Executive function deficits associated with symptoms of schizotypy and obsessive–compulsive disorder
Introduction
The relationship of obsessive–compulsive disorder (OCD) to schizophrenia has recently become the focus of much research in psychology and psychiatry. While OCD had previously been primarily associated with the anxiety disorders, many patients diagnosed with OCD also meet criteria for a diagnosis of schizophrenia (Rasmussen and Tsuang, 1986). A review of several follow-up studies suggested 7–12% of patients with OCD developed schizophrenia at a later time, suggesting that the presence of OCD increases the likelihood of developing schizophrenia as much as 24 times above the general population (Flor-Henry, 1983). The relationship between obsessive–compulsive and schizotypal symptomatology appears stronger than that between obsessive–compulsive symptomatology and symptoms of anxiety (Norman et al., 1996), and obsessive–compulsive features account for 24% of the variance in schizotypal symptoms (Roth and Baribeau, 2000). These findings suggest that OCD may be more closely aligned with the schizophrenia constellation than with anxiety disorders, a hypothesis consistent with current understanding that both OCD and schizophrenia can be linked to the frontal lobe (Malloy, 1987). In fact, researchers have recently suggested that there exists a subtype of schizophrenia with obsessive–compulsive features (Berman et al., 2000, Hwang et al., 2000, Lysaker et al., 2000, Reznik et al., 2001), and that there is a schizotypy subtype in OCD (Sobin et al., 2000).
Evidence suggests that the orbitofrontal cortex and basal ganglia are involved in OCD. Structural anomalies of the caudate nucleus are present in patients with OCD (Insel et al., 1983, Luxenberg et al., 1988, Scarone et al., 1992), and positron emission tomography (PET) studies demonstrate hypermetabolism in the caudate nucleus and orbitofrontal cortex relative to other areas of the brain in OCD patients (Baxter et al., 1987, Martinot et al., 1990). In contrast, many studies implicate dorsolateral prefrontal cortex involvement in disorders of the schizophrenia constellation. Structural abnormalities in the frontal lobe have been found in schizophrenia (Andreasen et al., 1986, Laroi et al., 2000, Raine et al., 1992, Williamson et al., 1989), and these findings are correlated with poor performance on the Wisconsin Card Sorting Test (WCST) (Laroi et al., 2000, Williamson et al., 1989). PET and other functional neuroimaging studies show hypofrontality in patients with schizophrenia (Brodie et al., 1988, Buchsbaum, 1990, Wolkin et al., 1988), particularly during performance of the WCST (Berman and Weinberger, 1990, Rubin et al., 1994, Weinberger et al., 1986, Weinberger et al., 1988).
Greater understanding of the associations between OCD and the orbitofrontal cortex, and schizophrenia and the dorsolateral prefrontal cortex, may arise from neuropsychological studies of executive function. Executive function deficits typically occur with damage to the prefrontal region (Tranel et al., 1994). Damage to the dorsolateral prefrontal cortex may cause disorders of certain cognitive functions such as spatial orientation, memory for temporal sequence, integration of cognitive activities, defects in control of movement, tendency to perseverate and failure to notice details of the environment (Goldberg and Tucker, 1979, Lezak, 1995, Luria et al., 1966, Perecman, 1987). In contrast, damage specific to the orbitofrontal cortex may result in changes in affect, initiative, spontaneity, and impulse control, as well as inability to maintain set and regulate behavior (Lezak, 1995, Perecman, 1987).
The Wisconsin Card Sorting Test (WCST; Heaton et al., 1993) is considered to be one of the most sensitive tests of executive function related to the dorsolateral prefrontal cortex (Goldberg and Weinberger, 1988) and it has been commonly used in studies of schizophrenic patients, in their family members, and in schizotypal persons, with all populations showing impairments relative to healthy controls (Bellack et al., 1990, Braff et al., 1991, Butler et al., 1992, Cadenhead et al., 1999, Laroi et al., 2000, Lenzenweger and Korfine, 1994, Marks et al., 2000, Park et al., 1995, Riley et al., 2000, Saoud et al., 2000, Seidman et al., 1995, Suhr, 1997, Vogelmaier et al., 1997). Findings of WCST impairment in subjects at risk for schizophrenia, such as family members and those with schizotypal personality disorder, suggest that impaired WCST performance is an indicator of fundamental executive dysfunction in schizophrenia. However, impaired WCST performance has also been found (although not consistently) in OCD; some authors have found no deficits (Abbruzzese et al., 1995, Abbruzzese et al., 1997, Boone et al., 1991, Cavedini et al., 1998), while others report impairment (Christensen et al., 1992, Head et al., 1989, Malloy, 1987). These inconsistent findings could be explained, at least in part, by lack of consideration of the potential diagnostic overlap in OCD and schizophrenia.
