Abstract

Visuospatial stimuli are normally perceived from the global structure to local details. A right-brain stroke often disrupts this perceptual organization, resulting in piecemeal encoding and thus poor visuospatial memory. Using a randomized controlled design, the present study examined whether promoting the global-to-local encoding improves retrieval accuracy in right-brain-damaged stroke survivors with visuospatial memory deficits. Eleven participants received a single session of the Global Processing Training (global-to-local encoding) or the Rote Repetition Training (no encoding strategy) to learn the Rey–Osterrieth Complex Figure. The result demonstrated that the Global Processing Training significantly improved visuospatial memory deficits after a right-brain stroke. On the other hand, rote practice without a step-by-step guidance limited the degree of memory improvement. The treatment effect was observed both immediately after the training procedure and 24 h post-training. Overall, the present findings are consistent with the long-standing principle in cognitive rehabilitation that an effective treatment is based on specific training aimed at improving specific neurocognitive deficits. Importantly, visuospatial memory deficits after a right-brain stroke may improve with treatments that promote global processing at encoding.

Introduction

Between 20% and 50% of persons who survive a stroke manifest learning and memory difficulties (Nys et al., 2005; Rasquin, Verhey, Lousberg, Winkens, & Lodder, 2002; Snaphaan & de Leeuw, 2007; Stewart, Sunderland, & Sluman, 1996). For right-brain-damaged stroke survivors who have memory deficits, their memory difficulty is often related to the suboptimal or abnormal processing of visuospatial information (Campos, Barroso, & Menezes, 2010; Nys et al., 2005). Right-brain lesions may disorient spatial attention, narrow the attention aperture, and disrupt perceptual organization (Barrett, Beversdorf, Crucian, & Heilman, 1998; Brain, 1941; Chen & Goedert, 2012; Irving-Bell, Small, & Cowey, 1999; Milner & Harvey, 1995). Consequently, stimuli may not be encoded efficiently or accurately for further processes such as storage and retrieval—resulting in visuospatial memory deficits (Akshoomoff, Feroleto, Doyle, & Stiles, 2002; Binder, 1982; Delis, Robertson, & Efron, 1986; Lange, Waked, Kirshblum, & DeLuca, 2000; Warrington, James, & Kinsbourne, 1966).

For people who do not have visuospatial disorders, it is typical and effortless to demonstrate the forest-before-trees phenomenon when visually perceiving and encoding an object or a scene that contains hierarchical layers of spatial information. The global precedence theory states that normal visuospatial perception is implicitly accomplished by processing global configural information before processing local detailed information, suggesting that the most efficient approach to encode perceived stimuli is “global processing”—from global to local, from coarse to fine, and from configural to detail (Greene & Oliva, 2009; Kimchi, 1992; Modigliani, Loverock, & Kirson, 1998; Navon, 1977; Newman & Krikorian, 2001; Poirel, Pineau, & Mellet, 2008). The right brain plays the dominant role supporting global processing in visuospatial perception. The critical regions in the right hemisphere may involve the inferior frontal (Chen, Marshall, Weidner, & Fink, 2009), temporo-parietal (Robertson, Lamb, & Knight, 1988), posterior temporal (Lamb, Robertson, & Knight, 1990), or temporo-occipital regions (Fink et al., 1996; Martinez et al., 1997; Peyrin et al., 2005). These various results may be due to differences in behavioral tasks or study methods; alternatively, some or all the critical brain locations reported previously may be part of a network responsible for global processing. Also, many studies suggest that dysfunction or injury in any part of the right cerebral cortical or subcortical structures may lead to impairments in global processing and thus visuospatial memory (Barrett et al., 1998; Chen & Goedert, 2012; Delis et al., 1986; Eslinger, Grattan, & Geder, 1995; Frank & Landeira-Fernandez, 2008; Goodarzi, Wykes, & Hemsley, 2000; Lange et al., 2000; Postma, Kessels, & van Asselen, 2008; Robertson & Lamb, 1991; Spiers et al., 2001). Therefore, after a right-brain stroke, it is possible that the survivor is compromised in visuospatial memory.

Visuospatial memory impairments occur in ∼25% of right-brain-damaged stroke survivors without spatial neglect or dementia (Stewart et al., 1996, present study, see Methods section). Visuospatial memory deficits are usually identified by asking individuals to reproduce an abstract complex figure from memory, avoiding confounds associated with language processing, for example, verbal mediation, verbal response, and vocabulary (Strauss, Sherman, & Spreen, 2006). Fig. 1 illustrates two right-brain-damaged stroke survivors' graphic production of the Rey–Osterrieth Complex Figure (ROCF; Osterrieth, 1944; Rey, 1941). In a complex figure test, examinees are required to produce a graphic copy of a hierarchical stimulus and reproduce it from memory immediately and/or 20–30 min after the copy trial (Strauss et al., 2006). People who copy the figure in a piecemeal fashion, not following the global-to-local configural organization, often reproduce the drawing with fewer correct features than those whose copies are drawn in a global-to-local orderly sequence (Deckersbach et al., 2000; Lange et al., 2000; Savage et al., 1999; Shorr, Delis, & Massman, 1992). Therefore, to improve recall accuracy, promoting global processing at encoding may be beneficial.

