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Auditory working memory and verbal recall memory in schizotypy
Schizophrenia Research 42 (2000) 101–110 www.elsevier.com/locate/schres
Auditory working memory and verbal recall memory in schizotypy M.F. Lenzenweger, Ph.D. a, *, J.M. Gold, Ph.D. b a Department of Psychology, Harvard University, 33 Kirkland Street, Cambridge, MA 02138, USA b Maryland Psychiatric Research Center and University of Maryland, Baltimore, MD, USA Received 16 April 1999; accepted for publication 14 June 1999
Abstract Deficits on verbal memory tasks, as well as on spatial and auditory working memory tasks, have been observed in schizophrenia patients. A useful strategy in the determination of the premorbid indicator status of specific cognitive and memory deficits observed in patients is to examine those persons at increased biological risk for schizophrenia (e.g. first-degree relatives), schizotypal personality disorder patients, and/or psychometrically identified schizotypes for comparable deficits, though perhaps less profound than those seen in actual patients. We examined verbal memory and auditory working memory functioning in 31 schizotypic and 26 normal control subjects from a large randomly ascertained non-clinical university population. Schizotypy status was determined psychometrically using the wellknown Perceptual Aberration Scale. Contrary to our theory-guided expectations, noteworthy deficits in verbal memory and auditory working memory were not observed in the schizotypic subjects and the two experimental groups did not differ significantly on any of the memory measures. These results were discussed in light of prior results obtained using the spatial delayed response task (i.e. spatial working memory) and Wisconsin Card Sorting Test performance on these same subjects. The theoretical implications of these findings are discussed in relation to the putative processes involved in the working memory system, as well as in relation to the schizotypy construct. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Auditory working memory; Memory; Recall; Schizophrenia; Schizotypal personality; Schizotypy; Verbal memory
1. Introduction Prior research has documented that schizophrenia patients reliably display evidence of a basic compromise in the ability to learn and retrieve new information (Saykin et al., 1991). Learning deficits have been documented in neuroleptic naive first episode samples, reducing concern that results * Corresponding author: Tel.: +1-617-495-9359; fax: +1-617-495-3728. E-mail address: [email protected] (M.F. Lenzenweger)
obtained from chronically treated populations simply reflect the potential negative impact of antipsychotic and anticholinergic medications on memory performance (e.g. Saykin et al., 1994). Deficits have been observed on both relatively effortful free recall tasks, as well as on tasks that make less of a demand on strategic encoding and retrieval processes, such as recognition and frequency estimation tasks (Gold et al., 1992). These behavioral findings have frequently been interpreted as implicating frontal and temporal lobe abnormalities, an inference consistent with neuroimaging and post mortem findings involving these regions
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(Bogerts, 1997; Goldman-Rakic and Selemon, 1997). Direct evidence supporting this inference was found in a recent PET study that demonstrated that patents show abnormalities including frontal hyperactivity combined with a failure to augment hippocampal activity during memory retrieval (Heckers et al., 1998). Thus, there is reason to believe that disturbed memory function in schizophrenia is an indicator of one of the central neurobiological abnormalities of the disorder (Gold et al., 1992), though the possibility of a generalized deficit in schizophrenia should always be kept in mind as well. Another area of active inquiry in schizophrenia concerns the working memory system (Baddeley, 1986, 1998) and the potential relations between dysfunction in working memory and symptom development in the illness (Goldman-Rakic, 1994). Working memory may be thought of as a system for temporarily maintaining information in order that the information can be used subsequently to guide behavior (Baddeley, 1986, Baddeley, 1998). Park and Holzman (1992, 1993) have demonstrated the existence of spatial working memory deficits in both schizophrenia patients and their biological first-degree relatives. Gold et al. (1997) developed a task of working memory for the auditory modality and also found evidence of deficits on this measure of auditory working memory in schizophrenia patients. These data suggest that a deficit in working memory, assessed in two different modalities, may be an important feature of schizophrenia, and potentially in their relatives. Taken together, the available data on verbal memory and working memory in schizophrenia suggest that each of these memory systems is disrupted in the illness. Perhaps, more importantly, they further suggest the possibility that illumination of the pathology of these systems may hold promise for specifying those processes that may be important to the pathogenesis of schizophrenia, or at least some dimension of schizophrenia. One of the features of some of the memory data (e.g. auditory working memory) discussed thus far, however, is that these studies have been confined to the study of clinically affected cases, i.e. persons who have already expressed schizophrenia. The
