Psychiatry and Clinical Neurosciences 2008; 62: 653–661
doi:10.1111/j.1440-1819.2008.01864.x
Regular Article
Verbal memory and verbal fluency in adolescents with schizophrenia spectrum disorders Nils Inge Landrø,
PhD1*
and Torill Ueland,
PhD2,3
1 Center for the Study of Human Cognition, Department of Psychology, University of Oslo, 2Sogn Centre for Child and Adolescent Psychiatry, and 3Section for Psychosis Research, Division of Psychiatry, Ullevål University Hospital, Oslo, Norway
Aim: Although impaired verbal memory and verbal fluency are frequently found in adults with schizophrenia, there has been a paucity of studies investigating adolescents with schizophrenia. Thus, the aim of the present study was to investigate the main subcomponents of verbal memory and verbal fluency in adolescents with schizophrenia spectrum disorders. Methods: Verbal learning and memory and verbal fluency was assessed in 21 adolescents with schizophrenia spectrum disorders (mean age, 15.4 years) compared with 28 healthy adolescents (mean age, 15.1 years). Results: The patient group performed significantly below healthy controls on measures of learning, delayed recall and on a frequency estimation task. No differences between the groups were found for
MPAIRED VERBAL MEMORY1 is well documented in adults with schizophrenia and occurs over and above normal general intellectual functioning2,3 and in neuroleptic-naïve first-episode patients.4 Memory is a multifaceted function consisting of various subprocesses such as learning, storage, recall and recognition. Based on findings of impaired recall along with intact recognition, it has been suggested that patients with schizophrenia show a retrieval
I
*Correspondence: Nils Inge Landrø, PhD, Department of Psychology, University of Oslo, Box 1094, Blindern 0317, Oslo, Norway. Email:
[email protected] Received 19 July 2007; revised 4 July 2008; accepted 2 September 2008.
measures of recognition, retention, implicit memory, or susceptibility to interference. Although they had impaired delayed recall the patients remembered most of what they actually learned. The patient group was impaired on phonological and semantic fluency, but there were no differences between the groups with respect to clustering or switching on the fluency tasks, when controlling for total output. There was no disproportionate impairment in semantic, as compared to phonological fluency, in the patient group.
Conclusions: Adolescents with schizophrenia spectrum disorders exhibit impairments in verbal learning and verbal fluency, which might have an impact on the individual’s everyday functioning. Key words: adolescents, fluency, verbal memory.
schizophrenia,
verbal
deficit.5 Others have reported impaired memory in schizophrenia under both free recall and under cued recall conditions, which could indicate a storage deficit.6 In general, however, the bulk of evidence indicates a primary deficit in the acquisition or learning of verbal material in adult patients with schizophrenia.7,8 Verbal fluency, frequently referred to as a semantic memory task, is another area consistently found to be impaired in schizophrenia samples.9,10 In two meta-analyses, including studies in which patients with schizophrenia and healthy controls completed both letter (phonemic) and category (semantic) fluency tasks, it was concluded that patients with schizophrenia were differentially deficient on category fluency.11,12 This finding is striking because numerous studies have demonstrated that in
© 2008 The Authors Journal compilation © 2008 Japanese Society of Psychiatry and Neurology
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healthy controls semantic fluency may be an easier task than letter fluency. Furthermore, fluency performance is multifactorial, and two important components of fluency performance are clustering (i.e. the production of words within semantic or phonemic categories), and switching (i.e. the ability to shift efficiently to a new subcategory).13 Adult patients with schizophrenia generate significantly fewer total words, cluster-related words and switches than healthy controls on both phonological and category fluency tasks.14 Only a few neuropsychological studies of adolescents with schizophrenia exist,15–18 and none of these undertook a systematic analysis of the various subcomponents of verbal memory. Impaired phonological fluency has been documented in one previous study of adolescents with schizophrenia,15 while, to our knowledge, no previous study of adolescents has included a measure of semantic fluency. Adolescents are an interesting group to investigate for several reasons. Research indicates that earlier age of onset is related to a poorer prognosis and outcome,19 and some studies also indicate poorer cognitive functioning.20 Further, progressive volumetric reductions of hippocampal regions have been documented in adolescents with schizophrenia,21 and impairments in verbal learning and memory are associated with earlier onset of illness.22 A significantly increased prevalence of neurological soft signs has also been reported in adolescents with first-episode psychosis as compared to healthy controls.23 Finally, a closer description of deficient and intact subcomponents of verbal memory and verbal fluency could potentially contribute to the development of more effective rehabilitation interventions. The first aim of the present study was to assess verbal learning, delayed recall and recognition in adolescents with schizophrenia. Specifically, we hypothezised that the patients would exhibit impaired learning ability. To further investigate verbal memory functioning in schizophrenia a paradigm including interference, and subtasks tapping an automatic aspect of verbal memory, as well as implicit memory, were included. The second aim was to examine verbal phonemic and semantic fluency and their underlying processes by estimating clustering and switching. We hypothezised that there would be a disproportionate impairment in semantic compared to phonological fluency in the patient group.
