Neuropsychologza, Vol. 27, No. 2, pp. 157-165, 1989 Prmted in Great Britam.

0028-3932:89 S3.00f0.00 t 1989 Pergamon Press plc

ANOMALIES IN THE LATERALITY OF OMISSIONS IN UNILATERAL LEFT VISUAL NEGLECT: IMPLICATIONS FOR

AN ATTENTIONAL THEORY OF NEGLECT

IAN ROBERTSON*

Principal dlinical Psychologist, Astley Ainslie Hospital, Grange Loan, Edinburgh EH9 2HL. Scotland. U.K

(Receiwd 29 September 1987; accepted 14 March 1988)

Abstract--Patients suffering from unilateral left visual neglect may show problems in deploying attention generally in space, particularly in “controlled processing” type tasks (Schneider and Shiffrin), in addition to showing specifically lateralized attentional difficulties. The prediction is made that cueing to the left should result in a significant increase in right-sided omissions because of this general attentional difficulty. This hypothesis was confirmed, and two patterns of results were observed. One group continued to neglect a left stimulus in the cued condition, in spite of accurately reading a word on the left side, while the other group showed a mainly right-sided omission pattern.

INTRODUCTION

UNILATERAL VISUAL neglect occurs more frequently on the left side of space, usually following lesions to cortical and/or sub-cortical areas of the right hemisphere [3,4], though some authors have found that neglect is equally common following both right and left hemisphere lesions [8, lo].

A central feature of almost all contemporary theories of left visual neglect is the assumption that perceptual omissions are predominantly, though not necessarily exclu- sively, lateralized to the left side ofany stimulus attended to. BISIACH et al. [l, 21, for instance, have advocated a representational model of neglect which postulates a “mutilated representation of space” as being the core deficit in unilateral neglect. In the above two studies, neglect of the left sides of purely mental images were demonstrated, and used as evidence to support their view that neglect is caused by a failure in the capacity to represent space on the contralateral side.

HEILMAN et al. [S] propose an attentional model of neglect, on the other hand, which assumes that unilateral lesions produce hypoarousal in the hemisphere which results in both an inattention for stimuli processed in that hemisphere as well as a hypokinesia of movements in the hemisphere contralateral to the damaged hemisphere. Heilman explains the greater incidence of left neglect as being due to the right parietal lobe being focally aroused by stimuli projected onto the entire visual field, while the left hemisphere is aroused only by stimuli in the contralateral visual field [6]. Thus, although he argues that there is

*Honorary Fellow, University of Edinburgh.

157

158 IAN RUBERTSON

bilateral reduction in cortical arousal, the theory predicts a strongly and consistently lateralized aspect to the disorder.

One recent theory of neglect [ 121 proposes that neglect may partly be explicable in terms of a directional deficit. In other words, the person finds difficulty in moving attention in a direction contralateral to the lesion when attention is “captured” by a stimulus ipsilesionally placed. A full review of the latest theories of neglect is available in a recent book edited by JEANNEROD [7].

The emphasis on the lateralization of omissions in neglect in all current theories is clear, however, and if it could be shown that this pattern could be partially reversed under experimental conditions, then this would present an interesting problem for theories of neglect. In order to justify such a prediction, some relevant theories and studies will be described.

SCHNEIDER and SHIFFRIN [15] have proposed two types of human information processing-controlled and automatic. The former is a type ofprocessing which occupies the limited focussed attention of the individual, for instance as in such tasks as letter cancellation in a dense array of random letters. Automatic processing is the type of processing which occurs without occupying the full focused attention of the individual, for instance when a task becomes very well practised and “automatic”, as indeed a letter cancellation task may become with repeated practice on the same material.

TREISMAN and GELADE [16] have proposed a related, though not identical, distinction. This is between “feature” and “object” detection in visual attention. The former is the search for a stimulus which differs from its surroundings by a basic feature such as colour or orientation. This search does not place demands on focussed attention, and is thus without channel limitation. This “parallel processing” is contrasted with search for a stimulus which differs from its surroundings through a constellation of features. Search for such stimuli places demands upon focussed attention, that is, it is a controlled processing system, in Schneider and Shiffrin’s terms. RIDDOCH and HUMPHREYS [ 131 have shown in three subjects suffering unilateral neglect how pre-attentive feature processing was relatively intact, while serial processing was impaired. Thus this study suggests that neglect is related to the controlled processing system, with its limited attentional capacity.