Schizophrenic patients also show impairments on other clinical measures of executive functioning, such as the Stroop Color and Word Test (SCWT; Golden, 1978), the Trail-making Test (TMT; Reitan, 1958), and word fluency (Abbruzzese et al., 1995, Braff et al., 1991, Cadenhead et al., 1999, Franke et al., 1993, Riley et al., 2000, Yurgelun-Todd & Kinney, 1993). Patients with schizotypy and relatives of schizophrenics have also demonstrated impairments on the SCWT, the TMT, and word fluency (Chen et al., 2000, Gilvarry et al., 2001, Laurent et al., 2000, Suhr, 1997). At least one study has demonstrated that OCD patients were impaired on the TMT (Hollander and Wong, 1996), but to our knowledge, no studies have utilized the SCWT or word fluency in examination of deficits associated with OCD.
In past research, the nature of executive functioning in OCD has been examined using the Object Alternation Test (OAT; Freedman, 1990), the Delayed Alternation Test and the Delayed Response Test (DAT and DRT; Freedman and Oscar-Berman, 1986a), which were originally developed for use with primates and have been shown to be related to frontal lobe functioning (Gold et al., 1996). The OAT is considered one of the best available neuropsychological measures of executive function relative to the orbitofrontal cortex; the DAT, while a spatial working memory task, has also shown some degree of sensitivity to orbitofrontal dysfunction (Freedman, 1990, Freedman et al., 1998, Freedman et al., 1998, Freedman and Oscar-Berman, 1986a, Mishkin, 1964). The DRT measures executive function relative to the dorsolateral prefrontal cortex (Freedman and Oscar-Berman, 1986a, Freedman and Oscar-Berman, 1986b, Rosvold and Szwarczbart, 1964).
Cavedini et al. (1998) found the OAT distinguished OCD from major depression, with a significantly larger number of OAT perseverative errors by the OCD group. However, poor OAT performance has also been linked to schizophrenia. Seidman et al. (1995) reported that patients with schizophrenia were impaired on the OAT and DAT but not on the DRT; Faraone et al. (1999) found that relatives of patients with schizophrenia had impaired performance on the OAT but not the DAT. Other studies using tasks similar to the DRT suggest that delayed response performance is not impaired in patients with OCD (Rosenberg et al., 1997), but may be impaired in patients with schizophrenia (Raine et al., 1992).
There are a few studies that have examined the nature of neuropsychological impairment in patients with features of both disorders. Schizophrenic patients with prominent OCD symptoms appear to have more psychosocial dysfunction, poorer clinical course, more negative symptoms of schizophrenia, more motor dysfunction (consistent with basal ganglia impairment), and greater impairment on tests of visuospatial skills, delayed non-verbal memory, and executive functioning (Berman et al., 1998, Hwang et al., 2000, Krueger et al., 2000, Lysaker et al., 2000).
Only two studies have attempted to compare OCD and schizophrenic patients in terms of executive functioning. Abbruzzese et al. (1995) compared cognitive functioning in inpatient schizophrenic, OCD patients, and normal controls. Seventy-five subjects (25 in each group) performed the WCST and the OAT. Schizophrenic patients demonstrated impairment on the WCST, with more total and perseverative errors than OCD patients and normal controls. OCD patients displayed deficits on the OAT, with more perseverative errors than schizophrenic patients and normal controls. In a replication, Abbruzzese et al. (1997) conducted the same comparison with 150 subjects (60 in each clinical group, 30 normal controls). OCD patients performed poorly on the OAT but showed better performance on the WCST, while schizophrenic patients were impaired on the WCST but not on the OAT. However, in neither study was the potential diagnostic overlap between OCD and schizophrenia considered.
The current study extends the findings of Abbruzzese et al., 1995, Abbruzzese et al., 1997 by examining differences in symptomatic, but non-clinical samples. Research indicates that individuals with schizotypal symptoms demonstrate similar genetic and developmental markers to those with schizophrenia. These include prevalence of schizotypy in biological relatives of patients with schizophrenia and the elevated risk for developing schizophrenia associated with schizotypy (see Walker and Gale, 1995, for an excellent review of neurodevelopment in schizotypy and schizophrenia). Use of schizotypal samples is increasingly accepted as a methodologically sound design for investigation of the schizophrenia spectrum, as these samples tend to be less confounded by the correlates of severe clinical symptoms (e.g. medication, institutionalization) (Raine and Lencz, 1995). OCD research suggests genetic markers exist on a similar familial spectrum (Samuels et al., 2000), but the risk associated with subclinical OCD symptoms for later development of clinical OCD has not yet been fully investigated.