Fig. 1.

(a) ROCF, (b) drawings produced by two right-brain-damaged stroke survivors when copying the ROCF, and (c) drawings reproduced immediately from memory after the copy trial.

Fig. 1.

(a) ROCF, (b) drawings produced by two right-brain-damaged stroke survivors when copying the ROCF, and (c) drawings reproduced immediately from memory after the copy trial.

Eslinger and colleagues (1995) investigated whether providing an encoding strategy that promotes global processing would improve visuospatial memory in persons with frontal lesions. Instead of producing a copy of a complex figure at once, the participants followed 17 steps from global configuration to local details to produce a copy of the ROCF or the Taylor Complex Figure. Eslinger and colleagues (1995) found that the global-to-local encoding strategy significantly increased recall accuracy. Independently, Diamond, DeLuca, and Kelley (1997) reported that a training procedure, which also promoted global processing, was found to be beneficial for amnesic patients after surgery treating ruptured aneurysms of the anterior communicating artery. In Diamond and colleagues' training procedure, the ROCF was decomposed into five subunits, also from global configuration to local details. The amnesic participants were sequentially exposed to the five-step global-to-local sequence to learn the figure, and this exposure was repeated five times or until the participants' recall performance reached the criterion based on healthy controls. Half of the amnesic participants responded well to the training procedure and their visuospatial memory improved significantly (Diamond et al., 1997).

Since memory deficits after right-brain damage may result from the deficiency of global processing (Lange et al., 2000; Robertson & Lamb, 1991), it is of theoretical and clinical importance to understand whether promoting global processing at encoding improves visuospatial memory deficits after a right-brain stroke. Visuospatial training focused on the stage of perceptual encoding is a well-established methodology in cognitive rehabilitation to regain related cognitive functions and thus to improve daily activities (Carter, Howard, & Oneil, 1983; Edmans, Webster, & Lincoln, 2000; Lincoln, Whiting, Cockburn, & Bhavnani, 1985; Neistadt, 1992; Taylor, Schaeffer, Blumenthal, & Grisell, 1971; Weinberg, Piasetsky, Diller, & Gordon, 1982). However, previous studies using visuospatial training specifically for improving memory were not dedicated to persons with right-brain lesions (Diamond et al., 1997; Eslinger et al., 1995). The present study aims to investigate whether right-brain-damaged stroke survivors are able to receive beneficial impact from a global-to-local encoding strategy, regain global processing, and improve their visuospatial memory deficits.

In addition, the study design in previous research did not include a control condition. In Diamond and colleagues’ study (1997), the global-to-local encoding sequence was repeated multiple times. It is possible that visuospatial memory deficits might improve due to learning the figure from global to local, or alternatively, the improvement might result from rote repetition, that is, repeated viewing and drawing the figure without an organized strategy (Bornstein & Dagostino, 1992; Ofen-Noy, Dudai, & Karni, 2003). In the present study, persons with visuospatial memory deficits after a right-brain stroke were randomly assigned to the treatment group, the Global Processing Training (global-to-local encoding), or the control group, the Rote Repetition Training (no encoding strategy). The aim of the study was to examine whether, in comparison to the Rote Repetition Training, the treatment—the Global Processing Training—significantly improved visuospatial memory deficits.

Methods

Participants

Persons with a right-brain stroke were recruited based on referrals from physicians and therapists of two acute inpatient rehabilitation hospitals. Sixty-six consecutive right-brain-damaged stroke survivors (66.1 ± 13.4 years old; 31 women and 35 men) were enrolled over 2 years. As inpatients in rehabilitation facilities, participants continued with their regular physical and occupational therapy (one session of each per day) without interruption. During the same period of time, community-dwelling, right-handed healthy individuals were recruited via solicitation flyers posted in the two hospitals and the investigators' organization. Forty-five healthy individuals (65.0 ± 9.7 years old; 24 women and 21 men) participated in the study to provide the norm of visuospatial memory. There was no statistical difference in the age or sex ratio between post-stroke participants and healthy participants. All the participants provided informed consent approved by the Institutional Review Board of either organization.

In order to continue their study participation, the enrolled stroke survivors had to meet the following inclusion and exclusion criteria. First, based on the medical records and radiology reports, the included participants had to have their first stroke during the past 6 months and had lesions in the right cerebral cortical or subcortical regions without involving the brain stem or any left-brain region; in addition, they had no history of brain tumor, neurological disorder other than stroke, or brain injury followed by loss of consciousness. Second, the included participants were right-handed, as determined by a 17-item handedness questionnaire (Raczkowski, Kalat, & Nebes, 1974), had no difficulty in reading or using writing instruments within the arm-reach distance, and had no impairment in ocular vision indicated by medical records. Therefore, no motor or ocular difficulty accounted for their drawing performances. Third, at the time of the screening, the participants did not suffer from depression (≤10/30; Geriatric Depression Scale, GDS; Yesavage et al., 1983), spatial neglect (<129/146; Behavioral Inattention Test, BIT; Halligan, Cockburn, & Wilson, 1991), or dementia (≥24/30; Mini-Mental State Examination, MMSE; Folstein, Folstein, & McHugh, 1975). Therefore, memory performance in the present study was not affected by depression, spatial neglect, or dementia.

