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Keywords:

  • Boston Qualitative Scoring system;
  • organizational strategy;
  • Rey–Osterrieth Complex Figure;
  • schizophrenia;
  • visual memory

Abstract

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. REFERENCES

Aims:  The aim of the present study was to examine how copy organization mediated immediate recall among patients with schizophrenia using the Rey–Osterrieth Complex Figure Test (ROCF).

Methods:  The Boston Qualitative Scoring System (BQSS) was applied for qualitative and quantitative analyses of ROCF performances. Subjects included 20 patients with schizophrenia and 20 age- and gender-matched healthy controls.

Results:  During the copy condition, the schizophrenia group and the control group differed in fragmentation; during the immediate recall condition, the two groups differed in configural presence and planning; and during the delayed recall condition, they differed in several qualitative measurements, including configural presence, cluster presence/placement, detail presence/placement, fragmentation, planning, and neatness. The two groups also differed in several quantitative measurements, including immediate presence and accuracy, immediate retention, delayed retention, and organization. Although organizational strategies used during the copy condition mediated the difference between the two groups during the immediate recall condition, group also had a significant direct effect on immediate recall.

Conclusion:  Schizophrenia patients are deficient in visual memory, and a piecemeal approach to the figure and organizational deficit seem to be related to the visual memory deficit. But schizophrenia patients also appeared to have some memory problems, including retention and/or retrieval deficits.

STUDIES HAVE SHOWN that deficits in a broad range of cognitive functions such as attention, executive function, learning, and memory are core features of schizophrenia, but a consensus has not been reached about whether patients with schizophrenia have generalized cognitive deficits1 or selective deficits in specific cognitive functions including memory, learning, and executive functions.2

Researchers have intensively studied verbal memory in schizophrenia patients, and have produced substantial evidence that these patients have a verbal memory deficit.2,3 In contrast, few studies have examined visual memory in schizophrenia patients.4 These studies have consistently reported that patients with schizophrenia are deficient in visual memory,5,6 but the mechanisms underlying this deficit are poorly understood.4,5 Some researchers have reported that non-verbal memory deficit is associated with problems related to consolidation,7 and others have suggested that visual memory impairment is associated with a deficit related to organization and encoding,6 or with a combined deficit in organization and retention.4 Glahn et al. recently examined non-verbal memory impairment in patients with schizophrenia and found that they performed worse than patients with bipolar disorder or normal controls, but observed differential impairment only when organizational demands were significant.5 These results indicate that non-verbal memory impairment in schizophrenia patients is related to organizational and encoding deficits, necessitating a direct examination of the organizational processes used in visual memory among these patients.

The Rey–Osterrieth Complex Figure Test (ROCF) is widely used to evaluate visual memory and visuospatial construction abilities.8 The ROCF task involves copying a geometric figure and then reproducing it from memory, either immediately or after a delay. Subjects can reproduce the figure in many ways, and the ROCF involves several visual components that can be perceived as large-scale organizational features (gestalts) or small details. Because of these complexities of the figure, ROCF testing can yield important, qualitative information about the subject's strategies and organizational approach.9 Many studies have reported that the ROCF is useful to assess executive functions, including organization and planning; for example, it has been used to evaluate organizational strategy in patients with obsessive–compulsive disorder.10,11

Few studies have applied the ROCF to investigate how organizational strategy affects recall in schizophrenia patients. Seidman et al. used it to compare visual memory and organizational function among patients with chronic schizophrenia and chronic bipolar disorder, and healthy controls,4 and found that patients with schizophrenia used a more detail-oriented style during copy and recall and had significantly worse visual memory than patients with bipolar disorder or healthy controls. These results indicate that patients with schizophrenia have a visual memory disorder characterized by both organizational processing deficits and retention difficulties. Kalinowski et al. also administered the ROCF to patients with schizophrenia and healthy controls and found that patients with schizophrenia were worse at organization and recall, which could result from their more detail-oriented style.12

