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Brain (1996), 119, 851-857

Beyond unilateral neglect


Edoardo Bisiach,
1
Luigi Pizzamiglio,
23
Daniele Nico
2
'
3
and Gabriella Antonucci
2
-
3
1
Dipartimento di Psicologia, Universita di Torino, Correspondence to: E. Bisiach, 22070 Lurago Marinone
2
Dipartimento di Psicologia, Universita di Roma and the (Como), Italy
3
IRCCS Clinica S. Lucia, Roma, Italy
Summary
When required to set the endpoints of an imaginary horizontal
line of a given length on the basis of its midpoint printed on a
sheet of paper, left neglect patients most frequently misplaced
endpoints leftwards. Though giving rise to the very same
disproportion usually found with these patients on canonical
line bisection tasks, this behaviour cannot be accommodated
by current explanations of unilateral neglect. When the task
was executed during leftward optokinetic stimulation (OKS),
a manoeuvre known temporarily to improve neglect symptoms,
the disproportion increased instead of vanishing. We therefore
suggest that unilateral neglect is a manifestation of a disorder
primarily implying a horizontal anisometry of space repres-
entation and that manipulations such as OKS may remove
neglect without normalizing the representational medium
itself.
Keywords: unilateral neglect; space representation; optokinetic stimulation
Abbreviations: OKS = optokinetic stimulation
Introduction
Damage to specialized circuits within one cerebral hemisphere
(most frequently and distinctly the right hemisphere) is
known to give rise to misrepresentation of the contralateral
side of single objects or more complex stimulus arrays,
including the patient's contralesional body parts (Bisiach and
Vallar, 1988). So far, the defective aspects of the disorder,
namely unilateral neglect, have captured most of the
researchers' attention and very little effort has been made
to integrate their interpretation with the interpretation of
productive phenomena such as somatoparaphrenia, i.e.
disavowal of contralesional body parts (Gerstmann, 1942).
The latter may combine with neglect and, most important,
may temporarily be removed like neglect by vestibular
stimulation (Bisiach et al., 1991; Rode el al., 1992;
Ramachandran, 1995). A change in research strategy appears
now to be demanded following the results of a recent
investigation (Bisiach et al., 1994) that have revealed, in left
neglect patients, a behavioural disorder uninterpretable along
the lines of current explanations of unilateral neglect, recently
brought collectively into question by Marshall and Halligan
(1994). In that investigation, two right brain-damaged patients
showing symptoms of contralesional neglect were given a
modified version of the time-honoured line bisection task.
Patients were first asked to mark the midpoint of a 15 cm
long horizontal line, where they made, as expected, the
typical rightward error. Thereupon, they were asked first to
Oxford University Press 1996
bisect the empty space between two dots corresponding to
the endpoints of the previously shown line, and then to set
both endpoints of an equally long (horizontal) virtual line on
the basis of its midpoint, printed at the centre of an A4 sheet
of paper. In executing the third of these tasks, both patients
misplaced the endpoints of the virtual line leftwards with
respect to one another and to the printed midpoint. This
resulted in a marked disproportion of the segments lying on
each side of the central point: namely, the very same
disproportion usually yielded by left neglect patients on the
canonical version of the line bisection task. In the case at issue,
however, such a disproportion cannot be readily explained by
current interpretations of unilateral neglect, overfocusing on
the defective aspects of patients' behaviour: indeed, it cannot
be entirely disposed of as consequent upon defective attention
within the contralesional hemispace (e.g. Heilman et al.,
1987), release of an attentional vector pointing towards the
ipsilesional side (Kinsbourne, 1987), impaired disengagement
of attention from ipsilesional stimuli (Posner et al., 1982),
contralesional loss of representational space (Bisiach and
Luzzatti, 1978), ipsilesional deviation of the egocentric frame
of spatial reference (Jeannerod and Biguer, 1987) or unilateral
directional hypokinesia, i.e. failure to initiate and complete
movements towards the contralesional side of space (Heilman
etal., 1985).
It is well known that manifestations of unilateral neglect

