Neuropsychological Rehabilitation
An International Journal
ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/pnrh20
Spatial exploration strategy training for spatial
neglect: A pilot study
Joan Toglia & Peii Chen
To cite this article: Joan Toglia & Peii Chen (2020): Spatial exploration strategy training for spatial
neglect: A pilot study, Neuropsychological Rehabilitation, DOI: 10.1080/09602011.2020.1790394
To link to this article: https://doi.org/10.1080/09602011.2020.1790394
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NEUROPSYCHOLOGICAL REHABILITATION
https://doi.org/10.1080/09602011.2020.1790394
Spatial exploration strategy training for spatial neglect: A
pilot study
Joan Toglia
a,b
and Peii Chen
c,d
a
School of Health and Natural Sciences, Mercy College, Dobbs Ferry, NY, USA; bRehabilitation Medicine
Department, New York Presbyterian Hospital, Weill Cornell Medical Center, New York, NY, USA;
c
Kessler Foundation, West Orange, NJ, USA; dDepartment of Physical Medicine and Rehabilitation,
Rutgers University, Newark, NJ, USA
ABSTRACT
ARTICLE HISTORY
Spatial neglect is a syndrome due to impaired neural
networks critical for spatial attention and related cognitive
and motor functions. Affected individuals also have
impaired self-awareness of their own neglect symptoms.
The present randomized controlled study was the first
proof-of-concept pilot examining the multi-context
treatment approach using a protocol of spatial exploration
strategy training in one brief session (20–30 minutes). The
therapist provided supportive feedback and semi-structured
guidance to promote strategy learning and self-discovery of
omission errors. 40 patients with left-sided neglect after
right brain stroke were included. The results showed that
the treatment reduced lateralized bias toward the
ipsilesional side of space but did not improve overall
detection performance. Impaired general self-awareness of
daily-life spatial difficulties was found independent of
treatment outcome. This implies that judgment regarding
responsiveness to treatment should not be made based on
an awareness interview or the severity of neglect
symptoms. Lastly, the treatment showed the potential of
improving online contextual self-awareness of spatial
abilities. A collaborative and interactive approach that
focuses on helping the patient self-discover, monitor and
self-manage their errors, appears to have a potential for
decreasing neglect symptoms. Future studies are required
to examine additional aspects of the multi-context
treatment approach.
Received 28 October 2019
Accepted 3 June 2020
KEYWORDS
Stroke rehabilitation; Brain
injury; Occupational therapy;
Cognitive rehabilitation;
Anosognosia
Introduction
Spatial neglect is a syndrome due to impaired neural networks critical for spatial
attention and related cognitive and motor functions. Affected individuals pay
little or insufficient attention toward the side of space contralateral to their
CONTACT Joan Toglia
jtoglia@mercy.edu
School of Health and Natural Sciences, Mercy College, 555
Broadway, Dobbs Ferry, NY 10522, USA
Supplemental data for this article can be accessed at https://doi.org/10.1080/09602011.2020.1790394
© 2020 Informa UK Limited, trading as Taylor & Francis Group
2
J. TOGLIA AND P. CHEN
injured cerebral hemisphere (Corbetta & Shulman, 2011; Mesulam, 1999), manifested as a failure to report, respond, or initiate movement toward stimuli presented in the contralesional side of space (Heilman et al., 2012). Left-sided
neglect after right brain stroke is more common than right-sided neglect after
left brain stroke (Chen, Chen, et al., 2015a). Spatial neglect is a major hidden disability post-stroke, slowing functional recovery and impeding rehabilitation outcomes (Chen, Hreha, et al., 2015b; Wee & Hopman, 2008).
Treatment for spatial neglect can be categorized into two major approaches:
the bottom-up stimulus-driven approach and the top-down strategy-learning
approach (Bowen et al., 2013; Marshall, 2009). The bottom-up approach may
facilitate neural changes in spatial functions through various sensory stimulation
or visuomotor adaptation pathways. Examples of the bottom-up approach to
spatial neglect rehabilitation include optokinetic stimulation (Kerkhoff et al.,
2006), neck vibration (Schindler et al., 2002) and prism adaptation (Goedert
et al., 2020). Unlike the bottom-up approach, the top-down approach is
focused on explicit learning of strategies and repetitive practice of strategy application. The most commonly used top-down treatment for spatial neglect is visual
scanning (Chen et al., 2018; Weinberg et al., 1977). During treatment, patients
with left-sided neglect learn to use a visual search pattern by placing a visually
salient stimulus (e.g., bright-coloured stripe) on the left edge of a defined workspace (e.g., a table or a newspaper page). They start searching from the salient
stimulus toward the right, non-neglected side of space. This strategy helps
patients to read and locate objects. The lighthouse strategy is also commonly
taught to patients with spatial neglect (Niemeier, 1998; Niemeier et al., 2001).
It is a visual imagery technique wherein patients learn to scan a scene by
turning their head from side to side, like a sweeping beam of light from a lighthouse. The literature shows that these top-down trainings improve spatial
neglect and functional activities (Bowen et al., 2013; Winstein et al., 2016).
However, the top-down treatment approach can be challenging, especially for
patients who have impaired self-awareness of their neglect symptoms or the
consequences of their spatial deficits, i.e., anosognosia for spatial neglect (Berti
et al., 1996; Chen & Toglia, 2019; Jehkonen et al., 2001; Ronchi et al., 2014),
and for patients who have difficulty in sustaining their attention on a specific
task for a period of time (I. H. Robertson, 1990; I. H. Robertson et al., 1995).