Previous studies of how organizational strategy affects recall in patients with schizophrenia using the ROCF have generally applied quantitative methods. For example, Seidman et al. used a scoring system developed by Osterrieth to measure organization; it assigns a score from 1 to 6 depending on the subject's strategy (a low score indicates a gestalt approach and a high score indicates a disorganized approach).4 Researchers have developed several other quantitative methods to score the ROCF.13,14 Although many of these methods have stressed the importance of executive functioning on ROCF performance, most have not provided a comprehensive system for evaluating executive functions that affect ROCF performance.8 Only one commercially available qualitative scoring system has been developed to assess executive functioning in adults: the Boston Qualitative Scoring System (BQSS) developed by Stern et al.15 The BQSS provides comprehensive sets of qualitative ratings in addition to quantitative summary scores. The BQSS for the ROCF also includes executive function variables that are composed of five scores: planning, fragmentation, neatness, perseverance, and organization. BQSS executive function variables are significantly associated with traditional executive measures, including perseverative errors on the Wisconsin Card-Sorting Test and the total number of responses on the Controlled Oral Word Association Test.8

We investigated the characteristics of visual memory deficit in patients with schizophrenia. Specifically, we used the BQSS for the ROCF to determine whether visual memory deficits were mediated by poor organizational strategies used by these patients while copying the figure, with the goal of clarifying the mechanisms that underlie visual memory deficit in these patients.

METHODS

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. REFERENCES

Participants

Subjects included 20 patients with schizophrenia living at the Institute for Social Return and 20 age- and gender-matched healthy controls. All patients satisfied the DSM-IV16 criteria for schizophrenia based on the Structured Clinical Interview for DSM-IV (SCID-IV).17 The severity of schizophrenia symptoms was evaluated using the Positive and Negative Syndrome Scale (PANSS).18 Of the 20 patients, eight had paranoid schizophrenia, 10 had undifferentiated schizophrenia, and two had residual schizophrenia. All patients were being treated with neuroleptic medication at the time of testing; 12 were taking typical antipsychotics (chlorpromazine equivalent dose: 529.16 ± 423.17 mg)19 and eight were taking atypical antipsychotics (risperidone, n = 4; olanzapine, n = 1; clozapine, n = 3). Among 20 patients, eight were taking anticholinergic medication (benztropine, n = 3, mean dose, 1.44 ± 1.01 mg/day; procyclidine, n = 5, mean dose, 7.00 ± 2.74 mg/day). Exclusion criteria for patients included any history of head injury, neurological disorders, substance abuse or any other psychiatric disorders.

The healthy controls were recruited through the Internet. We used the Structured Clinical Interview for DSM-IV, Non-Patient (SCID-NP)17 to ensure that none of the 20 controls had any history of psychiatric, medical, or neurological disorders, or drug or alcohol abuse. All participants were right-handed. All participants provided written informed consent after receiving a complete description of the study, and this study was approved by the Sungshin Women's University Institutional Bioethics Review Board.

Table 1 summarizes the demographic characteristics of the schizophrenia group and the control group. The groups differed significantly in the level of education (t = 4.34, d.f. = 38, P < 0.001), IQ (t = 6.54, d.f. = 38, P < 0.001), and depression (t = −2.44, d.f. = 38, P < 0.05).

Table 1.  Subject characteristics
VariableSchizophrenia (n = 20)Control (n = 20)t (38)
MeanSDMeanSD
  • *

    P < 0.05,

  • ***

    P < 0.001.

  • BDI, Beck Depression Inventory; PANSS, Positive and Negative syndrome Scale.

Gender
 Male1212 
 Female88 
Age (years)41.96.8439.357.69−1.11
Education (years)11.952.7015.352.234.34***
IQ99.559.69118.458.556.54***
BDI score15.0513.866.855.84−2.44*
Age of onset (years)26.947.31   
Duration of illness (years)14.447.39   
PANSS score
 Positive symptom15.832.23   
 Negative symptom16.502.59   
 General pathology30.175.04   

Instruments

We administered the ROCF to evaluate visual memory using three test conditions: a copy condition, an immediate recall condition (3 min after the copy condition), and a delayed recall condition (30 min after the copy condition).20

We used the BQSS15 to qualitatively analyze the ROCF data; this method scores ROCF data by dividing the figure into three sets of elements that are hierarchically arranged in terms of structural importance: configural elements, clusters, and details. These elements are then scored according to presence, accuracy, placement, and fragmentation. Configural elements are evaluated first, followed by clusters, and finally by details. All elements are initially scored for presence. If an element is present, then judgments are made about the element's accuracy, placement, and fragmentation, depending on which element of the figure is being evaluated. In addition to 17 specific qualitative scores for each condition, the method yields six summary scale scores: copy presence and accuracy, immediate presence and accuracy, delayed presence and accuracy, immediate retention, delayed retention, and organization. Each summary score is derived from combinations of qualitative scale scores and provides a more quantitative evaluation of each participant's overall ROCF performance. Interrater agreement on the performance of five randomly selected participants was relatively high; the kappa value of interrater agreement was 0.86 (P < 0.001).

