left hand movements and right hemisphere activation in unilateral spatial neglect- a test of the...

8/12/2019 Left Hand Movements and Right Hemisphere Activation in Unilateral Spatial Neglect- A Test of the Interhemispheri

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Neuropsychologia 40 (2002) 13501355

Left hand movements and right hemisphere activation in unilateral spatialneglect: a test of the interhemispheric imbalance hypothesis

Guido Gainotti a,, Roberta Perri b, Antonella Cappa a

a Neuropsychology Service, Universit Cattolica/Policlinico Gemelli, Largo A. Gemelli, 8 0016 8, Rome, Italyb IRCCS Clinica Santa Lucia, Rome, Italy

Received 20 March 2001; received in revised form 9 October 2001; accepted 10 October 2001

Abstract

The aim of the present study was to check one of the main assumptions of the interhemispheric imbalance hypothesis, namely, theprediction that the severity of neglect should be reduced by conditions activating the right hemisphere. To achieve this, a group of neglect

patients was studied using a slightly modified version of the limb activation technique. The (verbal or visuo-spatial) nature of the stimuli

to be processed by the patient and the (left or right) side of space where the left hand moved were considered as the critical variables to

check the interhemispheric imbalance hypothesis.

Three traditional and one new methods were used to measure changes induced in the severity of neglect by the material to be processed

or by the side of space where the left hand moved. The traditional methods, all based on counting omissions, consisted of measuring: (a)

the overall number of omissions; (b) the number of omissions made on the left half sheet; or (c) the difference between the omissions made

on the left and right sides of the sheet. The new index, based on the notion of the attentional field and defined as the spatial distribution

of stimuli detected by the patient, was operationally measured by computing the distance between each stimulus crossed out by the patient

and the right margin of the sheet. The study was conducted by rating the severity of neglect in 42 cancellation sheets which had used,

respectively letters (N = 21) and small geometric figures (N = 21) as targets. The two sets of cancellation sheets were obtained from

seven neglect patients during a limb activation task requiring the cancellation of a given target in three different conditions: (a) baseline;

(b) active movements of the left hand in the left half space; (c) active movements of the left hand in the right half space.

Results were at variance with the predictions based on Kinsbournes model, since the verbal or visual spatial nature of the material to beprocessed did not influence the severity of unilateral spatial neglect (USN) and since left hand movements produced a significant reduction

in the severity of neglect only when these movements were made on the left side of space. 2002 Elsevier Science Ltd. All rights reserved.

Keywords: Models of neglect; Limb activation technique; Hemispheric activation

1. Introduction

Unilateral spatial neglect (USN) can be considered the

most frequent and dramatic behavioral defect of patients

with right hemisphere damage [8,10] and as a major factor

in poor recovery after stroke [7]. Therefore, several authors

have tried to develop rehabilitation techniques or to search

for experimental conditions that can temporarily or persis-

tently reduce hemineglect. The best known and most effec-

tive experimental condition which can transiently reduce

USN is caloric vestibular stimulation, proposed by Rubens

[37] and developed by Cappa et al. [4], Vallar et al. [39,41],

and Rode et al. [36]. Rubens reasoned that if unilateral ne-

glect is partly due to a gaze and postural turning bias, then

caloric vestibular stimulation, producing eye deviation and

Corresponding author. Tel.: +39-6-3550-1945; fax: +39-6-3550-1909.

E-mail address: [email protected] (G. Gainotti).

past-pointing in the direction opposite to this bias, should

reduce the tendency to neglect stimuli in the contralateral

half space. His results strongly supported the hypothe-

sis since, even in patients with severe neglect, vestibular

stimulation markedly improved performance on tests of vi-

sual neglect. Effects similar to those observed after caloric

vestibular stimulation have since been obtained using other

techniques such as optokinetic stimulation [29,38], trunk

midline orientation [23], neck muscle vibration [21,23] and

transcutaneous electrical nervous stimulation [22,40].

However, the interpretation of these well-established

findings remains controversial. Some authors maintain that

the structures recruited during caloric vestibular stimulation

and other facilitatory techniques contribute to the genera-

tion of a body centered spatial map for directing attention

and movements toward extrapersonal space. According to

this interpretation, USN should be considered as an orient-

ing bias produced by defects in a central reference system,

0028-3932/02/$ see front matter 2002 Elsevier Science Ltd. All rights reserved.