PILLON [l l] reported that the degree of left-sided omissions shown by left neglect patients increased with the complexity of a number of geometric designs which they copied. A relatively simple figure produced little neglect, while a complex figure of the same size produced considerable neglect. This finding could be interpreted as support for the notion that neglect is a function in part of an impaired limited capacity controlled processing system, the more complex figure exceeding the individual’s capacity for serial visual search. POSNER’S 1121 “attentional capture” hypothesis could also explain such a finding, however.

It has been suggested above that controlled perceptual processing requiring serial attentional capacities is selectively impaired in visual neglect. Clearly there is skewing to one side in this disorder, but the above evidence suggests the possibility that not only is there a lateralization of attention, but also a limitation in the ability to deploy attention systematically irrespective of side.

This leads to the following prediction. If there is a general difficulty in deploying attention as well as a lateralized one, then under some circumstances the former should outweigh the latter and it may be possible to produce significant numbers of omissions on the ipsilesional side as well as on the contralesional side. More specifically, it is predicted that a group of patients showing left neglect will show a significantly greater number of omissions in the right

ANOMALIES IN THE LATERALITY OF OMISSIONS IN UNILATERAL LEFT VISUAL NEGLECT: IMPLICATIONS FOR AN ATT 159

visual field when cued to attend to the left field on a task than when not so cued, and that such cueing will eliminate the differences in left-right omissions detectable in normal testing.

METHOD Subjects

1. Neglect patients. Ten subjects showing unilateral left visual neglect were studied. The criteria for selecting these subjects were as follows: (1) presence of visual neglect as defined by the behavioural items of the Rivermead Behavioural Inattention Battery [I 81. This test comprises nine tests of practical activities such as reading, telephone dialling, address copying, identifying coins and others. All subjects showed neglect-type errors on at least three of the sub-tests lateralized on the left side; (2) presence of at least a total of eight omissions on the 80 trials of the computerized task described below where a left-sided stimulus was presented, and at least a 300% greater incidence of left over right omissions on the 80 non-cued trials; (3) absence ofgeneralized cognitive deficits sufficiently severe to produce disorientation in place or person; (4) age under 80; (5) willingness to give informed consent to participation m the study.

Consecutive admissions to a Rehabilitation Service showing left hemipareses or hemiplegias were assessed on the above tests, and all satisfying the above criteria were accepted. Sex, age and medical data on the 10 subjects are presented in Table 1 and the neuropsychological data in Table 2.

2. Control group. A control group of 10 hospitalized age- and sex-matched controls were selected from the wards of the Astley Ainslie Hospital. These were selected consecutively according to the matching criteria, though patients showing marked mental deterioration were excluded. This was assessed using the Digit Symbol subtest of the Wechsler Adult Intelligence Scale (Revised version). They were also given the National Adult Reading Test [9] to give an estimate of premorbid IQ. Subjects whose age-scaled score on this test was more than 1.5 standard deviations below their estimated premorbid IQ were excluded. Subjects included orthopaedic patients and coronary artery bypass patients, The two groups did not differ significantly in age (exp. 64.7, SD 9.5; control: 63.0, SD 9.5) premorbid IQ (exp. 104.5, SD 8.4; control 111.2, SD 7.0; t =2.1, P>O.O5,2-tailed) or sex (6 male and 4 female in each group).

Procedure

A computerized experimental procedure presented one or two stimuli at the left and/or right of a screen which was a television monitor 20 cm high and 27.5 cm wide placed directly in front of the seated patient with the centre of the screen at eye level. The stimuli were a Greek cross and a rectangle which subtended angles of 0.92” horizontally and 1.07” vertically, respectively. The distance between the two stimulus locations subtended an angle of 16” from the subject. Subjects were told that they would hear a “bleep” and that immediately afterwards one or two stimuli would appear on the screen, someties on the left, sometimes on the right, and sometimes on both left and right. Their task was simply to say what they saw and point to which side or sides they saw it or them. Stimuli appeared 0.1 set after the warning tone and had a duration ofO.1 sec. Five seconds separated each presentation. One cycle consisted of40 presentations, 10 with a single stimulus on the right, 10 with a single stimulus on the left, and 20 with two stimuli, which were never identical.

