Dissociation of body-centered and
stimulus-centered representations in
unilateral neglect
H. Ota, MSc; T. Fujii, MD; K. Suzuki, MD; R. Fukatsu, MD; and A. Yamadori, MD

Article abstract—Background: Previous studies on unilateral neglect have shown that there are at least two types of
neglect—i.e., body-centered and stimulus-centered neglect. These symptoms suggest that the human brain has at least
two different reference frames for processing external space. It is unknown, however, whether these two frames are
represented independently in the brain and if so, which areas (or networks) of the brain are responsible for each frame of
reference. Objective: To determine whether body-centered neglect and stimulus-centered neglect can be dissociated in
patients with brain injury. Methods: New figure discriminative cancellation tasks were designed to simultaneously assess
body-centered neglect and stimulus-centered neglect. Two neglect patients with lesions located in different anatomic
regions were required to circle every complete figure and to cross out every figure with a missing portion on a sheet of
white (29.7 ⫻ 42 cm) paper. Results: Patient 1 omitted leftward stimuli on the paper, but the stimuli he found were
correctly circled or crossed out. On the other hand, Patient 2 marked stimuli across the paper although he mistakenly
circled stimuli that were missing a portion of their left side. Neither patient manifested interaction between the two types
of neglect. Conclusion: The results of this study clearly showed double dissociation between the two types of neglect.
Furthermore, it not only provides evidence that there are two distinct systems of reference frame for external space in the
human brain, but also adds new knowledge indicating that these two systems function independently, at least in part.
NEUROLOGY 2001;57:2064 –2069

Unilateral neglect (UN) is defined as the failure to
attend to the side of contralesional space.1 This
symptom is often observed as left UN following damage to the right hemisphere. Previous studies have
reported different types of UN, suggesting that there
are different kinds of spatial representations that
likely reflect different aspects of spatial information
processing. It remains unknown, however, whether
these different frames are represented independently in the brain and if so, which areas (or networks) of the brain are responsible for each frame of
reference.
Previous studies on UN have shown the possible
presence of two frames of reference for external
space—i.e., viewer-centered and stimulus-related
frames. The viewer-centered frame is defined in relation to the midline of the body (or trunk) or body
parts and may be subdivided into retino-, head-, and
body-centered frames.2-10 Many researchers have argued that the body-centered frame is disrupted in
neglect patients.2,5-7,9
Stimulus-related neglect is an omission or inattention to one side of a stimulus irrespective of its
location in relation to the body and had been described as stimulus-centered11-14 or object-centered
neglect.15-20 Stimulus-centered neglect is defined as

an omission or inattention to the contralesional side
of an individual stimulus irrespective of whether the
stimulus has a canonical axis or not. In this type of
neglect, the direction of the gravity is applied as a
referential axis. Object-centered neglect is defined as
an omission or inattention to the contralesional side
of an individual object in canonical orientation and,
by definition, it is observed only when the stimulus
has a canonical axis. Axis-based neglect21 is a kind of
object-centered neglect because the neglected side of
an object is determined by the reference axis.
Some investigators have reported that bodycentered and stimulus-centered frames were simultaneously disrupted, suggesting that these two
frames of reference are not independent, but are
based on a certain common mechanism or an interacting mechanisms.22,23 From a review of UN studies,
it was concluded that body-centered and stimuluscentered neglect may not be clearly separated.24 So
far, no report has shown that body-centered and
stimulus-centered frames of reference function independently when stimuli to be attended to and stimuli
used as a frame are identical.
We investigated the effect of the body-centered
and stimulus-centered frames of reference on two
UN patients to elucidate whether the two frames can

From the Division of Neuropsychology (H. Ota and Drs. Fujii, Suzuki, and Yamadori), Department of Disability Medicine, Tohoku University Graduate
School of Medicine, Sendai; and Department of Neurology (Dr. Fukatsu), Miyagi National Hospital, Miyagi, Japan.
Part of this study was supported by a grant in aid to A.Y. for scientific research from the Ministry of Education, Science, and Culture of Japan (08279103)
and by a grant from the Japan Society for the Promotion of Science (JSPS-RFTF97L00202).
Received February 15, 2001. Accepted in final form August 29, 2001.
Address correspondence and reprint requests to Hisaaki Ota, Division of Neuropsychology, Department of Disability Medicine, Tohoku University Graduate
School of Medicine, 2-1, Seiryo-machi, Aoba-ku, Sendai 980-8575, Japan; e-mail: hisaaki@mail.cc.tohoku.ac.jp
2064 Copyright © 2001 by AAN Enterprises, Inc.

