Executive functioning in schizophrenia: A thorough examination of performance on the Hayling Sentence Completion Test compared to psychiatric and non-psychiatric controls

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Abstract

Background

The current study examined executive functioning in schizophrenia by assessing response initiation and suppression in a group of schizophrenia patients, and drawing comparisons with psychiatric and non-psychiatric control groups.

Method

The Hayling Sentence Completion Test was used as a measure of executive functioning and was completed by 39 schizophrenia patients, 40 bipolar disorder patients and 44 healthy control participants. Outcome measures included response initiation and response suppression latency and error rate.

Results

The schizophrenia group was significantly impaired on all measures of the Hayling Sentence Completion Test when compared to healthy control participants, and only on some of the measures when compared to the bipolar disorder group. The bipolar disorder group did not differ in performance compared to the healthy control group. Overall schizophrenia patients showed longer response initiation and response suppression latencies, and an increased error rate. Performance of the schizophrenia patients was associated with higher ratings of cognitive disorganisation. Performance was not related to age, gender, predicted IQ or any other clinical characteristics.

Conclusions

Schizophrenia patients show a slowing in baseline response initiation and slowed suppression of an inappropriate response. Considering the bipolar disorder patients demonstrated intact performance, altered executive functioning in schizophrenia appears relatively specific to the disorder rather than reflecting other characteristics common to mental illness. Investigations examining which neurocognitive domains are impaired in schizophrenia provide direct implications for treatment options tailored to an individual's cognitive strengths and weaknesses.

Introduction

Neurocognitive impairment is considered a core feature of schizophrenia (Elvevag and Goldberg, 2000), with impairment relatively resistant to antipsychotic medication (Goldberg et al., 1993). Impairment is apparent early in the illness, as it is observed in first episode patients (Saykin et al., 1994). Longitudinal studies have revealed no difference in the degree of impairment between first episode and previously treated patients, both initially and at 19-month follow-up (Censits et al., 1997), thus indicating that deficits are stable over the course of the illness. Individuals at high-risk for developing schizophrenia, i.e. first-degree relatives, also exhibit deficits, suggesting a familial link (Byrne et al., 1999, Faraone et al., 1995). Furthermore, schizophrenia patients who demonstrate the lowest ratings on assessments of global functioning exhibit greater neurocognitive impairment compared to higher functioning patients (Loughland et al., 2007).

One particularly important aspect of neurocognition is executive functioning. This is a broad term used to describe cognitive processes involving control, flexibility, inhibition, regulation, planning, fluency and execution of goal-oriented behaviour. Such processes commonly involve abilities mediated by the prefrontal cortex. Extensive research indicates deficient executive functioning in schizophrenia patients (Evans et al., 1997, Morice and Delahunty, 1996). The Hayling Sentence Completion Test (HSCT) was developed to assess functioning in patients with cerebral lesions (Burgess and Shallice, 1996), and is an established measure of executive functioning. It was used in the current study. The task was designed to assess basic initiation speed and response suppression (Burgess and Shallice, 1997). HSCT performance is impaired in schizophrenia, with investigations reporting a relationship between HCST and clinical presentation (Chan et al., 2004), cortical activation (McIntosh et al., 2008), schizotypal personality traits (Laws et al., 2008), early-onset psychosis (Groom et al., 2008) and high-risk factors (Byrne et al., 1999). Significantly, HSCT has been shown to be a strong predictor among genetically high-risk individuals as to who goes on to develop the illness (Whalley et al., 2008).

The HSCT is a useful measure as it provides an overall standardised score to determine level of global impairment. In addition, the HSCT permits division and analysis of specific executive abilities evaluated within the task, i.e. response initiation, response suppression, as well as the error pattern. The specific profile of impairment in schizophrenia on the HSCT has not yet been thoroughly examined. Some studies have evaluated either overall performance (McIntosh et al., 2005), the speed of response (Groom et al., 2008) or error rates (Waters et al., 2003), with only one study incorporating all measures of response latencies over conditions and type of errors (Marczewski et al., 2001). However, their group sample size was limited (n = 15). Further, few studies have looked at the standardised classification of performance according to the task guidelines. This classification guide provides useful labels for performance evaluation ranging from ‘impaired’ to ‘high average’ performance.

