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89

Organizational Strategy Influence on Visual Memory


Performance After Stroke: Cortical/Subcortical
and Left/Right Hemisphere Contrasts
Gudrun Lange, PhD, William Waked, PhD, Stephen Kirshblum, MD, John DeLuca, PhD
ABSTRACT. Lange G, Waked W, Kirshblum S, DeLuca J.
Organizational strategy influence on visual memory perfor-
mance after stroke: cortical/subcortical and left/right hemi-
I T IS NOW CLEARLY recognized that effective organiza-
tional strategies influence the encoding of information to be
learned. For instance, the use of a semantic clustering strategy
sphere contrasts. Arch Phys Med Rehabil 2000;81:89-94. significantly improves the encoding of verbal material.1 Similarly,
the use of a ‘‘perceptual cluster’’ strategy,2 defined as an organized
Objective: To examine how organizational strategy at encod- (in contrast to a piecemeal or disorganized) approach to encoding
ing influences visual memory performance in stroke patients. complex visual stimuli, is associated with increased visual memory
Design: Case control study. performance in patients with different neurologic disorders2 or
Setting: Postacute rehabilitation hospital. amnesics after anterior communicating artery aneurysm.3
Participants: Stroke patients with right hemisphere damage It is also recognized that visual spatial/constructional informa-
(n ⫽ 20) versus left hemisphere damage (n ⫽ 15), and stroke tion is processed differently in the two cerebral hemispheres in
patients with cortical damage (n ⫽ 11) versus subcortical humans. Left hemisphere damage disrupts the detailed reproduc-
damage (n ⫽ 19). tion of a visual pattern; right hemisphere damage interferes with
Main Outcome Measures: Organizational strategy scores, the configurational perception (ie, ‘‘gestalt’’) of a design.4
recall performance on the Rey-Osterrieth Complex Figure (ROCF). Several authors have employed the Rey-Osterrieth Complex
Results: Results demonstrated significantly greater organiza- Figure (ROCF) to study both the influence of side of stroke (left
tional impairment and less accurate copy performance (ie, versus right hemisphere), and the influence of strategy (orga-
encoding of visuospatial information on the ROCF) in the right nized versus disorganized), on construction and recall of visual
compared to the left hemisphere group, and in the cortical material. Such studies have shown that stroke patients with left
relative to the subcortical group. Organizational strategy and hemisphere lesions tend to reproduce the ROCF by breaking the
copy accuracy scores were significantly related to each other. design into separate configurational elements, whereas patients
The absolute amount of immediate and delayed recall was with right hemisphere lesions have difficulty forming an overall
significantly associated with poor organizational strategy scores. ‘‘gestalt’’ of the figure, often missing crucial configurational
However, relative to the amount of visual information originally units of the ROCF.5-7 As such, both left and right hemisphere
encoded, memory performances did not differ between groups. stroke subjects have significant difficulties in organizing com-
Conclusions: These findings suggest that visual memory plex visual stimuli. Thus, in stroke patients, the decreased ability to
impairments after stroke may be caused by a lack of organiza- organize complex information may lead to less efficient encoding of
tional strategy affecting information encoding, rather than an visual information,8 resulting in reduced memory performance on
impairment in memory storage or retrieval. complex visual tests such as the ROCF.
Key Words: Stroke; Cerebral hemispheres; Visual; Memory In addition to perceptual-organizational deficits, stroke pa-
disorders; Rehabilitation. tients also evidence difficulties on measures of visual memory.9,10
Although impaired visual memory performance has tradition-
r 2000 by the American Congress of Rehabilitation Medi- ally been associated with lesions of the right hemisphere and
cine and the American Academy of Physical Medicine and
verbal memory impairments have been attributed to left hemi-
Rehabilitation sphere damage,11 this lateralized distinction has recently come
under considerable scrutiny, particularly with reference to right
hemisphere specificity toward visual memory disturbance.12 An
alternative explanation for some form of right hemisphere
From the Department of Psychiatry (Dr. Lange), Department of Radiology (Dr. specificity toward impaired visual memory performance may
Lange), Department of Physical Medicine and Rehabilitation (Drs. Kirshblum, have less to do with recall and recognition and more to do with
DeLuca), and Department of Neurosciences (Dr. DeLuca), University of Medicine and
Dentistry of New Jersey–New Jersey Medical School, Newark, and the Research
the reduced encoding secondary to inefficient perceptual process-
Department, Kessler Institute of Rehabilitation (Dr. Kirshblum) and the Kessler ing. That is, the observed ‘‘visual memory’’ deficit in right
Medical Rehabilitation Research and Education Corporation (Dr. DeLuca), West hemisphere stroke patients may be rooted in the type of
Orange, NJ; and the Department of Rehabilitation, Mt. Sinai Medical Center, New organizational strategy used to encode the visual information
York, NY (Dr. Waked).
Submitted for publication March 18, 1999. Accepted in revised form May 8, 1999.
rather than be attributable to a global deficit in storage or
Supported in part by grant 110 from the Henry H. Kessler Foundation. retrieval from long- or short-term memory stores. A major
Presented in part at the 104th meeting of the American Psychological Association, purpose of this study was to examine the hypothesis that visual
Toronto, Canada. memory impairment after stroke is related more to reduced
No commercial party having a direct financial interest in the results of the research
supporting this article has or will confer a benefit upon the authors or upon any
encoding because of impaired organizational strategy rather
organization with which the authors are associated. than to material-specific deficits in recall.
Reprint requests to John DeLuca, PhD, Kessler Medical Rehabilitation Research In addition to studying lateralized differences in neuropsycho-
and Education Corporation, Neuropsychology and Neuroscience Laboratory, 1199 logic performance, clinical neuroscientists are interested in
Pleasant Valley Way, West Orange, NJ 07052.
understanding the functional organization of the brain by
r 2000 by the American Congress of Rehabilitation Medicine and the American
Academy of Physical Medicine and Rehabilitation contrasting the damage in cortical and subcortical regions of the
0003-9993/00/8101-5515$3.00/0 brain. Much of the current literature on the role of subcortical