Figure 1. CT scan of Patient 1 performed 9 months after the onset. The
lesion was located mainly in the right
putamen and the superior and posterior
subcortical portions of the surrounding
areas, the right insula, the anterior superior temporal gyrus, and the posterior inferior frontal gyrus. The left side
of the figure is the right side of the
brain.

be differentially damaged. For this purpose, newly
developed figure discriminative cancellation tasks
were employed.

ing the inferior parietal lobule and the posterior part of the
superior and middle temporal gyri. A small infarction in
the left putamen was also detected (figure 2).

Patients and methods. Patients. Two patients with
UN participated: Patient 1 9 months after the stroke and
Patient 2 5 months after the stroke. Patients gave their
informed consent prior to study.
Patient 1 was a 55-year-old, right-handed male truck
driver. He had right hemisphere intracerebral hemorrhage. On neurologic examination, he showed left homonymous hemianopia by confrontation, but had no limitation
of eye movement. He had a severe left hemiparesis including the face, a mild left sensory disturbance, and severe
left UN. On a 240-mm line bisection task, his subjective
midpoint was deviated 14.3% to the right. On a circle
crossing out task,25 he omitted stimuli on the left side of
the stimulus paper. A brain CT scan 9 months after the
stoke showed an extensive lesion involving mainly the
right putamen, the superior and posterior subcortical portions of the surrounding area, the right insula, the anterior
superior temporal gyrus, and the posterior inferior frontal
gyrus (figure 1).
Patient 2 was a 70-year-old, right-handed man who had
retired from fishery. He had right hemisphere cerebral
infarction. He had a history of subarachnoid hemorrhage
due to the rupture of an aneurysm of the right middle
cerebral artery and had undergone a clipping operation 23
years previously. This episode did not result in any aftereffects. On neurologic examination, he showed a left homonymous hemianopia by confrontation. There was no
limitation of eye movement. Severe left hemiparesis, including the face, and a left-sided sensory disturbance were
present. On a 240-mm line bisection task, his subjective
midpoint was deviated 11.7% to the right, but there was no
omission on the circle crossing out task.25 A brain CT scan
6 weeks after the stroke showed a large infarction in the
territory of the right middle cerebral artery, mainly involv-

Methods. Stimuli. To search for body-centered or
stimulus-centered neglect, new figure discriminative cancellation tasks were designed for this study.
Circle discriminative cancellation task. Twenty circles
and forty pseudo-circles, each with a diameter of 15 mm,
were drawn in a random manner on a sheet of white paper
(29.7 ⫻ 42 cm) and were arranged evenly on either side of
the vertical midline of the paper. Half of the pseudo-circles
had a missing portion on the right side, and the rest had a
missing portion on the left side. The size of the missing
portion of a pseudo-circle was one sixth of the circumference of the circle. Thus, it looked like a C or a reversed C.
Triangle discriminative cancellation task. Twenty
equilateral triangles and forty pseudo-triangles, each with
15-mm sides, were drawn in a random manner on a sheet
of white paper (29.7 ⫻ 42 cm). They were arranged evenly
to each side of the vertical midline of the paper. Half of the
40 pseudo-triangles had a missing portion on the right
side, and the rest had a missing portion on the left side.
Half of the three kinds of triangles were inverted. Each
triangle, with one-third of its apex missing at either side,
was like a tilted isosceles trapezoid, because the cut end
was closed, unlike the pseudo-circle, which was left open.
Procedure. A session consisted of four trials—i.e., two
circle and two triangle discriminative cancellation tasks.
The same tasks were performed successively so as not to
complicate a session; e.g., the first two trials were circle
discrimination tasks, the last two were triangle discrimination tasks. In the second application of each task, the
stimulus paper was presented upside down. Another session comprised of the same four trials was performed on
another day. Thus, each patient performed eight trials
(four circle and four triangle discriminative cancellation
tasks).
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Figure 2. CT scan of Patient 2 performed a month after the onset, showing a lesion in the territory of the right
middle cerebral artery. The lesion
mainly involved the inferior parietal
lobule and the posterior superior and
middle temporal lobes. A small infarction in the left putamen was also
present.