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852 E. Bisiach et al.
may transitorily disappear during vestibular stimulation (e.g.
Rubens, 1985; Cappa et al., 1987), OKS (Pizzamiglio et al.,
1990), neck muscle vibration (Karnath et al., 1993),
transcutaneous electrical neural stimulation (Vallar et al.,
1995) or, in patients without hemiplegia, during the execution
of finger movements with the contralesional hand in the
contralesional hemispace (Robertson and North, 1992). A
critical problem arises at this point. The results of all these
manoeuvres may indeed depend on either (i) true transitory
restoration of neural circuits to a normal functional level, or
(ii) temporary suppression or mitigation of a symptom,
leaving the underlying (distorted) spatial representation
unchanged. With no grounds for a priori predictions, we
addressed this problem by asking right brain-damaged patients
with and without left neglect to execute the modified line
bisection task during leftward or rightward OKS. The results
we obtained were in clear-cut support of the second
alternative.
Methods
Subjects
Two groups of subjects suffering from the consequences of
a vascular lesion were examined: 10 right brain-damaged
patients (Patients 1-10) with mild to severe visual neglect
(N + ), and 10 right brain-damaged patients (Patients 11-20)
without visual neglect (N-) as assessed by means of a
routine battery (Pizzamiglio et al., 1990) consisting of the
following tests.
Routine tests
Line cancellation
The patient is asked to cross out 21 slanted lines (2.5 cm)
randomly distributed over an A3 sheet of paper, 11 on the
left and 10 on the right half. The scores are the number of
lines crossed out on each half of the stimulus array.
Letter cancellation
The patient is asked to cross out 104 upper-case letter Hs
interspersed with 208 distractors; 53 targets are distributed
over the left and 51 over the right half of an A3 sheet of
paper. The scores are the number of letters crossed out on
each half.
Sentence reading
The patient is asked to read aloud six sentences ranging from
five to 11 words (21-42 letters). The score is the number of
correctly read sentences.
WundtJastrow illusion
Stimuli are two identical black fans shown one above the
other in such a way that one of them appears to be horizontally
Table 1 Clinical features ofN+ (1-10) and N- (11-20)
patients
Patient
no.
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
Sex
F
M
M
M
F
F
M
F
M
M
M
F
F
M
M
F
M
M
F
F
Age
69
45
55
68
73
63
63
65
69
72
42
75
61
65
56
73
67
65
46
74
Length of
illness (months)
93
25
12
4
4
12
33
4
18
3
11
20
6
3
4
9
1
16
3
10
Lesion site*
_
FTP
P.IC
TP (subc)
BG, IC
FT
TP
PO
TP, IC, CS
PO
TP
CS
TPO
FT
CI
TP (subc)
BG
Corona radiata
_
-
-, Missing data. *F = frontal; O = occipital; P = parietal;
T = temporal; CS = centrum semiovale; IC = internal capsule;
BG = basal ganglia; subc = subcortical.
wider. Forty pairs, 20 with left-side and 20 with right-side
illusory effect are shown in a fixed random order. The illusory
effect is reduced in neglect patients on the contralesional
side (for details, see Massironi et al., 1988). The scores are
the number of trials in which the normal illusory effect is
present on each side.
Contralesional motor impairment was slightly more
pronounced in N+ patients. Left hemianopia was found in
Patient 1 (N+) and in Patients 11 and 13 (N). Contralesional
visual extinction on double simultaneous stimulation was
found in Patients 2, 3, 4, 5, 8, and 9 (N+).
Informed consent was obtained from each subject.
Individual data are shown in Tables 1 and 2.
Tasks
Subjects were given the three tasks employed by Bisiach
et al. (1994). The stimuli used in the experiment were printed
in black and centred on A4 transparency films stuck in the
middle of the screen of a NEC MultiSync 5FG computer
monitor.
Task 1
Subjects were required to mark with a soft pen the midpoint
of a 15 cm long and 1 mm wide horizontal line.
Task 2
Only the endpoints of the line were shown; subjects were
required to bisect the virtual line (i.e. the empty space
between the two points) as in Task 1.

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Beyond unilateral neglect 853
Table 2 Scores of N+ (1-0) and N- (11-20) patients on the neglect test battery
Patient
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
-, Missing
Line
cancellation
9/11
9/11
2/11
1/11
8/11
0/11
11/11
2/11
2/11
10/11
11/11
11/11
11/11
11/11
11/11
11/11
11/11
11/11
11/11
11/11
data.
9/10
10/10
10/10
10/10
9/10
10/10
10/10
10/10
9/10
10/10
10/10
10/10
10/10
10/10
10/10
10/10
10/10
10/10
10/10
10/10
Letter
cancellation
13/53 18/51
38/53 46/51
0/53 24/51
0/53 19/51
0/53 20/51
0/53 22/51
30/53 37/51
0/53 16/51
0/53 14/51
49/53 50/51
53/53 50/51
53/53 51/51
52/53 51/51
53/53 51/51
52/53 51/51
51/53 48/51
53/53 51/51
50/53 51/51
53/53 51/51
50/53 51/51
Sentence
reading
1/6
6/6
0/6
5/6
0/6
3/6
6/6

