1085

Journal of Neurology, Neurosurgery, and Psychiatry 1994;57:1085-1090

Preserved leftward movement in left unilateral
spatial neglect due to frontal lesions
Sumio Ishiai, Sadakiyo Watabiki, Eiai Lee, Tadashi Kanouchi, Natsu Odajima

Department of
Rehabilitation, Tokyo
Metropolitan Institute
for Neuroscience,
Tokyo, Japan
S Ishiai
Musashino Red Cross
Hospital, Tokyo,
Japan
Department of
Neurology
S Watabiki
Departmnent of Speech
Therapy
E Lee
Department of
Neurology, Kakeyu
Hospital, Nagano,
Japan
T Kanouchi
Department of
Neurology, Saitama
Rehabilitation Centre
for the Disabled,
Saitama, Japan
N Odajima
Correspondence to:
Dr Ishiai, Department of
Rehabilitation, Tokyo
Metropolitan Institute for
Neuroscience, 2-6
Musashidai, Fuchu Tokyo,
183 Japan.
Received 7 October 1993
and in revised form
11 January 1994.
Accepted 7 February 1994

Abstract
Three patients with left unilateral spatial
neglect after predominantly frontal lobe
lesions were asked to extend a horizontal
line leftwards to double its original
length. In this line extension task, they
readily executed movements in or
towards the contralesional left space.
They performed the task in the left and
right hemispaces as well as in the midline. The mean extension lengths did not
differ significantly among these three
spatial conditions. These results suggest
that directional hypokinesia takes little
part in left unilateral spatial neglect due
to frontal lobe lesions. It is considered
that the patients could execute leftward
movements as the task oriented their
attention sufficiently to the left. Two of
the three patients, like reported cases
with frontal neglect, showed a typical
exploratory deficit for the left space in
the line cancellation test. Such a deficit
found in the traditional tasks, however,
does not mean the presence of directional
hypokinesia. All three patients showed
visual extinction on double simultaneous
stimulation. An attentional mechanism
seems to play a predominant part in unilateral spatial neglect due to frontal
lesions.

frontal lesions may produce multicomponent
neglect in which exploratory motor deficit is
relatively stressed. Several studies12-'5 reported
that exploratory motor deficit or directional
hypokinesial"4'1-9 (failure to execute movements fully in or towards the contralesional
space) predominates in unilateral spatial
neglect after lesions that involve the frontal
lobe as well as the parietal lobe. A few patients
with restricted frontal lesions20--22 showed
exploratory neglect without other obvious
signs of neglect.
Recently, Ishiai et al23 examined patients
with neglect and with right parietal lobe
lesions by means of a line extension task and
showed that directional hypokinesia takes little part in left unilateral spatial neglect. The
patients accurately extended a line leftwards
to double its original length, whatever the
severity of neglect found in the line bisection
test. They were considered to execute movements in or towards the contralesional space
as the task oriented their attention sufficiently
to the left. The present study applied the line
extension task to three patients with unilateral
spatial neglect due to predominantly frontal
lobe lesions to test if they had directional
hypokinesia and failed to perform the line
extension task.
Methods

(7 Neurol Neurosurg Psychiatry 1994;57:1085-1090)

Unilateral spatial neglect is the failure of brain
damaged patients to attend to and explore
stimuli presented in the space contralateral to
their lesions.' 2 Neglect in humans usually
occurs after right hemispheric lesions that
involve the parietal lobe,lA whereas in monkeys, it is a classical finding that neglect is
produced by frontal lobe lesions.56 Since the
report of Heilman and Valenstein,7 however,
frontal lobe lesions have also been known to
cause unilateral spatial neglect in humans,'89
although frontal neglect is infrequent compared with parietal neglect.47
Recent theories of unilateral spatial neglect
consider that neglect is a complex deficit with
multiple components, such as attentional,
exploratory-motor, and representational disorders.' 2 According to Mesulam's cortical
network theory for directed attention,'0"I the
frontal region centred around the frontal eye
field provides a mechanism for scanning and
exploring. Because the regions contributing to
directed attention are tightly interconnected,

LINE BISECTION TEST

All the subjects were first given a series of line
bisection tests.23 A line 200 or 100 mm long
was drawn horizontally across the centre of a
piece of A4 (210 x 297 mm) paper. Three
spatial conditions were examined: For the
centre condition, the paper with its line was
placed so that its centre lay in the sagittal midplane of the subject's trunk. For the right and
left conditions respectively, the left and right
edges of the paper were positioned in the
sagittal midplane of the trunk. The examiner
explained how to mark the centre by showing
an ideal bisection of a line, then asked the
subjects to bisect the lines presented in an
order randomised across the three spatial conditions and the two lengths. Each subject
bisected eight lines for each length in each of
the three spatial conditions, thereby completing 48 trials.
LINE EXTENSION TASK