The purpose of this study was three-fold: first, to further tease apart the differential executive dysfunction findings of Abbruzzese et al., 1995, Abbruzzese et al., 1997 by including a diagnostic overlap group of individuals with symptoms of both OCD and schizotypy; second, to further investigate the potential for inclusion of specific cognitive impairment in the OCD and schizophrenia spectra; and third, to establish a basis for longitudinal study of the relationship between cognitive deficits and potential symptom progression. In the current study, participants with symptoms of schizotypal personality disorder, OCD, or both disorders completed neuropsychological tests measuring executive functions and general intellect. It was hypothesized that general intellectual functioning would not differ between groups. It was expected that individuals in the OCD condition would demonstrate deficits on the OAT and DAT, reflecting orbitofrontal dysfunction, compared with individuals in the schizotypal and control conditions. It was also expected that individuals in the schizotypal condition would demonstrate deficits on the WCST and DRT, reflecting dorsolateral prefrontal dysfunction, relative to the control and OCD conditions. Given that there are very few studies examining cognitive impairment in patients with both schizophrenia and OCD, it was expected that the OCD-schizotypy group would perform poorly on both ‘orbitofrontal’ and ‘dorsolateral’ tests, relative to the controls. As no strong evidence linked the SCWT, TMT or word fluency specifically to either OCD or schizophrenia, it was expected that all three groups would be different from the controls on these measures.
Section snippets
Participants
Participants were selected from approximately 2000 college undergraduates using the Maudsley Obsessional–Compulsive Inventory (MOCI; Hodgson and Rachman, 1977), the Schizotypal Personality Questionnaire (SPQ; Raine, 1991), the Beck Depression Inventory-II (BDI-II; Beck et al., 1996), and a version of the Jackson Infrequency Scale (JIS; Jackson, 1984), a measure containing items of infrequent probability that when endorsed suggest invalid responding. Individuals with high scores on the JIS
Intelligence testing
As expected, analysis of variance (ANOVA) revealed no significant differences in intelligence across groups (as measured by the WASI estimated IQ), F3,66=1.58, P=ns. There was no significant difference among groups on the Vocabulary, F3,66=2.19, P=ns, or the Matrix Reasoning, F3,66=2.18, P=ns, subtests. This suggests that generalized cognitive deficits were not responsible for any differences in cognitive performance among the groups. (See Table 2).
Anxiety
Data from the STAI were partially missing for
Discussion
As expected, individuals reporting symptoms of OCD and/or schizotypy did not differ from normal controls in intelligence as measured by the WASI. Generalized deficits would thus not be expected, and any differential performance on the executive function measures may be attributable to cognitive deficits related to OCD or to schizotypal symptomatology.
Several of the hypotheses regarding the OCD condition were confirmed. Overall, individuals in the OCD condition demonstrated poorer performance on
Acknowledgments
The authors extend thanks to John Gunstad for assistance with data collection, to Kimi Carson for her comments on an earlier version of this article, and to the anonymous reviewers for their thoughtful suggestions.
References (92)
- et al.
Frontal lobe dysfunction in schizophrenia and obsessive–compulsive disorder: a neuropsychological study
Brain and Cognition
(1995) - et al.
The selective breakdown of frontal functions in patients with obsessive–compulsive disorder and in patients with schizophrenia: a double dissociative experimental finding
Neuropsychologia
(1997) - et al.
Cognitive functioning and positive and negative schizophrenia
Schizophrenia Research
(1991) - et al.
Differential relationships between positive and negative symptoms and neuropsychological deficits in schizophrenia
Schizophrenia Research
(1997) - et al.
Wisconsin Card Sorting Test in chronic paranoid schizophrenia: evidence for a relatively discrete subgroup?
Schizophrenia Research
(1992) - et al.
Cognitive functions in schizotypal personality disorder
Schizophrenia Research
(1999) - et al.
Frontal lobe dysfunction in obsessive–compulsive disorder and major depression: a clinical neuropsychological study
Psychiatry Research
(1998) - et al.
Semantic verbal fluency deficit as a familial trait marker in schizophrenia
Psychiatry Research
(2000) - et al.
Neuropsychological performance in obsessive–compulsive disorder
Biological Psychiatry
(1992) - et al.
The Schizotypal Personality Questionnaire and the Wisconsin Card Sorting Test in a population of DSM-III-R schizophrenic patients and control subjects
Comprehensive Psychiatry
(1998)