Psychiatry and Clinical Neurosciences 2008; 62: 653–661
METHODS Subjects Twenty-one adolescents with schizophrenia spectrum disorders and 28 healthy controls participated in the present study. The patient sample was recruited from an inpatient ward for psychotic patients at Sogn Centre for Child and Adolescent Psychiatry in Oslo, Norway. Inclusion criteria for entering the study were: age between 12 and 18 years, a diagnosis of a schizophrenia spectrum disorder, IQ > 70 and no evidence of organic brain disease. Diagnoses were based on the Structured Clinical Interview for DSM-IV Axis I disorders24 and patient case records. Diagnostic assessments were performed by an experienced clinical psychologist. The subdiagnoses of the patient sample were: disorganized, n = 5; paranoid, n = 6; undifferentiated, n = 5; schizoaffective, n = 3; schizotypal personality disorder (SPD), n = 2. For the two patients with SPD the Structured Clinical Interview for DSM-IV Axis II disorders was used for diagnostic assessment.25 Six participants were not using medication, while the remaining 15 were receiving antipsychotic medication. Seven patients were using atypical (olanzapine and risperidone) and five were using typical antipsychotic medication only. One patient was using both types. One patient was using an atypical together with lithium, and one, a typical together with methylphenidate. Six patients had never previously been hospitalized for psychotic symptoms, 12 patients had been hospitalized once and three had been hospitalized twice. Psychiatric symptoms were assessed using the 24-item Brief Psychiatric Rating Scale (BPRS)26 and psychosocial functioning using the Global Assessment Scale (GAS)27 by two independent raters. Inter-rater reliability intraclass corrections (ICC)28 was 0.92 for the BPRS total score and 0.94 for the GAS. Full-scale IQ was measured using the Wechsler Intelligence Scale for Children–Revised (WISCR)29 or the Wechsler Adult Intelligence Scale–Revised (WAIS-R)30 for subjects aged >16 years. The mean full-scale IQ in the patient group was 91 ⫾ 17 (range, 70–127). Scores from the subtests Similarities and Picture Completion are listed in Table 1 because they were the only IQ estimates obtained from the control group. Three patients did not have Norwegian as their first language, but all had been living in Norway for at least 5 years and spoke good Norwegian. The adolescents in the healthy comparison group were recruited on a voluntary basis from a local
© 2008 The Authors Journal compilation © 2008 Japanese Society of Psychiatry and Neurology
Psychiatry and Clinical Neurosciences 2008; 62: 653–661
Memory in adolescents with schizophrenia
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Table 1. Subject characteristics Schizophrenia group n = 21 Mean Male/female (ratio) Age (years) Similarities (WISC-R/WAIS-R) Picture Completion (WISC-R/WAIS-R) Medicated subjects (%) Global Assessment Scale Brief Psychiatric Rating Scale No. previous hospitalizations
13/8 15.4 9.8 8.7 71.4 30.7 54.7 1.0
SD
0.8 3.0 2.5 8.8 11.6 0.79
Control group n = 28 Mean 15/13 15.1 12.6 11.3 NA NA NA NA
SD
1.0 2.0* 3.2**
*P < 0.0001; **P = 0.004. WISC-R, Wechsler Intelligence Scale for Children-Revised; WAIS-R, Wechsler Adult Intelligence Scale-Revised.
school. The controls all attended regular school classes at normal grade levels. They were screened for psychiatric symptoms using the Youth Self-Report (YSR).31 The YSR is a self-report questionnaire for the assessment of psychopathology in children and adolescents. It contains eight problem syndrome scales: withdrawal, somatic complaints, anxious depressed, social problems, thought problems, attention problems, delinquent behaviour, and aggressive behaviour. The total score for all scales was included and participants with raw scores in the clinical range were excluded (n = 3). As an estimate of general intellectual functioning, participants were assessed on the subtests Similarities and Picture Completion using the WISC-R29 or the WAIS-R,30 when aged >16 years. These two subtasks are considered reliable and valid estimates of IQ30 and are highly correlated with verbal IQ and performance IQ, respectively. All participants provided written informed consent. The study was approved by the Regional Committee for Medical Research Ethics and the Norwegian Data Inspectorate. Demographic, psychometric and clinical characteristics of the two groups are given in Table 1. t-Tests were used to analyze differences between the groups for continuous measures and c2 tests for categorical variables. There were no significant differences between the groups with respect to age or the female/ male ratio. The patient group performed within the normal range on the estimated IQ measures Similarities and Picture Completion, but scored significantly below healthy controls (t(47) = 4.1, P < 0.0001; t(47) = 3.1, P = 0.004, respectively).