After completion of the set of line bisections,
the subjects were tested for their ability to
extend a line leftwards to double its original
length.2' A horizontal line 100 or 50 mm long

Ishiai, Watabiki, Lee, Kanouchi, Odajima

1086

length in each of the three spatial conditions,
thereby completing 48 trials.
Case reports
All patients gave informed consent to participate in this study.
CASE 1

A 63 year old right handed woman had a
stroke on 19 December 1989. The present
examination was performed nine months after
the onset. At this time, CT showed an infarction that involved almost all the right frontal
lobe and its subcortical structures, as well as
the anterior part of the right temporal lobe
(figure, A). The patient had a left hemiplegia
and a left sided moderate sensory loss. There
was no visual field defect on confrontation
testing. She exhibited left sided visual extinction, however, on bilateral simultaneous stimulation. Typical left unilateral spatial neglect
was found on neuropsychological examination. She omitted left sided 15 of 30 lines in
the line cancellation test2425 and copied only
the right half of a figure of a daisy.' 26 In the
line bisection test26 27 with lines 200 mm long,
she placed the mark about 15 mm to the right
of the true midpoint.
CASE 2

CT showing the predominantly frontal lesions of cases 1 (A), 2(B), and 3(C).
Left is on the right of the images.
was printed on a piece of A4 paper so that its
left endpoint, marked with a small vertical

symbol, corresponded to the centre of the
paper. The subjects were asked first to put the
tip of a pencil held in the right hand on the

symbol. They then had to extend the line leftwards the length of the printed line. They
were told not to remove the pencil from the
paper before judging that the trial had been
completed. The examiner explained the procedure by showing an ideal extension. The
subjects then performed a practice trial, in
which they were advised not to cover the line
with the hand that held the pencil. Three spatial conditions were examined: For the centre
condition, the paper was placed so that its
centre, which corresponded to the left end of
the printed line with the small vertical symbol,
lay in the sagittal midplane of the subject's
trunk. For the right and left conditions
respectively, the left and right edges of the
paper were positioned in the sagittal midplane
of the trunk. Each subject performed the task
in randomised order eight times for each

A 59 year old right handed man suddenly
developed a left hemiplegia and a left sided
moderate sensory loss on 22 July 1990. The
present examination was undertaken a month
after onset. CT at this time revealed an infarction that involved almost all the right dorsolateral frontal lobe and its subcortical
structures, as well as the insula (figure, B).
The lesion extended to the postcentral gyrus.
The patient had no visual field defect but
showed visual extinction, omitting about 50%
of the left sided targets on bilateral simultaneous stimulation. Typical left unilateral spatial
neglect was found on neuropsychological
examination. He copied only the right half of a
daisy and omitted left sided 15 of 30 lines in
the line cancellation test. When bisecting
200 mm lines, he placed the mark about
10 mm to the right of the true midpoint.
CASE 3

A 66 year old right handed man was admitted
to hospital with a sudden headache on 16
August 1992. CT and angiography showed
the rupture of an aneurysm of the anterior
communicating artery. An operation on the
aneurysm was performed next day and an
apparent left hemiparesis appeared six days
later. The present examination was performed
seven months after the operation. At this
time, CT showed an infarction that involved
almost all the right frontal lobe and its subcortical structures, as well as the anterior half of
the right temporal lobe (figure, C). The
patient had no visual field defect but showed
left sided visual extinction on bilateral simultaneous stimulation. Mild left unilateral spatial neglect was found on neuropsychological
examination. He copied all the petals of a

Preserved leftward movement in left unilateral spatial neglect due to frontal lesions

1087

Table 1 Deviations from true midpoint in the line bisection test
Kruskal-

Spatial condition

Post hoc comparisons

Wallis

Case

Left

Centre

Right

1
2
3

18-5 (7-4)
8-0 (5-5)
30-1(3-9)

13-8 (5-8)
9-8 (4-8)
20-6(7-8)

0-5 (7-3)
1-6 (4-8)
-4-8(9-5)

1
2
3

5-3 (4-1)
3-5(1-7)
15-6 (2-9)

2-9 (3-6)
1-9(1-0)
5-6 (3-3)