Lastly, the most crucial inclusion criterion for this study was having deficits in visuospatial memory. The Modified Taylor Complex Figure (MTCF) was used for assessing visuospatial memory in the screen/pretraining and next day post-training sessions because of its high compatibility to the ROCF, which was used as the training material (Hubley, 2010; Hubley & Jassal, 2006). The participants had deficits in visuospatial memory, which was determined by immediate recall (IR) accuracy of MTCF (see the test procedure in the next section). The cutoff for visuospatial memory deficits (IR of MTCF ≤ 9/36) was set at 1 SD below the mean of the healthy participants' IR of MTCF (M = 16.1; SD = 7.0), which was normally distributed, as revealed by a joint test of normality in skewness and kurtosis: χ2(2) = 1.66, p = .436.

As illustrated in Fig. 2, 11 stroke survivors met the inclusion/exclusion criteria. Among the excluded participants, 32 were excluded for not having visuospatial memory deficits. Thus, of the 43 right-brain-damaged stroke survivors who were screened with the MTCF test, 25.6% manifested visuospatial memory deficits. The included participants were randomized into the treatment or the control group, and nine of them completed the follow-up visuospatial memory tests next day, 2 weeks, and 4 weeks after the training session. The randomization procedure was performed by a laboratory associate, who was not an examiner, rater, or investigator of the present study. This person blindly drew one of 16 poker cards that contained equal numbers of A's and J's, without knowledge of the association between the card and the training condition. Participants were concealed from the assignment. Two examiners conducted all the sessions from consenting to follow-ups, assessing participants in both the Global Processing Training and the Rote Repetition Training, and administering the training procedure; thus, examiners were not blind to the training condition. Six participants were assigned to the treatment group receiving the Global Processing Training, and five were in the control group receiving the Rote Repetition Training. Table 1 summarizes demographic information and clinical characteristics of the treatment and control groups.

Table 1.

Participant characteristics

 Treatment group (Global Processing Training) Control group (Rote Repetition Training) 
Sex (women/men) 4/2 2/3 
Age (years) 73.8 ± 8.8 74.0 ± 8.4 
Education (years) 14.8 ± 1.6 12.6 ± 4.3 
Days between stroke and the training session 48.0 ± 17.2 35.0 ± 20.2 
GDS (≤10/30)a 4.8 ± 3.5 5.4 ± 4.4 
BIT (≥129/126)a 139.5 ± 5.6 136.8 ± 7.7 
MMSE (≥24/30)a 27.5 ± 2.1 26.6 ± 1.8 
Lesion locationsb of each participant G1: BG, WM R1: F 
G2: F, T, P R2: BG, Th 
G3: BG R3: Th 
G4: P, O R4: BG 
G5: F, T R5: T 
G6: Th, IC  
 Treatment group (Global Processing Training) Control group (Rote Repetition Training) 
Sex (women/men) 4/2 2/3 
Age (years) 73.8 ± 8.8 74.0 ± 8.4 
Education (years) 14.8 ± 1.6 12.6 ± 4.3 
Days between stroke and the training session 48.0 ± 17.2 35.0 ± 20.2 
GDS (≤10/30)a 4.8 ± 3.5 5.4 ± 4.4 
BIT (≥129/126)a 139.5 ± 5.6 136.8 ± 7.7 
MMSE (≥24/30)a 27.5 ± 2.1 26.6 ± 1.8 
Lesion locationsb of each participant G1: BG, WM R1: F 
G2: F, T, P R2: BG, Th 
G3: BG R3: Th 
G4: P, O R4: BG 
G5: F, T R5: T 
G6: Th, IC  

Notes: GDS = Geriatric Depression Scale; BIT = Behavioral Inattention Test; MMSE = Mini-Mental State Examination; G1–6 = participants receiving Global Processing Training; R1–5 = participants receiving Rote Repetition Training; BG = basal ganglia; Th = thalamus; F = frontal cortex; T = temporal cortex; P = parietal cortex; O = occipital cortex; IC = internal capsule; WM = white matter.

aNone of the participants meet the clinical criteria for depression, spatial neglect, or dementia.

bAll the lesions were in the right brain, confirmed with clinically obtained CT or MRI scans.

Fig. 2.

Study flowchart. IRB = Institutional Review Board; NOPP = Notice of Privacy Practices; HIPAA = Health Insurance Portability and Accountability Act; GDS = Geriatric Depression Scale; BIT = Behavioral Inattention Test; MMSE = Mini-Mental Status Exam; MTCF = Modified Taylor Complex Figure; ROCF = Rey–Osterrieth Complex Figure; MCGCF = Medical College of Georgia Complex Figure; IR = immediate recall; IPTR = immediate post-training recall; DR = delayed recall.

Fig. 2.