PII: S 0 0 2 8 -3 9 3 2 (0 1 ) 0 0 2 1 1 - 1


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G. Gainotti et al. / Neuropsychologia 40 (2002) 13501355 1351

and all the above mentioned techniques could contribute to

restoring this spatial map, thus reducing the imbalance in

the system [23,29,38].

An alternative interpretation, more in line with the

peripheral hypothesis that prompted Rubens seminal ex-

periment, assumes that all these manoeuvres act on the

output systems of this integrated reference frame, thus re-ducing the consequences of its imbalance. For example, by

provoking a forced automatic gaze displacement, caloric

vestibular stimulation and optokinetic stimulation could

prompt a correlative automatic displacement of attention,

since direction of eye movements and direction of attention

are closely related in spontaneous and uncontrolled con-

ditions [18]. Similar reasoning could be applied to other

techniques which influence the severity of neglect by manip-

ulating other components of the spatial orienting apparatus

(see [10,11] for a more thorough discussion of this issue).

An important contribution to clarifying this issue could

come from the study of other facilitatory techniques based

on the activation of body parts, such as the limbs, whichshould be less critically involved in the construction of the

body reference frame. However, it must be noted that even

if several authors have shown through the use of different

experimental paradigms that active movements of the left

hand can improve the severity of USN, the mechanism un-

derlying this improvement is still controversial.

Joanette and coworkers [19,20] and Robertson and

coworkers [3235] attributed the improvement of neglect

observed after left hand movements to the activation of

the right hemisphere premotor systems associated with the

use of the left hand. This interpretation, which is based on

premotor model of neglect of Rizzolatti and coworkers[30,31], assumes that since attentional and motor circuits

are intimately linked in the brain, the activation of the right

hemisphere motor circuits should lead to a recruitment of the

associated attentional mechanisms, thus improving attention

for the left side of space. On the other hand, Halligan and

coworkers [14,16] showed that the left hand advantage for

line bisection performance is reduced when this hand starts

from the right extremity of the line. These authors proposed

that the left hand acts as a cue enhancing attention to the

left side of space. Still other authors (e.g. [25,27]) proposed

that by increasing the activity of the right hemisphere, left

hand movements may counteract the interhemispheric im-

balance which, according to Kinsbourne [24,25], subserves

the clinical manifestations of neglect. In fact, Kinsbournes

influential model assumes: (a) that attention may be directed

along a vector resulting from the interaction of paired op-

ponents processors controlled, respectively by the right and

left hemisphere and (b) that neglect resulting from right

hemisphere damage may be modified by reducing (or in-

creasing) the interhemispheric imbalance via activation of

the right (or respectively of the left) hemisphere.

The aim of the present research was to try to check this

last hypothesis by means of a slightly modified version of

the limb activation technique proposed by Robertson and

North [3234]. In their basic experiment, conducted on pa-

tient TD, these authors showed that a reduction of left-sided

neglect can be observed when the patient voluntarily moves

the fingers of his left hand in the left half space. This effect,

evaluated by using the total number of omissions made on

the letter cancellation sub-test of the Behavioural Inatten-

tion Test [42] as a measure of neglect, was not dependenton the patients limb being in view, was not obtained when

the left hand moved in the right half space and was not

produced by a passive movement of the same hand. Robert-

son and Norths study was criticized on methodological

grounds by Cubelli et al. [6], and only in part confirmed by

Ladavas and coworkers [9,26]. Cubelli et al. [6] argued that,

since patients with USN usually also have a generalized

attentional impairment in addition to a lateralized defect of

space exploration, it is possible that left hand movements,

by improving the level of arousal, may reduce the total num-

ber of omissions without reducing the rightleft asymmetry

that is the hallmark of USN. Ladavas and coworkers [9,26],

on the other hand, showed that the severity of neglect canbe reduced not only by active, but also by passive move-

ments of the left hand. In spite of these minor objections,

several studies confirmed that active movements of the left

hand can reduce the severity of neglect [2,5] or of visual

extinction [28].