-2-7 (4-3)
-2-6(2-1)
-4-9 (5-2)

test

200 mm line
p < 0-001
p < 0-025
p < 0-001
100 mm line
p < 0-025
p < 0-001
p < 0-001

LvC

CvR

LvR

NS
NS
NS

p < 0-01
p < 001
p < 0-01

p < 0-01
p < 005

p < 0-01

NS
NS
p < 0-05

p < 005
p < 0-01
p < 0-05

p < 001
p < 0-01
p < 0-01

Values are means (SD).

daisy but omitted its left leaf. Although the
copying of a daisy was examined only once,
the omission of the easily recognisable left leaf
(40 mm long and 16 mm wide) was considered to show the presence of neglect. Thirty
age matched control subjects never omitted
this part of the figure. He placed the mark
about 20 mm to the right of the true midpoint
when bisecting 200 mm lines. In the line cancellation test, however, he marked all the
lines.
Results
LINE BISECTION TEST

The distance between the true midpoint and
the mark showing the subjective midpoint was
measured to the closest millimetre and
expressed as positive if the mark deviated to
the right. Table 1 shows the mean deviations
from the true midpoint and the statistical
results concerning the spatial effect for each
patient. All the three cases placed the mark to
the right of the true midpoint in the left and
centre conditions for both the 200 and 100
mm lines. The mean deviations found in these
bisections were significantly greater than
those of the 10 age matched normal controls
in our previous study.2' The mean deviations
of the normal controls for the 200 mm lines
were 1.1 (SD 2-1) mm, 1-3 (2-4) mm, and 2-1
(3.2) mm for the left, centre, and right conditions respectively, and those for the 100 mm
lines were 0 4 (SD 1-5) mm, 0 5 (1-4) mm,
and 0-6 (1-3) mm. When bisecting 200 mm
lines in the right condition, cases 1 and 2
marked near the true midpoint and case 3
marked to the left of it. When bisecting 100
mm lines in the right condition, all the three
cases marked slightly to the left of the true
midpoint. The mean deviations were significantly different among the three spatial conditions for each of the two lengths for each case

(Kruskal-Wallis test). Post hoc comparisons
(non-parametric equivalent of Williams'
test28) showed that the mean deviations were
significantly greater for the centre than for the
right condition and for the left than for the
right condition.
LINE EXTENSION TASK

The length of the overextension was calculated by subtracting the ideal extension (100
or 50 mm) from the length of subject's extension measured to the closest millimetre. When
the extension was less than the ideal length,
the calculated value was treated as a negative
overextension. Table 2 shows the mean
overextensions and the statistical results concerning the spatial effect for each patient. The
mean overextensions were all positive for each
spatial condition for each line length. In our
previous study,2' the mean overextensions of
the 100 mm lines of the 10 normal controls
were 0-6 (SD 4 0) mm, 1-8 (4 0) mm, and 2-5
(4-3) mm for the left, centre, and right conditions respectively. Those of the 50 mm lines
were 2-2 (SD 6 2) mm, 2-2 (6 1) mm, and 2-8
(4.9) mm. The three cases of the present
study extended the 100 mm lines significantly
longer (about 10 mm) than the normal controls except when cases 2 and 3 extended the
lines almost accurately in the centre and right
conditions respectively. In the extension of 50
mm lines, the mean overextension for each
spatial condition was within the mean +2
SDs of the normal controls. The effect of the
three spatial conditions was not significant for
each length for each case (Kruskal-Wallis test).
Discussion
The three patients showed left unilateral spatial
neglect after predominantly frontal lobe
lesions. Their lesions extended to the postcentral gyrus or the subcortical structures, but

Table 2 Overextensions in the line extension task
Spatial condition
KruskalCase

Left

Centre

Right

Wallis
test

1
2
3

12-8 (4-6)
13-0(13-4)
11-7(10-9)

12-9 (3-7)
35(7-9)
13-4(7-9)

12-5 (32) NS
11-8(8-6) NS
98(10-3) NS

1
2
3

25 (1-9)
4-8 (8-6)
6-1 (64)

0-1 (4-1)
11-6 (12-6)
6-0 (59)

4-0 (8-3)
5-1 (7-5)
8-3 (8-9)

Values are means (SD).