Study flowchart. IRB = Institutional Review Board; NOPP = Notice of Privacy Practices; HIPAA = Health Insurance Portability and Accountability Act; GDS = Geriatric Depression Scale; BIT = Behavioral Inattention Test; MMSE = Mini-Mental Status Exam; MTCF = Modified Taylor Complex Figure; ROCF = Rey–Osterrieth Complex Figure; MCGCF = Medical College of Georgia Complex Figure; IR = immediate recall; IPTR = immediate post-training recall; DR = delayed recall.

General Procedures of Complex Figure Tests

As illustrated in the study flowchart (Fig. 2), five complex figure tests were employed over the course of the study. The complex figures used at the pretraining/screening, training, next day, 2-week, and 4-week follow-up sessions were the MTCF, the ROCF, the upside-down MTCF, the Medical College of Georgia Complex Figure 1 (MCGCF1), and MCGCF2, respectively. The reason for using different complex figures was to reduce the practice effect and to ensure that either the training procedure (Global Processing Training or Rote Repetition Training) was to improve visuospatial memory in general rather than to facilitate memory for a particular figure. Also in order to reduce the practice effect of viewing and drawing the MTCF during screening/pretraining as well as next day post-training sessions, the figure was placed upside down in the next day post-training assessment. Each complex figure test followed the incidental learning procedure in which the participants were not informed in advance that there would be IR and delayed recall (DR) trials following the copy trial. No participants reported that they might have anticipated a recall trial after the copy trial in the complex figure tests over the course of the study.

During the copy trial, the participants viewed the complex figure printed clearly in black ink (a 5½ × 4 inch image) on an 11 × 8½ inch white paper sheet with the longer edge of the paper parallel to the participant's coronal plane. The copy period was at least 2 min 30 s long to assure the minimal time of visual exposure, and the examiner emphasized the instruction that “please take your time to copy this figure as accurately as possible” (Strauss et al., 2006). Immediately after their copies were completed and removed, participants were asked to reproduce the complex figure from memory (IR). In the pretraining/screening and post-training sessions, upon completion of the IR, participants spent the next 30 min completing a series of non-visuospatial tasks or questionnaires, and then reproduced the complex figure one last time (DR). In the training session, the training procedure was inserted between the IR and the DR (see below).

Training Session

The training session, which lasted ∼90 min, consisted of three phases. In the pretraining phase, the participants produced a copy of the ROCF and immediately reproduced the figure (IR). The training phase started right after IR; in the training phase, the participants received the Global Processing Training or the Rote Repetition Training. Thirty minutes after the training phase was the post-training phase, during which the participants in both training conditions reproduced the ROCF one last time (DR) and performed a recognition test. The details of the training conditions and the recognition test are described in the following paragraphs.

Treatment condition: global processing training

After completing the copy and IR trials, the treatment group was provided with the first of the five ROCF subunits (Fig. 3a). The presentation order of the subunits was from the global structure to the local details. Each subunit, except for the first subunit, was presented in dashed lines with the previous subunits in solid lines for participants to trace dashed lines with a pencil. The verbal instruction accompanying each subunit presentation was “please trace all the dashed lines on the paper.” Upon completing the tracing of a subunit, the examiner immediately replaced it with the subsequent subunit. Once the entire complex figure was traced and easily visible at the presentation of the last subunit, it was replaced with a blank paper sheet, and participants were asked to reproduce the figure, which was Trial 1 of the immediate post-training recall (IPTR). This sequential tracing from global to local repeated five times, generating five IPTRs.

Fig. 3.

Tracing materials used in the training procedure: (a) tracing material for Global Processing Training and (b) tracing material for Rote Repetition Training.

Fig. 3.

Tracing materials used in the training procedure: (a) tracing material for Global Processing Training and (b) tracing material for Rote Repetition Training.

Control condition: Rote Repetition Training

The control group, after copy and IR trials, performed a tracing exercise on the entire ROCF printed with dashed lines (Fig. 3b). Immediately after the tracing completed, an IPTR was required. This rote tracing repeated five times, generating five IPTRs. The control group received the same verbal instruction and produced the same number of drawings as the treatment group.

ROCF Recognition Test

Following the DR trial, the participants of both groups were administered a recognition test on the ROCF. The recognition test consisted of three subtests: subunit recognition (to recognize an ROCF feature out of a pair for five pairs; each pair was presented on an 11 × 8½ inch sheet of paper; Fig. 4a), spatial recognition (to point out a misplaced ROCF feature; each of the four stimuli was presented by itself on an 11 × 8½ inch sheet of paper; Fig. 4b), and whole-figure recognition (to point out one correct figure out of five that were presented on the same sheet of paper; Fig. 4c). Because the number of trials in each subtest was different, recognition was described by the total number of test trials multiplying the sum of the ratio of the number of correct responses over the number of total trials in each subtest, that is, 10 × (i/5 + j/4 + k/1), where i, j, and k are the numbers of correct responses in subunit recognition, spatial recognition, and whole-figure recognition, respectively. The maximum score for recognition was 30.

Fig. 4.

Recognition test on ROCF: (a) subunit recognition; (b) spatial recognition; and (c) whole-figure recognition.

Fig. 4.

Recognition test on ROCF: (a) subunit recognition; (b) spatial recognition; and (c) whole-figure recognition.