interpretation of data derived from patients is, of course, complicated and limited in terms of generalizability by the well-known third-variable confounds attending the study of expressed schizophrenia [i.e. deterioration, institutionalization, and motivation effects; see Lenzenweger (1998)]. More importantly, perhaps, one must be aware of the limited contribution data from expressed cases of the illness can make to the establishment and understanding of the premorbid indicators (or early expressions) of underlying liability for schizophrenia. This pattern of empirical relationships, as well as a desire to determine if memory deficits can be detected in non-psychotic, but schizotypic subjects, suggested a question for further study in research on schizotypy. The study of the schizotype, conceptualized as an alternative expression of schizophrenia liability, can be undertaken from three distinct vantage points. Namely, schizotypic subjects may be defined as (a) biological relatives of persons affected with schizophrenia, (b) those persons diagnosed with DSM-IV schizotypal personality disorder (PD), or (c) those persons who display deviance on a laboratory measure known to be associated with schizophrenia liability (e.g. psychometric measures) (Lenzenweger, 1994, 1998). Prior work focusing on either psychometrically identified [strategy (c)] or clinical [strategy (b)] schizotypes has been limited and characterized by the use of typically only one memory measure per study (LaPorte et al., 1994; Lyons et al., 1995; Voglmaier et al., 1997; Bergman et al., 1998), with no prior study examining multiple memory measures in the same clinical or psychometrically identified schizotypic subjects. Two studies have examined multiple memory measures in the biological relatives of schizophrenia patients [strategy (a)] (Cannon et al., 1994; Faraone et al., 1995). Upon testing with extensive neuropsychological test batteries, Faraone et al. (1995) found verbal memory deficits (i.e. logical memory for story material ) among the relatives of schizophrenia patients compared with controls, and Cannon et al. (1994) found the siblings of schizophrenia patients performed worse on verbal and spatial memory measures relative to controls. The incremental value of a study in which multiple memory systems
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were evaluated using multiple memory measures appeared noteworthy to the present investigators. The current study used the psychometric strategy [strategy (c), deviance on a laboratory measure] in detecting schizotypic persons and sought to determine whether such individuals would display evidence of both recall memory and auditory working memory deficits consistent with what has been observed in the study of schizophrenia patients. Furthermore, the subjects for the current study were also assessed on a measure of spatial working memory (Park et al., 1995), thus allowing for an important evaluation of relations among verbal recall, auditory working memory, and spatial working memory.
2. Method 2.1. Subjects Subjects for the present study were drawn from a randomly ascertained sample of first-year undergraduates at Cornell University who voluntarily completed a 250-item psychological inventory entitled ‘Attitudes, Feelings, and Experiences Questionnaire’ that included the Perceptual Aberration Scale (PAS; Chapman et al., 1978; see below for detail ). We chose this approach in order to maximize diversity within our pool of potential study subjects, as well as to minimize the effects of both subject self-selection factors and grouprelated test-taking attitudes often found in introductory psychology course-based sampling procedures. A total of 2000 individuals were initially selected at random from a university roster of all first-year students who entered during a recent fall semester (approximately 3000 students per year). A team of research assistants individually approached each of the potential study participants and asked them to voluntarily complete the psychological inventory noted above. The subjects were informed that their inventory responses would remain completely confidential and would be used for research purposes only. Study subjects were asked to complete the inventory within 48 h and the completed inventories were picked up by study staff in sealed
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envelopes. Of the 2000 potential subjects, 1684 (51.3% women, 48.7% men) completed the inventory. The response rate of 84.2% is consistent with representative sampling ( Kalton, 1983). To control for pseudo-random responding and invalid test-taking attitudes, a 14-item version of Jackson’s (1984) Infrequency Scale from his Personality Research Form was included in the 250-item screening inventory. Subjects scoring greater than three on the Infrequency Scale were dropped from the sample; 35 (2.1%) were excluded from our sample on this basis. Three additional subjects were dropped because of extensive missing data on the inventory. The final sample consisted of 1646 cases, from which two subject groups were composed for the experimental assessments described below. Separate group means and standard deviations for males and females on the PAS were computed and served as the basis for subject selection. Following Chapman and Chapman (1985), high PAS subjects were required to have scored at least 2.0 standard deviations above the group mean on the PAS, whereas normal controls were required to have scored no higher than 0.5 standard deviations above the group mean. Study subjects for each of the two groups were selected at random from the two sub-samples of subjects meeting the specified criteria. Testing was carried out blind to the group membership. A total of 26 (14 female) normal control subjects and 31 (16 female) high PAS subjects were tested. The proportions of male and female subjects across the two subject groups did not differ significantly [X2 (1, N=57)=0.03, p=n.s.]. The mean ages of the high and low PAS subjects were 19.00 years (SD=0.52) and 18.96 years (SD=0.53) respectively. The mean PAS scores of the high and low PAS subjects were 19.77 (SD=6.35) and 0.77 (SD=0.99) respectively. There were no differences among the two groups in terms of agreement to participate in the study described below. Although the individuals contained in the pool of 1646 potential study subjects had been preselected initially for academic achievement (i.e. university admission), academic ability does not preclude a risk for psychopathology (see Stangler and Printz, 1980; Depue et al., 1989). The population from which the sample was drawn was most probably somewhat biased against particularly
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early-onset variants of severe psychopathology. However, one would not necessarily anticipate any diminution in the prevalence of schizophrenia spectrum-related personality disorders in the undergraduate population studied (Lenzenweger et al., 1997).