0/6
5/6
6/6
6/6
6/6
6/6
6/6
6/6
6/6
6/6
6/6
6/6
Wundt-Jastrow
illusion
12/20 20/20
10/20 20/20
20/20 20/20
11/20 20/20
20/20 20/20
2/20 20/20
20/20 20/20
4/20 20/20
9/20 18/20
10/20 20/20
20/20 20/20
20/20 20/20
20/20 20/20
20/20 20/20
20/20 20/20
20/20 20/20
20/20 20/20
20/20 20/20
20/20 20/20
20/20 20/20
Task 3
Only the midpoint of the line was shown; subjects were told
it was the midpoint of the line they had bisected in Task 1
and accordingly required to set, on its basis, both endpoints
of that line.
Each task was executed by patients in the following three
conditions, (i) Baseline: stimuli were superimposed on a
background constituted by alternating yellow and blue
stationary vertical stripes 14 mm wide, (ii) OKL (OKS,
leftwards): background stripes moved leftwards at a constant
speed of 13.13 s"
1
(Permobil Meditech Ober II System),
(iii) OKR (OKS, rightwards): background stripes moved
rightwards at the same speed as in condition (ii).
Procedure
Tasks were executed in a darkened room. Subjects sat in
front of the screen of which the vertical midline was located
in their head's sagittal midplane, at a distance of ~45 cm
from the eyes. The sequence of the three tasks was first
repeated 10 times in the baseline condition. After that, it was
repeated 10 times in the OKL condition and then 10 times
in the OKR condition with five N- and five N+ patients;
this order was reversed with the remaining patients. The
whole session therefore comprised 90 trials.
Score
In Tasks 1 and 2, the score was the distance in millimetres
between the objective and the subjective midpoint; negative
and positive values corresponding to leftward and rightward
mislocation of the subjective midpoint, respectively. In Task 3,
two scores (negative and positive, respectively) corresponded
to the distances of the subjective left and right endpoints
of the virtual line from its objective midpoint shown on
the screen.
Results
While looking at moving backgrounds before starting the
action required by each task, all subjects showed OK
nystagmus, although both phases were abnormal with
rightward stimulation in neglect patients (Incoccia et al.,
1995).
Mean scores (and standard deviations) recorded on the
three tasks in the three conditions of the experiment are
shown in Table 3.
Task 1
The bisection error in the baseline condition was significantly
different from zero in group N+ (t = 3.55, P = 0.0062) but
not in group N- {t = 1.89, P = 0.092). A comparison between
performances with and without OKS (ANOVA with group
by condition as repeated measure) showed no significant
difference between groups N- and N+, but a highly
significant difference between conditions (F = 28.61,
P< 0.0001). The interaction groupXcondition was also
highly significant (F = 12.41, P< 0.0001). Post hoc
comparisons (/ tests) showed that both the differences
baseline versus OKL and baseline versus OKR were
significant (P < 0.05) in group N + , whereas in group N-
only the difference baseline versus OKL was significant
(P < 0.05).

