Neuropsychologia 47 (2009) 2948–2952

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Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia

Severity of neglect predicts accuracy of imitation in patients with right

hemisphere lesions
Georg Goldenberg a,b,∗ , Udo Münsinger a , Hans-Otto Karnath c
a
Department of Neuropsychology, Bogenhausen Hospital, Munich, Germany
b
Department of Neurology, Technical University Munich, Munich, Germany
c
Section of Neuropsychology, Centre of Neurology, Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Goldenberg [Goldenberg, G. (1996). Defective imitation of gestures in patients with damage in the left
Received 14 March 2009 or right hemisphere. Journal of Neurology, Neurosurgery, and Psychiatry, 61, 176–180] proposed that the
Received in revised form 15 June 2009 vulnerability of the imitation of meaningless gestures to right or left brain damage depends on the body
Accepted 22 June 2009
parts that are involved in the gestures. Whereas imitation of hand postures was disturbed only in patients
Available online 30 June 2009
with left brain damage, imitation of finger postures was affected to similar degrees in left and right brain
damage. Subsequent studies confirmed the selective vulnerability of hand postures to LBD but failed
Keywords:
to replicate the severe disturbance of finger postures in RBD. In contrast to Goldenberg’s studies, these
Apraxia
Neglect
studies excluded RBD patients with neglect. The present investigation aimed to explore the relationship
Attention between spatial neglect and imitation of finger postures in RBD patients.
Hemisphere dominance Presence and severity of spatial neglect and accuracy of imitation of hand and finger postures were
Body parts tested in 50 RBD patients. Disturbance of imitation was much more severe for finger than hand postures
and was tightly correlated with severity of neglect. The number of errors was higher for fingers which
from the patient’s perspective were located on the left side of the examiner’s demonstrating hand but
this spatial bias was not sufficient to explain all errors. Possible causes for non-lateralized errors could be
a general narrowing of the focus of attention and reduced capacity for processing of visual information
which have been postulated to be regular companions of the lateral displacement of attention in spatial
neglect.
© 2009 Elsevier Ltd. All rights reserved.

1. Introduction clear. Group studies comparing LBD and RBD patients confirmed
disturbance of imitation by LBD, but documented difficulties also in
In his seminal group study exploring the laterality of lesions a substantial proportion of RBD patients (De Renzi, Motti, & Nichelli,
causing apraxia, Liepmann examined not only the execution of 1980; Haaland & Flaherty, 1984; Kimura & Archibald, 1974; Kolb &
meaningful gestures on command but also their imitation. Whereas Milner, 1981; Ogura & Yamadori, 1983).
about one half of the patients with right-sided hemiplegia had dif- Like Liepmann’s original study, all modern studies examined
ficulties and committed errors, patients with left sided hemiplegia the ipsilesional, non-plegic hand, but in contrast to Liepmann they
performed virtually flawlessly. Liepmann noted: “The examination included, or used exclusively, meaningless gestures for assessing
of these left plegic patients was always astonishingly swift, the imitation. Goldenberg (1996, 1999) and Goldenberg and Strauss
movements went like clockwork” (Liepmann, 1908, p 18). (2002) proposed that the vulnerability of the imitation of meaning-
Modern research confirmed that disturbed performance of less gestures to right or left brain damage depends on the body parts
meaningful gestures on command is a consequence of left brain that are involved in the gestures. He examined imitation for two
damage (LBD) (e.g., Barbieri & De Renzi, 1988; Goldenberg, kinds of meaningless gestures: imitation of hand postures required
Hartmann, & Schlott, 2003; Goodglass & Kaplan, 1963), but the lat- the patients to copy different positions of the hand relative to the
erality of lesions causing disturbed imitation turned out to be less head and face, while the configuration of the fingers remained
invariant. For imitation of finger postures patients were asked to
replicate different configurations of the fingers, while the position
of the whole hand relative to the body was not considered for scor-
∗ Corresponding author at: Klinik für Neuropsychologie, Klinikum Bogenhausen,
ing (see Fig. 1). Whereas imitation of hand postures was disturbed
Englschalkingerstrasse 77, D 81925 Munich, Germany. Tel.: +49 89 9270 2106;
fax: +49 89 9270 2089. only in patients with LBD, imitation of finger postures was affected
E-mail address: [email protected] (G. Goldenberg). to similar degrees in LBD and RBD.