Assessment of verbal learning and memory Verbal learning and memory were assessed using a multi-trial, free-recall paradigm. The task involves the presentation of 12 words to be remembered, followed by the immediate recall of as many of the words as possible. On trials 2–8 the subject was reminded only of words that were missed on the preceding trial, but required to again recall all words on the list during the next trial (a selective reminding procedure).32 If all of the words were recalled before the eight trials were completed, this part of the task was terminated. In such cases all of the remaining trials were scored as 12 correct responses. A sum score of all correctly recalled words over the eight trials of list A quantified the rate of learning. Interference effects were measured by using another 12-word list (list B) once, after completing the learning trials of list A. After recall of this new list, recall from list A was again requested immediately. This measure is called short delay recall. Proactive interference was examined by comparing recall performance on the first trial of list A with the recall performance of list B. Delayed free recall was evaluated by requesting recall of list A after 45 min of doing other cognitive tasks. This measure is called long delay recall. Retention rate was estimated by calculating the proportion of words retained from list A over the 45-min delay period, as compared to the number of words retained on the trial presented immediately after list B. Following the delayed free-recall task, a recognition task was administered. The 12 words from list A
© 2008 The Authors Journal compilation © 2008 Japanese Society of Psychiatry and Neurology
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were interspersed with 48 distracters, the task being to respond ‘yes’ if the word was on list A and ‘no’ if the word was not. Six of the distracters were from list B. The recognition score was defined as the number of hits minus the number false alarms. A frequency of estimation task, presumably reflecting an automatic memory process,33 was also performed. The basis for this task was disguised in the recognition task. Of the 42 distracters, which were not on list B, some were presented once, others twice, three, four and up to five times. After the recognition task, pairs of words were presented to the subject, who was requested to indicate which of the two words had been presented most frequently during the test. The score was the number correct answers. Finally, a stem completion memory task, presumably tapping implicit memory, was given. This task consisted of completing word-stems with the 12 words from list A. The subjects were told to fill in the remaining letters making up the first word that came to mind. The score was the number of completed stems matching words from list A. The stimulus words in the two lists (A and B) were common one- or two-syllable Norwegian words such as elv (river), kniv (knife), hus (house), and tog (train).
Phonological and semantic fluency For the phonological fluency tasks participants were instructed to generate words beginning with f or a, excluding proper names and variants of the same word (e.g. the same word with suffixes). For the semantic fluency task the participants were instructed to generate names of animals. Each trial lasted 60 s. The total number of words generated, excluding perseverative errors and intrusive errors, were obtained for each fluency test. Then mean cluster size and number of switches were calculated. The scoring rules for clustering and switching were identical to those proposed by Troyer et al.13 In short, phonemic clusters consisted of successively generated words including perseverations and intrusions beginning with at least the same first two letters (e.g. arm and art), differing only by a vowel sound (e.g. sat, soot, sight, and sought), rhyming (such as sand, stand) or homonyms, that is, words with two or more different spellings. On the semantic tasks, clusters were defined as groups of successively generated words belonging to the same semantic subcategory, such as farm animals, pets, animals from different continents, and various zoological categories. Cluster size
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was counted, beginning with the second word in each cluster, and mean cluster size was calculated for the phonemic and semantic tasks. Phonemic and semantic switches were calculated as the number of transitions between clusters, including single words.
Data analysis Statistical analyses were performed using the SPSS for Windows Release 9.0 (SPSS, Chicago, IL, USA). Two multivariate analyses of variance (MANOVA) were performed, first with group as the between-group factor, and the main verbal memory measures (verbal learning, delayed recall, recognition, frequency estimation and stem completion) as dependent factors, and second, with the fluency measures as withingroup factors. Follow-up univariate analyses of variance (ANOVA) were performed on the various tests. Interference effects, retention and clustering and switching were analyzed using separate univariate ANOVA. Analyses of clustering and switching were repeated with total output as a covariate (ANCOVA). Associations between the verbal learning and memory measures and the fluency measures were examined on correlational analyses, as was the relationship between neuropsychological performance and severity of symptoms and psychosocial functioning.
RESULTS Analyses of the verbal learning and verbal memory measures Means and standard deviations for all test results are given in Table 2. MANOVA indicated an overall group difference over the six verbal memory tasks, with patients scoring lower than controls (Wilks l, F(5,43) = 4.8, P = 0.001). There was also a significant diagnosis by verbal memory measures interaction (Wilks l, F(5,43) = 5.7, P = 0.0001). Subsequent ANOVAs indicated significant differences between the groups in verbal learning (F(1,47) = 22.2, P < 0.0001), short delay recall (F(1,47) = 8.6, P = 0.005), long delay recall (F(1,47) = 6.2, P = 0.016), and frequency estimation (F(1,47) = 5.9, P = 0.019). There were no significant differences between the groups on the recognition task or the implicit memory task. A more detailed analysis showed that patients had fewer hits than controls, whereas they did not make more false alarms. Repeated measures ANOVA,
© 2008 The Authors Journal compilation © 2008 Japanese Society of Psychiatry and Neurology
Psychiatry and Clinical Neurosciences 2008; 62: 653–661
Memory in adolescents with schizophrenia
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Table 2. Verbal memory and fluency measures Schizophrenia group
Control group
Variable
Mean
SD
Mean
SD
P
Verbal memory Verbal learning Short delay recall Long delay recall Recognition Frequency estimation Stem completion
64.8 8.0 8.1 9.9 9.1 4.4
16.4 2.9 3.3 2.5 1.6 3.1
81.2 10.0 9.9 10.8 10.2 5.4
7.4 2.0 1.6 1.6 1.4 2.6