The patient was seated at a desk. Each stimulus sheet
was placed on the desk at the midsagittal plane of the
patient’s body. The patients were instructed to circle every
complete circle (or triangle) and to cross out every incomplete circle (or triangle) with a pen held in the right hand.
No restrictions were imposed on movement of the head or
eyes. When they finished a task, they were asked whether
they had checked all of the stimuli, and whether they were
sure they had not made any mistakes. There was no time
limit.
Analysis. Omissions on a left side of the paper were
regarded as body-centered neglect. Circling of a stimulus
with a missing left portion was regarded as stimuluscentered neglect.
To investigate body-centered and stimulus-centered neglect, two analyses were carried out for each patient. The
first analysis was performed to examine whether bodycentered neglect was present using the total number of
responses. The total number of stimuli that were either
circled or crossed out was calculated, regardless of whether
subjects made correct judgments about which stimuli to
circle or cross out. Second, to investigate whether
stimulus-centered neglect was present, the number of
stimuli that were correctly circled and crossed out (consistent with appropriate attention to and processing of both
sides of the pertinent stimulus) was calculated. Each patient’s data were analyzed using two-way analysis of variance (ANOVA) with the body-centered frame (right, left)
and stimulus-centered frame (left side missing, no missing
part, and right side missing).
Results. Figures 3 and 4 show typical performances of
each patient. The number of responses (body-centered effect). Patient 1. The results of ANOVA revealed a main
effect for the body-centered frame (F ⫽ 32.06, df ⫽ 1,42; p
⬍ 0.001). There were fewer responses for the left side of
the body-centered frame (M ⫽ 17.00, SD ⫽ 9.96) than for
the right side (M ⫽ 29.00, SD ⫽ 1.07). There was no main
2066 NEUROLOGY 57

December (1 of 2) 2001

effect for the stimulus-centered frame (F ⫽ 0.38, df ⫽ 2,42,
ns; left side missing: M ⫽ 15.38, SD ⫽ 3.38; no missing
part: M ⫽ 14.63, SD ⫽ 2.92; right side missing: M ⫽ 16.00,
SD ⫽ 3.63), and no interaction between these two factors
(F ⫽ 0.45, df ⫽ 2,42, ns).
Patient 2. The results of ANOVA showed no main effects for either the body-centered frame (F ⫽ 0.78, df ⫽
1,42, ns; left side of the body: M ⫽ 28.38, SD ⫽ 1.69; right
side of the body: M ⫽ 27.50, SD ⫽ 4.21), or the stimuluscentered frame (F ⫽ 0.48, df ⫽ 2,42, ns; left side missing:
M ⫽ 18.75, SD ⫽ 2.19; no missing part: M ⫽ 18.50, SD ⫽
1.69; right side missing: M ⫽ 18.63, SD ⫽ 2.07). There was
no interaction between these two factors (F ⫽ 0.16, df ⫽
2,42, ns).
Figure 5 shows the mean number of total responses for
each stimulus in the left and right space.

Figure 3. Example of Patient 1’s typical performance. The
left side of the sheet was located on the left side of the
body axis.

Figure 4. Example of Patient 2’s typical performance.
The number of correct responses (stimulus-centered effect). Patient 1. The results of ANOVA revealed a main
effect of the body-centered frame (F ⫽ 31.35, df ⫽ 1,42; p ⬍
0.001). There were fewer correct responses for the left side
of the body-centered frame (M ⫽ 17.00, SD ⫽ 9.96) than
for the right side (M ⫽ 28.75, SD ⫽ 0.89), indicating that
he responded to fewer stimuli on the left side of the paper
than on the right. There was no main effect for the
stimulus-centered frame (F ⫽ 0.38, df ⫽ 2,42, ns; left side
missing: M ⫽ 15.25, SD ⫽ 3.58; no missing part:
M ⫽ 14.50, SD ⫽ 2.83; right side missing: M ⫽ 16.00,
SD ⫽ 3.63) and no interaction between these two factors
(F ⫽ 0.38, df ⫽ 2,42; ns).
Patient 2. The results of ANOVA revealed a main effect for the stimulus-centered frame (F ⫽ 27.27, df ⫽ 2,42;
p ⬍ 0. 001). There was no main effect for the body-centered
frame (F ⫽ 0.77, df ⫽ 2,42, ns; left side of the body: M ⫽
23.00, SD ⫽ 3.89; right side of the body: M ⫽ 21.50, SD ⫽

Figure 5. Mean number of total responses for each stimulus in the left and right space. Solid columns represent
mean number of responses for stimuli that had a missing
portion of their left side, open columns for stimuli that
had no missing portion, and hatched columns for stimuli
that had a missing portion for their right side. The lines
above each column represent the SD of the mean.