A new task was then superimposed on the original one. Immediately under the left stimulus (or immediately under where it would be if not present), a word which was the name of a colour (red, green, yellow, blue) appeared 0.1 set after the warning tone and lasted 0.2 sec. The same randomized non-verbal stimulus as before appeared 0.2 set after the warning tone and lasted 0.1 sec. The task here was for the subject to say the colour and then say in the same way as before what symbols appeared where on the screen. All words appeared at the left of the screen only.

Subjects responses were recorded on the microcomputer. In the case of the cued sessions. note was made whenever a word was omitted or mis-read. Four cycles were run in the order-(l) task alone; (2) task plus word; (3) task plus word; (4) task alone, giving a total of 160 trials, 80 with single stimuli and 80 with double stimuli, and 80 with word task added, and 80 without this task.

No attempt was made to control for eye-position, and thus no fixation point was used. The reasons for this was to allow subjects with field defects the opportunity of compensation for these by anticipatory deflection of their gaze to the left, as indeed some would do in real life. To have induced eye-fixation would have necessitated the exclusion of neglect patients who also had field defects-a clearly impractical move.

RESULTS

Table 3 summarizes the results. The difference between the number of omissions on the right between the word and the no word conditions was statistically significant for the neglect group in the predicted direction (t=3.82; P<O.O5; l-tail). It should be noted that the difference for left omissions between the two tasks for this group was not statistically

Tab

le

1. A

ge,

sex

and

med

ical

da

ta

on

ten

negl

ect

subj

ects

No.

Se

x A

.w

Sour

ce

of

lesi

on

Loc

atio

n (C

T

scan

if

ava

il.)

No.

w

eeks

po

st

onse

t (C

VA

) H

emia

nopi

a M

acul

a V

isua

l ex

tinct

N

egl.

on

or

op.

(oth

er)

pres

ent

spar

ed

(if

no

hem

ian)

C

OPY

1 F

51

Men

ingi

oma

Pitu

itary

fo

ssa:

ri

ght

basa

l ga

nglia

17

Y

N

N

A*

N

2 F

13

CV

A

Rig

ht

tem

p.-p

arie

t. 26

Y

N

N

A

Y

3 M

52

C

VA

R

ight

pa

riet

.-occ

ipit.

in

farc

t. 9

Y

N

NA

Y

4 F

63

CV

A

Sub-

arch

n.

haem

m.

righ

t fr

onta

l 12

Y

N

N

A

Y

and

Sylv

ian

area

5

M

77

CV

A

Non

e av

ail.

10

Y

Y

NA

N

6 M

19

C

VA

N

one

avai

l. 12

N

Y

N

o N

I M

69

C

VA

R

ight

te

mp.

-par

iet.

infa

rct.

I N

Y

Y

es

Y

8 M

56

C

VA

R

ight

in

tern

. ca

psul

e in

farc

t. 5

Y

N

NA

Y

9 F

56

CV

A

Rig

ht

pari

et.-o

ccip

it.

infa

rct.

6 Y

Y

N

A

N

10

M

65

CV

A

Non

e av

ail.

5 Y

Y

N

A

Y

(Not

es

on t

he t

able

: th

e pr

esen

ce

of h

emia

nopi

a w

as a

sses

sed

usin

g co

nfro

ntat

ion

test

ing,

an

d th

e qu

estio

n of

mac

ular

sp

arin

g as

sess

ed

usin

g a

Bje

rrum

sc

reen

. N

ot

all

visu

al

fiel

d de

fici

ts

wer

e de

nse

hem

iano

pias

. V

isua

l ex

tinct

ion

was

as

sess

ed

by c

onfr

onta

tion

test

ing

also

. T

he c

olum

n he

aded

“N

egle

ct

on C

opy”

re

fers

to

the

pre

senc

e of

cl

ear

omis

sion

s to

the

le

ft s

ide

on

the

copy

of

a c

ompl

ex

geom

etri

c fi

gure

.) *N

ot

appl

icab

le

as f

ield

def

icit

pres

ent.

