Topics in Stroke Rehabilitation

ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/ytsr20

Integrating visual search, eye movement training
and reversing prism exposure in the treatment of
Balint-Holmes syndrome: a single case report
Francesco Panico, Angela Arini, Pierluigi Cantone, Claudio Crisci & Luigi
Trojano
To cite this article: Francesco Panico, Angela Arini, Pierluigi Cantone, Claudio Crisci & Luigi
Trojano (2021): Integrating visual search, eye movement training and reversing prism exposure
in the treatment of Balint-Holmes syndrome: a single case report, Topics in Stroke Rehabilitation,
DOI: 10.1080/10749357.2021.1923319
To link to this article: https://doi.org/10.1080/10749357.2021.1923319

Published online: 07 May 2021.

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TOPICS IN STROKE REHABILITATION
https://doi.org/10.1080/10749357.2021.1923319

Integrating visual search, eye movement training and reversing prism exposure
in the treatment of Balint-Holmes syndrome: a single case report
Francesco Panico

a

, Angela Arinib, Pierluigi Cantoneb, Claudio Criscib, and Luigi Trojano

a

a

Department of Psychology, University of Campania “Luigi Vanvitelli”, Caserta, Italy; bNeurorehabilitation Unit, Clinic Center Rehabilitation
Institute, Napoli, Italy
ABSTRACT

ARTICLE HISTORY

Objective: For the first time, we administered reversing prism exposure to treat optic ataxia in
a single patient with Balint-Holmes Syndrome (BHS), who also underwent specific trainings for
simultanagnosia and ocular apraxia.
Method and Results: By an introduction and withdrawal experimental design, we observed that
the active treatment periods improved patient’s visuospatial defects and functional autonomy.
Conclusions: We thus provided a proof of principle supporting the use of reversing prism exposure
in optic ataxia within an integrated and personalized rehabilitative approach for BHS.

Received 14 April 2021
Accepted 24 April 2021

Introduction

Balint-Holmes Syndrome (BHS) is characterized by
simultanagnosia, ocular apraxia, and optic ataxia.1
Simultanagnosia has been described in a “dorsal”
form, precluding the detection of multiple objects,
and in a “ventral” form, causing difficulties in
simultaneously recognizing the individual parts of
an object.2 Ocular apraxia is an impairment of
visual fixation related to defective saccade initiation
and limited visual pursuit.3 Optic ataxia corre­
sponds to the difficulty in performing arm move­
ments directed at visual objects, in the absence of
primary visual, proprioceptive or motor disorders.4
Usually BHS follows bilateral stroke in the par­
ieto-occipital cortex,2,5 is highly disabling and
shows poor spontaneous recovery.6 Previous reha­
bilitative interventions aimed at exploiting residual
cognitive abilities by compensatory strategies, or at
recovering the impaired functions by intensive
training, but no large-scale clinical trials are avail­
able [for a review7] Optic ataxia has been treated by
encouraging the patient fixating an object before
grasping,6 and very recently, by a one-day session
of intensive repetitive pointing.8 Nonetheless, the
treatment of optic ataxia remains quite overlooked.
Here, we applied, for the first time, a prism expo­
sure training for optic ataxia in a patient with BHS,
CONTACT Francesco Panico
Caserta 81100, Italy
© 2021 Taylor & Francis Group, LLC

francesco.panico@unicampania.it

KEYWORDS

Balint-Holmes syndrome;
rehabilitation; optic ataxia;
prism exposure; visuo-spatial
disorders

aimed at increasing patient’s awareness on discre­
pancy between the aimed movement and the actual
motor output, to prompt strategic motor correc­
tion. The individualized rehabilitation plan also
included visual search tasks for treating dorsal
simultanagnosia and eye movement training for
gaze apraxia, as described in the literature.7
Case report

DG, a 55-year-old male teacher, developed wide
cortico-subcortical ischemic lesions in the right
temporo-parieto-occipital and left parietooccipital regions following SARS-CoV2 infection.9
One month after admission to the rehabilitation
unit, the patient was alert and cooperative, well
oriented and aware of his condition. Bedside exam­
ination revealed severe simultanagnosia, ocular
apraxia, and optic ataxia, consistent with a fullblown BHS, and mild left neglect. A formal neu­
ropsychological evaluation based mainly on verbal
task revealed word finding difficulties and mild
executive dysfunction (Table 1).
The neuropsychological treatment started three
months after stroke and was in line with the CARE
Guidelines.17 In an ABAB introduction and with­
drawal experimental design,18 we performed two
rehabilitation cycles, each including three sessions

Department of Psychology, University of Campania “Luigi Vanvitelli”, Viale Ellittico 31,

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F. PANICO ET AL.