0028-3932/$ – see front matter © 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuropsychologia.2009.06.024
 G. Goldenberg et al. / Neuropsychologia 47 (2009) 2948–2952 2949

Fig. 1. Hand and finger postures. Reprinted from Goldenberg, Hermsdörfer, and Laimgruber (2001) with permission by Elsevier.

Goldenberg (1996, 1999), Goldenberg and Strauss (2002), and RBD patients scored below the cut-off of controls. A possible rea-
Goldenberg and Karnath (2006) concluded that different mech- son for this discrepancy are different inclusion criteria for RBD
anisms may underlie defective imitation in LBD and RBD. The patients. Both studies excluded RBD patients with spatial neglect.
problems of LBD patients were explained by deficient body part By contrast, Goldenberg’s studies explicitly included RBD patients
coding and those of RBD by insufficient perceptual exploration of with either spatial neglect or visuo-constructional difficulties to
the demonstrated gesture. Fig. 1 illustrates the different sensitivity make the general severity of impairment comparable to that of LBD
of hand and finger postures to these two sources of error. Imitation patients with aphasia. The suspicion that this difference might be
of hand postures puts high demands on body part coding because important is endorsed by Della Sala et al.’s observation of 3 RBD
determination of the spatial relationship between hand and face patients who had been excluded from the main analysis because
demands a selection from a multitude of very different body parts of their spatial neglect. Their scores on imitation of finger postures
like chin, lips, back and tip of the nose, cheek or ears. Because of their were far below the cut-off and also distinctly below the mean of
diversity these body parts are easy to discriminate perceptually. By the other RBD patients.
contrast, finger configurations pose lower demands on knowledge The present investigation thus aimed to explore the relationship
about body parts because, with a possible exception for the thumb, between spatial neglect and imitation of finger postures in RBD
they are constituted by a set of uniform elements which differ only patients in detail.
in their serial position, but for the same reasons their perceptual
discrimination is difficult. 2. Patients
Two recent studies by other groups probed the reliability of the
dissociation between hand and finger postures (Bekkering, Brass, Fifty patients admitted to the ward or the day care unit
Woschina, & Jacobs, 2005; Della Sala, Faglioni, Motto, & Spinnler, of the Neuropsychological Department of Bogenhausen Hospital
2006). Both confirmed the selective vulnerability of hand postures were examined. This department admits patients in the suba-
to LBD but failed to replicate the severe disturbance of finger pos- cute or chronic phases of brain injury whose medical condition,
tures in RBD. In Bekkering et al.’s study imitation of finger postures basic mobility and attentional and communicative abilities allow
by 8 RBD patients did not significantly differ from a group of 8 for intensive neuropsychological rehabilitation. Consecutive right-
controls, while in the study of Della Sala et al. only 2 out of 24 handed patients (14 women and 36 men) were included who had
2950 G. Goldenberg et al. / Neuropsychologia 47 (2009) 2948–2952

