Cognitive retraining for organizational impairment in obsessive–compulsive disorder

Psychiatry Research 144 (2006) 109 – 116 www.elsevier.com/locate/psychres

Cognitive retraining for organizational impairment in obsessive–compulsive disorder Ulrike Buhlmann a,*, Thilo Deckersbach a, Iris Engelhard b, Laura M. Cook a, Scott L. Rauch a, Norbert Kathmann c, Sabine Wilhelm a, Cary R. Savage d a

d

Department of Psychiatry/OCD Clinic, Massachusetts General Hospital, Harvard Medical School, 185 Cambridge Street, Boston, MA 02114, USA b Department of Clinical Psychology, Utrecht University, Utrecht, The Netherlands c Department of Clinical Psychology, Humboldt University of Berlin, Berlin, Germany Hoglund Brain Imaging Center and Department of Psychiatry and Behavioral Sciences, University of Kansas Medical Center, Kansas City, KS, USA Received 14 March 2005; received in revised form 26 August 2005; accepted 27 October 2005

Abstract Individuals with obsessive–compulsive disorder (OCD) have difficulties in organizing information during encoding associated with subsequent memory impairments. This study was designed to investigate whether impairments in organization in individuals with OCD can be alleviated with cognitive training. Thirty-five OCD subjects and 36 controls copied and recalled the Rey– Osterrieth Complex Figure Test (RCFT) [Osterrieth, P.A., 1944. Le test de copie d’une figure complexe: Contribution a l’e´tude de la perception et de la memoire (The test of copying a complex figure: A contribution to the study of perception and memory). Archive de Psychologie 30, 286-350.] before being randomly assigned to a training or non-training condition. The training condition was designed to improve the ability to organize complex visuospatial information in a meaningful way. The intervention phase was followed by another copy and recall trial of the RCFT. Both OCD and control subjects who underwent training improved more in organization and memory than subjects who did not receive organizational training, providing evidence that the training procedure was effective. OCD subjects improved more in organizational during encoding than control subjects, irrespective of whether or not they had received training. This suggests that organization impairment in OCD affects primarily the ability to spontaneously utilize strategies when faced with complex, ambiguous information but that the ability to implement such strategies when provided with additional trials is preserved. These findings support a distinction in OCD between failure to utilize a strategy and incapacity to implement a strategy. D 2005 Elsevier Ireland Ltd. All rights reserved. Keywords: Obsessive–compulsive disorder; Neuropsychology; Nonverbal memory; Organization; Recall; Rey–Osterrieth Complex Figure; Taylor Complex Figure

1. Introduction * Corresponding author. Tel.: +1 617 726 5374; fax: +1 617 643 3080. E-mail address: [email protected] (U. Buhlmann).

Obsessive–compulsive disorder (OCD) is characterized by recurrent obsessions and compulsions that cause marked distress and/or interfere with daily functioning (American Psychiatric Association, 1994). Des-

0165-1781/$ - see front matter D 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.psychres.2005.10.012