Scoring Methods of Complex Figures

Over the course of the study, all participants produced 20 drawings of complex figures: copy, IR, and DR of the MTCF at pretraining; copy, IR, five IPTRs, and DR of the ROCF during the training session; copy, IR, and DR of the upside-down MTCF next day post-training; copy, IR, and DR of the MCGCF1 2 weeks post-training; copy, IR and DR of the MCGCF2 4 weeks post-training. Each drawing was scored for accuracy by two independent raters who followed the L.B. Taylor scoring criteria (Strauss et al., 2006). The two raters were blind to the participant's training condition. For each of the 18 components, a score of 2 was assigned for correct drawing and allocation, 1 for correct drawing placed poorly or for recognizable poor drawing but placed properly, 0.5 for poor drawing with poor placement, and 0 for unrecognizable or missing component. The maximum score for accuracy was 36.

The drawings produced in the copy trial were also scored by the two independent raters for organization in order to quantify the global-to-local sequential configuration at encoding. Using a method inspired by Binder's method (1982), the organization score was obtained with the emphasis on the sequencing of three basic configural elements. The elements included the framing box (the large rectangle of ROCF and MCGCF1 and the large square of MTCF and MCGCF2), the horizontal midline, and the vertical midline, for the reason that all the complex figures used in this study had them in common as the global configural structure. The correct sequencing was that the initial element must be the framing box, immediately followed by one midline after the other. For the ROCF or MTCF, the inserted element between the box and the first produced midline was allowed if it was the diagonals. A score of 2 was assigned to an element for correct sequencing and completeness; a score of 1 for correct sequencing but fragmented drawing; a score of 0.5 for incorrect sequencing but completed drawing; a zero for incorrect sequencing with fragmented drawing or for missing element. The maximum score for organization was 6. The two independent raters yielded an excellent inter-rater reliabilities on accuracy and organization scores (r = .96 and .90, respectively).

Dependent Variables

A training effect was the difference between performance pre- and post-training within a training condition. A treatment effect was the difference in performance post-training between the treatment and the control conditions (i.e., Global Processing Training vs. Rote Repetition Training). The treatment effect was the main interest of the present study and was operationally defined as the following: In the training session, especially in the training and post-training phases, the dependent variables were the accuracy scores of IPTRs, the DR over IPTRs ratio, and the recognition score. They reflected memory performance in the forms of recall, retention, and recognition, respectively. In the post-training follow-up sessions, memory performance was assessed with recall (i.e., the accuracy score at IR) and retention (i.e., the DR-over-IR ratio); in addition, the organization score at copy was the covariate, examining whether the treatment effect was mediated by configural organization at encoding.

Analyses

All the analyses were performed using with Stata/IC version 12.1. Because of the small sample size and the non-normal distribution of the data, a Mann–Whitney U-test was used in group comparisons without a covariate. For example, Mann–Whitney U-tests were used to compare differences between groups in demographic information, except for the sex ratio which was compared by Fisher's exact test. An α of 0.05 was used.

A multilevel modeling (MLM) with mixed-effects linear regression analysis, also referred to as hierarchical linear modeling and linear mixed modeling, was used when examining the treatment effect over time or while controlling pre-training performance. MLM confers a number of advantages over standard repeated-measures analysis of variance (ANOVA) or linear regression. While standard regression or ANOVA methods assume that the residuals are independent of one another and identical, MLM takes into account the correlated nature of the data when multiple observations are collected from the same participant (Fitzmaurice, Laird, & Ware, 2011; Rabe-Hesketh & Skrondal, 2012; Singer & Willett, 2003). In standard regression and ANOVA, the correlated variability due to between-subject heterogeneity (in baseline performance and recovery trajectory) is not modeled and becomes part of the residual variability. In MLM, however, both the random effects of participants' intercepts and slopes (i.e., change over time) and the fixed-effect predictors of interest can be directly modeled. Thus, MLM is more sensitive for detecting effects when there is variability in the data due to between-subject differences. Furthermore, unlike standard regression and ANOVA, MLM is not sensitive to unbalanced data (i.e., different cell sample sizes) and is tolerant of missing data.

The MLM analyses in the present study used an unstructured covariance structure and a maximum likelihood estimation. A given dependent variable to be examined in an MLM was tested for normality; if it was non-normal, the dependent variable would be square-root transformed. Results were reported with the F distribution with between-within denominator degrees of freedom for testing the fixed effects of categorical predictors and with the χ2 distribution for testing the fixed effects of predictors in continuous measures (West, Welch, & Galecki, 2007). Post-estimation analyses of the linear slopes for the treatment and control groups were performed when the fixed effect of training condition was significant, and each group's improvement trajectory (i.e., change over time) was reported with the coefficient (b), standard error (SE) of the coefficient, and 95% confidence interval (CI). When the treatment effect in a given variable did not reach significance, the effect size, Cohen's d, was calculated. Throughout, an α of 0.05 was used in MLM.

Results

Group Characteristics at Screening

The treatment and control groups who were to receive the Global Processing Training and the Rote Repetition Training, respectively, did not differ statistically in sex ratio (p = .567), age (p = .784), years of education (p = .454), days post-stroke (p = .202), or scores of GDS (p = 1.000), BIT (p = .520), or MMSE (p = .348). Table 1 summarizes the means and standard deviations.