We administered the Beck Depression Inventory (BDI)21 and the Korean version of the Wechsler Adult Intelligence Scale (K-WAIS)22 to evaluate the severity of depression and IQ, respectively.

Statistical analysis

We conducted a multivariate analysis of variance to investigate group differences in ROCF performances using covariates of IQ, level of education, and BDI score, and we used hierarchical multiple regression to examine the mediating effect of organizational strategy on visual memory as measured by the ROCF.

RESULTS

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. REFERENCES

ROCF qualitative scales

Table 2 lists the means and standard deviations of 17 qualitative scores on ROCF copy, immediate recall, and delayed recall conditions for each group. In the copy condition, the schizophrenia group and the control group differed only in fragmentation (F1,35 = 6.29, P < 0.05); scores were lower among patients with schizophrenia.

Table 2.  Qualitative score in ROCF copy, immediate recall, and delayed recall conditions
VariableCopy conditionImmediate recall conditionDelayed recall condition
Schizophrenia (n = 20)Control (n = 20)Schizophrenia (n = 20)Control (n = 20)Schizophrenia (n = 20)Control (n = 20)
MeanSDMeanSDMeanSDMeanSDMeanSDMeanSD
  • *

    P < 0.05,

  • **

    P < 0.01,

  • ***

    P < 0.001.

  • ROCF, Rey–Osterrieth Complex Figure Test.

Configural presence3.950.224.000.002.65*0.883.750.442.75***0.853.850.37
Configural accuracy2.150.812.150.671.701.302.450.762.000.862.300.73
Cluster presence4.000.003.950.221.650.592.500.691.90**0.552.500.67
Cluster accuracy2.450.893.250.911.301.302.200.891.351.041.650.88
Cluster placement3.100.723.450.512.251.402.850.751.90**1.202.750.79
Detail presence3.400.683.700.571.100.301.450.600.95*0.511.450.60
Detail placement3.900.313.700.922.701.753.101.212.05**1.703.351.04
Fragmentation2.95*0.763.850.373.300.923.800.413.35*0.933.750.44
Planning2.200.953.200.831.95*1.103.100.642.05***1.053.250.72
Neatness2.650.753.050.392.550.692.950.512.55*0.832.900.31
Vertical expansion3.800.703.800.523.800.893.850.373.800.893.750.44
Horizontal expansion3.650.753.600.753.551.053.251.203.301.342.951.39
Reduction3.850.674.000.003.800.523.950.223.800.524.000.00
Rotation3.650.493.700.473.800.413.850.373.950.223.750.44
Perseveration3.750.443.950.223.400.883.000.923.001.033.000.92
Confabulation3.950.224.000.003.301.133.900.313.400.883.800.41

In the immediate recall condition, the schizophrenia group and the control group differed in scores for configural presence (F1,35 = 5.95, P < 0.05), and planning (F1,35 = 3.59, P < 0.05); both scores were lower among patients with schizophrenia.

In the delayed recall condition, significant differences appeared between the schizophrenia group and the healthy control group for several qualitative variables: configural presence (F1,35 = 23.04, P < 0.001), cluster presence (F1,35 = 7.68, P < 0.01), cluster placement (F1,35 = 8.16, P < 0.01), detail presence (F1,35 = 6.76, P < 0.05), detail placement (F1,35 = 8.96, P < 0.01), fragmentation (F1,35 = 4.06, P < 0.05), planning (F1,35 = 17.16, P < 0.001), and neatness (F1,35 = 4.50, P < 0.05). Patients with schizophrenia scored lower than healthy controls on all these qualitative scales, indicating impaired ability to recall the figure's overall appearance and details.

ROCF quantitative scales

Table 3 lists the means and standard deviations of quantitative ROCF summary scores between the schizophrenia group and the control group. Patients with schizophrenia scored lower than healthy controls on immediate presence and accuracy (F1,35 = 4.70, P < 0.05), immediate retention (F1,35 = 8.10, P < 0.05), delayed retention (F1,35 = 4.19, P < 0.05), and organization (F1,35 = 5.84, P < 0.05), suggesting impaired ability in the immediate and delayed recall of a complex figure and poor organizational strategies.