Patients with self-awareness deficits may not actively seek treatment or be
engaged in treatment activities. Patients with sustained attention deficits may
be limited in their learning ability.
Beyond the dichotomy of the bottom-up vs. top-down approaches, the multicontext treatment approach, based on a Dynamic Interactional Model of Cognition (Toglia, 2011; Toglia & Cermak, 2009; Toglia et al., 2019), suggests a highly
personalized strategy training approach that focuses on helping a patient to
self-recognize, monitor and manage cognitive symptoms across variations in
tasks. The multi-context treatment approach aims to remediate spatial neglect
NEUROPSYCHOLOGICAL REHABILITATION
3
through supportive guidance and collaborative interaction between the patient
and the therapist to facilitate self-awareness and optimize functional performance. Others have also proposed solutions using verbal or video feedback
during a specific visuospatial task (Tham & Tegner, 1997) or every day activities
(Soderback et al., 1992; Tham et al., 2001). For example, Soderback and colleagues (1992) video-recorded four patients with left-sided neglect who were
asked to find a piece of dough in a refrigerator, cut the dough into sixteen
pieces and distribute them evenly on a baking tray. During video review, the
patient was guided in identifying neglect symptoms to increase self-awareness.
Strategies for improving performance were suggested, including systematic
search from left to right, and exploration of the entire workspace by feeling
the left-end edge of the baking tray. The same tasks and procedures were
repeated four times over 7 days. In addition to increased performance on the
baking tasks, performance also improved on the Albert’s Test (Albert, 1973), a
target cancellation test (Soderback et al., 1992). Another case series study conducted by Tham and colleagues (2001), asked four patients to perform the
same self-selected activity again (e.g., reading newspaper or gardening) immediately after receiving feedback and discussing strategies. After four weeks of intervention (one hour a day, five days a week), spatial neglect improved based on a
target cancellation test and the Baking Tray Test (Tham & Tegner, 1996). In
addition to spatial neglect, self-awareness of one’s own disability improved as
well (Tham et al., 2001). However, the self-awareness deficit addressed in
Tham et al. (2001) was not specifically related to spatial neglect, and the
measure used did not separate general, offline self-awareness from contextual,
online self-awareness (Toglia & Kirk, 2000).
The present study was the first proof-of-concept pilot examining the multicontext treatment approach for spatial neglect as well as self-awareness
deficits using a randomized controlled study design. Specifically, we created a
protocol for spatial exploration strategy training. The therapist guides a patient
in specific research-informed strategies based on the patient’s performance of
a spatial task at the time. The methods used for guidance adhere to supportive
feedback and help the person self-discover omission errors themselves (Schrijnemaekers et al., 2014). The protocol also incorporates common neurorehabilitation principles such as repetition (i.e., multiple practice trials in a given
session) and includes varying task features (i.e., changes in size of explored
space and in distractor items). To this end, we examined three a priori hypotheses in the present study. Hypothesis 1 was that a single session of spatial
exploration strategy training would improve spatial neglect symptoms. By
definition, patients who are generally unaware of their own spatial difficulties
(offline anosognosia) do not recognize the need for treatment of spatial
neglect, and thus may receive little benefit from strategy training. Thus, Hypothesis 2 was that better general, offline self-awareness of spatial neglect symptoms
in real-life situations would be associated with better treatment outcomes. Lastly,
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J. TOGLIA AND P. CHEN
the protocol was focused on helping patients with spatial neglect to self-recognize, monitor and manage their own symptoms during strategy training. Thus,
Hypothesis 3 was that online self-awareness of spatial difficulties would be
better after intervention in the treatment group, relative to the control group.
Materials and methods
Participants and Procedures. Forty-four individuals were recruited from five inpatient rehabilitation facilities in the metropolitan area of New York City and provided informed consent, from January to December 2003. The study was
approved by each facility’s Institutional Research Board. While participating in
the study, all the patients were receiving rehabilitation services. Informed
consent and authorization to disclose protected health information for research
was obtained prior to testing. Inclusion criteria for study participation were (1)
right unilateral cerebrovascular accident, diagnosed by neuroradiologic
findings (CT or MRI scan), (2) presence of spatial neglect as shown in at least
one of the four designated tests (described in the following section), administered by an occupational therapist, (3) ability to follow two-step directions and
to provide informed consent, as determined by the primary unit physician, (4)
functional use of one hand, (5) visual acuity of at least 20/80 (with corrective
lenses if applicable), and (6) no prior history of significant previous psychiatric
disorder, neurological disorder, or chronic alcoholism.
Participating patients were randomly assigned to one of two intervention
groups: the control group or the treatment group. Randomization was based
on the last digit of a patient’s medical record number, reported by the patient’s
primary therapists to the research therapist. Recruitment terminated once each
of the two intervention groups reached 20 participants who completed five
activities in the sequence shown in Figure 1. During intervention, the treatment
group received a semi-structured, therapist-guided spatial exploration strategy
training while completing a 12-page object search task; the control group completed the task without receiving any guidance or feedback from the therapist.
Object Search Task. A patient was presented with 12 pages of line drawings of
objects, one page at a time. There were four task conditions based on page size
and the presence of background non-object distractors. The task condition
Figure 1. Sequence of the activities in the present study.