110

U. Buhlmann et al. / Psychiatry Research 144 (2006) 109–116

pite effective pharmacologic and behavioral treatments, the course of OCD is often chronic with symptoms waxing and waning over time (Rasmussen and Eisen, 1990). Neuropsychological studies of OCD have identified abnormalities in a variety of cognitive domains including impairments in selective attention and visuospatial skills (e.g., Otto, 1992; Tallis, 1995; Alarcon et al., 1994), cognitive inhibition (e.g., Enright, 1996), and difficulties in executive functioning, such as goal setting or set-shifting (Christensen et al., 1992; Boone et al., 1991). One of the most consistently reported neuropsychological impairments in OCD is impairment in learning and episodic memory (Savage, 1998; Head et al., 1989), specifically the ability to encode and explicitly recollect information encountered in a previous study episode (e.g., Graf and Schacter, 1985). For an event to be remembered, it must be encoded, stored and consolidated over time, and then retrieved from storage (Kapur et al., 1996). Encoding refers to the processes that convert a perceived event into an enduring cognitive representation. Meaningful organization of information during encoding is known to enhance recollection. For example, verbal learning benefits from grouping items into semantic categories, or imposing a subjective structure on a set of words (Tulving, 1962). Likewise, organizing complex visuo-spatial information into meaningful perceptual units during encoding has been shown to enhance subsequent free recall from memory (Waber and Holmes, 1986; Shorr et al., 1992; Savage et al., 1999, 2000). We have conducted a series of studies (Deckersbach et al., 2000; Mataix-Cols et al., 2003; Savage et al., 1999, 2000) that investigated the characteristics of memory impairment in individuals with OCD using the Rey–Osterrieth Complex Figure Test (Osterrieth, 1944) and the California Verbal Learning Test (CVLT; Delis et al., 1987). We found that OCD patients’ impairment in learning new information was attributable to difficulties in organizing verbal and nonverbal information during encoding, whereas their ability to retain information once learned was preserved. For example, Deckersbach et al. (2000) and Savage et al. (1999, 2000) found that when asked to copy a complex geometric figure, OCD subjects, unlike healthy control subjects, did not organize the figure with respect to meaningful organizational units (e.g., a large rectangle, diagonals) while copying the figure. This accounted for subsequent difficulties redrawing the figure from memory (Deckersbach et al., 2000; Savage et al., 1999, 2000). These findings have recently been replicated and extended by other groups (Shin et al., 2004; Penades et

al., 2005). Similar results have been obtained in OCD using verbal information. For example, when asked to learn a list of shopping items, individuals with OCD have difficulties reorganizing the items into their respective categories (e.g., fruit, spices and herbs). This mediated subsequent difficulties recalling the words after a 20-min delay (Deckersbach et al., 2000; Savage et al., 2000). The purpose of the present study was to determine whether impairment in organizational abilities in OCD can be remediated by a specific training procedure that aims to teach effective organizational strategies. Specifically, we investigated the effect of brief organizational training on strategy use and memory in individuals with OCD and matched healthy control subjects. 2. Methods 2.1. Subjects Study subjects were 35 patients with DSM-IV OCD (17 females) and 36 healthy control subjects (22 females). Diagnostic status of patients and healthy control subjects was determined using the Structured Clinical Interview for DSM-IV-Inpatient Version (SCID-I/P; First et al., 1995). All subjects were right-handed, as determined by the Edinburgh Handedness Inventory (Oldfield, 1971). For OCD patients, comorbid diagnoses included panic disorder (n = 10), social phobia (n = 5), generalized anxiety disorder (n = 4), posttraumatic stress disorder (n = 3), major depression (n = 2), body dysmorphic disorder (n = 2), bulimia nervosa (n = 1), specific phobia (n = 1), and Tourette’s disorder (n = 1). In all cases, OCD was the primary diagnosis. Twenty-four OCD subjects were taking selective serotonin reuptake inhibitors at the time of the study (including fluoxetine, fluvoxamine, and sertraline). All medicated OCD subjects had been on a stable dose of medication for at least 2 months. At the time of the study, OCD subjects were treated in the OCD Clinic at Massachusetts General Hospital (MGH) but were fully symptomatic for OCD. Control subjects were recruited through advertisements at MGH and at Harvard University. For OCD subjects, the Yale–Brown Obsessive—Compulsive Scale (YBOCS; Goodman et al., 1989) indicated moderate OCD symptoms (M = 20.1, S.D. = 6.3) and mild depressive symptoms as assessed with the Beck Depression Inventory (BDI; Beck and Steer, 1986; M = 13.7, S.D. = 6.6). OCD and control subjects had a mean education of 15.3 years (S.D. = 2.4) and 15.9 years