Arch Phys Med Rehabil Vol 81, January 2000


90 ORGANIZATIONAL STRATEGY IN STROKE, Lange

structures in neurobehavioral processing results from work with Table 1: Demographic Characteristics for the Four Stroke Groups
progressive neurodegenerative disorders such as Huntington RCVA LCVA CCVA SCVA
disease, Parkinson disease, and Alzheimer disease. Such studies (n ⫽ 20) (n ⫽ 15) p (n ⫽ 11) (n ⫽ 19) p
have described a ‘‘subcortical dementia,’’ characterized by
Age 57.85 (3.0) 61.67 (2.5) .3 57.36 (4.1) 58.47 (2.4) .8
slowing of cognition, memory disturbance, difficulty with
Education 14.06 (0.8) 13.50 (0.8) .5 14.30 (1.0) 14.06 (0.6) .8
complex intellectual tasks, visual-spatial abnormalities, and
IQ 107.89 (1.8) 110.73 (1.7) .2 108.20 (2.5) 111.00 (1.4) .3
disturbances in mood and affect.13 Cummings13 and Brandt and
BDI total 8.94 (1.5) 5.87 (1.9) .2 6.22 (1.6) 7.68 (1.5) .5
coworkers14 have argued that subcortical dementia differs both
score
quantitatively and qualitatively from the pattern of neurobehav-
Days post- 44.6 (11.3) 31.0 (2.8) .3 41.4 (13.2) 43.5 (10.1) .9
ioral deficits observed in cortical dementias.
stroke
It is unclear, however, whether the findings of cognitive
deficits associated with progressive neurologic disorders can be Data reported as mean (SEM). All comparisons are nonsignificant.
generalized to patients with focal lesions after cerebrovascular Abbreviations: RCVA, right hemisphere stroke; LCVA, left hemi-
accident (CVA). One of the few studies that examined neuropsy- sphere stroke; CCVA, cortical stroke lesions; SCVA, subcortical stroke
lesions.
chologic functioning in patients with cortical versus those with
subcortical vascular lesions was done by Wagner and Cush-
man.10 They found that the subcortical group was impaired on (BDI) score (ie, BDI score of ⬎17, more than mild depression)
measures of attention, memory, and intellectual performance were excluded. While some individuals with a BDI score of
and did significantly worse than the cortical group on these ⬍17 may have been mildly depressed, we had no reason to
measures. Although it is not clear why the subcortical group expect that mild depression would adversely influence ROCF
performed so poorly on tasks traditionally ascribed to cortical performance. Subjects were classified into the stroke category
processing, factors such as lesion size and location may groups based on a physician’s review of patients’ medical
contribute significantly to the performance. Whether the ob- records, the clinical diagnosis at admission to the rehabilitation
served memory deficits in stroke patients with lesions confined setting, and computed tomography (CT) scans obtained from
to subcortical structures result from deficits in retrieval from acute care hospital records. Subjects were first dichotomized
long-term storage (as suggested by the subcortical dementia into either right hemisphere CVA (ie, cortical as well as
hypothesis15 ) or to disorganization at the encoding stage has not subcortical structures within the right hemisphere) or left
been studied. hemisphere CVA (ie, cortical as well as subcortical structures
This study examined the hypothesis that impaired visual- within the left hemisphere) groups. To examine the influence of
perceptual recall in stroke patients may be caused by compro- damage to either cortical or subcortical structures on perfor-
mised organizational processing of the ROCF during encoding, mance, these same subjects were again divided into either the
and not by visual memory storage or retrieval failure. The cortical CVA (ie, frontal, temporal, parietal, and occipital
reduced ability to use an efficient perceptual organizational cortex) or subcortical CVA (ie, basal ganglia, cerebellum, pons,