Figure 6. Mean number of correct responses for each stimulus in the left and right space. Solid columns represent
mean number of correct responses for stimuli that had a
missing portion of their left side, open columns for stimuli
that had no missing portion, and hatched columns for
stimuli that had a missing portion for their right side.
The lines above each column represent the SD of the
mean.
4.69) and no interaction between these two frames (F ⫽
0.40, df ⫽ 2,42; ns). Post-hoc analysis using Fisher’s protected least significant difference method revealed that
correct responses were fewer for the left side missing stimuli (M ⫽ 8.86, SD ⫽ 5.38) than for the no missing part
stimuli (M ⫽ 18.00, SD ⫽ 1.69; p ⬍ 0.001) and the right
side missing stimuli (M ⫽ 17. 63, SD ⫽ 2.32; p ⬍ 0.001).
No difference was found between the number of correct
responses for stimuli with no missing part and for those
with the right side missing.
Figure 6 shows the mean number of correct responses
for each stimulus in the left and right space.

Discussion. In this study we developed a task that
distinguishes body-centered and stimulus-centered
neglect within one task. Neglect that could be identified as failure to attend to the stimuli on a sheet of
paper in relation to the midline of the body was
regarded as body-centered neglect, whereas neglect
that could be identified at the level of a component
stimulus was regarded as stimulus-centered neglect.
The multiple line bisection task,26 in which subjects
are asked to bisect each of the horizontal lines distributed across a white paper, may fulfill the same
objectives as our new task, if the lines do not go
across the midline of a stimulus paper. The original
line cancellation task,27 in which subjects are requested to check every line across a white paper,
may also fulfill the same objectives if the lines are
arranged horizontally and we ask subjects not to
simply check but to bisect each of the lines.
Patient 1 omitted more stimuli on the left side of
the stimulus paper irrespective of the types of stimulus. Yet for the stimuli he marked, responses were
fairly accurate. There was no interaction between
body-centered neglect and stimulus-centered neglect
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2067

with regard to either the total number of responses
or correct responses. Thus he showed body-centered
neglect without stimulus-centered neglect. In contrast, Patient 2 responded to stimuli on both sides of
the paper, but he made more mistakes with the stimuli having a missing portion on the left than with the
other two types of stimuli. No interaction was detected between the two types of neglect with regard
to either the total number of responses or correct responses. He thus showed stimulus-centered neglect
without body-centered neglect. This double dissociation
is most interesting as it suggests that the underlying
mechanisms that support the two types of attention—
i.e., body-centered attention and stimulus-centered attention— can operate independently.
Body-centered attention or a body-centered frame
of reference for spatial vision has been extensively
studied. Ocular exploration of left neglect patients
was found to deviate to the right in darkness.7 The
reaction time to stimuli located in the left visual field
was prolonged in left neglect patients, but shortened
when they rotated their trunks to the left.5 Tactile
exploration is also improved when stimulus is presented to the right relative to the body.9 These data
suggest the importance of the body-centered frame
for spatial attention. Other studies have reported
that left neglect patients showed deviation of the
pointing hand to the right relative to the body when
they were asked to point straight ahead.2,6 This general deviation of body-centered attention toward the
right can be explained as a disruption of the frame of
body-centered reference on the left. Neglect shown
by Patient 1 belongs to this type.
Stimulus-centered attention or a stimuluscentered frame of reference for spatial vision has
also been well studied. Some patients with left neglect failed to copy the left side of each figure in a
scene.28 Patients with stimulus-centered neglect misread the left portion of words12,13 and omitted the left
side of pictures.11 Another patient omitted the left
side of a chimeric face even when it was presented in
the right space of the body.14 Furthermore, a neglect
patient was able to recognize the right contour of a
geometric figure on the left side of a page, but failed
to recognize its left contour located on the right side
of the page.29 These cases were interpreted as showing disruption of attention toward an object, but not
toward the wider space. Similarly, subjective midpoints on the line bisection task deviated to the right
even when lines were placed in the right hemispace
relative to the midline of the body, indicating the
effect of stimulus-centered neglect.8 Patient 2’s neglect belongs to this type of neglect.
Some studies have attempted to manipulate two
types of attentional frames in the same subject. For
instance, neglect patients were asked to take photographs so that an object appeared to be in the center.
Some put the object on the right side, showing bodycentered neglect, whereas others put the object on
the left side, showing stimulus-centered neglect.30
Even though neglect patients may show only one
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December (1 of 2) 2001