inventory used to measure depressive/dysphoric symptoms in the study subjects. The State–Trait Anxiety Inventory ( Form Y; Spielberger, 1983) is a well-known 40-item selfreport inventory was used to measure state and trait anxiety in the study subjects.
2.2. Schizotypy measure
2.4. Cognitive processing speed and general intellectual functioning measures
The PAS is the well-known 35-item true–false self-report measure of disturbances and distortions in perceptions of body image and of other objects (Chapman et al., 1978). It includes items like ‘Occasionally I have felt as though my body did not exist’ (keyed true) and ‘I have never felt that my arms or legs have momentarily grown in size’ (keyed false). Extensive literature reviews bearing on the reliability and validity of the PAS as schizotypy (or, perhaps more broadly, psychosisproneness) measures can be found elsewhere (Chapman et al., 1995; Edell, 1995; Lenzenweger, 1994, 1998). We chose the PAS for this study because of the importance attached to body-image and perceptual distortions in theoretical views of schizotypy (Rado, 1960; Meehl, 1964). Rado (1960, pp. 88, 90) viewed such distortions as deriving fundamentally from the putative proprioceptive (kinesthetic) diathesis hypothesized to be one of the two basic dimensions of pathology underlying schizotypal personality organization. Meehl (1964, pp. 24–27) identified body-image aberrations as a schizotypic sign in his ‘Manual’, which provides rich descriptions of the clinical manifestations of such phenomena. In addition to the work of Rado (1960) and Meehl (1964), perceptual and body-image distortions as phenomenological manifestations of schizophrenia (and other psychoses) have a long history in descriptive psychopathology, and this history has been reviewed extensively by Chapman et al. (1978). Therefore, as a measure of body image distortions and perceptual aberrations, we are suggesting that the PAS taps at least some of the symptoms of schizotypy. 2.3. Psychological state measures The Beck Depression Inventory (BDI; Beck et al., 1961) is a well-known 21-item self-report
A focal assessment of overall cognitive processing speed in the study subjects was done using the Digit Symbol subtest of the Wechsler Adult Intelligence Scale-Revised ( WAIS-R) ( Wechsler, 1981). In addition, every subject provided us with a formal release of information that allowed us to obtain their official Scholastic Aptitude Test (SAT ) scores, verbal and quantitative, from their Cornell University record. All participants were given the self-administered computerized screening version of the Diagnostic Interview Schedule (DIS-Screen; Robins et al., 1981) to assess lifetime presence of several psychopathological conditions, namely major depression– dysthymia, mania–hypomania, and schizophrenia– schizophreniform psychosis. No participant in either group met definite criteria for an affective disorder or schizophrenia–schizophreniform psychosis. 2.5. Procedures and memory tasks Potential study participants were contacted by telephone and were invited to participate voluntarily in a study of ‘Young Adult Development’ for which they would receive $50.00. A complex coding scheme was employed to disguise the group status of the subjects and all study staff were blind to a subject’s group membership throughout the study. The subjects completed the schizotypy, psychological state, and memory measures, along with other laboratory measures described in other reports (e.g. thought disorder, Coleman et al., 1996; antisaccade performance, O’Driscoll et al., 1998; working memory, Park et al., 1995). Subjects were tested in a quiet darkened room, the study measures were counterbalanced for administration order, and all subjects gave informed consent.