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854 E. Bisiach et al.
Table 3 Mean scores (millimetres), standard deviations (within parentheses), and ranges (decimals omitted) recorded in the
three tasks in the three conditions of the experiment
N +
N-
N +
N-
Task 1
OKL
-33.74
(8.96)
8 to -95
-6.25
(6.80)
0 t o-18
Task 3
OKL
Left
endpoint
-120.79
(21.29)
73 t o-146
-72.35
(20.25)
48 to-114
Baseline
7.00
(6.24)
5 to 18
2.33
(3.90)
-2 to 11
Right
endpoint
52.46
(35.42)
99 to 0
62.12
(14.99)
82 to 36
OKR
36.45
(22.68)
1 to 73
8.18
(8.96)
1 to 26
Baseline
Left
endpoint
-84.82
(13.86)
-106 to -69
-64.09
(11.81)
-85 t o-51
Task 2
OKL
^5. 35
(33.09)
5 to -98
^1.20
(8.10)
9 to -20
Right
endpoint
76.19
(19.83)
29 to 100
68.85
(10.10)
58 to 85
Baseline
1.77
(5.82)
-10 to 10
1.83
(4.70)
-6 to 11
OKR
Left
endpoint
-53.27
(45.13)
-133 to 5
-59.25
(22.56)
-90 to -12
OKR
33.29
(24.62)
0t o76
7.46
(11.27)
-2 to 37
Right
endpoint
116.19
(23.93)
60 to 140
80.46
(23.55)
53 to 122
Task 2
The bisection error in the baseline condition was not
significantly different from zero in group N+ and in group
N-. An analysis similar to that of Task 1 showed no significant
differences between groups N- and N + , but a highly
significant difference between conditions (F = 29.30,
P < 0.0001); the interaction groupXcondition was also highly
significant (F = 16.23, P < 0.0001). Post hoc comparisons
(t tests) showed that both the differences baseline versus
OKL and baseline versus OKR were significant in group N +
(P < 0.05 and P<0 . 0 1 , respectively), while in group N-
only the difference baseline versus OKL was significant
(P < 0.05).
Task 3 (see Fig. 1)
The distances of the left and right endpoints from the midpoint
were compared across the three conditions: baseline, OKL
and OKR (ANOVA with groupXconditionXside as repeated
measure). Only a significant main effect of group was found
(F = 5.32, P < 0.04). The groupXside interaction was not
significant. The condition X side interaction was highly
significant (F = 31.83, P < 0.0001), as was the interaction
groupXconditionXside (F =11.99, P< 0.0001). The post
hoc analysis of the three-way interaction showed the
following: (i) the location of the left endpoint was not
significantly influenced in the N- group by OKS in either
direction, while it was significantly influenced by it in the
N+ group in both directions (baseline versus OKL: t = 4.13,
P < 0.005; baseline versus OKR: t = 2.41, P < 0.05); (ii)
the location of the right endpoint was significantly influenced
N-
i-Kv:-:-:-:-:-:-:-"
HS///////77777,
OKS RIGHT
BASELINE
Q OKS LEFT
Y/////////M
- 1 4 0 - 1 2 0 - 1 0 0 - 80 - 60 - 40 - 20 0 20 40 60 80 100 120 140
Fig. 1 Average lengths (in millimetres) generated in the three
conditions of Task 3 by patients with and without neglect (N+
and N-, respectively). Point 0 on the horizontal axis corresponds
to the midpoint of the virtual line of which subjects had to mark
the left and right endpoints.
by leftward OKS in the N- group (baseline versus OKL: / =
2.35, P < 0.05) and by rightward OKS in the N+ group
(baseline versus OKR: t = 5.92, P < 0.005).
Table 4 shows the partition of subjects showing significant
left- or rightward bias in the baseline condition of each task.
Significance, from level P < 0.05 to higher levels was
assessed by means of / tests on the difference between
subjective and objective midpoint in Tasks 1 and 2; as for
Task 3, t tests were computed on the differences between the
distances of subjective left and right endpoints from the
printed midpoint. As regards Task 1, it is evident that a