In our study, we intended to replicate this experiment

in an unselected group of neglect patients by keeping

under control two variables which (according to the inter-

hemispheric imbalance hypothesis) should influence the

severity of neglect in a predictable way. These variables

are the following: the (right or left) half space where the

left hand moves and the (verbal or visualspatial) natureof the material used to measure the severity of neglect. We

predicted that if left hand movements reduce the severity of

neglect by activating the right hemisphere, then: (a) these

movements should improve the severity of USN, irrespec-

tively of the half space where the left hand moves since,

in any case, the left hand movements should activate the

right hemisphere; (b) neglect should be more severe with

visualspatial stimuli, which activate the right hemisphere,

than with verbal stimuli, which activate the left hemisphere.

This last prediction had been previously checked with con-

flicting results by other authors [3,5,17], but perhaps these

contrasting results could be explained by methodological

considerations. One of these could be the measures used

to evaluate the severity of neglect since, according to Kins-

bourne [24,25], in USN the attentional defect is not limited

to the left half space, but shifts along a continuum from

the extreme right to the extreme left half space. Now, since

the standard measures used to evaluate the severity of ne-

glect on a cancellation task are substantially based on the

number of omissions made on the right and left half sheet,

they are probably inappropriate for testing the interhemi-

spheric imbalance hypothesis and it was necessary to find

a more appropriate measure of neglect to test this dynamic

model.


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1352 G. Gainotti et al. / Neuropsychologia 40 (2002) 13501355

Therefore, in our study we used a new method, labeled

the center of the attentional field, devised to evaluate the

spatial distribution of the patients attention, in keeping with

Kinsbournes construct of neglect, in addition to three tra-

ditional measures of the severity of neglect. The latter were

based on the total number of omissions made on the cancel-

lation sheet, the number of omissions made on the left halfsheet and on the difference between the omissions made on

the right and left half sheet.

2. Patients and methods

2.1. Patients

Data used to check our working hypothesis were gathered

on seven right brain-damaged patients with clinical evidence

of left neglect, but spared ability to move the left hand, at

least in part.These patients were selected from a consecutive series of

patients who had been referred to the Policlinico Gemelli in

Rome over a 2-year-period (from June 1997 to June 1999)

due to a recent stroke. The main selection criteria were the

following: (a) a single right hemisphere lesion due to a re-

cent stroke, as documented by clinical and neuroimaging

data; (b) the presence of left visuo-spatial neglect in at least

three out of the following four standard tests of neglect: (i)

line cancellation [1], (ii) line bisection [15], (iii) identifica-

tion of overlapping figures [12], (iv) copy of a composite

figure [13]; (c) a spared ability to move at least in part the

forefingers of the left hand.

Patients ages ranged from 67 to 78 years, educational

level from 4 to 17 years of schooling and duration of illness

from 1 week to 3 months. Neglect was mild in two patients,

moderate in three and severe in the last two patients. The

left hand motor defect was moderate in three patients, mild

in two and absent in the last two patients.

2.2. Experimental procedure used to study

the effects of limb activation

The method used to check the influence of the active

movements of the left limb on the severity of neglect was

very similar to that of experiment 2 by Robertson and North

[34]. Two A4 sheets of paper, each containing 420 small

stimuli (upper case letters on sheet 1 and small geometric

figures on sheet 2) scattered across the sheets, were pre-

sented to the patients. On sheet 1, the 420 stimuli corre-

sponded to seven letters, each of which was repeated 60

times, i.e. 15 times for each quadrant of the sheet. On sheet

2, the stimuli corresponded to seven geometric figures, each

of which was again reported 60 times (15 for each quad-

rant of the sheet). The patient was requested to cancel each

example of a given stimulus (an upper case letter on sheet

1 and a small geometric figure on sheet 2) under three dif-

ferent conditions. The first condition was a standard can-

cellation test. The second was a cancellation task made in

conjunction with an active movement of the left hand in

the left half space (the left hand was lying on the patients

left knee, invisible below the table). The third condition was

again a cancellation task in conjunction with an active move-

ment of the left hand; but this time the patients hand wascrossed on his right knee and was, therefore, placed in the

right half space. In both conditions 2 and 3, the order to

move the left hand fingers was given to the patient every

10 s and in each case, the patient had to move the fingers

for 1s.