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2.6. Memory tasks 2.6.1. Verbal memory (recall) measures Each subject received three trials of a 38 word list for immediate recall and a delayed recall trial that followed approximately 20 min after the third recall trial. The word list was adapted from those used in Gold et al. (1992). The lists were composed of five exemplars from each of six taxonomic categories that were constructed so that related items never appeared consecutively. The first and last four items on the list were drawn from eight other taxonomic categories so that primacy and recency items were not semantically related to other list items. 2.6.2. Letter–number (LN) span task The LN span task, developed by Gold et al. (1997), involves the auditory presentation by an examiner of a mixed series of alternating numbers and letters. The task has been conceptualized as a test of auditory working memory (Gold et al., 1997). The subject is asked to respond by first saying the numbers in order from the smallest to largest, followed by saying the letters in alphabetical order. For example, a subject would hear ‘w7t4’, and the correct answer is ‘47tw’. Following a series of practice trials, the test involves four trials at each string length, beginning with twoitem strings (such as ‘m3’) and proceeding up to seven-item strings (such as ‘c7g4q1s’) for a total of 24 items. The total number of correct responses is then computed out of a possible total of 24. The test is terminated when a subject fails all four trials at any one string length. The internal consistency of the LN span is high (a=0.85) and, in terms of criterion validity, the LN span association with prominent neuropsychological and cognitive measures, among schizophrenia patients, appears robust, even when the effects of IQ and general memory ability are removed (Gold et al., 1997). 2.6.3. Preliminary pilot evaluation of memory measures In order to ensure that both the verbal memory and LN span tasks were sufficiently difficult for the undergraduate subjects to be tested in the current study, a pilot study was undertaken involv-
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ing 27 randomly selected university undergraduate students. Each of the 27 students completed both the verbal memory and LN span tasks, counterbalanced for order of administration, and an examination of the means and distributions for the tasks revealed that the student subjects, as a group, were not performing at or near the ceiling on any of the measures. These data may be made available upon request. 2.6.4. Statistical analysis The verbal memory trials, four total, were scored simply as the total number of correct items recalled. These data were analyzed using a repeated measures analysis of variance (ANOVA) approach, with one between-subjects factor (group, two-levels) and one within-subjects factor (trial, three-levels). The fourth trial of the verbal memory measure was treated as a separate measure of delayed recall. For the LN span, two performance scores were computed. The first was the total number of correct trials achieved, out of 24 possible, and the second was the highest string length attained, where at least one item of that string length was passed. Correlational analyses were conducted using the Pearson product-moment correlation coefficient. Effect-size estimates were computed as per Cohen (1988); for the ANOVA analyses the effect size is reported as partial g2 and for the t-test, Cohen’s d is used.
3. Results The means and standard deviations for the verbal memory and auditory working memory tasks are contained in Table 1. The repeated measures ANOVA for the verbal memory task revealed a significant main effect for trial [F(2, 110)=46.08, p<0.001; effect size (partial g2)=0.46 ], but neither the main effect for group [F(1, 55)=0.002, p= 0.96; effect size (partial g2)=0.000] or the group by list interaction [F(2, 110)=0.35, p=0.71; effectsize (partial g2)=0.006 ] were statistically significant. A t-test comparison of the two groups on the delayed recall trial of the verbal memory task
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Table 1 Means and standard deviations for the verbal memory and auditory working memory measuresa Schizotype (n=31)
Controls (n=26)
Mean
SD
Mean
SD
higher levels of state-anxiety ( p<0.001), traitanxiety ( p<0.001), and dysphoric (BDI ) features ( p<0.001) relative to controls. However, none of the memory indexes was correlated significantly with state-anxiety, trait-anxiety, or depression scores (all p>0.20).1
Verbal recall Trial 1 Trial 2 Trial 3 Delay trial
15.29 19.58 21.65 25.58
5.32 5.19 5.76 4.63
14.73 19.35 22.27 24.58
3.40 5.05 6.84 5.15
3.2. Relations with spatial working memory (delayed response task; DRT) and Wisconsin Card Sorting Test (WCST) performance (Park et al., 1995)
LN span Total correct Longest string
18.16 6.45
2.44 0.62
18.88 6.62
2.53 0.57
Measure
a The final trial of the verbal memory task was a delayed recall trial (delay trial ), whereas trials 1, 2 and 3 were immediate recall. Values for the verbal recall trials are the total number of words correctly recalled out of a possible 38. Longest string indicates the longest string length at which at least one item on the LN span was passed correctly.