U. Buhlmann et al. / Psychiatry Research 144 (2006) 109–116

(S.D. = 2.4), respectively. Moreover, the two groups were matched with respect to verbal intelligence, as determined by the Shipley Institute of Living Scale (Zachary, 1991). Twenty OCD subjects and 18 control subjects were randomly assigned to a training condition designed to improve organization. The remaining 15 OCD subjects and 18 control subjects completed a control condition without training. The four groups (OCD Training, OCD Non-training, Control Training, Control Non-training) did not differ with respect to age [ F(3, 70) =0.65, P = 0.59], years of education [ F(3, 70) = 0.45, P = 0.72], gender [v 2(3) = 1.61, P =0.66] and verbal intelligence [ F(3, 70) = 0.99, P = 0.40]. In addition, the OCD Training and Non-training groups did not differ with respect to their YBOCS scores [t(33) = 0.99, P = 0.33; OCD Training: M = 21.0, S.D. = 6.9; OCD Non-training: M = 18.9, S.D. = 5.4], nor with respect to their BDI scores [t(33) = 0.76, P = 0.45; OCD Training: M = 12.9, S.D. = 7.4; OCD Non-training: M = 14.7, S.D. = 5.5]. Thirteen subjects were medicated in the OCD Training group, and 11 subjects were medicated in the OCD Nontraining group [v 2(1) = 0.28, P = 0.60]. Nine subjects had comorbid diagnoses in the OCD Training group, and 10 subjects had comorbid diagnoses in the OCD Non-training group [v 2(1) = 1.62, P = 0.20].

111

and a protractor). The three criteria for each element are independent of each other. Thus, a participant may get credit for one criterion within each component but not the others. The scores range from zero to 72. 2.2.2. RCFT copy organization The organizational approach used during the copy conditions was assessed using a method devised by Savage and colleagues (Savage et al., 1999; Deckersbach et al., 2000). In this approach, the RCFT geometric figure is subdivided into five configural elements: the large rectangle, the diagonal cross, the vertical midline, the horizontal midline, and the vertex of the triangle on the right (see Fig. 1). Subjects receive points for constructing each element as an unfragmented unit. An organizational element is considered to be drawn as an unfragmented unit whenever each side constituting a unit (e.g., each of the four sides of the rectangle) is drawn as a continuous line without interruption, and all sides are drawn one after another. The large rectangle is assigned two points to reflect its importance to the fundamental organization of the figure. All other elements are assigned one point, resulting in a range of scores from 0 to 6. Drawing accuracy is not considered in this score. 2.3. Procedures

2.2. Materials The experiment included two complex geometric figures, namely the Rey–Osterrieth Complex Figure (RCFT; Osterrieth, 1944) and the Taylor Complex Figure (Lezak, 1995; see Fig. 1). As part of the experiment, OCD and control subjects were asked to copy the RCFT figure and redraw it from memory. For copy and recall drawings, subjects were provided with colored pencils that were changed every 10–15 s to obtain a record of the order in which the RCFT figure was drawn. Copy and recall drawings of the RCFT were scored with respect to accuracy (i.e., number of correctly copied or recalled elements). In addition, copy drawings were scored with respect to organization (i.e., to what extent a participant copied the RCFT figure using meaningful organizational units). The Taylor complex figure was used for the training only (i.e., no copy or recall trials). 2.2.1. RCFT copy accuracy Copy accuracy was scored using the Denman (1984) scoring system. This system identifies 24 elements of the RCFT figure that are scored with respect to the following three criteria: correctness of size, location, and relation to other components (measured with a ruler

The experiment took place in a quiet testing office in the OCD Clinic at MGH. Subjects were first asked to copy the Rey–Osterrieth Complex Figure (RCFT; Osterrieth, 1944) using colored pencils (Copy I). Immediately following the copy trial, subjects were asked to redraw the RCFT figure from memory (Recall I). Subsequently, the subjects were presented with the Taylor Complex Figure (Lezak, 1995; see Fig. 1). Depending on the condition (Training vs. Non-training), the subjects received different instructions. In the Training group, subjects received the instructions that complex geometric figures, such as the presented Taylor Figure, can be broken down into simpler, meaningful components. Subjects were told that a good general strategy for copying the Taylor Figure (and other figures) is to draw the basic meaningful units first before filling in the details to finish the figure. Next, subjects were asked to identify each meaningful unit of the Taylor Figure (the large rectangle, the vertical and horizontal lines and the vertex of the triangle) by tracing the outline of each meaningful unit with a pencil. If subjects made an error in identifying/tracing a meaningful unit, they were corrected until they identified/ traced all meaningful units correctly.

112

U. Buhlmann et al. / Psychiatry Research 144 (2006) 109–116 Rey-Osterrieth Complex Figure (RCFT) Organizational Units RCFT

•

• •

RCFT Copy I

RCFT Recall I

No Training

Taylor Complex Figure

Training in Organizational Units Taylor Figure

•

•

•

•

•

•

•

RCFT Copy II

RCFT Recall II

RCFT Delayed Recall

Fig. 1. Procedural Flow Diagram.