suffered a right-sided cerebrovascular accident at least 3 weeks requiring cancellation of 27 “T” dispersed among 300 “L” on a horizontally aligned
before and who had no MRI evidence of diffuse or bilateral lesions. 21 cm × 29.7 cm sheet. For this test, the sequence of cancellation was recorded by
the examiner on an additional protocol sheet. For both tests omission of 3 or more
The mean age was 54.9 years (range 36–77). Brain damage was
targets located within a continuous left-sided sector of the sheet were considered
caused by ischemia in 37, and by bleeding in 13 patients. Mean time indicative of severe neglect. For the custom made test, starting with a target on the
post-onset was 12.3 weeks (range 3–44). Hemiparesis was present right margin and slow progression to the left side leading ultimately to cancellation
in 35 patients. Visual fields were assessed by dynamic and static of all targets indicated mild neglect.
perimetry: 13 patients had left-sided hemianopia, and 11 incom- Table test (Kerkhoff, 1993): This test consists of a horizontally aligned
100 cm × 80 cm tablet with 40 everyday life objects (e.g., key, eraser, cork, lighter)
plete left-sided visual field defects. No patient had been included fixed upon it. Patients were handed one after the other, replica of 20 of these objects
in previous studies of imitation. and asked to show the matching piece on the tablet. Search time was measured with
All patients or their relatives gave their informed consent for a stop-watch. A failure was recorded when a patient did not find an object within
participation in the study which was performed in accordance with 1 min. One or more failures justified a diagnosis of severe neglect whereas longer
search times for left- than right-sided objects with eventual detection of all objects
the ethical standards laid down in the 1964 Declaration of Helsinki.
was compatible with mild neglect.
Line bisection was tested with the subtest of the B.I.T. and with a second test pre-
3. Methods
senting 3 lines of 16–24 cm length on a horizontally aligned 21 cm × 29.7 cm sheet.
Deviation of more than 5% of the total length from the true midpoint to the right
3.1. Imitation of finger and hand postures
indicated severe neglect.
Copying was tested for the stimuli contained in the B.I.T. as well as for drawings
Imitation was tested for meaningless hand and finger postures (Fig. 1). The pro-
of a flower pot with two stems of flowers and leaves and of a dice. Omissions of left
cedure for testing and scoring was the same for both kinds of gestures. The examiner
sided details or their transmission to the right side indicated severe neglect, whereas
demonstrated the gesture with the left hand and patients imitated with their right
a complete copy achieved piecemeal from right to left or with lower spatial accuracy
hand “like in a mirror”. The patients were allowed to start imitation as soon as the
on the left than on the right side was compatible with mild neglect.
demonstration was terminated. The examiner took care that patients directed their
Reading and writing: Reading was tested for a list of compound nouns filling a
gaze to the examiner’s hand and attended to the demonstration. For a correct imita-
horizontally aligned 21 cm × 29.7 cm sheet. Omissions or distortion of whole words
tion on first trial, 2 points were credited. Otherwise the demonstration was repeated
on the left end of a line or of the left half of words anywhere in the line indicated spa-
and 1 point was given for a successful second trial. Scoring considered only the final
tial neglect. Writing to dictation was probed on a vertically aligned 21 cm × 29.7 cm
position of the relevant body part and did not take into account hesitation, search-
sheet. Progressive deviation of the start of lines to the right side justified a diagnosis
ing movements, or self-corrections during the course of the movement. There were
of severe neglect.
10 hand and 10 finger postures, resulting in maximum scores of 20 for each. 95%
Graphic fluency: The “5-dot test” of graphic fluency (Regard, Strauss, & Knapp,
of a control sample (23 female; mean age 54.9; Goldenberg, 1996) scored above 18
1982) consists of a grid of 7 rows and 5 columns on a vertically aligned
for hand and 17 for finger postures. Scoring was done by the examiner (G. G.) dur-
21 cm × 29.7 cm sheet. In each of the rectangular cells there are 5 dots and patients
ing the examination. A previous study had demonstrated high inter-rater reliability
are required to produce as many different figures as possible by connecting dots.
between immediate scoring by the examiner and independent scoring from video
Whereas most subjects proceed row-by-row, patients with left-sided spatial neglect
by another rater (Goldenberg & Strauss, 2002). Video recordings of the examina-
frequently complete first the right-most column and then proceed column by col-
tion were made nonetheless when circumstances allowed, to collect material for
