates and selected by an attentional system devoted
to the analysis of this portion of visual space. Conversely,
when information falls outside the reachable space, its
representation appears to be largely allocentric and selection is carried on by a second attentional system, working
mainly on the far portion of visual space.
Acknowledgements
C.U. was supported by grants from CNR and MURST.
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