NEUROPSYCHOLOGICAL REHABILITATION
5
changed every 3 pages (Figure 2), in this order: Small-sized page (8 ½ x11 in.)
with no distractor, large-sized page (17 × 22 in.) with no distractor, small-sized
page with distractors, and large-sized page with distractors (see examples of
stimuli in Figure 3). The small-sized and large-sized page conditions differed in
the blank space among stimuli while the stimulus size remained the same
across conditions (i.e., stimuli were more scattered on a large than small
page). Each page contained 24 common and recognizable objects, such as
door, spoon, bell, etc. 12 of the objects scattered on the left side, and the
other 12 objects on the right side. Each page was presented in midline of the
patient who was instructed to, “tell me all of the objects that you see.” If the
patient was unable to name the object, the therapist instructed him/her to
describe the object’s function or point to it. Inaccurate naming or inability to
recognize objects were documented, but the person was given full credit for
ability to locate an object, even when misidentification occurred. Thus, performance on each page was rated based on object detection, ranging from 0 to 24. In
addition, we also assessed performance using the laterality index and the
location of the first object detected. The laterality index was calculated to determine the degree of asymmetrical performance (i.e., the ratio of the number of
items detected on the left side to the total number of items detected). The
location of the first object detected was recorded and coded as 1, 2, or 3 to indicate the left, centre, or right region of a given page.
Spatial Exploration Strategy Training. The therapist provided the spatial
exploration strategy training to patients in the treatment group during the
object search task. The objectives were to teach the patient exploration strategies, to help increase self-awareness, and to promote a sense of control over
symptoms of spatial neglect (Toglia, 2004; Toglia & Cermak, 2009). The same
steps were followed for each of the 12 object search pages (see further information in the Supplemental Material).
Step 1: Object Search. The therapist presented the patient with a new page of
stimuli and asked them to report all the objects they detected. Performance was
recorded and coded as described above.
Step 2: Verbal Feedback. If omissions occurred during step 1, the therapist generally informed the patient where objects were missed (left or right side) but did
not point out errors or orient the patient to the neglected space. The objective
was to encourage the patient to spontaneously orient to the general area where
the objects had not been detected.
Figure 2. Sequence and conditions of the 12-page object search task.
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J. TOGLIA AND P. CHEN
Figure 3. Examples of stimuli used in the object search task: (a) small page without distractor
and (b) small page with distractors.
Step 3. Strategies. If there were still missing objects after verbal feedback, the
therapist proceeded to strategy exploration training. This included use of a
tactile and spatial imagery strategy, a visual anchor strategy, and a stimulus
reduction strategy, in this order or until all objects on a page were detected.
The tactile and mental imagery strategies were designed to assist the person
in creating a representation of space and orienting them to space that had
not been explored. Errors were not directly pointed out. Instead, guidance was
provided to help the patient attend to neglected space and self-discover omissions themselves. The visual anchor strategy was designed to build upon the
tactile and mental imagery strategy by suggesting the utilization of an external
stimulus visible to the patient. The stimulus served as the visual anchor as well as
visual feedback for the person to know that their exploration reached the left
side. Finally, the stimulus reduction strategy encouraged the patient to cover
part of the page using a blank piece of paper to reduce visual stimuli so that
they could self-recognize missed items.
Step 4: Self-reflection and Strategy Reinforcement. Before proceeding to the
next page regardless of the performance, the therapist would ask the participant
“Why do you think you originally may have missed some of those items?” The
person was encouraged to answer using their own words. The therapist would
end the conversation with “The methods I showed you will help you check yourself
to make sure you have seen everything on both sides of space. Remember to use [the
strategies above]. It will help you monitor the tendency to miss things.” The patient
was provided positive feedback each time spontaneous initiation of the strategies was observed on subsequent pages.
Spatial Neglect Assessment Battery. We considered two outcome measures that
determined patients’ performance of a battery of four tests for spatial neglect
including line crossing, star cancellation, baking tray task, and picture scanning.
Except for the baking tray task (Tham & Tegner, 1996), all the other tests were
extracted from the Behavioral Inattention Test (B. Wilson et al., 1987) and were
NEUROPSYCHOLOGICAL REHABILITATION
7
included in the total detection score (i.e., the total number of items detected),
which was one of the outcome measures. The other outcome measure was
the overall laterality index of the four tests, which was defined as the total
number of items detected on the left side divided by the total number of
items detected. A laterality index between 0.48 and 0.52 was considered
within the normal “unbiased” range while we determined an index above
0.52 as right-sided neglect and below 0.48 as left-sided neglect (Halligan
et al., 1991). It is important to note that a given patient can demonstrate
a poor performance below the abnormality cutoff but does not show lateralized neglect.
Line Crossing. The test consists of 40 lines, each 2.5 cm in length, in various
orientations, printed on a piece of paper (20 × 26 cm). The lines are arranged
in seven columns of six lines each, except for the central column of four lines
(not included in scoring). The examiner demonstrated by crossing out two of
the four centre lines and asked the participant to cross out all the other lines.
The maximum score is 36 (18 left and 18 right).
Star Cancellation. The test is a visual search task for small stars on a 30 × 21 cm
page, where there are distractor items that included 52 large stars, 10 short
words, and 13 capital letters. All stimuli are randomly interspersed. Among the
56 small stars (targets), there are two small stars in the centre of the page that
the examiner crosses out for demonstration before the patient begins taking
the test. The maximum score is 54 (27 left and 27 right).
Baking Tray Task. The test presents a 50 × 75 cm hardboard and 16 blocks of
wood, and the task is to place the blocks over the hardboard as symmetrically as
possible, as though the blocks were buns being placed on a baking tray to be put
in the oven. Symmetrical placement required that eight blocks be placed on
each half of the tray. The number of blocks placed on each half of the board
is counted (maximum score = 16). When a block is placed directly in midline, a
score of .5 is counted for each area. Due to the scoring method, this test was
only included in the overall laterality index but excluded from the total detection
score of the entire battery.