Tab

le

2. N

euro

psyc

holo

gica

l da

ta

on

ten

negl

ect

subj

ects

No.

WA

ISR

W

AIS

R

bloc

k pi

ctur

e de

sign

ag

e co

mpl

etio

n ag

e sc

aled

sc

ore

scal

ed

scor

e

WA

ISR

di

git

sym

bol

age

scal

ed

scor

e

Wis

cons

in

card

so

rtin

g te

st

% T

otal

%

Pe

rsev

. er

ror

erro

r

Let

ter

canc

ella

tion

(E’s

and

C

’s)

% e

rror

s T

otal

L

eft

Rig

ht

faile

d

Riv

erm

ead

Beh

avio

ural

In

atte

ntio

n B

atte

ry

test

s N

o.

faile

d (M

ax.

poss

= 9

)

1 8

5 8

95

41

27

2 14

7

2 I

3 6

30

13

100

87

93

8 3

5 2

6 30

43

10

0 17

92

9

4 4

3 1

22

10

100

90

95

9 5

7 2

7 2

i 21

4

13

3 6

12

6 6

7 t

17

19

18

3 7

3 2

2 22

54

29

2

15

8 8

11

4 3

38

100

94

8 51

9

9 7

3 *

* *

* *

* 5

10

4 4

* 4

t 10

0 96

94

9

*Dat

a no

t av

aila

ble.

tE

rror

ra

te

too

smal

l io

r ca

lcul

atin

g th

is.

162 IAN RUBERTS~N

significant, however (t= 1.21; P>O.l). Although there was a greater number of total omissions in the word compared with the no word conditions, this was not statistically significant also (t = 1.86; P> 0.1). In the no word condition, there were significantly more left than right omissions in the neglect group (t=6.5; P-cO.005). This difference almost disappeared in the word condition. Thus the hypothesis was confirmed.

Table 4 shows the results for each individual subject.

Fab!e 3. Mean number of left vs right omissions in the two conditions for the two subject groups

Neglect subjects Control subjects Mean No. left Mean No. right Mean No. left Mean No. right

omissions omissions omissions omissions

No word 33.6 4.5 0.2 0.8 SD (15.4) (3.6) (0.4) (1.9) Word presented on left 26.0 23.5 1.5 5.7 SD (21.1) (16.7) (1.9) (6.8)

Though the neglect group showed an increase in right-sided omissions when cued to the left as predicted, there were several individual exceptions to this. Table 4 shows the scores of each individual in the neglect group, where it is clear that cases 1,2,4 and 7 all fail to show an increase of more than 10 in the number of omissions on the right. Close scrutiny of this table shows that cases 2,4 and 7 all continued to make substantial numbers of left-sided omissions in the absence oflarge increases in right-sided omissions. This was in spite of the fact that they were continuing to read the word on the left side, making only 11, 7 and 0 mis-readings or omissions respectively out of a maximum of 80 possible. (There was a mean of 10 errors of this type for the experimental group.) This is interesting because of the fact that omissions continued to be made on the left, in spite of the fact that words immediately under the omitted stimuli were being accurately read. In other words, some information was being neglected in a spatial location where other information was being detected and responded to. Case 1 presents a slightly different picture, as the reduction in left-sided omissions occurred without a significant increase in right-sided omissions.

In the four cases in question, no statistically significant results appeared between word and no word conditions in the single or the double stimulus conditions. However, the incidence of left omissions in the word condition increased under double stimulus as compared with single stimulus conditions (t = - 3.1; P < 0.1 ), though this was just as true for no word as for the word conditions.

For the remaining six subjects, that is those showing mainly right-sided omissions in the cued condition, the mean number of omissions left and right under single stimulus conditions were 5.8 and 5.5 respectively. The equivalent means for double stimuli conditions were 12.3 and 28.8, respectively. The difference between the former two means was not statistically significant, while the difference between the latter two means was statisticaliy significant (t=2.8; P<O.O5).