Table 1. Neuropsychological examination.
Test
Montreal Cognitive Assessment (10, 11)
Digit Span – forward (12)
Verbal Span – words (13)
Constructional Apraxia (13)
Rey Auditory Verbal Learning Test –
immediate (14)
Rey Auditory Verbal Learning Test –
delayed (14)
Babcok Memory Test (13)
Word Fluency: phonemes (14)
Word Fluency: categories (13)
Frontal Assessment Battery (15, 16)

Baseline
(T0)
11/30*
2*
3*
1/14*
13/75*

After Treatment
(T6)
18/30*
3*
3*
4/14*
43/75

2/15*

8/15

11,3/16
14*
7,25*
7/18*

13,6/16
12*
15,25
12/18*

* = pathological performance according to age- and education-adjusted
Italian normative studies

in a week. DG provided his written consent to take
part in the rehabilitation plan; procedures were in
line with the 1978 Helsinki Declaration.
In each session, the three trainings were given in
random order. In the visual search training,19 the
patients had to look for the grayscale pictures of
objects named by the examiner within centrally
presented 4 × 4, 6 × 6 or 9 × 9 matrices (size:
21 × 29,7 cm; distance from the patient: 50 cm).
During eye movement training,20 the patient had to
place his index fingers at a distance of 15 cm from
his face and to move his gaze to one or the other
alternately during a 5-min period. Distance
between the two index fingers was increased from
5 to 15 and 30 cm (15 trials per distance; total trials
per session: 45). The reversing prism exposure
training21 involved pointing movements while the
patient wore prism glasses whose base changed
every few trials. This procedure makes the partici­
pant unable to develop full adaptation but stimu­
lates error correction and error compensation
mechanisms.21 In our training, the patient was
asked to point with his right hand toward
a centrally placed target (a 1-cm dot) while wearing
glasses shifting the visual field by 10°. The direction
of the prism shift was reversed (left to right and vice
versa) every 5 trials and the same sequence was

repeated three times (total trials: 30). The patient
was encouraged first to search for the target, then to
develop a movement plan, and finally to execute
a fast, one-shot movement toward the target.
Verbal feedback and instructions were provided
during the planning phase for identifying object
position6 and coding knowledge about object posi­
tion and limb position; in case of error, verbal feed­
back aimed at noticing the misplacement of
movement outcome and at correcting it were given.
Before and after each cycle, we evaluated simul­
tanagnosia, gaze apraxia, and optic ataxia (T0-T6;
Figure 1). At the end of the rehabilitation period,
the patient underwent a general neuropsychologi­
cal assessment (Table 1).
To assess ventral simultanagnosia, we asked the
patient what he could see when looking at 10 large
silhouettes made up of small parts (e.g. a large letter
‘G’ formed by small letters ‘E’). To assess dorsal
simultanagnosia, the patient was asked to name
single objects in the right (n = 6) or left (n = 6)
visual field, or two centrally located objects (n = 6).
To assess gaze apraxia, the patient was required
to look at statically presented objects in four possi­
ble locations (left, right, upper, or lower visual field;
n = 5 each), without making concurrent head
movements. The examiner visually checked
whether each patient’s eye movement was quick
and direct or slow, hesitant and inaccurate.
To assess optic ataxia, the patient was required to
reach for a visually displayed object (a yellow cup)
in the left, right or central visual field with his left or
right hand. Five trials for each hand and field com­
bination were given for a total of 20 trials.
A response was considered correct when the patient
could touch the target at his first direct attempt, or
immediately self-corrected his mistake.
Before and after the rehabilitation program (T0,
T6), we also assessed DG’s functional autonomy in
10 specific daily life activities (eating, grooming,

Figure 1. Timeline of neuropsychological rehabilitation plan (D means days, T assessments).

TOPICS IN STROKE REHABILITATION

3

Figure 2. Percentage of correct responses at the tasks assessing optic ataxia, gaze apraxia and ventral and dorsal simultanagnosia at
the different stages of the rehabilitation period. The evaluations after the active rehabilitation period correspond to T1 and T4 (see
Figure 1 for the whole timeline).

Figure 3. Examples of patient’s performance in copying geometrical figures (top row) at baseline assessment (T0, middle row) and at
the end of the rehabilitation period (T6, bottom row).

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F. PANICO ET AL.