strategy at the encoding stage of visual-spatial processing internal capsule, and thalamus) groups. Subjects who could not
(while the subject copies the ROCF) may be a primary reason be classified into these broad groups were not included in the
for impaired immediate and delayed memory recall. As such, it study. Five subjects had negative CT scans. Classification of
was hypothesized that a disorganized strategy will significantly these subjects was based on a review of medical records, on
reduce copy performance on the ROCF, which in turn will clinical presentation, and on neurologic examination during
significantly correlate with recall performance. That is, immedi- their acute care stay and at admission to the rehabilitation
ate and/or delayed visual memory recall scores will be signifi- institute (2 were classified left CVA, 2 right CVA, 1 subcortical
cantly affected by the degree of organizational fragmentation on CVA). No significant differences between the right CVA and
the copy component of the ROCF. Specifically, we hypoth- left CVA subjects and cortical CVA and subcortical CVA
esized that (1) right hemisphere and cortical lesions will have a patients on age, education, premorbid IQ, and BDI scores were
significantly greater influence on organizational strategy than found (table 1).
lesions in the left hemisphere or subcortical regions, respec-
tively, (2) a disorganized strategy will result in decreased Procedure
immediate and delayed recall performance on the ROCF, and All neuropsychologic tests were administered and evaluated
(3) once information is encoded, recall will not differ between by a senior neuropsychologist. Every reasonable attempt was
groups after controlling for differences in original learning (ie, made to keep the examiner blind to group assignment (ie,
savings score). anonymous identification numbers, standardized test administra-
tion, no chart review before neuropsychologic examination).
METHOD Subjects were administered a brief battery of standard neuropsy-
Subjects were 28 men and 9 women who were admitted to a chologic tests of approximately 45 to 60 minutes in duration.
secondary care rehabilitation hospital. All subjects were right- The ROCF copy, immediate recall, and 30-minute delayed
handed and without a previous history of CVA. Demographic recall conditions were administered in accordance with pub-
data are presented in table 1. On the average, the neuropsycho- lished procedures,17 and time to completion was recorded for
logic test battery was administered 39 days postonset each condition. Each subject was presented with a sheet of
(x ⫽ 39.25; SD ⫽ 38.65; range ⫽ 11 to 208 days). Age of paper with a copy of the ROCF placed in the top half of the page
stroke patients ranged from 29 to 75 years, with a mean of 58 and asked to copy the figure into the space below as quickly as
years. Inclusion criteria included a minimum verbal IQ of 85, as possible. Upon completion, the subject’s copy of the ROCF was
assessed by the North American Reading Test; no aphasia or removed and the subject was asked to reproduce the figure from
only mild aphasia based on clinical assessment; English as a memory (immediate recall) on a blank sheet of paper. Thirty
first language; and no history of prior neurologic illness, minutes after the immediate recall condition, the subject was
psychiatric disorder, or substance abuse. Subjects exhibiting again asked to recall the figure from memory (delayed recall).
symptoms of disorientation, psychiatric complications, or post- During the 30-minute period between immediate and delayed
stroke depression as assessed by the Beck Depression Inventory free memory recall of the ROCF, the following tests were