Picture Scanning. The test consists of three 11 × 14′ coloured photographs of
(1) meal on a plate, (2) bathroom sink with toiletries, and (3) view of a room. Each
photograph has various objects arranged about the midline. The instruction is to
name and point to all the objects in each picture. There are two alternate versions of the test. The two versions present the same objects in different locations,
in each of the photographs. In the present study, pictures were presented in the
same order to each patient, with version A used before intervention and version
B after intervention. The score is the total number of items detected on the right
and left side of each photograph. Centre items are not scored. The maximum
score or total number of objects across the three photographs is 24 (12 left
and 12 right). Errors in naming or misidentification of objects are recorded but
do not lower the score.
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J. TOGLIA AND P. CHEN
General Self-Awareness for Spatial Difficulty. After completing the spatial
neglect assessment battery as the baseline measure (Figure 1), we asked the
patients to answer 17 questions about their self-perceived spatial difficulties in
daily-life situations (Table 1). The answer to each question could be “not at
all,” “a little,” “somewhat,” or “a lot,” which were coded from 1 to 4 respectively.
Their primary occupational therapists were also asked to answer those questions.
These therapists had interacted with the patients a minimum of four days and
completed assessment for functional independence with the patients, and
thus they had observed their patients in various daily-life situations. If an activity
described in a given question was not applicable to the patient or not observed
by the therapist, then the question was skipped. The final score of each questionnaire was the average of all the available answers provided. We then generated
the offline self-awareness deficit score by subtracting the patient self-rated score
from the therapist-rated score, with a greater value indicating that a greater level
of general self-awareness deficits.Toglia, 2004).
Online Self-Awareness Deficit. Immediately after intervention, the patient was
asked to estimate their performance in the 12-page object search task (Figure
1). The self-estimation was compared to the total number of objects detected
across the 12 pages (maximum number of objects = 288) and scored dichotomously. Specifically, under the following circumstances, a score of 0 was
assigned for no online self-awareness deficit: (1) if they rated performance as
“no difficulty” and if they detected at least 91% (≥ 262) of the objects, (2) if
they indicated they had a “little difficulty” and if they detected at least 71% (≥
204) of the objects, (3) If they indicated they had “some difficulty” and if they
detected at least 50% (≥ 144) of the objects, and (4) if they indicated they had
“lot of difficulty” and if they detected fewer than 50% (≤ 143) of the objects. If
Table 1. Questionnaire for self-perceived spatial difficulties in daily-life situations.
1. Since your stroke, do you experience … difficulty locating, finding or seeing everything around you?
2. Since your stroke, do you experience … difficulty understanding what you read?
3. Since your stroke, do you experience … tendency to miss food or items on your plate / food tray?
4. Since your stroke, do you experience … tendency to make errors dialing phone numbers?
5. Since your stroke, do you experience … tendency to misread time on clock or watches?
6. Since your stroke, do you experience … difficulty finding items in the bathroom closet or sink?
7. Since your stroke, do you experience … difficulty finding all the items on tables, shelves, closets, draws or
counters?
8. Since your stroke, do you experience … tendency to skip words or sentences when reading?
9. Since your stroke, do you experience … a tendency to miss things on the left side?
10. Since your stroke, do you experience … a tendency to bump into walls, doorways, furniture or people on the
left side?
11. Since your stroke, do you experience … tendency to forget about your left arm or foot?
12. Since your stroke, do you experience … a tendency to miss numbers, letters or words on the left side?
13. Since your stroke, do you experience … a tendency to shave only one side of your face or put makeup only on
one side?
14. Since your stroke, do you experience … a tendency to comb one side of your hair?
15. Since your stroke, do you experience … a tendency to miss food on the left side?
16. Since your stroke, do you experience … a tendency to crowd writing on the right side of a page?
17. To what extent are any difficulties in finding or seeing things on the left side interfering with your overall ability
to function?
NEUROPSYCHOLOGICAL REHABILITATION
9
a given patient did not meet any of the above circumstances, it was determined
that they overestimated their performance and were given a score of 1 for the
presence of online self-awareness deficits.
Analysis Methods. All the analyses were performed using STATA/SE16.0, and
the alpha level was set at .05. We described participant characteristics (nonmodifiable variables) using median and interquartile range (IQR) for continuous
variables, and percentages for categorical variables, and performed group comparisons using the U test for continuous variables and chi-squared for categorical
variables. If any of the non-modifiable variables showed a potential difference (p
< .1) between groups, they would be included in the main analyses that examined a given a priori hypotheses.
Results and discussion
Participant Characteristics. Three patients (two in the control group and one in
the treatment group) did not meet all the inclusion criteria. One patient in the
treatment group was unable to complete testing because of medical problems
unrelated to the study procedures. A total of 40 patients, 20 in each group,
were included in the final analysis. Table 2 presents the characteristics of participating patients within each group. Two variables were potentially different
between groups. The treatment group was younger and had more male participants than the control group (both p < .1). These two variables, age and sex, were
then included in the following analyses that examined a priori hypotheses.
Hypothesis 1: A single session of spatial exploration strategy training would
improve spatial neglect symptoms.
To test this hypothesis, we conducted a 2 × 2 repeated-measure ANCOVA with
the intervention group (control vs. treatment), assessment time (before vs. after
intervention), and the interaction term of the two as predictors to examine each
of the two outcome measures (the total score and the overall laterality index of
the spatial neglect assessment battery), and added age and sex as covariates.