Table 3.  ROCF summary score
VariableSchizophrenia (n = 20)Control (n = 20)F
MeanSDMeanSD
  • *

    P < 0.05.

  • ROCF, Rey–Osterrieth Complex Figure Test.

Copy presence and accuracy15.901.9217.051.761.52
Immediate presence and accuracy8.402.5812.352.164.70*
Delayed presence and accuracy8.902.1511.752.150.37
Immediate retention47.3814.9627.4710.358.10*
Delayed retention11.8033.768.8513.624.19*
Organization5.151.577.050.945.84*

Mediating effect of organizational strategy on visual memory

We tested direct and indirect models of the group effects to investigate whether the visual memory deficit among patients with schizophrenia was mediated by poor organizational strategies during copying. These models have been described previously by Savage et al.23 First, we used a composite score of immediate presence and accuracy and immediate retention of summary scores as the dependent variable and the copy organization score as the mediating variable.

Baron and Kenny proposed that for all linkages to be supported in a mediated model, significant associations must appear between the independent variable (group), the dependent variable (composite score), and the mediator (copy organization score).24 We found significant correlations between group and organization scores (r = −0.60, P < 0.001), between group and composite scores (r = −0.63, P < 0.001), and between composite score and organization score (r = 0.58, P < 0.001).

Figure 1 presents a path model representing direct and indirect effects based on standardized coefficients (β) and significance levels. In the direct model, group differences in ROCF immediate recall are expressed directly as a significant regression coefficient between group and immediate recall (β = −0.63, P < 0.001). In the mediated model, the group effect on immediate recall is expressed indirectly based on the influence of copy organizational strategy. Organizational strategy appeared to mediate the difference between the two groups under the ROCF immediate recall condition (β = 0.31, P < 0.05), but group also had a significant direct effect on ROCF immediate recall (β = −0.44, P < 0.01).

image

Figure 1. Two path models showing group differences in immediate recall on the Rey–Osterrieth Complex Figure Test (ROCF). Organizational strategy appeared to mediate the difference between the two groups under the ROCF immediate recall condition (β = 0.31, P < 0.05), but group also had a significant direct effect on ROCF immediate recall (β = −0.44, P < 0.01).

Download figure to PowerPoint

Relationship between ROCF quantitative scales and the duration of illness

We found no significant associations between quantitative BQSS scores and the duration of illness in the schizophrenia group. We also found no significant correlations between quantitative BQSS scores and schizophrenia symptoms as measured by PANSS.

DISCUSSION

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. REFERENCES

We investigated whether the visual memory deficit in patients with schizophrenia is related to organizational deficit during the copying of a complex figure using the BQSS to qualitatively analyze ROCF performance.

Patients with schizophrenia performed worse than healthy controls on ROCF fragmentation scores under the copy condition. Fragmentation scores represent how well respondents integrate information; a low fragmentation score indicates a piecemeal approach to the figure, characterized by disjointed and poorly integrated elements.25 Therefore, the present results indicate that patients with schizophrenia used a piecemeal approach while copying the figure and had difficulty processing the gestalt of a complex visual stimulus. This finding supports previous studies, which have reported that patients with schizophrenia use a detail-oriented style of information processing. Several researchers have reported that patients with schizophrenia are impaired in processing global features, but not the local features in a local–global paradigm in which hierarchical visual stimuli composed of small local forms are arranged into a large global form. They suggested that this detail-oriented type of processing results in an overemphasis on non-critical features and a depletion of available attention resources before the subject can process the critical features or interpret wholes as meaningful gestalts.26,27 Therefore, the piecemeal approach to the figure used by patients with schizophrenia appears to indicate an inefficient organizational strategy, resulting in an inability to recall the figure.

Patients with schizophrenia scored lower than healthy controls on configural presence in the immediate recall condition, which measures the ability to recall the figure's elements. Low configural presence scores indicate significant difficulty in recalling complex visual information.25 Therefore, the low scores among patients with schizophrenia indicate that these individuals have significant difficulties in the immediate recall of complex visual stimuli, and also indicate that they have a deficit in visual memory. These results support the findings of previous studies, which reported that patients with schizophrenia were impaired in immediate recall.6

Patients with schizophrenia also scored lower than healthy controls on planning. Planning scores are based on the order in which the elements are drawn, the overall placement of the figure on the page, the placement of the elements within the figure, and the integrity of the overall structure of the figure.25 Poor planning can be considered as an inability to identify and organize the steps and actions necessary to complete an intention or reach a goal.20 Therefore, the low planning scores among patients with schizophrenia indicate that these individuals did not approach the task in an organized way, but rather drew the figure in a piecemeal, fractionated manner. This result, together with the low fragmentation scores in the copy condition, confirms that patients with schizophrenia have difficulties in processing the gestalt of a Rey–Osterrieth figure.