In the Non-training condition, subjects were only told to look at the Taylor Figure for 1 min and the organizational features were not pointed out. Following the Training and Non-training condition, all subjects were presented again with the RCFT figure and asked to draw another copy (Copy II). This was followed by an immediate recall of the RCFT figure (Recall II) and a 30-min delayed recall (Delayed Recall). Delayed Recall was only assessed after the Training and Nontraining condition, because the main purpose of the study was to assess whether impairment in organization could be alleviated with cognitive training rather than

memory performance (including delayed recall), per se. Furthermore, previous research has demonstrated that OCD patients show impaired performance on the immediate recall condition of the RCFT without additional loss of information over a delay (e.g., Savage et al., 1999). 2.4. Statistical analyses Data were analyzed using mixed-model analyses of variance (ANOVAs) with group (OCD vs. controls) and training (Training vs. Non-training) as the between-

U. Buhlmann et al. / Psychiatry Research 144 (2006) 109–116

113

jects. Specifically, OCD subjects had lower copy organization scores than control subjects at Copy I [t(69) = 2.04, P b 0.05, d = 0.50] but did not differ from control subjects in organization scores at Copy II [t(69) = 0.49, P = 0.63, d = 0.10; see Table 1].

subjects factors. For the copy organization scores, condition (Copy Organization I vs. Copy Organization II) was the within-subject factor. For the copy accuracy scores, condition (Copy Accuracy I vs. Copy Accuracy II) was the within-subject factor. For the memory scores, condition (Recall I, Recall II, Delayed Recall) was the within-subject factor. Significant main effects and interactions were followed up by paired or unpaired t-tests. Effect sizes were computed using Cohen’s d. Assumptions of normality and homogeneity of variances were met.

3.2. Copy accuracy The mixed model ANOVA yielded a significant group by condition interaction [ F(1, 67) = 7.69, P = 0.02] but no other main effects or interactions. Follow-up t-tests indicated a trend towards lower copy accuracy scores for OCD subjects at Copy I [t(69) = 1.93, P = 0.06, d = 0.45] but no group differences between OCD and control subjects in copy accuracy scores at Copy II [t(69) = 1.00, P = 0.32, d = 0.24].

3. Results Scores for copy organization, copy accuracy and recall for OCD and control subjects for the Training and Non-training groups are shown in Table 1.

3.3. Memory 3.1. Copy organization The mixed model ANOVA yielded a significant main effect for group [ F(1, 67) = 7.79, P b 0.01], a significant main effect for condition [ F(2, 134) = 106.05, P b 0.001], and a significant group by condition interaction [ F(2, 134) = 3.40, P = 0.04], but no other significant main effects or interactions. Post hoc t-tests indicated that OCD subjects, compared with control subjects, recalled significantly fewer elements of the RCFT figure at Recall I [t(69) = 3.43, P = 0.001, d = 0.82]. To investigate improvement in recall from Recall I to Recall II, we computed absolute difference scores between Recall I and Recall II. Although OCD subjects improved their recall performance from Recall I to Recall II more than control subjects did [t(69) = 2.18, P = 0.03, d = 0.50], they continued to recall fewer elements than control subjects at Recall II [t(69) = 2.10, P = 0.04, d = 0.50] and at the Delayed Recall [t(69) = 2.07, P = 0.04, d = 0.42].

The mixed model ANOVA yielded a significant main effect for condition [ F(1, 67) = 75.40, P b 0.001], a training by condition interaction [ F(1, 67) = 4.13, P = 0.04] and a significant group by condition interaction [ F(1, 67) = 5.36, P = 0.03], but no other significant main effects or interactions. Collapsed over OCD and control subjects, follow-up t-tests indicated that there was no difference in copy organization scores between the Training and Non-training groups at Copy I [t(69) = 0.07, P = 0.94, d = 0.06]. At Copy II, following the training procedure, the Training group (collapsed over OCD and control subjects) organized the RCFT figure significantly better than the Non-training group [t(69) = 3.72, P b 0.001, d = 0.98]. In addition, as shown in Table 1, OCD subjects, irrespective of whether they received training, improved their copy organization score from Copy I to Copy II more than control sub-

Table 1 Summary of the RCFT copy organization and accuracy scores Test score

RCFT organization Copy I Copy II RCFT accuracy Copy I Copy II Recall I Recall II Delayed recall

OCD Training (N = 20)

OCD Non-training (N = 15)

Control Training (N = 18)

Control Non-training (N = 18)

M

M

M

M

S.D.