umn to the left side. In patients who do not fulfil criteria for severe neglect such a
analysing the laterality of errors (see below).
strategy is indicative of mild neglect.
Mild neglect was diagnosed when one or more of the tests fulfilled criteria for
3.2. Laterality of finger imitation errors
mild, but none those for severe neglect. The diagnosis of severe neglect was given
even when some tests indicated only mild neglect if other tests indicated severe
Patients imitated with the right hand while the examiner demonstrated the
neglect. Tests were administered partly by G. G., and partly by U. M. during the same
gesture with his left hand. From the patient’s perspective, the thumb and the index
week as testing for imitation which was always made by G. G. Even when U. M. tested
of the examiner’s hand were located left of the middle finger, and the ring finger and
later than G. G. he was not informed about the results of imitation testing. In the rare
small finger right. If imitation errors in patients with RBD were due to neglect of the
cases where G. G. and U. M. differed in their estimation of the severity of neglect,
left side of the examiner’s demonstration, they should affect postures of thumb and
the judgement of U. M. was decisive.
index more than postures of the forth and fifth fingers.
To investigate this possibility we analyzed the Video recordings of the imitation
of finger postures and recorded for each wrong imitation which of the fingers devi-
4. Results
ated from the model. The gesture consisting of a ring made by thumb and index (see
Fig. 1) was omitted from this analysis because the examiner usually demonstrated
it with the ring aligned in a frontal plane so that the ulnar fingers were placed in Neglect was absent in 14 patients, mild in 17, and severe in
front rather than right of the radial fingers. We included consecutive Video record- 19. Demographic and clinical data of the 3 groups are displayed
ings until we had reached 100 incorrect postures. This number was achieved in the
in Table 1. Neither the ratio of female to male patients (2 = 4.7,
midst of evaluating the 28th patients. We completed the evaluation of the remaining
gestures of this patient and thus ended up with 102 incorrect postures.
p = 0.09) nor that of ischemia to bleeding (2 = 3.7, p = 0.16) var-
To control the possibility that an asymmetric distribution of errors could be due ied significantly. Severity of neglect increased significantly with
to the inherent asymmetries of the gestures (see Fig. 1) rather than to the spatial increasing age (F(2, 47) = 3.5, p = 0.04. Time since lesion did not differ
position of their demonstration, we also analyzed the distribution of incorrect finger across severity of neglect (F(2, 47) = 1.3, p = 0.28). Hemiparesis was
postures in 100 incorrect imitations made by patients with left brain damage (LBD).
less frequent in patients without neglect than in the other groups
Video recordings of finger imitation by LBD patients were taken from a previous
study (Goldenberg & Karnath, 2006). LBD patients imitated with their left hand (2 = 6.9; p = 0.03), but as all patients used the non-paretic right
while the examiner demonstrated the gesture with his right hand. However the hand for imitation this difference is unlikely to have influenced the
spatial position of fingers relative to the side of brain damage was the same as in main results. There was no significant interaction between visual
RBD patients, in that the examiner’s thumb and index were located contralesionally field defects and spatial neglect (2 = 4.5, p = 0.36).
and ring and small fingers ipsilesionally. The target of 100 incorrect postures was
achieved with 30 patients. As we completed the evaluation of the 30th patient, the
total number of analyzed postures was 106. Because error trials could concern more
Table 1
than one finger per posture, the number of incorrectly configured fingers was higher
Clinical and demographic data.
than the number of errors.
Spatial neglect
3.3. Assessment of spatial neglect
Absent Mild Severe
Assessment of spatial neglect distinguished between severe and mild neglect. Female/male 7/7 3/14 4/15
Mild neglect was diagnosed in patients who passed conventional tests of spatial Age 50.0 (10.4) 55.2 (7.6) 58.4 (9.0)
neglect within normal limits but tended to begin exploration of space and body Weeks since lesion 10.1 (6.0) 14.6 (10.3) 11.8 (6.6)
on the right side and neglected left sided stimuli under distraction or in dual task Ischemia/bleeding 13/1 11/6 13/6
conditions. Hemiparesis absent/present 8/6 3/14 4/15
The following tests were administered in each subject: Hemianopia absent/partial/complete 7/3/4 12/3/2 7/5/7
Cancellation: Patients performed the star cancellation test of the Behavioural
Inattention Test (Wilson, Cockburn, & Halligan, 1987) and a custom made test Values in parentheses are standard deviations.
 G. Goldenberg et al. / Neuropsychologia 47 (2009) 2948–2952 2951