Under delayed recall condition, patients with schizophrenia scored lower than healthy controls on several qualitative scales: configural presence, cluster presence, cluster placement, detail presence, detail placement, fragmentation, planning, and neatness. The hierarchical organization of the ROCF elements used in the BQSS is designed to tap into differential processing of the contextual and featural characteristics of a stimulus. Configural elements represent a figure's contextual aspects, whereas cluster and detail elements represent its featural aspects.25 The low scores on cluster presence/placement and detail presence/placement, in combination with low scores on configural presence, suggest that patients with schizophrenia have difficulties not only with delayed recall of the figure's contextual aspects, but also with delayed recall of its featural aspects. In addition, these results indicate that these patients have difficulties integrating contextual and featural information. Low scores on the BQSS neatness scale indicate messy reproduction of the figure, which might be related to an impulsive and speedy approach and a lack of motivation, both of which are characteristics of schizophrenia.28

Patients with schizophrenia scored lower than healthy controls on summary scales including immediate presence and accuracy, immediate retention, delayed retention, and organization. Immediate presence and accuracy scales generally represent the amount and accuracy of information immediately recalled, whereas the immediate retention scale represents the percentage of information lost or gained between the copy condition and the immediate recall condition.25 Patients with schizophrenia lost more information than healthy controls from the copy condition to the immediate recall condition and from the immediate recall condition to the delayed recall condition, indicating that patients with schizophrenia are impaired in visual memory, supporting the results of previous studies.6 Patients with schizophrenia also scored lower than healthy controls on organization; the organization summary score is a sum of fragmentation and planning scores under the copy condition. Low scores indicate impaired executive function and/or impaired ability to synthesize and integrate visual information.25

The results of the BQSS qualitative and quantitative scales indicate that patients with schizophrenia have a visual memory deficit. These patients displayed characteristics such as a piecemeal and disorganized approach to the figure and had difficulty integrating the figure's contextual and featural aspects. In other words, patients with schizophrenia exhibited an organizational deficit. Previous studies have reported that non-verbal memory impairments mediated by organizational deficits are caused by primary executive dysfunction.10,29 Therefore, the organizational deficit illustrated by the present study may reflect an executive dysfunction among patients with schizophrenia.1,2 Furthermore the organizational deficit might indicate the prefrontal dysfunction frequently observed in these patients.30,31

We also examined whether organizational deficit mediates visual memory impairment among patients with schizophrenia. In other words, we scrutinized whether the poor visual memory exhibited by patients with schizophrenia on the ROCF was caused by poor organizational strategy during copying, rather than a true memory dysfunction. While patients with schizophrenia had poor immediate recall, statistically mediated by poor organizational skills, they also had problems with visual memory. These results support previous findings, which indicated that visual memory deficits in patients with schizophrenia are characterized by both organizational processing impairments and retention difficulties4 or problems during consolidation.7 We found that patients with schizophrenia lost more information than controls between the immediate recall condition and the delayed recall condition, indicating possible retention and/or retrieval deficits.

In conclusion, patients with schizophrenia appear to have a visual memory deficit. Their organizational deficits, including a piecemeal approach to the figure and poor planning ability, seem to be related to this visual memory deficit. But they also appear to have other memory deficits such as retention and/or retrieval impairment.

The present results may be limited by several factors. All patients with schizophrenia were taking medication including anticholinergic drugs at the time of testing, which could have affected their ROCF performances. Therefore, future studies should examine the potential effects of neuroleptics on ROCF performance. Furthermore, the tests for memory were not comprehensive, and we did not include tests evaluating executive functions. Future studies should use more comprehensive measures of neuropsychological functions, including executive functions and frontal lobe functions to clarify the characteristics and mechanisms of visual memory deficit in patients with schizophrenia. In addition, because ROCF performance declines with age,32 further studies should also include young patients.

ACKNOWLEDGMENTS

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. REFERENCES

This work was supported by the Korea Science and Engineering Foundation (KOSEF) grant funded by the Korea government (MOST), M10644000002-06N4400-00210.

REFERENCES

  1. Top of page
  2. Abstract
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. REFERENCES
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