2.3. Parameters used to evaluate the effects of the left

hand movements on the severity of visual neglect

For each patient, six cancellation sheets (two kinds of

stimuli three conditions) were available to evaluate the in-

fluence of the left hand movements on the two sides of space

and the influence of the stimulus material on the severity

of neglect. For each sheet, the following parameters were

computed: (a) total number of omissions of the target stim-

ulus made on the whole sheet; (b) total number of omis-

sions made on the left half sheet; (c) difference between the

number of omissions made on the left and right half sheet;

(d) central point of the patients attentional field. This last

parameter was operationally defined as the portion of the

sheet taken into account by the patient during the cancella-

tion task. Its central point was computed by measuring the

distance of the center of each stimulus cancelled by the pa-

tient from the right margin of the sheet and considering the

mean value of these measures as the center of the attentionalfield.

3. Results

3.1. The influence movements of the left hand on the right

and left sides of space can have on severity of neglect

Due to the small size of our experimental sample, the

influence movements of the left hand on the right and left

sides of space can have on the severity of neglect was stud-

ied by pooling together results obtained with verbal and

visualspatial stimuli. Data necessary for this analysis were

obtained by computing four kinds of measures (namely, to-

tal number of omissions, left-sided omissions, left minus

right-sided omissions and center of attentional field) for each

patient in three experimental conditions: (1) baseline; (2)

left hand movements on the left side of space; (3) left hand

movements on the right side of space.

The number of observations was 14 (a verbal and a

visualspatial cancellation sheet seven neglect patients)

for each experimental condition.

Paired t-tests were used to check the significance of

differences observed between the baseline and the two


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Table 1

Mean values of the severity of neglect obtained with our different measures in the baseline condition and during left hand movements on the left and

right sides of spacea

Left hand movements

in the left half space

Baseline Left hand movements

in the right half space

Overall number of omissions 26.14 (15.95) t= 2.84 (P < 0.015) 32.93 (19.03) t= 1.97 (n.s.) 27.64 (17.34)

Left-sided omissions 17.6 (9.64) t= 3.65 (P < 0.003) 21.6 (9.09) t= 1.52 (n.s.) 19.9 (9.79)

Difference between left-sided

and right-sided omissions

9.1 (5.23) t= 0.78 (n.s.) 10.3 (5.87) t= 1.23 (n.s.) 12.2 (7.14)

Center of the attentional field 11.63 (3.68) t= 3.53 (P < 0.005) 10.07 (3.93) t= 0.72 (n.s.) 10.42 (3.47)

a Standard deviations are reported within brackets and significant differences in bold.

Table 2

Relationships between the verbal or visualspatial nature of the stimuli and results obtained on cancellation tasks

Method Letter cancellation mean (S.D.) Figure cancellation mean (S.D.) t P

Overall number of omissions 30.2 (16.2) 29.5 (14.9) 0.14 n.s.

Left-sided omissions 21.0 (12.4) 19.5 (10.1) 0.89 n.s.

Left-sided minus right-sided omissions 10.3 (6.4) 9.2 (5.1) 0.65 n.s.

Center of the attentional field 12.3 (4.23) 12.0 (4.09) 0.74 n.s.

experimental conditions. Results of this analysis are re-

ported in Table 1.

In three out of the four measures of severity of neglect

(namely, overall number of omissions, left-sided omissions

and center of the attentional field), left hand movements in

the left half space produced a significant reduction in the

severity of neglect. On the contrary, left hand movements in

the right half space did not significantly influence severity

of neglect in any of these measures.

3.2. Relationships between results obtained

with verbal and with visualspatial stimuli

Table 2 reports the severity of neglect, evaluated with the

four different measures mentioned in the previous sections,

based on number of omissions and on center of the atten-

tional field, as a function of the verbal or visualspatial

nature of the stimuli to be cancelled. The number of obser-

vations was 21 for each kind of stimuli, corresponding to

the seven patients the three experimental conditions.

The results reported in Table 2 show that the (verbal or

visualspatial) nature of the stimuli used for the task has

no influence on the severity of neglect. As a matter of fact,

on none of the parameters used in our study was the sever-

ity of neglect greater with letters (activating the left hemi-

sphere) than with geometric figures (activating the right

hemisphere). In particular, the center of the attentional field,

which should be very appropriate to test Kinsbournes model

[24,25], based on the dynamic notion of an attentional field

moving along a right-to-left gradient, is not shifted to the

left, but minimally to the right with visualspatial stimuli.

This finding is clearly at variance with the right hemisphere

activation hypothesis.