S.D.

S.D.

S.D.

3.0 5.6

1.9 0.6

3.1 4.7

1.9 1.2

3.9 5.5

1.8 0.9

3.6 4.7

1.5 1.1

64.7 68.5 31.0 47.4 46.1

7.3 4.0 13.4 8.8 11.3

65.9 68.0 28.1 45.0 42.8

6.0 3.0 14.8 15.2 17.5

68.3 67.7 41.8 54.8 53.6

3.9 5.4 13.1 12.3 12.5

67.5 66.8 40.3 50.1 49.2

5.9 4.4 15.0 14.7 13.1

114

U. Buhlmann et al. / Psychiatry Research 144 (2006) 109–116

3.4. Psychotropic medication and comorbidity To evaluate the effects of medication and comorbidity on organizational performance during encoding and subsequent free recall, we correlated medication (no = 0, yes = 1) and comorbidity (no = 0, yes = 1) with copy organization and recall scores before and after training/non-training. Medication and comorbidity explained less than 4% of the variance of organizational and recall scores in the OCD group (all rs b F 0.20), suggesting that the pattern of results did not reflect effects of medication and comorbidity. 4. Discussion The purpose of the study was to investigate in individuals with OCD whether impairments in organization of information during encoding can be remediated using a training procedure designed to teach effective organizational skills. Our results indicate that subjects in the training condition (both OCD and control groups) improved more in organizational skills than subjects in the non-training condition. This indicated that the training was an effective means of improving organizational skills. Contrary to our hypothesis, however, we did not find that OCD subjects who underwent training improved more in organizational abilities and memory than OCD subjects who did not receive training. Rather, our results showed that OCD subjects improved more in organizational skills and memory than control subjects irrespective of whether or not they received training. This finding cannot be attributed to group differences in age, education or verbal IQ because the groups were comparable with respect to these variables. In addition, it is unlikely that medication or comorbidity accounted for this pattern of results because including medication and comorbidity as a covariate did not change the pattern of results. Thus, our findings suggest that when exposed to the complex geometric figure, OCD subjects initially have difficulties employing effective organizational strategies; however, they subsequently improve in their use of organizational strategies when given a second opportunity to copy the figure even without a special training procedure. Results from this study are consistent with a recent study by our group that investigated characteristics of verbal memory impairment in patients with OCD and bipolar disorder (Deckersbach et al., 2005). In this study, subjects were presented with lists of words that included items from different categories (e.g., fruit, spices). OCD and bipolar subjects spontaneously

grouped these words into their respective categories to a lower extent than did control subjects. However, when explicitly instructed to use a grouping strategy, subjects with OCD performed as well as control subjects. This was not the case for bipolar subjects, who continued to be less organized than the control group. These findings indicate that OCD subjects have difficulties with the spontaneous initiation of organizational strategies during encoding, whereas their basic ability to implement such strategies appears to be preserved. Results from Deckersbach et al. (2005) also indicate that current findings in nonverbal memory may extend to other domains, including verbal memory. The mechanisms whereby OCD subjects in the current study were able to overcome their deficit in spontaneously generating organizational strategies are still unclear. On the one hand, it is possible that OCD subjects have difficulties recognizing structure. On the other hand, they may be able to recognize the structure of complex figures but underestimate its importance for improving encoding and memory. Our findings suggest that OCD subjects have difficulty initiating effective strategies in ambiguous situations in which the best strategy is not immediately clear. Given little guidance, they initially choose poor strategies that make it difficult to efficiently copy and recall the figure. They appear to be able to learn from this experience and select a more effective and organized strategy. This suggests that organizational impairment in OCD affects primarily the ability to spontaneously utilize strategies when faced with complex, ambiguous information, but that the ability to implement such strategies when provided with additional trials is preserved. These findings support a distinction in OCD between failure to utilize a strategy and incapacity to implement a strategy (Savage, 2002). Neurobiological studies in OCD suggest involvement of fronto-striatal pathology. Specifically, functional neuroimaging studies have consistently provided evidence for altered blood flow and/or metabolism in the striatum as well as in the orbitofrontal cortex, while there is little evidence to suggest involvement of brain structures such as the dorsolateral prefrontal cortex (Benkelfat et al., 1990; Swedo et al., 1992). Functional neuroimaging studies investigating the neural basis of organizational strategies, however, suggest that the implementation of organizational strategies itself relies heavily on working memory processes, such as monitoring, manipulating and updating information in working memory. These in turn rely on intact dorsolateral prefrontal cortex functioning (Savage et al., 2001; Wagner et al., 2001; Fletcher et al., 1998). In the