Arch Phys Med Rehabil Vol 81, January 2000


ORGANIZATIONAL STRATEGY IN STROKE, Lange 91

Table 2: Rey-Osterrieth Complex Figure Test Indexes


RCVA LCVA CCVA SCVA
Index (n ⫽ 20) (n ⫽ 15) p (n ⫽ 11) (n ⫽ 19) p

Organizational strategy score 86.40 (10.7) 55.26 (10.7) .05 105.00 (13.29) 49.74 (6.95) ⬍.001
Copy accuracy score 46.75 (4.5) 59.07 (3.7) .05 38.73 (6.8) 62.32 (1.5) ⬍.001
Immediate recall score 18.05 (3.40) 23.73 (4.76) .32 15.64 (3.93) 25.95 (4.31) .12
Delayed recall score 16.95 (3.14) 23.73 (4.92) .23 13.82 (3.52) 25.68 (4.26) .07
Savings ratio* .40 (.06) .37 (.07) .79 .41 (.08) .40 (.06) .92
Forgetting ratio† .94 (0.2) .97 (0.1) .90 .89 (0.1) .93 (.09) .77
Copy‡ 209.00 (23.06) 251.86 (44.97) .37 196.20 (35.64) 243.88 (37.80) .41
Immediate recall‡ 127.70 (11.85) 162.07 (19.0) .12 109.0 (16.05) 168.47 (13.91) .01
Delayed recall‡ 96.0 (14.57) 124.23 (12.83) .16 84.38 (13.87) 136.33 (10.81) .01
Scores reported as mean (SEM).
Abbreviations: RCVA, right hemisphere stroke; LCVA, left hemisphere stroke; CCVA, cortical stroke lesions; SCVA, subcortical stroke lesions.
*Immediate recall/copy score.
†Delayed/immediate recall score.
‡Time to completion (seconds).

administered: North American Reading Test, Wechsler Adult ROCF). If 1 of the 3 main elements was not completed, a score
Intelligence Scale–Revised Digit Span, Controlled Oral Word of 50 was assigned for that element. The total organizational
Association, and Animal Word Fluency. The BDI was adminis- strategy score served as the dependent variable for analyses.
tered after the ROCF delayed free recall reproduction was While there was no control for differences in motor ability
obtained. across subjects, the scoring system was such that quality of
construction had little impact on the organizational strategy
Scoring Procedure score.
A copy accuracy score and an organizational strategy score
were obtained for the copy component of the ROCF. Copy RESULTS
accuracy was defined as the degree of resemblance of the Planned comparisons were conducted using separate one-
subject’s copy to the original model and was scored in way analysis of variance (ANOVA) comparing right and left
accordance with standardized and published scoring proce- hemisphere CVA groups and cortical and subcortical CVA
dures.18 Immediate and delayed free memory recall of the groups.
ROCF was scored in the same manner. Raw scores served as a
dependent variable of the absolute amount of visual information
encoded/learned and recalled. Left Versus Right CVA
Organizational strategy was defined as the perceptual ap- The mean organizational strategy score for the right CVA
proach used to copy the original figure. Prior research has group in copying the ROCF was significantly more fragmented/
shown that subjects often employ 1 of 2 strategies in copying detailed and less configurational/holistic (F(1, 33) ⫽ 4.04,
the ROCF: either a fragmented and detail-oriented approach, or p ⫽ .05) than the approach used by the left CVA group (table 2).
a configurational/‘‘gestalt’’ approach.19 Although no data are In addition, the mean copy accuracy scores were significantly
available regarding the reliability and validity of the organiza- lower in the right CVA group than in the left CVA group (F(1,
tional scoring procedure for the ROCF used in this study, the 33) ⫽ 4.06, p ⫽ .05). This suggests a lower degree of construc-
procedure was similar to that used by Binder.5 For the present tional accuracy in the right CVA group than in the left CVA
study, an organizational strategy score was obtained by summat- group. No group differences were observed on immediate and
ing the number of lines it took the subject to draw three key delayed ROCF recall scores. Organizational strategy scores
elements of the ROCF: central rectangle, central cross, central were significantly correlated with copy and immediate and
diagonal. To obtain these scores, the examiner traced the delayed recall scores for both groups (table 3).
subject’s path of the ROCF on a separate piece of paper while To specifically examine the influence of organizational
the subject was drawing the figure, numbering the lines strategy on ROCF immediate and delayed recall performance,
consecutively as the subject proceeded. Each of the three main two groups were formed based on the median split of the
structural elements could be completed in a noncontiguous organizational strategy score. The two groups, the lower
manner and in any order. The lower the organizational strategy organizational strategy (LOS) group (score of ⬍60, n ⫽ 17)
score (ie, the fewer number of lines), the more organized or and the higher organizational strategy (HOS) group (score of
configurational was the subject’s approach. Thus, the best ⬎60, n ⫽ 18) were compared on immediate and delayed recall
possible organizational strategy score was an 8 (ie, one point for performance. In the HOS (more impaired) group, there were
each line drawn to complete the three main elements of the more subjects with right hemisphere stroke (14 of 20 subjects)