First, we examined the total detection score of the spatial neglect assessment
battery, and the analysis showed a main effect of group, F(1,36) = 39.77, p
< .001, partial η² = .51, but no main effect of assessment time, F(1,36) = .34, p
= .561. The group by assessment time interaction was significant, F(1,36) =
6.59, p = .014, partial η² = .15. Post hoc Tukey Honest Significant Difference
(HSD) tests revealed that (1) at baseline, the control group had a better score
than the treatment group but after the intervention, the two groups did not
differ, and (2) the control group’s score declined after intervention by an
average of 6.8 points (Table 3) while the interaction did not change the treatment group’s score statistically. Figure 4(a) illustrates this interaction.
Next, we examined the overall laterality index of the spatial neglect assessment battery using the same analysis model and procedures. The analysis
yielded no main effect of group, F(1,36) = 3.71, p = .062, or assessment time, F
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J. TOGLIA AND P. CHEN
Table 2. Participant characteristics.
Variable
Control Group (n =
20)
Treatment Group (n =
20)
Group comparison result:
p value
Age (in year)
75 (63–78.5)
64.5 (57–74.5)
.066
Sex:
.058
Male
7 (35%)
13 (65%)
Female
13 (65%)
7 (35%)
Race/Ethnicity:
.387
White
17 (85%)
13 (65%)
Black
3 (15%)
5 (25%)
Asian
0
1 (5%)
Hispanic
0
1 (5%)
Education:
.394
< High School
2 (10%)
3 (15%)
High school
7 (35%)
6 (30%)
Associate degree or some college
1 (5%)
5 (25%)
College
4 (20%)
3 (15%)
Graduate school
6 (30%)
3 (15%)
Time post stroke (in day)
26 (16.5–39)
22 (18–41)
.828
Stroke type:
.429
Ischemic
17 (85%)
15 (75%)
Hemorrhage
3 (15%)
5 (25%)
Visual field cut:
.758
Yes
11 (55%)
9 (45%)
No
9 (45%)
9 (45%)
Missing information*
0
2 (10%)
Infarct location in the right cerebral
.116
hemisphere:
Cortical with frontal involvement
2 (10%)
5 (25%)
Cortical without frontal
6 (30%)
4 (20%)
involvement
Subcortical
6 (30%)
3 (15%)
Mixed
2 (10%)
8 (40%)
Missing information*
4 (20%)
0
General (offline) self-awareness
1.35 (1–1.93)
1.38 (1.12–1.85)
.764
deficit score
Notes: Categorical variables are described in counts (%) and analysed using X 2. Continuous variables are summarized in median (IQR) and compared using the U test.
*Missing information was information unavailable from medical charts of a given rehabilitation hospital and was
not included in group comparison analysis.
(1,36) = .82, p = .370, but the group by assessment time interaction was significant, F(1,36) = 4.76, p = .035, partial η² = .11. Post hoc Tukey HSD tests showed
that (1) at baseline, the control group was less lateralized than the treatment
group, and the two groups were not different after intervention, and (2) the
control group’s laterality index did not change significantly after intervention
but the treatment group’s became less lateralized (see Table 3 and Figure 4(b)).
In summary, although patients were randomly assigned to a group, the
control group had better performance than the treatment group at baseline,
shown in both the detection score and the laterality index. The control
group’s performance declined after intervention, in terms of the detection
score, but not in terms of the laterality index, suggesting that their lateralized
spatial bias remained unchanged but their ability to make correct responses in
the spatial neglect assessment battery deteriorated. In contrast, the treatment
group’s performance improved after the spatial exploration strategy training,
Table 3. Scores of the Spatial Neglect Assessment Battery before and after intervention, in means (SD).
Line crossing
Group
Baking tray task
Picture scanning
Overall
After
Before
After
Before
After
Before
After
Before
After
30.0 (8.6)
.38 (.21)
27.3 (9.4)
.34 (.22)
34.7 (13.4)
.32 (.20)
31.5 (15.4)
.30 (.21)
NA
.29 (.29)
NA
.35 (.30)
17.0 (4.4)
.39 (.17)
16.0 (5.1)
.28 (.18)
81.6 (22.9)
.34 (.16)
74.8 (27.7)
.32 (.19)
26.1 (10.5)
.31 (.22)
27.6 (8.8)
.35 (.18)
30.6 (15.1)
.23 (.20)
31.7 (15.3)
.31 (.19)
NA
.06 (.11)
NA
.20 (.27)
15.3 (4.9)
.34 (.17)
17.0 (5.3)
.31 (.19)
71.9 (28.2)
.23 (.15)
76.2 (27.3)
.29 (.17)
Notes: The overall detection score is the sum of three test scores (excluding the Baking Tray Task; see the Methods section for the scoring method of this test), and the overall laterality index is the
average of the indices from all four tests. Abbreviation: NA, not applicable.
NEUROPSYCHOLOGICAL REHABILITATION
Control Group (n = 20)
Detection Score
Laterality Index
Treatment Group (n = 20)
Detection Score
Laterality Index
Star cancellation
Before
11
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Figure 4. Treatment efficacy on spatial neglect severity in terms of (a) detection score and (b)
laterality of the spatial neglect assessment battery before and after intervention. The higher the
detection score, the better the visuospatial performance. The higher the laterality index, the
more symmetrical the performance (less bias toward the ipsilesional side of space). Error bar
= SE.
in terms of laterality but not of detection ability, suggesting that the treatment
was effective in reducing lateralized spatial bias but did not change their ability
to make correct responses in visuospatial tasks. Thus, the finding on laterality
was consistent with the a prior hypothesis. However, the finding of the detection
score was not as expected.