4. Discussion

The aim of the present research was to check the ba-

sic prediction of Kinsbournes interhemispheric imbalance

hypothesis, which assumes that conditions leading to an ac-

tivation of the right hemisphere should reduce the severity

of contralateral neglect. This prediction was checked in a

group of neglect patients with a slightly modified version of

the limb activation technique [3234] by considering the

following critical variables: (1) the (verbal or visualspatial)nature of the stimuli used to assess the severity of neglect; (2)

the side of space where the left hand moved. Regarding the

first variable, it was reasoned that since verbal stimuli should

mainly activate the left hemisphere, whereas visualspatial

stimuli should lead to a prevalent activation of the right

hemisphere, neglect should be more severe on the letter can-

cellation than on the geometric figures cancellation task. Re-

garding the second variable, it was argued that if left hand

movements improve the severity of neglect by activating

the right hemisphere [24,25,27], then the space where the

left hand moves should have only a marginal influence on

this improvement, since in any case left hand movements

activate the right hemisphere. This approach to the prob-

lem is not quite new. On one hand, other authors [3,5,17]

have already tried to check the influence of the nature of

the material to be processed on the severity of USN. On

the other hand, Robertson and North [34] claimed that ne-

glect improves only when the left hand moves in the left

side space. However, results obtained following the first

line of research were rather controversial. Data reported by

Heilman and Watson [17] supported Kinsbournes hypoth-

esis, whereas data reported by Caplan [3] and Cermak et al.

[5] did not support this model. Furthermore, the data re-

ported by Robertson and North [34] was obtained on a single


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1354 G. Gainotti et al. / Neuropsychologia 40 (2002) 13501355

patient and has been criticized on methodological grounds

by other authors [6]. To overcome these difficulties, we de-

vised a method for measuring the severity of neglect more

appropriate to test Kinsbournes dynamic interpretation of

the nature of USN and we studied the influence of left hand

movements on the right and left side space in a group of

neglect patients. Our results are clearly at variance withthe predictions based on the interhemispheric imbalance

hypothesis since the severity of neglect was no greater with

letters than with small geometric figures on any of the pa-

rameters considered in our study. From this point of view,

our results support the conclusions of authors who previ-

ously obtained similar results [3,5] by showing that their

conclusions were not due to the static nature of the method

used to measure the severity of USN. Identical results were

obtained in our study with a more dynamic method which

consists of measuring the differences between the center

of the attentional fields obtained with letters and with

small geometric figures. It might be objected that read-

ing single letters in a cancellation task failed to activatethe left hemisphere because the patients treated the letters

like simple shapes. However, this hypothesis is unlikely be-

cause letters, which are automatically treated as verbal ma-

terial, can be treated as non-verbal shapes only if there are

strategic reasons for doing so. Here, this strategy would

be counter-productive, since it requires the subject to keep

visualspatial material in working memory during the exe-

cution of the visualspatial cancellation task, with the risk of

overloading the right hemisphere. Furthermore, the results

obtained by studying the influence of the stimulus material

were corroborated by those obtained studying the influence

of the side where the left hand moves, since only left handmovements on the left side space produced a significant re-

duction of the severity of neglect in our study and a simi-

lar effect was not observed during left hand movements on

the right side space. These results are consistent with some

data recently obtained with similar experimental paradigms

by Mattingley et al. [28] and by Brown et al. [2]. The for-

mer reported a reduction in left-sided extinctions and the

latter a reduction in left-sided word omissions in text read-

ing, not only with left hand movements but also with right

hand movements executed in the left side space. All these

data, which stress the importance of the half space where

the hand is moved, are more consistent with the premotor

model of Rizzolatti and coworkers [30,31] and even more

with spatio-motor cueing hypothesis of Halligan et al.

[14], than with Kinsbournes interhemispheric imbalance

hypothesis.

It must be acknowledged, however, that both the premo-

tor and the spatio-motor cueing interpretation are at variance

with results obtained by Ladavas et al. [26] in their above

mentioned paper, which seemed to show that the premotor

and the cueing explanation are not tenable. Therefore, we

believe that even if the value of a theoretical model cannot

be assessed on the basis of a single study, but requires the

critical evaluation of several, even contrasting studies, the

controversy over the mechanisms by which left hand move-

ments produce a transient reduction of visual neglect cannot

be solved with our present knowledge.

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