Table 3: Pearson Correlations of Organizational Strategy Score with Copy Accuracy Score and Immediate and Delayed Recall Scores
Organizational Strategy Scores
RCVA (n ⫽ 20) LCVA (n ⫽ 15) CCVA (n ⫽ 11) SCVA (n ⫽ 19)

Copy Accuracy score ⫺.87, p ⬍ .001 ⫺.93, p ⬍ .001 ⫺.91, p ⬍ .001 ⫺.87, p ⬍ .001
Immediate Recall score ⫺.76, p ⬍ .001 ⫺.52, p ⫽ .05 ⫺.95, p ⬍ .001 ⫺.51, p ⫽ .03
Delayed Recall score ⫺.82, p ⬍ .001 ⫺.50, p ⫽ .05 ⫺.85, p ⫽ .001 ⫺.54, p ⫽ .02
Abbreviations: RCVA, right hemisphere stroke; LCVA, left hemisphere stroke; CCVA, cortical stroke lesions; SCVA, subcortical stroke lesions.

Arch Phys Med Rehabil Vol 81, January 2000


92 ORGANIZATIONAL STRATEGY IN STROKE, Lange

than with left hemisphere stroke (4 of 15) (Fisher’s Exact Test,


two-tailed, p ⫽ .02). The HOS group had significantly de-
creased immediate recall scores (x ⫽ 9.94, standard error of the
mean [SEM] ⫽ 1.96) compared with the LOS group (fig 1)
(x ⫽ 31.65, SEM ⫽ 3.91) (F(1, 33) ⫽ 25.47, p ⬍ .001). The
same pattern was observed for the delayed recall scores in the
HOS group (x ⫽ 10.0, SEM ⫽ 2.04) versus the LOS group
(x ⫽ 30.29, SEM ⫽ 4.0) (F(1, 33) ⫽ 21.08, p ⱕ .001).
To examine if the relative amount of visual information
stored and retrieved differed between right and left CVA groups,
a savings ratio (immediate memory/copy score) and a forgetting
ratio (delayed/immediate memory score) were calculated for
each subject (table 2). No significant differences were found
between groups. Right and left hemisphere stroke groups also
did not differ in time to completion of copy or immediate or
delayed recall productions of the ROCF (table 2).
Cortical Versus Subcortical CVA
Both the mean organizational strategy (F(1, 28) ⫽ 16.57,
p ⬍ .001) and mean copy accuracy (F(1, 28) ⫽ 18.18, p ⬍ .001) Fig 2. Mean immediate and delayed recall performance for high
were significantly more impaired in the cortical CVA group organizational strategy (HOS) versus low organizational strategy
than in the subcortical CVA group (table 2). No significant (LOS) groups of the cortical/subcortical CVA subjects.
group differences were observed on either immediate or
delayed recall scores. Organizational strategy was significantly immediate (F(1, 24) ⫽ 7.0, p ⫽ .01) and delayed (F(1,
related to copy and immediate and delayed memory recall 21) ⫽ 8.38, p ⫽ .009) conditions.
performance for both the cortical and subcortical CVA groups
(table 3). To directly examine the influence of visual informa- DISCUSSION
tion encoding on the absolute amount of material recalled, the This study investigated the influence of organizational strat-
median split of the organizational strategy score was calculated egy on visual memory performance in stroke patients. The
(LOS, score ⬍58, n ⫽ 15; HOS, score ⬎58, n ⫽ 15) (fig 2). results clearly show that decreased organizational skills during
The HOS (more impaired) group (x ⫽ 11.47, SEM ⫽ 2.34) learning (ie, poor encoding) result in significantly reduced
immediately recalled significantly less visual information than recall from long-term storage. The ability to perceive the ROCF
the LOS group (x ⫽ 32.87, SEM ⫽ 4.48) (F(1, 28) ⫽ 17.92, configurationally (ie, using a holistic or ‘‘gestalt’’ approach, as
p ⬍ .001). The same pattern held true after a 30-minute delay measured by the organizational strategy score) was strongly
(HOS group, x ⫽ 11.6, SEM ⫽ 2.49; LOS group, x ⫽ 31.07, associated with improved accuracy in copying the ROCF (copy
SEM ⫽ 4.57) (F(1, 28) ⫽ 13.97, p ⬍ .001). accuracy score), resulting in better subsequent recall of the
When savings and forgetting ratios were calculated and material. These findings support the hypothesis that recall of