Hypothesis 2: General, offline self-awareness of spatial difficulties was associated
with better treatment outcome. Based on the U test, the two groups did not differ
in self-awareness deficit score (p = .764; see the last row of Table 2), suggesting
they had a similar level of general, offline self-awareness deficits. To examine the
hypothesis, we performed a multivariate regression analysis on each outcome
measure. Intervention group, self-awareness deficit score, and the interaction
of the two were independent variables, and the baseline outcome measure,
age, and sex were included as covariates. The hypothesis would be supported
if the interaction effect was significant. For the total detection score, none of
the independent variables showed a significant effect (all p values > .1). For
the overall laterality index, none showed a significant effect either (all p values
> .3). Thus, we did not find evidence supporting the hypothesis, suggesting
that general self-awareness of spatial deficits might be independent of treatment outcome.
Hypothesis 3: Online emergent self-awareness of spatial difficulties would be
better after intervention in the treatment group, relative to the control group. 15
(75%) of the control group and 8 (40%) of the treatment group showed online
self-awareness deficits as defined by overestimation of their own performance
relative to their actual performance over the 12 pages of object search. This
group difference was found significant, X 2(2) = 5.01, p = .025. Thus, the hypothesis was supported by the result, suggesting that the spatial exploration strategy
training improved online self-awareness of spatial difficulties among patients
with spatial neglect.
Post hoc Hypothesis: Performance continued improving during the spatial
exploration strategy training. In order to explore the possible accounts for the
NEUROPSYCHOLOGICAL REHABILITATION
13
unexpected finding related to Hypothesis 1, we inspected the two groups’ performance during intervention. Due to the small sample size, we were unable to
perform statistical analyses to examine the effect of object search condition
embedded in the fixed page order (Figure 2). Thus, we described the apparent
pattern as shown in Figure 5 and performed between-group comparisons in
the differences between the 1st and 12th pages.
While the number of objects detected by the control group declined (Figure 5
(a)), the treatment group appeared to improve from the first trial to the last trial
within the first condition (small page without distractor) and within the third
condition (small page with distractors) although the overall trend was also a
decline of the number of objects detected over the 12 pages. The control
group declined more than the treatment group (M ± SD = −7.6 ± 1.3 vs. −3.2 ±
1.3; t test: p = .020). The spatial exploration strategy training appeared to
reduce lateralized bias (laterality index closer to .5) after the first page, and the
laterality changed little from the 2nd to the 6th pages over two task conditions
where there were no background distractors (Figure 5(b)). Then the laterality
index dropped (more biased toward the right side) at the 7th page when the
third condition (small page with distractors) was introduced, but after provided
with feedback and strategies, laterality improved again over the next two task
conditions (Figure 5(b)). On the other hand, the control group’s laterality index
declined most apparently at the 7th page and declined further, probably due
to too few of the objects detected in the later conditions and later trials.
Overall, the control group became more biased but the treatment group
improved (M ± SD = −.17 ± .05 vs. .06 ± .05; t test: p = .002). Lastly, the treatment
group changed their initial search location from the right side toward the centre
after the first two trials of the first condition and eventually more toward the left
side during the last task condition (pages 10–12). The control group kept initiating their search more on the right side over the entire intervention period (Figure
5(c)). In comparison to the control group, the treatment group showed greater
difference between the 1st and 12th pages (M ± SD = .05 ± .20 vs. −.7 ± .24; t
Figure 5. Performance during intervention in terms of (a) numbers of objects detected, (b) laterality index, and (c) initial search location across the four consecutive task conditions: small page
without distractor (S w/o D), large page without distractor (L w/o D), small page with distractors
(S w/ D), and large page with distractors (L w/ D) over 12 pages. Each data point is the median
value of each group corresponding to a given trial. The white circles and dash lines represent the
control group, and the black circles and solid lines represent the treatment group.
14
J. TOGLIA AND P. CHEN
test: p = .022). Overall, the spatial exploration strategy training prevented the
treatment group’s detection performance from decline, and led the treatment
group to initiate their object search from a centre-left location.
General discussion
We conducted a randomized controlled study that examined the effect of a brief
20-to-30-minute session of spatial exploratory strategy training among individuals with left-sided spatial neglect after right-brain stroke. The design and delivery methods of the intervention were based on principles from the multi-context
treatment approach of the Dynamic Interactional Model of Cognition (Toglia,
2011; Toglia et al., 2019; Toglia & Cermak, 2009). The therapist provided supportive feedback and semi-structured guidance to promote strategy learning and
self-discovery of omission errors. The spatial exploratory strategy training
focused on helping the patient recognize the need to use strategies for deploying attention to the entire workspace and preventing omission errors. In particular, the guidance provided by the therapist involved hands-on and
conversational interactions with the patient. This may have enhanced online
self-awareness and self-efficacy. Self-efficacy is an individual’s perceived belief
in their capabilities to manage performance errors or complete tasks successfully. As the person recognizes that they have missed items on the left side,
motivation for change requires the belief that there are methods that one can
use to prevent errors or enhance performance. In acquired brain injury, selfefficacy for managing symptoms has been associated with a better treatment
engagement and quality of life (Belanger et al., 2019; Brands et al., 2014). It
has also been found to be a mediating variable for perceived functional improvements in people with stroke (Nott et al., 2019). Although self-efficacy has not
been specifically studied in patients with neglect, evidence from other studies
suggests that using methods that provide an opportunity for patients to recognize and manage their own neglect symptoms, may be important in improving
self-efficacy and functional outcomes (Brands et al., 2017; Nott et al., 2019).