Treatment Effect during the Training Session

Fig. 5 presents the mean accuracy scores of the ROCF drawings from the pre-training phase to the post-training phase. In the pre-training phase, there was no statistical difference between the treatment (Global Processing Training) and the control groups (Rote Repetition Training) in the accuracy of the ROCF copy, indicated by a two-tailed Mann–Whitney U-test (p = .715). There was also no statistical difference in the IR of ROCF (p = .782). This result confirmed that both groups demonstrated equally poor recall prior to training.

Fig. 5.

Accuracy scores over copy and recall trials of ROCF drawings. The error bars denote standard errors. IR = immediate recall; IPTR = immediate post-training recall; DR = delayed recall.

Fig. 5.

Accuracy scores over copy and recall trials of ROCF drawings. The error bars denote standard errors. IR = immediate recall; IPTR = immediate post-training recall; DR = delayed recall.

In the training phase, accuracy scores from IPTR1 to IPTR5 were examined with an MLM. Because accuracy scores were positively skewed and non-normal, the joint test of normality in skewness and kurtosis: χ2(2) = 9.38, p = .009, and the square-root transform improved the distribution's shape, χ2(2) = 1.60, p = .450; therefore, the MLM used the square-root transformed accuracy scores as the dependent variable. Specifically, the MLM included (a) fixed effects of training condition, IPTR trial, and the “training condition × IPTR trial” interaction, and (b) the random effects of participant intercepts and slopes. Overall, the correlation between participants' intercepts and slopes was not significant, r = −.03, SE = .40, 95% CI [−0.67, 0.63], suggesting that individual baseline performance was independent of individual improvement over the course of the training phase. IPTR trial showed a significant effect, χ2 = 30.62, p < .001, and the “training condition × IPTR trial” interaction was also significant, F(1, 9) = 7.37, p = .024. This result indicated that recall accuracy improved more in the group who received the Global Processing Training than those receiving the Rote Repetition Training (Fig. 5). Post-estimation analyses of the linear slopes for the treatment and control groups revealed that the treatment group's linear improvement was significantly different from zero, b = 0.42, SE = 0.08, 95% CI [0.27, 0.57], p < .001, whereas that of the control group was not, b = 0.12, SE = 0.08, 95% CI [−0.40, 1.61], p = .169.

Of clinical importance, four participants showed improvement above the memory deficit cutoff (accuracy > 9) after the Global Processing Training, and so did two participants after the Rote Repetition Training. Among these individuals, the Global Processing Training showed a very large effect relative to the Rote Repetition Training, IPTR5 = 19.13 ± 5.51 (n = 4) versus 12.25 ± 2.83 (n = 2), Cohen's d = 1.69.

In addition, the treatment group showed a significantly higher retention rate after 30 min than the control group: the DR over IPTR5 ratio = 1.00 ± 0.20 versus 0.46 ± 0.34, examined with a two-tailed Mann–Whitney U-test, p = .018. Therefore, it was hypothesized that the treatment group would have better recognition of ROCF than the control group. The result, as summarized in Table 2, showed exactly that the treatment group outperformed the control group in the ROCF recognition test, recognition score = 20.6 ± 5.7 versus 13.2 ± 6.0 (one-tailed p = .041). These results suggest that the Global Processing Training significantly improves visuospatial memory in recall, retention, and recognition.

Table 2.

ROCF recognition test results

 Global Processing Rote Repetition 
Number of correct responses 
 Subunit recognition 4.8 ± 0.5 3.6 ± 1.1 
 Spatial recognition 1.8 ± 1.5 1.6 ± 1.3 
 Whole-figure recognition 0.7 ± 0.5 0.2 ± 0.4 
 Total 7.2 ± 1.5 5.4 ± 1.9 
Recognition score 20.6 ± 5.7 13.2 ± 6.0 
 Global Processing Rote Repetition 
Number of correct responses 
 Subunit recognition 4.8 ± 0.5 3.6 ± 1.1 
 Spatial recognition 1.8 ± 1.5 1.6 ± 1.3 
 Whole-figure recognition 0.7 ± 0.5 0.2 ± 0.4 
 Total 7.2 ± 1.5 5.4 ± 1.9 
Recognition score 20.6 ± 5.7 13.2 ± 6.0 

Treatment Effects at Follow-ups

Table 3 summarizes accuracy and organization scores of complex figure drawings in pretraining and follow-up assessment sessions. Scores of IR accuracy and copy organization are plotted in Fig. 6a and b. To examine whether the treatment group's trajectory of memory improvement was significantly better than that of the control group', an MLM was performed to examine IR accuracy scores from four sessions (i.e., pre-training/screening and follow-ups next day, 2 weeks, and 4 weeks post-training). Because IR accuracy scores were positively skewed and non-normal, the joint test of normality in skewness and kurtosis: χ2(2) = 6.90, p = .032, and the square-root transform improved the distribution's shape, χ2(2) = 0.14, p = .934, the MLM used the square-root transformed IR accuracy score as the dependent variable. The MLM included (a) fixed effects of training condition, session, and the “training condition × session” interaction, and (b) the random effects of participant intercepts and slopes. Overall, the correlation of participants' intercepts and slopes, r = .84, SE = 0.44, was not significant as indicated by the wide range of the 95% CI [−0.93, 0.99], suggesting that individual baseline performance was independent of individual improvement over time. No fixed effect was statistically significant.