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Beyond unilateral neglect 855
Table 4 Number of subjects with or without significant
(left or rightword) bias in the baseline condition of each
experimental task
Task 1
N +
N-
Total
Task 2
N +
N-
Total
Task 3
N+
N-
Total
Left bias
0
2
2
2
2
4
5
1
6
No bias
3
2
5
5
3
8
4
3
7
Right bias
7
6
13
3
5
8
1
6
7
Total
10
10
20
10
10
20
10
10
20
rightward bias in line bisection was also present in the
majority of N- patients, despite absence of neglect on
screening tests. The rightward bias was reduced in Task 2
with respect to Task 1 in both groups of patients; more
definitely so in N+ patients. The performance of the two
groups of patients was strikingly divergent in Task 3. In the
N+ group, five patients (Patients 1, 3, 5, 6 and 10 in Table 1)
showed a significant leftward bias and only one (Patient 2)
a significant rightward bias; the remaining four patients
showed a non-significant leftward bias. In the N- group, a
significant leftward bias was observed only in one patient
(Patient 19) and a significant rightward bias in six patients
(Patients 11, 12, 15, 16, 17 and 20); two out of the remaining
three patients showed a non-significant rightward bias and
one a non-significant leftward bias.
No significant correlation was found in N+ patients
between the degree of leftward/rightward bias in Task 3 and
the standardized scores from the screening tests for the
detection of unilateral neglect. No relationships were apparent
between lateralization bias and locus of the brain lesion (cf.
preceding paragraph and Table 1).
Discussion
Earlier results showing that unilateral neglect patients may
manifest a paradoxical contralesional bias in setting the
endpoints of a virtual horizontal line given its midpoint
(Bisiach et al., 1994; also see Ishiai et ai, 1994a, b) have
been confirmed by our experiment. Moreover, we have found
this bias to be remarkably frequent: in fact, it was evident
in nine out of 10 N+ patients, although statistically significant
only in five.
Most right brain-damaged patients who did not show overt
manifestations of neglect on screening tests (though showing
in some instances a significant error on line bisection, as
reported in Table 4) manifested an opposite, i.e. rightward,
bias (significant in six subjects and non-significant in two)
in the execution of Task 3. So far, we have no convincing
explanation to offer for this puzzling contrast.
As regards Task 2 (bisection of the empty space between the
two endpoints of a horizontal virtual line), our results show
that the most frequent outcome is a reduction, especially
evident in N+ patients, of the rightward error found on the
canonical line bisection task. This was not unexpected, since
it is most likely to depend on the fact that in Task 2 the left
endpoint of the virtual line constitutes a much more effective
attentional cue than the endpoint of a real line [see Riddoch
and Humphreys (1983) as regards the effects of contralesional
cues in line bisection]. A further point, resulting from the
baseline condition of Task 3, is that there seems to be no
apparent correlation between the degree of leftward bias
shown by left neglect patients in setting the endpoints of a
virtual line and the severity of neglect or the intrahemisferic
locus of the lesion.
Turning to the crucial aspect of our study, it is un-
questionably evident that leftward OKS, known to improve
errors made by neglect patients on canonical line bisection,
does not reduce the disproportion between the two virtual
segments resulting from the execution of Task 3 by such
patients, but significantly increases it. We will not consider
here whether this effect is simply due to the horizontal
motion of a visual background, independent of OK effects
(for example, see Mattingley et al., 1994). We also leave
out, since rather premature and not strictly relevant, any
conjecture about the mechanisms through which OKS, caloric
vestibular stimulation, etc. may temporarily improve or
remove neglect phenomena (however, see Vallar et al., 1995,
p. 80). What we anticipated in the Introduction and want to
underline here, instead, is that the effect of manoeuvres such
as OKS on neglect is equivocal. Indeed, assuming neglect to
be consequent upon a polarized disuniformity of the medium
for the representation of spatial relationships, the normaliza-
tion of, for example, line bisection by OKS could either
be due to (temporary) rectification of the representational
medium, or modulation of attentional processes within the
disordered medium. The earlier study (Bisiach et al., 1994)
suggested that the results of an experiment such as that
exemplified by our Task 3 falsify current explanations of
unilateral neglect in terms of a merely defective attentional
dysfunction; it also stressed the need to reconsider neglect
as a symptom of a more complex disorder implying a left-
right anisometry of space representation and consequently
the need to look for any kind of productive (as opposed to
defective) manifestations of such a disorder. In other words,
those results suggested not only that we must take notice of
what patients fail to do on the contralesional side of space
(e.g. in a letter cancellation task), but also that we must
induce them to do something on that side (e.g. setting the
left endpoint of a virtual line) and analyse how they perform.
The results of the present study reinforce that suggestion: in
agreement with earlier data and speculation (Bisiach et al.,
1984; Milner, 1987, pp. 264-5), they show that in patients
manifesting symptoms of unilateral neglect, the left-right
dimension of space representation is settled, as it were, on a
logarithmic scale, with compression on the ipsilesional side

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856 E. Bisiach et al.
and expansion on the contralesional. (Note that, if a segment
is drawn and then bisected over a horizontal axis subdivided
according to a logarithmic scale, the bisection would mimic,
according to Euclidean metric, the error usually made by
left neglect patients.) They also show that a manoeuvre
(contralesional OKS) known to reduce neglect as assessed
by conventional line bisection may not bring remedy to the
underlying dysfunction, of which some productive
manifestations (such as the leftward bias in setting the
endpoints of a virtual line), far from being removed, may be
exaggerated by that manoeuvre through mechanisms still
awaiting elucidation. Further investigation is required in
order to ascertain whether this is also true of the effects of
vestibular stimulation, neck muscle vibration, etc.
Of particular interest is the abnormal susceptibility to OKS
shown by neglect patients, as regards both contralesional
and ipsilesional directions of stimulation, if compared with
patients without neglect {see Fig. 1). A similar phenomenon
had already been observed in the study by Pizzamiglio et al.
(1990). This suggests that lesions giving rise to unilateral
neglect are also followed by a general pathological
unsteadiness and susceptibility of space representation, whose
mechanisms are worth further research.
To conclude, the results of our study further support
Marshall and Halligan's (1994) scepticism as to the adequacy
of current explanations of unilateral neglect. They also give
further support to the hypothesis according to which neglect
is a symptom of a more complex dysfunction affecting the
left-right dimension of space representation, a dysfunction
the explanation of which must wait definition of the changes
induced in the receptive or motor fields of neurons involved
in the processing of spatial relations (for example, see Fogassi
et al., 1992; Galletti et al., 1993) through manipulation of
other brain structures.
Acknowledgement
This work was supported by European Community grant
No. BMH1-CT94-1133 to E.B. and L.P.
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Received September 29, 1995. Revised December 14, 1995.
Accepted January 23, 1996

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