U. Buhlmann et al. / Psychiatry Research 144 (2006) 109–116

context of learning and memory, the orbitofrontal cortex, on the other hand, appears to mediate the initiation of strategic processing (e.g., Savage et al., 2001; Tremblay and Schultz, 1999; Dias et al., 1997). For example, in healthy individuals, regional cerebral blood flow in the orbitofrontal cortex is positively correlated with the degree to which individuals spontaneously initiate organizational strategies to improve their memory for words (Savage et al., 2001). Our finding of improvement in organizational strategies with repeated trials in OCD subjects in the present study is consistent with neurobiological and neuropsychological studies in OCD indicating fronto-striatal pathology and impairments in the spontaneous use of strategic processing. It is perhaps surprising that OCD subjects continued to be worse than control subjects on the Recall II and Delayed Recall conditions, despite improved organizational scores. It should be noted, however, that the OCD group did, in fact, improve more than the control group on memory scores from Recall I to Recall II and Delayed Recall (OCD = 53% improvement, control = 28% improvement). This disproportionate improvement is unlikely to come from a ceiling effect in the control group, because their average delayed recall score (51.4) did not approach the maximum recall score of 72. The most likely explanation for higher post-training recall scores in the control group is the fact that they had two well-organized encoding trials, whereas the OCD group had only one (the OCD group was organizationally impaired on the first). The current study has several limitations. First, given the somewhat small sample size, our finding warrants replication in a larger sample. However, Cohen’s d effect sizes were in the medium to large range, suggesting that the study was sufficiently powered to detect existing effects. Second, it is possible that OCD subjects showed more improvement, relative to controls, in organization because of ceiling effects among control subjects, who were well organized from the beginning. Third, a better control condition for the Non-training group may have been to ask subjects to copy the Taylor Figure rather than just to look at it, since the Training group traced the organizational features with their fingers. Fourth, the duration of exposure to the Taylor Figure may have varied slightly between the Training and Non-training groups. Specifically, subjects in the Non-training group were asked to look at the figure for 1 min, whereas subjects in the Training group did not have a time restriction when studying its basic meaningful units (mean duration was roughly 1 min). Thus, we cannot rule out the possibility