Table 3.

Accuracy scores (M ± SD) of complex figure tests pre- and post-training

 Global Processing Rote Repetition 
Pre-training 
 Copy 23.5 ± 6.9 20.3 ± 6.6 
 IR 5.2 ± 3.0 5.2 ± 2.2 
 DR 4.7 ± 3.2 5.1 ± 2.9 
Next day post-training 
 Copy 24.2 ± 5.1 19.8 ± 10.9 
 IR 7.2 ± 5.0 5.4 ± 3.0 
 DR 6.5 ± 4.1 4.9 ± 3.1 
Two weeks post-training 
 Copy 25.8 ± 5.1 22.8 ± 6.9 
 IR 10.4 ± 10.0 7.4 ± 4.8 
 DR 9.7 ± 8.9 6.3 ± 3.3 
Four weeks post-training 
 Copy 21.3 ± 10.0 23.0 ± 7.0 
 IR 9.5 ± 9.2 7.1 ± 2.8 
 DR 9.3 ± 6.8 6.5 ± 3.2 
 Global Processing Rote Repetition 
Pre-training 
 Copy 23.5 ± 6.9 20.3 ± 6.6 
 IR 5.2 ± 3.0 5.2 ± 2.2 
 DR 4.7 ± 3.2 5.1 ± 2.9 
Next day post-training 
 Copy 24.2 ± 5.1 19.8 ± 10.9 
 IR 7.2 ± 5.0 5.4 ± 3.0 
 DR 6.5 ± 4.1 4.9 ± 3.1 
Two weeks post-training 
 Copy 25.8 ± 5.1 22.8 ± 6.9 
 IR 10.4 ± 10.0 7.4 ± 4.8 
 DR 9.7 ± 8.9 6.3 ± 3.3 
Four weeks post-training 
 Copy 21.3 ± 10.0 23.0 ± 7.0 
 IR 9.5 ± 9.2 7.1 ± 2.8 
 DR 9.3 ± 6.8 6.5 ± 3.2 

Notes: IR = immediate recall; DR = delayed recall.

Fig. 6.

(a) IR accuracy scores and (b) copy organization scores at pretraining/screening (preT) and at follow-ups next day (postT1), 2 weeks (postT2), and 4 weeks post-training (postT3).

Fig. 6.

(a) IR accuracy scores and (b) copy organization scores at pretraining/screening (preT) and at follow-ups next day (postT1), 2 weeks (postT2), and 4 weeks post-training (postT3).

Although the effect of the Global Processing Training was not statistically significant over 4 weeks, it was important to determine whether there was a more short-term effect of training condition. To test this possibility, the IR accuracy score was examined session by session from 1 day to 4 weeks post-training. Normality analyses of the IR accuracy scores in each session revealed that the distribution of IR accuracy was not significantly skewed in pre-training (p = .633), 1 day post-training (p = .634), 2 weeks post-training (p = .653), or 4 weeks post-training (p = .553). Therefore, the raw data (rather than square-root transformation) were used in the following MLMs. Separate MLM analyses, controlling for pre-training IR accuracy, showed the significant effect of training condition on IR accuracy 1 day post-training, F(1, 9) = 8.49, p = .017. However, the effect did not reach statistical significance 2 weeks post-training, p = .427, Cohen's d = 0.42 (medium effect size), or 4 weeks post-training, p = .552, Cohen's d = 0.37 (small effect size). To examine retention (the DR-over-IR ratio), another set of MLMs, controlling for pre-training retention, was conducted session by session. The treatment effect was not significant on retention next day post-training, p = .441, Cohen's d = 0.51 (medium effect size), 2 weeks post-training, p = .165, Cohen's d = 0.55 (medium effect size), or 4 weeks post-training, p = .302, Cohen's d = 0.61(medium effect size). In summary, although the treatment effect on retention was significant only immediately after the Global Processing Training, the treatment effect on IR accuracy was significant not only immediately after the training but also 1-day post-training.

To examine whether the Global Processing Training improved the recall because of better configural organization at encoding, training condition and copy organization were included as fixed effects in the following MLM. The rationale of this causal hypothesis is that if copy organization was to significantly estimate recall accuracy, then training condition would not yield a significant effect (as it had showed in the previous model examining the IR accuracy in the follow-up 1 day post-training). The result supported the hypothesis: rather than training condition (p = .826), copy organization had a significant effect, χ2 = 4.15, p = .042, suggesting that the treatment effect of better memory performance observed 1 day post-training was mediated by better configural organization at encoding.