A further issue common to neurocognitive investigation in schizophrenia involves the diagnostic specificity of the impairment. That is, are the performance deficits secondary to the illness and instead a result of psychopathological characteristics common to all mental illness, or are the deficits specific to the underlying aetiology of schizophrenia? This issue has been addressed in the current study by incorporating a bipolar disorder (BD) sample as a psychiatric control group. BD patients also show consistent neurocognitive impairment (Bearden et al., 2001), including executive functioning (Stoddart et al., 2007). Further, neurocognitive impairment appears to be independent of current affective state (Dixon et al., 2004). Both BD and schizophrenia patients experience psychotic symptoms and as a result share several psychopathological characteristics. While distinctly separate disorders, both groups of patients can become severely unwell, experiencing long periods of time in psychiatric institutions or hospitalisation. As a consequence they often show a reduced ability to maintain employment and/or social networks. Both groups are often prescribed with antipsychotic medication for extended periods of time. Considering these similarities, a BD group is an advantageous addition as a psychiatric control group within schizophrenia research, providing the opportunity to take into account factors such as medication, hospitalisation and length of illness. Previous HSCT studies have addressed this issue to a degree. One study included a group of attention-deficit hyperactivity disorder (ADHD) adolescents as a neurodevelopmental control group for HSCT performance comparisons to adolescent schizophrenia spectrum patients (Groom et al., 2008). Another study included a sample of schizophrenia and BD patients; however, they only reported one overall measure of HSCT performance (McIntosh et al., 2008). Therefore, to our knowledge, there have been no other studies to date to compare detailed behavioural performance on the HSCT between schizophrenia and BD patients.

The aim of the current study was to improve upon previous research in two main ways. Firstly, by examining HSCT performance in schizophrenia in greater detail than has been described previously; and secondly, drawing performance comparisons to both psychiatric and non-psychiatric control groups. Specifically, the HSCT was used to assess response initiation, response suppression and an error pattern. It was expected that the schizophrenia and BD patients would demonstrate performance deficits compared to the healthy control group in the form of longer response latencies and increased error rate. It was further hypothesised that deficits shown by schizophrenia patients would be greater than those of the BD patients indicating a diagnosis-specific impairment rather than an impairment that is secondary to the disorder.

Section snippets

Participants

The current study included 39 patients diagnosed with schizophrenia and 40 patients diagnosed with BD. Patients were recruited via community support groups and community care units and were all out-patients. Diagnosis was confirmed using the Structured Clinical Interview for DSM-IV (SCID: First et al., 1996). Current symptomology was acquired using the Positive and Negative Syndrome Scale (PANSS: Kay et al., 1987). Only patients with no other co-morbid Axis 1 diagnoses were included in the

Demographics

As shown in Table 1, there was no significant difference in age, gender or predicted IQ between the three groups. There was no significant difference in age of illness onset or length of illness between the two patient groups. Schizophrenia patients scored significantly higher on the negative factor of the PANSS, however there were no significant patient group differences for the positive factor, general factor or total PANSS scores. Overall, both patient groups were well matched and showed

Discussion

To our knowledge this is the first study to report comprehensive HSCT data in schizophrenia patients with the inclusion of both psychiatric and non-psychiatric control groups for comparison. Consistent with expectations, schizophrenia patients' revealed impaired performance compared to healthy control participants. Discordant with expectations the BD patients were more similar in their performance to the healthy controls than the schizophrenia group.

As expected, overall HSCT performance of the

Role of funding source

Nicole Joshua was funded by the Sir Robert Menzies Memorial Research Scholarship for Allied Health Sciences from The Menzies Foundation. Further, Andrea Gogos was supported by a National Health and Medical Research Council (NHMRC) fellowship (ID 435690). This research was also supported by Operational Infrastructure Support (OIS) from the Victorian State Government. The funding bodies had no further role in study design; in the collection, analysis and interpretation of data; in the writing of

Contributors

Authors Nicole Joshua and Andrea Gogos designed the study and collected the data. Nicole Joshua managed literature searches, undertook the statistical analysis and wrote the first draft of the manuscript. Andrea Gogos provided thorough edits to the first draft of the manuscript. Author Susan Rossell managed the study design, data collection and data analysis and edited the first draft of the manuscript. All authors contributed to and have approved the final manuscript.

Conflict of interest

The authors declare they have no conflicts of interest.

Acknowledgements

The authors would like to acknowledge the Menzies Foundation and the National Health and Medical Research Council (NHMRC) for the financial support of Nicole Joshua and Andrea Gogos. Many thanks also go to Alison O'Regan for assistance with some of the clinical interviewing and Prof David Castle for assistance with patient recruitment.

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