was non-significant [t(55)=0.78, p<0.44; d= 0.20]. For the LN span, the two groups performed virtually identically for both the total number of correct responses and the longest string achieved. For the total correct on the LN span [t(55)=1.10, p=0.278; d=0.29] and for the longest string achieved [t(55)=1.03, p=0.310; d=0.29]. With respect to the relations between the LN span and performance on the four verbal memory trials, there were no statistically significant correlations between with the LN span total score or LN span longest string achieved score and any of the four verbal memory trials. 3.1. Intellectual functioning and psychological state analyses In terms of general intellectual functioning, the schizotypic subjects did not differ significantly from the controls on either the SAT Quantitative ( p>0.80) or SAT Verbal ( p>0.52) scores. With respect to speed of processing, there was a nonsignificant trend for the schizotypic subjects to have lower digit symbol raw scores [t(55)=1.71, p<0.10]. As would be expected, based on model of Meehl (1990), schizotypic subjects did display
As noted above, the subjects in this study were also evaluated for performance on a DRT known to assess spatial working memory, as well as on the WCST ( Heaton, 1981) (Park et al., 1995). Park et al. (1995) found that the schizotypic subjects in this sample displayed significantly lower accuracy on the spatial working memory task, as well as an increase in the failure to maintain set ( FMS) variable on the WCST. The availability of these data presented the opportunity to examine auditory working memory in relation to spatial working memory and WCST performance in the same subjects. The DRT accuracy score was minimally related to the LN span total score (r=0.09), whereas DRT performance was significantly associated with the longest string achieved on the LN span (r=0.32, p<0.02, two-tailed ). The LN span total score was correlated with the WCST FMS score (r=−0.20, p<0.15, two-tailed ); LN span longest string achieved was correlated with the FMS score (r=−0.13, p<0.33). We note also that the LN span total score was correlated 0.25 ( p<0.07, two-tailed ) with the WCST categories completed score; LN span longest string achieved was correlated 0.13 ( p<0.35, two-tailed ) with the WCST categories completed score.
4. Discussion The primary results of this study reveal that schizotypic subjects, selected on the basis of 1 The psychological state data both across the groups and in relation to the memory indexes have been presented in summary form. The complete set of means, standard deviations, t-tests, correlations, and associated p-values may be requested from the authors.
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psychometric deviance on the PAS, do not differ from control subjects on measures of verbal recall memory and auditory working memory. The effect sizes associated with group membership in relation to recall memory were essentially zero, whereas the effect sizes for the LN span were larger, though still small by accepted standards (Cohen, 1988). In order to place the LN span findings into a more readily understood context, in order to detect the effect that we observed for the LN span correct with 80% power and to have it be significant at the 0.05 level would have required 188 subjects in each subject group (376 total ). Clearly, neither verbal recall memory or auditory working memory appear to be associated with psychometrically identified schizotypes. The failure to find subtle verbal memory and/or auditory working memory deficits in the schizotypes is inconsistent with the memory literature for schizophrenia patients, which suggests verbal memory (Gold et al., 1992) and auditory working memory (Gold et al., 1997) deficits are present in clinically affected individuals. Our findings are especially interesting in light of the fact that positive, but not negative, symptoms are most closely related to auditory processing deficits in schizophrenia (Strauss, 1993) and one might arguably consider the PAS to assess a positive symptom-like form of phenomenology. Moreover, the failure to find differences between the schizotypes and controls on the two memory tasks is generally inconsistent with the prevailing pattern of results in the schizotypy research area, wherein the modal finding in such studies is that schizotypes do usually differ from controls on a task of interest and schizotypic performance is usually consistent with, albeit in attenuated form, deficits seen in schizophrenia patients (see Lenzenweger, 1998). The challenge to us, therefore, has been to try to understand our results for the verbal memory and auditory working memory measures and extract meaning and direction from them. Our findings for auditory working memory provide us with an interesting pattern of results when combined with those reported previously by Park et al. (1995) using the same subjects. Whereas the schizotypes in this study did display a significant difference from normal controls on the DRT task,
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which is suggested to be a measure of visual– spatial working memory, the same subjects did not display a deficit on a task of auditory working memory (LN span). Moreover, for those subjects who completed both the LN span and the DRT, the performance accuracy on the DRT was not correlated with overall accuracy on the LN span, but it was correlated with the longest string passed successfully on the LN span. Performance on the LN span was uncorrelated with the FMS variable from the WCST, which was also completed by these same subjects. At a minimum, this general pattern of results suggests less of a connection (or diminished association) between the LN span and the other measures putatively involved with working memory assessed in the visual modality (i.e. the DRT and WCST ). In attempting to better understand our current results, we have considered the following possibilities: namely modality-based differences across tasks, the processes tapped by the measures under consideration, differences in the progressive impairment of memory systems, and the nature of psychometrically assessed schizotypy. First, regarding the modality-based differences issue, it is clearly evident that the aspect of working memory tapped by the DRT (Park et al., 1995) is fundamentally involved with the visual processing nature of the task. The visual–spatial DRT may involve activation of the so-called visuo-spatial sketchpad in the tripartite model of working memory suggested by Baddeley (1994), whereas the LN span may involve the activation of the so-called phonological loop of the tripartite working memory system. In this view, one might argue that our results suggest that the psychometrically identified schizotypes have a modality specific working memory deficit, which involves the visual– spatial sketchpad (or channel ) but not the phonological loop. A complication in this view, however, concerns the fact that both the DRT and LN span are sufficiently demanding tasks and, presumably, they both should make demands on (or involve) the ‘central executive,’ which is argued to subserve the coordination, manipulation, and updating of contents in the working memory slave sub-systems (Baddeley, 1998). It strikes us as somewhat odd to think that the central executive could function