115

that the duration of studying the Taylor Figure is related to subsequent performance in organization and recall. Results from this study have potentially important clinical implications. This study and others indicate that OCD subjects experience most cognitive difficulties in ambiguous situations that require strategic processing. Thus, cognitive rehabilitation approaches to OCD should focus on teaching patients to recognize potential structure and initiate strategic behavior in ambiguous and complex situations. Furthermore, consistent with previous research (Savage, 1998; Head et al., 1989), OCD subjects had memory difficulties. It is conceivable that such difficulties may affect response to learningbased treatments such as cognitive-behavior therapy for OCD. Future treatment(s) should maximize the ability to encode rich new memories, thereby maximizing the likelihood that they will be retrieved in daily life. Additional studies are also needed to evaluate the impact of cognitive remediation on clinical symptoms in individuals with OCD. References Alarcon, R.D., Libb, J.W., Boll, T.J., 1994. Neuropsychological testing in obsessive–compulsive disorder: a clinical review. Journal of Neuropsychiatry and Clinical Neurosciences 6, 217 – 228. American Psychiatric Association, 1994. Diagnostic and Statistical Manual of Mental Disorders, 4th edition. American Psychiatric Association Press, Washington, DC. Beck, A.T., Steer, R.A., 1986. Beck Depression Inventory Manual. Psychological Cooperation, San Antonio, TX. Benkelfat, C., Nordahl, T.E., Semple, W.E., King, C., Murphy, D.L., Cohen, R.M., 1990. Local cerebral glucose metabolic rates in obsessive–compulsive disorder. Archives of General Psychiatry 47, 840 – 848. Boone, K.B., Ananth, J., Philpott, L., 1991. Neuropsychological characteristics of nondepressed adults with obsessive–compulsive disorder. Neuropsychiatry, Neuropsychology, and Behavioral Neuropsychology 4, 96 – 109. Christensen, K.J., Kim, S.W., Dysken, M.W., Hoover, K.M., 1992. Neuropsychological performance in obsessive–compulsive disorder. Biological Psychiatry 31, 4 – 18. Deckersbach, T., Otto, M.W., Savage, C.R., Baer, L., Jenike, M.A., 2000. The relationship between semantic organization and memory in obsessive–compulsive disorder. Psychotherapy and Psychosomatics 69, 101 – 107. Deckersbach, T., Savage, C.R., Dougherty, D.D., Bohne, A., Loh, R., Nierenberg, A., Sachs, G., Rauch, S.L., 2005. Spontaneous and directed application of verbal learning strategies in bipolar disorder and obsessive–compulsive disorder. Bipolar Disorders 7, 166 – 175. Delis, D.C., Kramer, J.H., Kaplan, E., Ober, B.A., 1987. California Verbal Learning Test Research Edition Manual (Adult Version). The Psychological Cooperation, San Antonio, TX. Denman, S.B., 1984. Denman Neuropsychology Memory Scale. SB Denman, Charleston, SC. Dias, R., Robbins, T.W., Roberts, A.C., 1997. Dissociable forms of inhibitory control within prefrontal cortex with an analog of the

116

U. Buhlmann et al. / Psychiatry Research 144 (2006) 109–116

Wisconsin Card Sort Test: restriction to novel situations and independence from bon-lineQ processing. Journal of Neuroscience 17, 9285 – 9297. Enright, S.J., 1996. Obsessive–compulsive disorder: anxiety disorder or schizotype? In: Rapee, R.M. (Ed.), Current Controversies in the Anxiety Disorders. The Guilford Press, New York, pp. 161 – 190. First, M.B., Spitzer, R.L., Gibbon, M., Williams, J.B.W., 1995. Structured Clinical Interview for DSM-IV Axis I Disorders—Patient Edition. Biometrics Research Department, New York Psychiatric Institute, New York. Fletcher, P.C., Shallice, T., Dolan, R.J., 1998. The functional roles of prefrontal cortex in episodic memory: I. Encoding. Brain 121, 1239 – 1248. Goodman, W.K., Price, L.H., Rasmussen, S.A., Mazure, C., Fleischmann, R.L., Hill, C.L., Heninger, G.R., Charney, D.S., 1989. The Yale–Brown Obsessive–Compulsive Scale (Y–BOCS). Archives of General Psychiatry 46, 1012 – 1018. Graf, P., Schacter, D.L., 1985. Implicit and explicit memory for new associations in normal and amnestic subjects. Journal of Experimental Psychology. Learning, Memory, and Cognition 13, 45 – 53. Head, D., Bolton, D., Hymas, N., 1989. Deficits in cognitive shifting ability in patients with obsessive–compulsive disorder. Biological Psychiatry 25, 929 – 937. Kapur, S., Tulving, E., Cabeza, R., McIntosh, A.R., Houle, S., Craik, F.I.M., 1996. The neural correlates of intentional learning of verbal materials: a PET study in humans. Cognitive Brain Research 4, 243 – 249. Lezak, M.D., 1995. Neuropsychological Assessment. Oxford University Press, New York. Mataix-Cols, D., Alonso, P., Hernandez, R., Deckersbach, T., Savage, C.R., Manuel Menchon, J., Vallejo, J., 2003. Relation of neurological soft signs to nonverbal memory performance in obsessive– compulsive disorder. Journal of Clinical and Experimental Neuropsychology 25, 842 – 851. Oldfield, R.C., 1971. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9, 97 – 113. Osterrieth, P.A., 1944. Le test de copie d’une figure complexe: contribution a l’e´tude de la perception et de la memoire [The test of copying a complex figure: a contribution to the study of perception and memory]. Archive de Psychologie 30, 286 – 350. Otto, M.W., 1992. Normal and abnormal information processing. A neuropsychological perspective on obsessive–compulsive disorder. Pediatrics Clinics of North America 15, 825 – 848. Pen˜ades, R., Catalan, R., Andres, S., Salamero, M., Gasto, C., 2005. Executive function and nonverbal memory in obsessive–compulsive disorder. Psychiatry Research 133, 81 – 90. Rasmussen, S.A., Eisen, J.L., 1990. Epidemiology and clinical features of obsessive–compulsive disorder. In: Jenike, M.A., Baer, L., Minichiello, W.E. (Eds.), Obsessive–Compulsive Disorders.