Post hoc comparisons

LvC

CvR

LvR

NS
NS
NS

NS
NS
NS

NS
NS
NS

NS
NS
NS

NS
NS
NS

NS
NS
NS

100 mm line

50 mm line

NS
NS
NS

Ishiai, Watabiki, Lee, Kanouchi, Odajima

1088

not to the parietal region around the inferior
parietal lobule, where lesions are known to
cause unilateral spatial neglect."1A They readily
executed leftward movements in the line
extension task, in which they had to extend a
line leftwards to double its original length.
There was no significant difference in the
length of line extension among the left, centre,
and right conditions, although the line bisection errors were affected by these spatial conditions, as Heilman et al '7 reported. These
results suggest that an exploratory motor
component'01' 152022 or directional hypokinesia 2-1417-19 2 takes little part in left unilateral
spatial neglect due to frontal lesions. As we
did not record reaction times, our results do
not exclude the type of directional hypokinesia reported by Heilman et al18-namely,
prolonged reaction times for leftward movements. We found that the three patients
started to extend the lines leftwards, however,
immediately after presentation of the test
sheets.
Absence of directional hypokinesia has
been reported in neglect due to predominantly parietal lesions2329 but not in frontal
neglect. In our line extension task, the
patients seemed to look continually at the left
extreme of the line during the process of leftward extension, as fixation usually centres on
the pencil tip during manual drawing.2330
Selection of a motor plan should automatically produce a shift of attention towards the
spatial sector in which the action will be executed.3' We thus consider that the patients
could execute movements in or towards the
contralesional space as the line extension task
oriented their attention sufficiently to the left.
In the studies with traditional diagnostic
tasks for neglect, several authors5 20-22 have
emphasised an exploratory motor component
or directional hypokinesia in unilateral spatial
neglect due to frontal lesions. The patients of
Daffner et al 20 and Bottini et al,2' and patient 2
of Liu et al22 showed severe exploratory
neglect without other obvious signs of neglect.
Binder et al 15 found that the combination of
abnormal cancellation and normal line bisection was always associated with a frontal or
basal ganglia localisation. We also found that
two of the three patients with frontal lesions
(cases 1 and 2) neglected the left hemispace
typically in the line cancellation test but
bisected the lines with small rightward errors.
Case 3, however, who also had a large frontal
lesion, marked all the lines in the line cancellation test, whereas his rightward bisection
errors were greater than those of cases 1 and
2. Such a dissociation in performances in
these two tasks has been reported in patients
with lesions that involved the parietal lobe32
but not in patients with predominantly frontal
lesions. Despite the variability of neglect manifestations, however, all the three patients
readily executed leftward movements in the
line extension task. These findings suggest
that the traditional diagnostic tasks cannot
distinguish among the components of mechanisms underlying unilateral spatial neglect.
Not only unilateral spatial neglect itself but

also insufficient motivation for tasks25 may
affect performances in exploration tasks, such
as the cancellation test. Our cases 1 and 2
showed improvement of left unilateral spatial
neglect in the line cancellation test when
motivated with the use of numbering of lines
instead of simple crossing out.
Some experimental studies'3 14 33 tried to
differentiate an exploratory motor component
from an attentional component by decoupling
the direction of a visual stimulus and the
direction of hand or eye movement. The task
of Bisiach et al 13 was a modified line bisection
task with an apparatus with pulleys. The task
of Tegner et al 14 was a line cancellation task
with a looking glass. These groups of authors
suggested that the motor component or directional hypokinesia is more pronounced in
patients with lesions involving the frontal
lobe. The lesions of their patients were large,
however, and involved the parietal lobe as
well as the frontal lobe. The patient of Butter et
al 33 had a frontal infarction with only a slight
extension to the postcentral gyrus. After left
sided inattention abated, the patient showed
directional hypokinesia of eye movement only
when a stimulus on the right required a leftward eye movement. Although the deficits
found in these crossed motor tasks seem to be
explained by directional hypokinesia, other
factors may affect the performances of
patients with frontal lesions. The crossed
motor tasks are difficult in that when patients
desired to move the pointer for bisection"3 or
the hand image through mirror view'4 to the
right (or left), they had to move the hand
oppositely to the left (or right). Some of the
patients of Tegner et al 14 showed difficulties
for hand movements towards either side in the
mirror view condition. Frontal patients have
difficulty in following rules34 and tend to continue their automatic action regardless of the
instructions that they have just received.'5 In
the line extension task, the site and direction
of motor execution correspond to those of
attention as in the other typical tests for
neglect, such as the line cancellation test,2425
the line bisection test,26 27 and the copying of
figures.' 26 We therefore consider that absence
of directional hypokinesia shown in the line
extension task is convincing. The present
study did not examine the three patients with
the tasks of Bisiach et al 13 and Tegner et al.'4
Further studies that contrast performances in
these tasks and the line extension task should
contribute to our understanding of the mechanisms of unilateral spatial neglect due to
frontal lesions.
After a unilateral frontal eye field lesion,
monkeys tend to deviate the eyes and the head
towards the side of the lesion, show rare spontaneous eye movements contralateral to the
lesion, and neglect stimuli in the contralateral
space.56 Incapacity to move towards the contralesional stimuli cannot fully explain their
unilateral spatial neglect. Latto and Cowey5
reported that these monkeys could not
respond to visual stimuli presented contralateral to the lesion even when the required
response was the pressing of a lever with the