During the intervention, the treatment group showed improvement in laterality, and greater initiation of search on the left side, despite increasing task
difficulty. The overall number of items detected on the outcome measure
using the 4-test spatial neglect assessment battery, however, did not significantly
change after intervention. The control group’s performance showed a decline in
the number of items detected and unchanged laterality or search origin. These
findings suggest that the spatial exploratory strategy training improves lateralized spatial bias, which was the signature symptom of spatial neglect but may
not improve sustained attention that is required to complete visuospatial
tasks. Moreover, findings from the control group suggest that repetition of
visual search activities in the absence of therapist guidance and feedback
does not improve spatial bias and may lead to fatigue or reduced engagement
NEUROPSYCHOLOGICAL REHABILITATION
15
in visual search tasks. Given the brevity of the spatial exploratory strategy training protocol in the present study, the changes observed in attention to the left
side are impressive. The findings suggest, however, that once the lateralized bias
is decreased, intervention may need to also address non-lateralized spatial attention deficits.
Strategy learning can be challenging, especially for patients who have
impaired self-awareness of their neglect symptoms or the consequences of
their spatial deficits (Berti et al., 1996; Chen & Toglia, 2019; Jehkonen et al.,
2001; Ronchi et al., 2014). In the present protocol, we specifically included supportive feedback, semi-structured guidance and strategy training to help the
person self-detect and self-monitor errors in visuospatial tasks. Our second a
priori hypothesis was that patients with greater degrees of general, offline
self-awareness deficits would have more difficulty learning strategies, indicated
by poorer treatment outcomes. The findings, however, did not support the
hypothesis. The severity of general self-awareness deficits, outside the context
of the task, did not appear to be associated with treatment outcome.
However, online, emergent awareness of spatial difficulties improved in the
treatment group compared to the control group, thus supporting our third a
priori hypothesis. The ability to participate in and thus respond to the spatial
exploration strategy training appears to be more dependent on online awareness or that which emerges from direct experience with task performance.
The experience of performing repeated visual search tasks with guidance to
facilitate self-recognition and attend to omitted parts of space, appears to
have facilitated online awareness and attention to the left side in some patients,
regardless of initial general, offline awareness.
This disassociation between general, offline awareness and online awareness
has been observed in patients with spatial neglect (Chen & Toglia, 2019) and
different clinical populations (Goverover et al., 2014; O’Keeffe et al., 2007; Robertson & Schmitter-Edgecombe, 2015), supporting the Dynamic Comprehensive
Model of Awareness (Toglia & Kirk, 2000). General offline awareness is based
on patients’ daily-life experience, which relies on retrospective self-report, knowledge of task attributes (e.g., clock reading, hair brushing, way finding) as well as
self-perceptions of abilities and beliefs about certain tasks or in general. Selfawareness of neglect symptoms after performing tasks that help the patient
self-recognize task errors (Chen & Toglia, 2019) appears to be important in strategy learning and thus may be associated with treatment outcome. The Dynamic
Comprehensive Model of Awareness hypothesizes that offline awareness is
slower and more resistant to change, compared to online awareness. With
repeated online awareness experiences over time, and across different situations, offline awareness is hypothesized to gradually improve, however this
requires future study.
The present findings are of great importance in the development of personalized treatment for spatial neglect and related self-awareness deficits. Currently,
16
J. TOGLIA AND P. CHEN
no treatment protocol exists to improve self-awareness in patients with spatial
neglect following a stroke. The majority of recommended treatment options
(Bowen et al., 2013; Hebert et al., 2016; Winstein et al., 2016) rarely take selfawareness deficits into account although anosognosia is a common symptom
among patients with spatial neglect (Chen & Toglia, 2019). For patients with
spatial neglect, their self-awareness of their own neglect symptoms is impaired,
presenting an obstacle to rehabilitation efforts. Thus, the treatment for selfawareness cannot be isolated from the treatment for spatial neglect in this
population.
Addressing self-awareness when treating patients for spatial neglect can
enhance treatment outcome, which is the core idea of the multi-context treatment approach of the Dynamic Interactional Model of Cognition (Toglia, 2011;
Toglia et al., 2019; Toglia & Cermak, 2009). As online awareness emerges, the
patient is immediately encouraged to use strategies to manage neglect symptoms, thus simultaneously building a sense of mastery and encouraging active
participation in treatment. It is important that methods used to enhance
online awareness are closely integrated with strategy training and efforts to
foster self-efficacy Lower self-efficacy has been associated with anxiety and
depression (Brands et al., 2019). If awareness of neglect symptoms emerges
without tools for the person to use to manage their neglect symptoms, there
may be a risk of negative emotional responses such as anxiety or depression
(for related clinical implications, see Chen & Toglia, 2019).
One interesting finding from the present study is the effect (or lack of) on the
spatial neglect assessment battery, which consisted of four tests including line
crossing, star cancellation, baking tray task (not included in the total detection
score), and picture scanning. The treatment group showed no change in the
total number of items detected after intervention although their lateralized
bias was reduced, and the control group showed a lower number of items
detected after intervention while their lateralized bias was unchanged. This indicates that patients were able to locate targets on both left and right sides of the
space in a more symmetrical manner after intervention but they were unable to
locate more targets overall. Thus, the present protocol is in favour of improving
spatial neglect, but only partially. Spatial neglect has been evaluated and defined
by abnormal lateralized bias toward the ipsilesional side of space. Non-lateralized
spatial symptoms exist as part of the spatial neglect syndrome but have received
relatively little attention. Halligan and colleagues (1991) classified patients who
omitted approximately equal numbers of items on both sides of a paper-andpencil test, i.e., the Behavioral Inattention Test (Wilson et al., 1987), as having
non-lateralized inattention. These patients’ test scores may be below the
cutoff score for the diagnosis of spatial neglect but their performance does
not necessarily manifest lateralized bias. It is possible that patients have
limited global attentional capacity and difficulty sustaining attention over the
course of a test. The spatial exploration strategy training examined in the
NEUROPSYCHOLOGICAL REHABILITATION
17
present study was not designed to improve sustained attention (Robertson et al.,
1995; Wilson et al., 2000) but may have helped keep sustained attention at the
same level pre and post-intervention, preventing the treatment group from performance decline.