Theory and Management (2nd ed.). Year Book Medical Publishers, Chicago, pp. 10 – 29. Savage, C.R., 1998. Neuropsychology of obsessive–compulsive disorder. Research findings and treatment implications. In: Jenike, M.A., Baer, L., Minichiello, W.E. (Eds.), Obsessive–Compulsive Disorder: Practical Management and Change (3rd ed.). Year Book Medical, Chicago, pp. 254 – 275. Savage, C.R., 2002. The role of emotion in strategic behavior: insights from psychopathology. In: Feldman Barrett, L., Salovey, P. (Eds.), The Wisdom in Feeling: Psychological Processes in Emotional Intelligence. Guilford Press, New York, pp. 211 – 236. Savage, C.R., Baer, L., Keuthen, N.J., Brown, H.D., Rauch, S.L., Jenike, M.A., 1999. Organizational strategies mediate nonverbal memory impairment in obsessive–compulsive disorder. Biological Psychiatry 45, 905 – 916. Savage, C.R., Deckersbach, T., Wilhelm, S., Rauch, S.L., Baer, L., Reid, T., Jenike, M.A., 2000. Strategic processing and episodic memory impairment in obsessive–compulsive disorder. Neuropsychology 14, 141 – 151. Savage, C.R., Deckersbach, T., Heckers, S., Wagner, A.D., Schacter, D.L., Alpert, N.M., Fischman, A.J., Rauch, S.L., 2001. Prefrontal regions supporting spontaneous and directed application of verbal learning strategies: evidence from PET. Brain 124, 219 – 231. Shin, M.S., Park, S.J., Kim, M.S., Lee, Y.H., Ha, T.H., Kwon, J.S., 2004. Deficits in organizational strategy and visual memory in obsessive–compulsive disorder. Neuropsychology 18, 665 – 672. Shorr, J.S., Delis, D.C., Massman, P., 1992. Memory for the Rey– Osterrieth Figure: perceptual clustering, and storage. Neuropsychology 6, 43 – 50. Swedo, S.E., Pietrini, P., Leonard, H.L., Schapiro, M.B., Rettew, D.C., Goldberger, E.L., Rapoport, S.I., Rapoport, J.L., Grady, C.L., 1992. Cerebral glucose metabolism in childhood-onset obsessive–compulsive disorder. Revisualization during pharmacotherapy. Archives of General Psychiatry 49, 690 – 694. Tallis, F., 1995. The neuropsychology of obsessive–compulsive disorder: a review and consideration of clinical implications. British Journal of Clinical Psychology 36, 3 – 20. Tremblay, L., Schultz, W., 1999. Relative reward preference in primate orbitofrontal cortex. Nature 398, 704 – 708. Tulving, E., 1962. Subjective organization in free recall of bunrelatedQ words. Psychological Review 69, 344 – 354. Waber, D.P., Holmes, J.M., 1986. Assessing children’s memory productions of the Rey–Osterrieth Complex Figure. Journal of Clinical and Experimental Neuropsychology 8, 563 – 580. Wagner, A.D., Maril, A., Bjork, R.A., Schacter, D.L., 2001. Prefrontal contributions to executive control: fMRI evidence for functional distinctions within lateral prefrontal cortex. NeuroImage 14, 1337 – 1347. Zachary, R.A., 1991. Shipley Institute of Living Scale: Revised Manual. Western Psychological Services, Los Angeles, CA.