DISCUSSION

One possible criticism of the finding of an increase in right-sided omissions following left cueing is that the effect of the word presented in the left visual field was simply to draw the remaining partial visual field to the left half of the screen such that stimuli to the right fell outside of the functional fields. By this argument, the increase in right-sided omissions could

Tab

le

4. I

ncid

ence

of

lef

t- a

nd

righ

t-si

ded

omis

sion

s in

the

w

ord

and

no

wor

d co

nditi

ons

for

all

ten

subj

ects

sh

owin

g le

ft v

isua

l ne

glec

t

Cas

e

No

wor

d W

ord

(pre

sent

ed

on

left

) L

eft

omis

sion

s R

ight

om

issi

ons

Lef

t om

issi

ons

Rig

ht

omis

sion

s Si

ng.

Dou

b.

Tot

. L

Si

ng.

Dou

b.

Tot

. R

Si

ng.

Dou

b.

Tot

. L

Si

ng.

Dou

b.

Tot

. R

1 12

18

30

2

16

40

56

3 13

31

44

4

14

34

48

5 1

8 9

6 I

12

19

I 0

33

33

8 9

21

30

9 8

10

18

10

15

34

49

0 0

2 9

1 4

1 2

0 2

2 1

0 1

3 I

0 4

1 5

0 0

2 2

3 1

4 11

10

39

49

4

13

17

5 1

0 1

3 37

40

3

17

38

55

0 0

0 2

0 3

3 0

22

22

3 2

6 8

2 37

39

1

6 39

45

0

6 6

10

12

22

34

9 21

30

4

10

29

39

7 21

28

6

10

14

24

14

35

49

164 IAN ROBERTSON

be explained by an artificially contrived sensory deficit induced by the artificially produced attentional focus to the left side of space.

In order to examine this criticism, it is necessary to compare these trials where there were double stimuli on the screen with those where single stimuli appeared. If the increase in right- sided omissions is equally great in both conditions, then it is difficult to argue against the proposal in question. If, on the other hand, the increase in omissions was greater for double stimuli trials, then this would be difficult to explain by the visual field argument, and would be better explained by an attentional hypothesis, for if the field is simply cut, then it should not matter whether there is a stimulus on the left or not. In order to test this subsidiary hypothesis, the left and right omissions under double vs single stimulus conditions were compared in the six subjects who showed the pattern of increased right-sided omissions in the word condition, namely subject numbers 3,5,6,8,9 and 10 in Table 4 above. The results are reported in the previous section. Comparing the incidence of right omissions under double vs single stimulation provides clear evidence against the sensory hypothesis and for the attentional hypothesis: the number of right-sided omissions clearly increased in the double, but did not increase in the single, stimulus conditions.

The finding that in some subjects left omissions predominated in spite of largely accurate left word reading is puzzling. It may be compatible, however, with the findings of VoLPE et al. [ 171, who have shown that some amount of pre-attentive processing is detectable in the neglected fields. In their research, neglecting patients have been shown to be able to make accurate basicjudgements about stimuli in the neglected field which they deny any awareness of. It may be the case that the fact that a word was a sufficiently salient stimulus, and the reading of it a sufficiently overlearned response, that it did not place extra demands upon the limited capacity for controlled processing of the patients, while the detection of an unfamiliar stimulus did make such demands. This finding remains problematic, however, and of particular interest is the difference between the patients who show the two different patterns, which will be the subject of future research.

The above data provide some support for the hypothesis that a general difficulty in deploying attention in space exists in unilateral neglect in addition to any lateralized deficits. Other evidence suggests that this problem is most marked in attentional tasks requiring serial, controiled processing. Quite why this might be is not satisfactorily explained by any of the major theories of neglect, though the above results would be partially compatible with the work of Heilman, who argued that the neglect patient would sufler bilateral hypoarousal problems because of a presumed right hemisphere dominance for regulation of arousal in both sides of space. He argues, however, that it is the particular role in responding to events in left hemispace for right brain damaged people which results in a lateralized deficit. This is not supported by the work reviewed by Roy et al. [ 141, who found no such specialized role for the right hemisphere.

Acknowledgemenrs-I would like to thank the following colleagues at Astley Ainslie Hospital for their help and support in carrying out this study: John Gray, Lorna Waite, Karina Townsend and Katrina Cox. 1 am also most grateful for extremely helpful comments made by Peter Halligan of Rivermead Rehabilitation Centre. Oxford on an earlier draft of this paper. Finally, I would like to thank an anonymous reviewer for helpful criticisms of the manuscript.

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