Preserved leftward movement in left unilateral spatial neglect due to frontal lesions

preferred hand. Rizzolatti et a16 reported that
the presentation of contralesional threatening
stimuli does not elicit emotional responses.
Furthermore, after the oculomotor disturbance had disappeared, the monkeys still preferred the ipsilateral visual stimulus in the test
with two stimuli in far space. In the present
study, we examined all the three patients one
month or more after onset. None of them
showed any obvious deviation of the eyes or
head towards the right. The range of eye
movement was not restricted on routine
neurological examination. All of them, like
most of the reported cases with frontal
neglect,7 9 21 33 showed visual extinction on
double simultaneous stimulation. Attentional
mechanism' thus seems to play a predominant
part also in human unilateral spatial neglect
due to frontal lesions. The results of the present study suggest that the underlying mechanism is essentially the same in frontal and
parietal neglect. The patient of Daffner et a120
and patient 2 of Liu et a122 showed exploratory
motor neglect but did not, however, exhibit
visual extinction. They had smaller frontal
lesions than our patients whose lesions
involved most of the frontal lobe. To clarify
the nature of frontal neglect in humans, we
need further studies on patients with frontal
lesions of various sizes and sites in either acute
or chronic phase.
All the three frontal patients extended 50
mm lines accurately but extended 100 mm
lines about 10 mm longer than the normal
controls. Ishiai et al23 reported that the
patients with unilateral spatial neglect due to
parietal lesions accurately performed the line
extension task for both line lengths (50 and
100 mm), whatever the severity of neglect
found in the line bisection test. Thus we do
not consider that the excessive extensions by
the patients with frontal lesions resulted from
unilateral spatial neglect. The excessive extension might be caused by continuous perseverance36 or visual grasp3337 that was disengaged
by frontal lesions, although at present, we do
not know why it occurred for only the longer
lines.
Patients with left unilateral spatial neglect
sometimes bisect lines with greater deviations
in the left hemispace than in the midline and
in the midline than in the right hemispace.1723
Our patients with frontal lesions also showed
such a spatial effect in the line bisection test.
As both the patients with frontal lesions and
those with parietal lesions23 could readily execute leftward movements, directional hypokinesia cannot explain the spatial effect. This
effect may result from attentional imbalance,'8
with attention biased to the right side after
right hemisphere damage. The leftward deviations found in our patients' bisection in the
right condition, however, seem paradoxical to
this explanation. Patients with neglect with
parietal lesions may also occasionally show
leftward bisection errors in the right hemispace.2326 Ishiai et at'6 considered that unilateral spatial neglect cannot be excluded by the
absence of rightward deviation, because they
found the eye fixation pattern characteristic of

1089

unilateral spatial neglect in such bisections.
They, however, analysed the eye fixation pattern only from the time of the first fixation on
the stimulus line. What determines the point
on the line at which patients with neglect first
fixate remains unspecified.26 Marshall and
Halligan39 interpreted the line bisection performances of patients with neglect in terms of
two constructs: the size of the Weber fraction40 (the "just noticeable difference"
between two magnitudes) and the attentional
direction of approach to a psychological
"indifference zone", the extent of which is
determined by the Weber fraction. Patients
with left unilateral spatial neglect may usually
adopt a right to left scan track of attention and
place the mark when the scan reaches the
indifference zone that is expanded consequent
on cerebral damage. When asked to bisect a
line in the right hemispace, however, our
patients had first to search toward the right
space where the line was presented, as they
showed no deviation of the eyes or head when
no visual stimulus was presented. According
to the interpretation by Marshall and
Halligan,'9 in the right condition, they may
have approached from the left endpoint to the
indifference zone and placed the subjective
midpoint to the left of the true midpoint.
Once neglect patients fixate a point on the
line, they tend to persist with this point.26 The
first rightward search may thus have had a
strong effect on the bisection in the right
hemispace.

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