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effectively for an auditory working memory task, but function ineffectively for visuo-spatial information (i.e. DRT ) in the same people. How then to best understand these data? One could consider the possibility that the two tasks (DRT versus LN span) each represent one of two types of working memory task, that is a task that requires storage, maintenance, and evaluation of representations (i.e. ‘maintenance’ tasks) versus those that also require manipulation and updating of the contents of working memory (i.e. ‘maintenance+’ tasks) (see Schacter et al., 1999). From this standpoint, we might suggest that schizotypes have reliable deficits on the first type of working memory task (operationalized as the DRT ), but do not have deficits on the second type of working memory task (operationalized as the LN span). However, from this standpoint, it is somewhat difficult to conceptualize poor performance on a task that requires only maintenance functioning (e.g. DRT ), but uncompromised performance on a task that calls for maintenance plus manipulation functioning (e.g. LN span) in the same schizotypic subjects. Alternatively, one could also consider the possibility that central executive processes could be impaired on a modality specific basis. An alternative speculation regarding these results would rely on the concept of disinhibition, which has enjoyed increasing prominence in discussions of cognitive deficits in schizophrenia (e.g. Park et al., 1996; O’Driscoll et al., 1998). Other data from these same subjects is consistent with disinhibition as a characteristic of the psychometric schizotypes in terms of their functioning on neurocognitive tasks that require intact inhibitory functioning and are processed through the visual modality. For example, in this sample of subjects the psychometric schizotypes reveal increased tendency to lose set on the WCST, increased antisaccade errors, and poorer smooth pursuit eye tracking (O’Driscoll et al., 1998). Therefore, one might differentiate the processes tapped respectively by the DRT and the LN span. One could consider that possibility that performance on the visual–spatial DRT is actually better conceptualized as an index of disinhibition. That is, the DRT involves holding target information over a filled delay, perhaps providing for greater opportunity
for distraction, drift, or interference from prior trials. The LN span, on the other hand, involves discrete trials and no delay period, allowing for less involvement of disinhibitory effects. A third alternative to consider would involve the point in the developmental progression of the putative schizophrenia-related process observed in these subjects in relation to auditory working memory and verbal memory. It may be, perhaps, that one might only see auditory working memory and verbal (semantic) memory deficits after a clinical illness began to express itself in a more definitive manner. That is, perhaps auditory working memory and verbal (semantic) memory deficits are most noted only once an illness has begun to unfold in patients. If, however, one were to detect such deficits in the non-psychotic biological relatives of schizophrenia patients, then such evidence would tend to argue against this view. Verbal memory deficits (i.e. logical memory for story material ) have been found among the relatives of schizophrenia patients (Cannon et al., 1994; Faraone et al., 1995), and auditory working memory deficits have yet to be studied in firstdegree biological relatives of schizophrenia patients. Therefore, data are not yet available from relatives to address directly the verbal and auditory working memory measures used in this study. Finally, we must consider the possibility that psychometrically assessed schizotypy does not overlap perfectly with the construct of schizophrenia liability. It could very well be the case that the construct defined by psychometric schizotypy, at least insofar as it is assessed with the PAS, does not capture all aspects of schizophrenia liability. Thus, psychometric schizotypy is but an imperfect measurement of the true latent construct of schizophrenia liability. It is also conceivable that the PAS possesses some appreciable measure of validity with respect to underlying schizophrenia liability, as indicated by the multitude of findings on high PAS subjects that are highly comparable to what is observed in clinical schizophrenia patients [see Lenzenweger (1998) for review], yet the scale generates an admixture of true-positive cases for schizophrenia liability as well as false-positive cases whose PAS scores are not reflective of genuine schizotypy. In the absence of a gold standard for
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schizophrenia liability (e.g. a gene or genes), such a conjecture is difficult to evaluate empirically. The weight of the evidence from prior studies using the PAS, however, is against this particular explanation of the results obtained (see Lenzenweger, 1998). In summary, the present study did not find evidence of verbal memory or auditory working memory deficits in psychometrically identified schizotypes. The effect-size estimates, particularly for the verbal memory measures, suggest the absence of group differences on the memory measures was not due to unduly small groups; moreover, the sample sizes used in this study were comparable to those used consistently in this line of research. We have offered several alternative interpretations of these data in relation to other data we have available on the same subjects. This study has provided us with additional useful information regarding schizotypy and may best be viewed for its heuristic value.