Alternative to the account of sustained attention, which is focused on the
time-related sustainability, abnormality in the size of the attended spatial area
at a given moment may be another possibility. We hypothesize that spatial
neglect does not only impair the ability to allocate attention to the contralesional
side of space but also narrow the attended spatial area. The metaphor of a
moving spotlight has been used to theorize and generate discussions about
mechanisms of spatial attention (Cave & Bichot, 1999; Eriksen & Murphy, 1987;
Hamilton et al., 2010; Posner et al., 1980). The moving feature is emphasized
much more than other features, such as the aperture size, of the attention spotlight. This is true in both cognitive psychology (studying spatial attention) and
neuropsychology (studying spatial neglect). In the scenario of the present
study, patients might be able to attend to the left and right side after intervention (in which they had learned spatial exploration strategies), but the area
covered by their attentional searchlight remained abnormally narrowed so
that they find a limited number of items even after they shifted attention. This
argument is supported by a previous study suggesting abnormally small attention aperture being a feature of spatial neglect. Chen and Goedert (2012) asked
stroke survivors with right brain damage and healthy individuals to draw a clock
face on a blank piece of paper, which is a task that participants determine the
workspace (clock perimeter) before allocating specific information within the
workspace (clock numbers and hands). The authors found that patients
without spatial neglect produced the clock in a similar size to that produced
by healthy controls, but patients with spatial neglect produced smaller clocks.
The size of the clock did not correlate with the location of the drawing on the
paper (Chen & Goedert, 2012). Either way, the spatial exploration strategy training was not designed to address impairment in sustained attention or attention
aperture. Future studies may address these possibilities into strategy training for
improving spatial exploration.
Study Limitations. This is a pilot study on a novel treatment approach for
spatial neglect. Only one brief session was conducted. It is unknown how
many sessions are required to observe effects being transferred to real-life situations or whether there is any long-term effect. However, we demonstrated that
in the current relatively small sample size, the intervention improved lateralized
bias. Future studies are required to examine the efficacy of multiple sessions in
larger sample sizes and with a better-balanced study design, which avoids any
potential violation of assumptions for utilizing repeated-measures ANCOVA or
other parametric analyses. Another limitation is the difference between groups
at baseline where the control group had better performance in both detection
score and laterality index than the treatment group. This could create some
18
J. TOGLIA AND P. CHEN
ambiguity in interpretation. Nonetheless, the analysis results supported the presence of the treatment effect. In addition, the study included patients with a
variety of symptom severity. Patients with milder neglect might score at
ceiling in any test included in the outcome measure before or after intervention,
and their performance changes could not be adequately measured. A larger
sample size would allow for analyses of learning patterns within subgroups
that differ in level of severity.
Conclusion
A brief 20–30 minutes spatial exploration strategy training, which integrates supportive feedback and semi-structured guidance to promote strategy learning,
reduces lateralized bias toward the ipsilesional side of space among individuals
with left-sided spatial neglect after right-brain stroke. Impaired general selfawareness of daily-life spatial difficulties was found to be independent of treatment outcome. This implies that judgment regarding responsiveness to treatment should not be made based on an awareness interview or the severity of
neglect symptoms. A collaborative and interactive approach that focuses on
helping the patient self-discover, monitor and self-manage their errors,
appears to have a potential for decreasing neglect symptoms. The intervention
appeared to have improved self-awareness deficits within the task, which in turn,
helped patients learn the strategies and attend to the left side of space. Methods
that capture patterns of intra-individual change, learning and online awareness
along with transfer to other activities need to be further explored.
Future students need to examine additional aspects of this approach, particularly transfer and generalization beyond the visual object search task. The current
intervention provided the opportunity to observe carryover of strategies from
one page to the next across similar search tasks (near transfer). A next step
would be to incorporate techniques to help the person apply strategies to
other situations. For example, after the visual object search task, the patient
could be given the opportunity to apply the same strategies to functional
tasks such as searching for specific items in a cabinet or closet, or on a
webpage for an online store. Guided questions that ask the patient to identify
other situations that the same strategies could apply, could be used across
different tasks or situations (Toglia, 2011). Finally, the role of online awareness
and self-efficacy in contributing to functional outcome needs to be further
explored.
Acknowledgements
We thank occupational therapists and participating patients in the Rusk Institute of New York
University Medical Center, Burke Rehabilitation Hospital, Helen Hayes Hospital, New York Presbyterian Hospital, and Kings Harbor Multicare Center.
NEUROPSYCHOLOGICAL REHABILITATION
19
Disclosure statement
No potential conflict of interest was reported by the author(s).
Funding
This research was partially supported by an Extramural Research Development Award (Eunice
Kennedy Shriver National Institute of Child Health and Human Development), National Institutes of Health No. 2G11HD035965, Pilot grant awarded to Joan Toglia, through award
received by Mercy College, Dobbs Ferry, NY.
ORCID
Joan Toglia
http://orcid.org/0000-0002-6902-6853
Peii Chen
http://orcid.org/0000-0002-6724-7046
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