Table 2. Measures of functional outcome.
Daily life activities
Eating
Grooming
Bathing
Upper dressing
Lower dressing
Toileting
Wheelchair driving
Stairs
Comprehension
Expression
Total score

Baseline (T0)
1
1
1
1
1
1
1
1
5
3
16

After Treatment (T6)
4
3
2
4
3
2
2
1
5
3
31

1 = complete assistance, 2 = moderate assistance, 3 = minimal assistance, 4 = moderate independence, 5 = complete independence.

bathing, upper and lower dressing, toileting, wheel­
chair driving, going up and down stairs, compre­
hension, and expression) on a 5-point scale (from
1 = complete assistance to 5 = complete
independence).
Visual inspection of the curves18 depicting
patient’s performance during the rehabilitation
period (Figure 2) suggests that at the end of the
first treatment period (T1), optic ataxia, gaze
apraxia, and dorsal simultanagnosia improved,
whereas ventral simultanagnosia did not. When
treatment was withdrawn, performance returned
to baseline levels (T2-T3). Crucially, at the end of
a new cycle of treatment (T4), optic ataxia, gaze
apraxia, and dorsal simultanagnosia improved
further and then remained stable or decreased
a little, without returning to the baseline level
after treatment withdrawal (T5-T6). Such improve­
ments enhanced copying abilities (Figure 3), and
autonomy in daily life activities (Table 2).

Discussion

Here, we described a rehabilitative approach for
BHS, in which we applied for the first time rever­
sing prism exposure,21 along with visual search and
eye movement trainings already described in the
literature. After each treatment session patient’s
performance improved, while it remained
unchanged or worsened when no specific treatment
was delivered. The visual search treatment amelio­
rated patient’s ability to allocate attention toward
visual objects (dorsal simultanagnosia), but not to
identify multipart objects (ventral simultanagno­
sia), and the eye movement training produced
more accurate and larger saccades and visual pur­
suit, in line with previous studies addressing

rehabilitation of BHS.7,19,20 The novel finding here
is that the implementation of prism exposure21
contributed to improve patient’s ability to plan
and execute reaching movements, thus reducing
optic ataxia. The reversing prism exposure training
promoted more accurate voluntary object reaching
movements, likely by exploiting residual recalibra­
tion abilities. In the prism adaptation literature,
recalibration is conceptualized as a fast, explicit,
strategic mechanism of error correction and com­
pensation, depending on a brain network including
cerebello-parieto-motor areas.22,23 The present
results would suggest that exposure to prism shift
in a condition where the visual shift is frequently
changed (before full adaptation occurs) could train
residual recalibration abilities and induce more
accurate movements. During the training session,
DG received frequent verbal feedback and instruc­
tions for planning movements, and, in case of error,
for noticing distance between the aimed object and
the actual movement outcomes, and for correcting
them. These verbal feedback followed the compen­
sative approaches already applied for rehabilitation
of BHS,7 and paralleled the rehabilitative
approaches
for
visuo-constructional
24
impairments. Our results might also be in line
with the finding that intense movement repetition
is able to improve reaching abilities.8 However,
future studies are needed to compare improve­
ments in optic ataxia following mere repetition of
pointing movements versus pointing movements
during reversing prism exposure.
The improvements in allocating attention
toward objects, in directing gaze, and in performing
movements toward objects, improved patient’s per­
formance on copying tasks, and in everyday activ­
ities, such as eating, grooming and dressing, which

TOPICS IN STROKE REHABILITATION

depend on accurate control of upper limb move­
ments. DG himself, his relatives, and health-care
personnel appreciated the higher level of indepen­
dence achieved.
The above-described findings have to be inter­
preted with caution due to the limitations related
to the single case design adopted here. Indeed, we
could not control possible confounding variables,
such as test–retest effects. Moreover, we could not
assess the long-term effects of the training after
discharge. It is also to be acknowledged that spon­
taneous recovery could be relevant during the first
months after a brain lesion. However, as improve­
ments in patient’s performance closely followed
treatment periods (and were null during treat­
ment withdrawal), and ventral simultanagnosia
did not ameliorate during the rehabilitation per­
iod, we would suggest that spontaneous recovery
was not a likely explanation of our results. It
remains to be assessed whether a more compre­
hensive rehabilitation plan, including training for
the ability of integrating multipart objects, could
contribute to ameliorate the entire spectrum of
BHS.
Author contributions
FP and AA collected the data and wrote the first draft; LT, CC
and PC revised original manuscript. All authors read and
approved the final manuscript.

Funding
FP received funding from the program V:ALERE2019
Università della Campania “Luigi Vanvitelli”, D.R. 907/2019,
prot. n. 148008, 4/10/2019.

ORCID
Francesco Panico
http://orcid.org/0000-0001-8346-5484
Luigi Trojano
http://orcid.org/0000-0002-0328-9642

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