Acknowledgements We thank Daniel Schacter, Ph.D., for his helpful comments regarding working memory. We also thank Michael Raulin, Ph.D., and an anonymous reviewer for their helpful comments on an earlier version of this article.
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schizophrenic symptoms. Schizophrenia Bulletin 23, 423–435. Cannon, T.D., Zorrilla, L.E., Shtasel, D., Gur, R.E., Gur, R.C., Marco, E.J., Moberg, P., Price, A., 1994. Neuropsychological functioning in siblings discordant for schizophrenia and healthy volunteers. Archives of General Psychiatry 51, 651–661. Chapman, L.J., Chapman, J.P., 1985. Psychosis proneness. In: Alpert, M. ( Ed.), Controversies in schizophrenia: Changes and constancies. Guilford Press, New York, pp. 157–172. Chapman, L.J., Chapman, J.P., Raulin, M.L., 1978. Bodyimage aberration in schizophrenia. Journal of Abnormal Psychology 87, 399–407. Chapman, J.P., Chapman, L.J., Kwapil, T.R., 1995. Scales for the measurement of schizotypy. In: Raine, A., Lencza, T., Mednick, S. ( Eds.), Schizotypal Personality. Cambridge University Press, New York, pp. 79–106. Cohen, J., 1988. Statistical Power Analysis for the Behavioral Sciences. 2nd edition, Erlbaum, Hillsdale, NJ. Coleman, M.J., Levy, D.L., Lenzenweger, M.F., Holzman, P.S., 1996. Thought disorder, perceptual aberrations, and schizotypy. Journal of Abnormal Psychology 105, 469–473. Depue, R.A., Krauss, S., Spoont, M.R., Arbisi, P., 1989. General behavior inventory identification of unipolar and bipolar affective conditions in a nonclinical university population. Journal of Abnormal Psychology 98, 117–126. Edell, W.S., 1995. The psychometric measurement of schizotypy using the Wisconsin scales of psychosis-proneness. In: Miller, A. ( Ed.), The Behavioral High-Risk Paradigm in Psychopathology. Springer, New York, pp. 3–46. Faraone, S.V., Seidman, L.J., Kremen, W.S., Pepple, J.R., Lyons, M.J., Tsuang, M.T., 1995. Neuropsychological functioning among the nonpsychotic relatives of schizophrenic patients: a diagnostic efficiency analysis. Journal of Abnormal Psychology 104, 286–304. Gold, J.M., Randolph, C., Carpenter, C.J., Goldberg, T.E., Weinberger, D.R., 1992. Forms of memory failure in schizophrenia. Journal of Abnormal Psychology 101, 487–494. Gold, J.M., Carpenter, C., Randolph, C., Goldberg, T.E., Weinberger, D.R., 1997. Auditory working memory and Wisconsin Card Sorting Test performance in schizophrenia. Archives of General Psychiatry 54, 159–165. Goldman-Rakic, P.S., 1994. Working memory systems in schizophrenia. Journal of Neuropsychiatry and Clinical Neurosciences 6, 348–357. Goldman-Rakic, P.S., Selemon, L.D., 1997. Functional and anatomical aspects of prefrontal pathology in schizophrenia. Schizophrenia Bulletin 23, 437–458. Heaton, R.K., 1981. Wisconsin Card Sorting Test Manual. Psychological Assessment Resources, Odessa, FL. Heckers, S., Rauch, S.L., Goff, D., Savage, C.R., Schacter, D.L., Fischman, A.J., Alpert, N.M., 1998. Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nature Neuroscience 1, 318–323. Jackson, D.N., 1984. Manual for the Personality Research Form. 3rd edition, Research Psychologists Press, Port Huron, MI.