Fig. 2. Dependence of accuracy of imitation from severity of neglect (means and

standard errors).
Fig. 3. Distribution of errors in RBD and LBD.

Fig. 2 shows scores on imitation of hand and finger postures

broken down by severity of neglect. A MANOVA with the between ger (binomial test, both p < 0.0005), and the total number of errors
subject factor neglect (none–mild–severe) and the within subject was higher in LBD (binomial test, p = 0.005). As predicted by the
factor body part (hand–finger) revealed significant main effects of assumption that neglect of the contralesional side of demonstra-
neglect (F(2, 47) = 20.0, p < 0.0005) and body part (F(1, 47) = 59.8, tion influences accuracy of imitation in RBD but not in LBD, the
p < 0.0005), as well as a significant interaction between them (F(2, difference between LBD and RBD was greater on the contralesional
47) = 14.7, p < 0.0005). Inspection of Fig. 2 suggests that the inter- than on the ipsilesional side (Fisher Exact Test, one-tailed p = 0.038).
action stems from the increase of the difference between hand
and finger postures with increasing severity of neglect. Imitation 5. Discussion
of hand and finger postures did not significantly differ in patients
without neglect (paired t-test: t = 1.9, p = 0.09), while the difference We found a strong association between severity of left-sided
between them was highly significant for patients with mild (t = 4.1, spatial neglect and disturbed imitation of finger postures in RBD
p = 0.001) and with severe neglect (t = 7.3, p < 0.0005). patients. This dependency might explain why studies that excluded
Separate one-factorial ANOVAs for hand and finger postures patients with spatial neglect failed to find significant impairment
showed that for both of them imitation deteriorated with increas- of imitation in RBD patients (Bekkering et al., 2005; Della Sala et al.,
ing severity of neglect. For finger postures the effect of neglect 2006).
was highly significant (F(2, 47) = 24.8, p < 0.0005). Post hoc pairwise The association of defective imitation with spatial neglect does
comparisons with Bonferoni corrections showed that patients with not necessarily indicate a causal relationship. A strong argument in
severe neglect scored significantly lower than both other groups favour of a causal relationship would be provided by an asymmetric
which did not differ from each other. For hand postures the effect of distribution of errors with errors concerning mainly the thumb and
neglect was weaker but still statistically significant (F(2, 47) = 11.8, index fingers which from the patient’s perspective were located on
p = 0.01), and post hoc comparisons revealed a significant pairwise the left side of the examiner’s demonstrating hand. Indeed, when
difference between patients with severe and mild neglect, whereas analyzing the distribution of errors across fingers we found that
those without neglect differed from neither of the other groups. incorrect configurations of thumb and index were more frequent
Across all patients the mean scores were 16.2 (SD 3.1) for fin- than those of ring and small fingers. The same bias of error distribu-
ger postures and 18.7 (SD 1.7) for hand postures. These values are tion was also detected in LBD patients who saw the demonstration
very similar to those obtained in previous studies administering the of thumb and index finger on the right side of the examiner’s hand,
same set of gestures to other samples of RBD patients (Goldenberg, but the asymmetry of error distribution was stronger in RBD.
1996, 1999; Goldenberg & Strauss, 2002). While this difference in asymmetry could be ascribed to RBD
We also analyzed how many patients scored below the 5th per- patients’ neglect of the contralesional left side of the examiner’s
centile of normal controls. Two of the 14 patients without neglect hand, a certain portion of errors remain that cannot be explain by
scored below this cut-off for finger postures and one for hand pos- the neglect of the left side of the examiner’s hand. About one third
tures. Out of 17 patients with mild neglect four scored below cut-off of RBD patients’ errors concerned ring and small fingers which
for finger postures and one for hand postures. Out of 19 patients from the patient’s perspective were located on the right side of
with severe neglect 16 were below cut-off for finger postures and the examiner’s demonstrating hand. Possibly these errors charac-
seven for hand postures. terize a basic error rate distributed more or less evenly across all
fingers. Possible causes for such non-lateralized errors could be
4.1. Laterality of finger imitation errors a narrowing of the focus of attention and reduced capacity for
processing of visual information which have been postulated to
The mean number of incorrectly configured fingers per incorrect be regular companions of the lateral displacement of attention in
finger posture was 1.56 in the present RBD group and 1.98 in the spatial neglect (Halligan & Marshall, 1994; Heilman, 1980; Husain
group of LBD patients taken from the previous study by Goldenberg & Rorden, 2003; Karnath, 1988). A similar relationship between
and Karnath (2006). Fig. 3 shows the number of errors concern- laterality of errors and spatial neglect has been documented for
ing the contralesional (thumb and index) and the ipsilesional (ring another aspect of apraxia, the performance of multi-step actions
and small finger) part of the hand in RBD and LBD. Both groups involving multiple tools and objects: In RBD patients the number
made more errors of thumb and index than of ring and small fin- of errors correlates with the severity of neglect, but errors are dis-
2952 G. Goldenberg et al. / Neuropsychologia 47 (2009) 2948–2952

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