type of neglect, it is impossible to evaluate how much
another type of neglect contributes to their performance. Another study reported that one patient with
neglect misread first letters of words irrespective of
their spatial positions, whereas another patient with
neglect misread the first letters of words and his
performance became worse when the words were
presented to the left.31 From these results, it is possible to say that the stimulus-centered frame may be
disrupted alone, but it is not clear whether the bodycentered frame may be disrupted alone, because the
latter seemed to show both stimulus-centered and
body-centered neglect. In another study,22 line drawings of various objects within which letters were randomly scattered were used to dissociate stimuluscentered and body-centered representation. Left
neglect patients were asked to identify a drawing on
a sheet of paper and read all the letters in it. Subjects’ axes were changed 90 degrees by having them
lie down on either side, while the paper’s axis was
changed 90 degrees by rotating it clockwise or counterclockwise to manipulate the axis of representational reference. Based on their results, the authors
concluded that both types of reference were affected
to the same degree in their left neglect patients.
However, recent reanalysis32 of their data showed
that the two references were in fact differentially
affected. Thus, one patient showed body-centered neglect only, and the others showed stimulus-centered
neglect only. This finding is consistent with the current results. However, there is a difference between
two studies that should be emphasized. In their
study, the stimulus used to detect stimulus-centered
neglect (letter) and that used as a stimulus-centered
frame (drawing) were different. In our study the
stimuli served for both references. In this regard, the
testing method employed in this study is more suitable for dissociating the two types of neglect.
We interpreted the results of this study within the
context of body-centered and stimulus-centered
frames of reference. Alternatively, our results may
be interpreted as a dissociation between a disorder of
intention and attention,1 or between exploratorymotor and sensory-perceptual components of
attention.33
It is clear that the type of attention needed to
span the whole paper must employ motor or intentional activity such as ocular scanning or head motion more often than the type of attention needed to
identify a small target like a triangle or a circle.
Unfortunately, we have not collected the kind of data
that would allow us to address the relationship between the traditional attentional theories of neglect
and the reference frame theory of neglect.
Patient 1 had lesions in the right putamen, its
surrounding region including the insula, the anterior
portion of the superior temporal gyrus, and the posterior portion of the inferior frontal gyrus. Patient 2
had cortico-subcortical lesions in the right parietotemporo-occipital area. Both types of neglect have
been reported in patients with lesions in the right

parietal area, although the extent of lesion is not
consistent even with the same type of neglect.6,9,14,25,29
With the extensive lesions of the two patients in
this study, it is difficult to make anatomic-behavioral
correlations between lesion sites and the two types of
neglect, but it may be speculated that body-centered
neglect of Patient 1 was more closely related to the
anterior and medial extension of lesions than those
of Patient 2, whereas the stimulus-centered neglect
was more closely related to the lateral and posterior
extension of the lesions than those of Patient 1. This
locational difference is not inconsistent with the notion33 that the right frontal lobe and its connections
with basal ganglia subserve an exploratory-motor
component of attention, whereas the right parietal
lobe subserves the sensory-perceptual component of
attention. To elucidate areas responsible for the dissociable functions, further data are needed for both
behavioral and lesion analyses, regardless of which
of the theories best explains the data.
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Dissociation of body-centered and stimulus-centered representations in unilateral
neglect
H. Ota, T. Fujii, K. Suzuki, et al.
Neurology 2001;57;2064-2069
DOI 10.1212/WNL.57.11.2064
This information is current as of December 11, 2001
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