compared, scores were not significantly different between visual material is significantly influenced by the quality of
cortical and subcortical CVA groups (table 2). Time to comple- initial encoding of complex visual information.
tion of the ROCF copy component was not different between The results of our study are consistent with other studies in
groups. However, the group with subcortical lesions was both stroke patients8 and in those with other neurologic
significantly slower recalling the visual information on both the conditions2 that show that efficient, well-organized categoriza-
tion, configuration, or cluster strategies result in more efficient
visual memory encoding, storage, and retrieval. In contrast, a
piecemeal, perceptually disorganized approach to the acquisi-
tion of visual information results in significantly reduced recall
performance.5 Taken together, these results show that the level
of perceptual-organizational deficiency directly affects the
acquisition (or encoding) of visual information. In addition, the
quality of encoding of visual material on the ROCF in turn
directly influences absolute immediate and delayed recall
performance.
The right CVA group showed the most severe organizational
impairment, a finding consistent with previous research.5 The
finding of decreased organizational skills in the right CVA
group suggests that the previously reported sensitivity of the
ROCF to right hemisphere lesions may not be due to reduced
recall and recognition, but to poor encoding secondary to
reduced use of an organizational approach to copying the
design.12
Importantly, once information was encoded, the groups did
not differ in the subsequent recall or forgetting of the visual
material (ie, savings and forgetting ratios). Specifically, regard-
Fig 1. Mean immediate and delayed recall performance for high
less of how much visual information was originally learned and
organizational strategy (HOS) versus low organizational strategy stored, all groups were able to retrieve a similar percentage of
(LOS) groups of the right/left CVA subjects. the ROCF information initially encoded (ie, intact storage and

Arch Phys Med Rehabil Vol 81, January 2000


ORGANIZATIONAL STRATEGY IN STROKE, Lange 93

retrieval). Note, however, that because a healthy control group mance was now within normal limits). Future studies could
was not included in the present design, it is not clear whether examine the relative efficacy of treatments designed to improve
the rate of forgetting in the stroke groups was accelerated or encoding strategies versus treatments that focus primarily on
within normal limits. The only thing that can be concluded from improving recall and recognition (eg, memory books).
this study is that the forgetting rates did not differ between the
stroke groups contrasted. CONCLUSIONS
Memory is composed of multiple processes or stages. Thus, Our results suggest that visual memory impairment after
looking at memory as a single system is clearly too simplis- stroke may result from deficient encoding of information
tic.20-22 Among other classifications, memory can be divided secondary to decreased organizational skills, rather than to an
into encoding, consolidation, storage, and retrieval processes.23 impairment in memory storage or retrieval.
Consequently, evaluation of the nature of memory performance
or impairment can be viewed within this framework. Using this Acknowledgment: The authors thank Dr. Leo Korn for his
statistical assistance.
approach, studies examining memory impairment in other
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