Discussion

Global processing is the intrinsic organizational strategy for efficient learning and accurate memory. Promoting global processing at encoding, via the Global Processing Training, significantly improved visuospatial memory deficits after a right-brain stroke. The treatment effect was confirmed using a randomized controlled study design. Specifically, the beneficial effect of the Global Processing Training was not limited to one type of memory retrieval such that significant treatment effects were found in both recall and recognition at the end of the training session. This suggests that the Global Processing Training effectively facilitates the process of encoding information to a representational storage available to different mechanisms of retrieval. On the other hand, rote repetition without a step-by-step guidance limited the degree of memory improvement. The treatment effect on recall accuracy was observed both immediately after the training procedure and 24 h post-training. With the present sample size, the medium effects found 2 and 4 weeks post-training are promising and encouraging for further studies investigating whether the treatment effect can be sustained for a longer period of time. Overall, the present findings are consistent with the long-standing principle in cognitive rehabilitation that an effective treatment is based on specific training aimed at improving specific neurocognitive deficits.

The treatment effect observed in the present study was a novel and promising finding that differs from previous research. The present study demonstrated that persons with visuospatial memory deficits after a right-brain stroke are able to benefit from a visuospatial training that promotes global processing. What makes this a major finding is that global processing in these individuals may have been impaired because of their right-brain damage. With the regained ability of global processing after the Global Processing Training, their visuospatial memory deficits improved significantly. This finding replicates existing work in using similar training procedures in persons with amnesia after frontal damage (Diamond et al., 1997; Eslinger et al., 1995) but also extends the treatment effect to those with visuospatial disorders after right-brain damage who benefitted from the Global Processing Training in the present study. More importantly, by the nature of the randomized controlled design and of the different complex figures used in different assessments, the finding of significantly improved memory with the Global Processing Training could not be due to rote repetition or mere practice, a finding that could not be concluded from previous studies which did not control for rote repetition or mere practice. Therefore, with confounding factors minimized, the result strongly suggests that the Global Processing Training effectively helps the regaining of efficient encoding via global processing, which consequently improves visuospatial memory deficits after a right-brain stroke.

In one study focused on persons with obsessive-compulsive disorder, Buhlmann and colleagues (2006) found no treatment effect (global-to-local encoding strategy vs. repeated viewing) on memory improvement. The discrepancy between Buhlmann and colleagues' (2006) and the present study may come from differences in the training procedure and clinical population. The training procedure in Buhlmann and colleagues' study contained two training trials, which may not be as effective as five training trials used in the present study where treatment effects were apparent starting at the 4th trial (IPTR4; Fig. 5). In addition, it was not reported whether Buhlmann and colleagues' participants had visuospatial memory deficits at baseline. It is possible that people without memory deficits may receive little benefit from a single session of memory training.

In addition to the major outcome of the treatment effect, the present study also provides insight to the field of rehabilitation research on visuospatial memory deficits. 25% of a right-brain stroke survivors screened in the present study had visuospatial memory deficits. This incidence rate may be an underestimate of the actual prevalence because participants with symptoms related to depression, spatial neglect, or dementia were excluded before getting screened for visuospatial memory. It is suggested that about ≥25% of people, who survive a right-brain stroke, may live with visuospatial memory deficits, which is rather alarming considering the large number of stroke survivors. Translating to everyday activities, visuospatial memory deficits may limit the ability to remember unfamiliar faces and environments, to learn geographical maps, to retrace routes for navigation (Ostrosky-Solis, Jaime, & Ardila, 1998; Spiers et al., 2001), and to drive vehicles (Bliokas, Taylor, Leung, & Deane, 2011; Ott et al., 2008). However, there is close to no rehabilitative method targeting visuospatial memory deficits post-stroke (Cicerone et al., 2011). Much more work is needed for acknowledging memory problems in the visuospatial domain and for seeking effective treatment.

The present study initiated the first step for establishing a theory-driven, evidence-based rehabilitative technique for treating visuospatial memory deficits after a right-brain stroke. Using a randomized controlled study, significant treatment effects were obtained immediately and 24 h after a single session of training, even with a relatively small sample. However, this effect did not seem to carry-over in follow-up assessments. A couple of limitations may account for this. The first and mostly likely is the very small sample size. The fact that effect sizes of follow-up assessments were generally in the moderate range suggests that significant longer-term follow-up findings would be significant with increased sample size. A second potential variable may be the number of training trials provided. Future studies are needed to examine how the number of training trials, or even the influence of additional training sessions, will influence the longer-term follow-up. The fact that the findings were observed with such limitations holds promise for the utilization of the Global Processing Training. In the context of clinical intervention, the Global Processing Training may be incorporated with other approaches to treat visuospatial memory deficits; the training protocol reported here may be used as part of a treatment strategy during cognitive rehabilitation for a purpose more general to global cognition rather than specific to visuospatial- or memory-related functions.

Funding

This work was supported by the Kessler Foundation and the Eunice Kennedy Shriver National Institute of Child Health & Human Development (1R03HD063177 to P.C.).

Conflict of Interest

None declared.

Acknowledgements

The authors thank Kimberly Hreha and Tara Riccardi for assistance with data collection and test scoring; Kelly Goedert and Jeffrey Yangang Zhang for statistical advice; Anna Barrett and Nancy Chiaravalloti for their comments on earlier versions of the manuscript.

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