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Kalton, G., 1983. Introduction to Survey Sampling. Sage, Beverly Hills, CA. LaPorte, D.J., Kirkpatrick, B., Thaker, G.K., 1994. Psychosisproneness and verbal memory in a college student population. Schizophrenia Research 12, 237–245. Lenzenweger, M.F., 1994. The psychometric high-risk paradigm, perceptual aberrations and schizotypy: an update. Schizophrenia Bulletin 20, 121–135. Lenzenweger, M.F., 1998. Schizotypy and schizotypic psychopathology: mapping an alternative expression of schizophrenia liability. In: Lenzenweger, M.F., Dworkin, R.H. ( Eds.), Origins and Development of Schizophrenia: Advances in Experimental Psychopathology. American Psychological Association, Washington, DC, pp. 93–121. Lenzenweger, M.F., Loranger, A.W., Korfine, L., Neff, C., 1997. Detecting personality disorders in a nonclinical population: application of a two-stage procedure for case identification. Archives of General Psychiatry 54, 345–351. Lyons, M.J., Toomey, R., Seidman, L.J., Kremen, W.S., et al., 1995. Verbal learning and memory in relatives of schizophrenics: preliminary findings. Biological Psychiatry 37, 750–753. Meehl, P.E., 1964. Manual for Use with Checklist of Schizotypic Signs. University of Minnesota, Minneapolis, MN. Meehl, P.E., 1990. Toward an integrated theory of schizotaxia, schizotypy and schizophrenia. Journal of Personality Disorders 4, 1–99. O’Driscoll, G., Lenzenweger, M.F., Holzman, P.S., 1998. Antisaccades and smooth pursuit eye tracking and schizotypy. Archives of General Psychiatry 55, 837–843. Park, S., Holzman, P.S., 1992. Schizophrenics show working memory deficits. Archives of General Psychiatry 49, 975–982. Park, S., Holzman, P.S., 1993. Association of working memory deficit and eye tracking dysfunction in schizophrenia. Schizophrenia Research 11, 55–61. Park, S., Holzman, P.S., Lenzenweger, M.F., 1995. Individual differences in working memory in relation to schizotypy. Journal of Abnormal Psychology 104, 355–363.
Park, S., Lenzenweger, M.F., Pu¨schel, J., Holzman, P.S., 1996. Attentional inhibition in schizophrenia and schizotypy: a spatial negative priming study. Cognitive Neuropsychiatry 1, 125–149. Rado, S., 1960. Theory and therapy: the theory of schizotypal organization and its application to the treatment of decompensated schizotypal behavior. In: Scher, S.C., Davis, H.R. ( Eds.), The Outpatient Treatment of Schizophrenia. Grune and Stratton, New York, pp. 87–101. Robins, L.N., Helzer, J.E., Croughan, J., Ratcliffe, K.S., 1981. National Institute of Mental Health Diagnostic Interview Schedule: its history, characteristics, and validity. Archives of General Psychiatry 38, 381–389. Saykin, A.J., Gur, R.C., Gur, R.E., Mozley, D., Mozley, L.H., Resnick, S.M., Kester, B., Stafiniak, P., 1991. Neuropsychological function in schizophrenia: selective impairment in memory and learning. Archives of General Psychiatry 48, 618–624. Saykin, A.J., Shtasel, D.L., Gur, R.E., Kester, D.B., Mozley, L.H., Stafiniak, P., Gur, R.C., 1994. Neuropsychological deficits in neuroleptic naive patients with first-episode schizophrenia. Archives of General Psychiatry 51, 124–131. Schacter, D.L., Wagner, A.D., Buckner, R.L., 1999. Memory systems of 1999. In: Tulving, E., Craik, F.I.M. (Eds.), Handbook of Memory. Oxford University Press, New York, in press. Spielberger, C.D., 1983. Manual for the State–Trait Anxiety Inventory. Consulting Psychologists Press, Palo Alto, CA. Stangler, R., Printz, A., 1980. DSM-III: psychiatric diagnosis in a university population. American Journal of Psychiatry 137, 937–940. Strauss, M.E., 1993. Relations of symptoms to cognitive deficits in schizophrenia. Schizophrenia Bulletin 19, 215–231. Voglmaier, M.M., Seidman, L.J., Salisbury, D., McCarley, R.W., 1997. Neuropsychological dysfunction in schizotypal personality disorder: a profile analysis. Biological Psychiatry 41, 530–540. Wechsler, D., 1981. Wechsler Adult Intelligence Scale-Revised ( WAIS-R) Manual. The Psychological Corporation, New York.
Auditory working memory and verbal recall memory in schizotypy M.F. Lenzenweger, Ph.D. a, *, J.M. Gold, Ph.D. b a Department of Psychology, Harvard University, 33 Kirkland Street, Cambridge, MA 02138, USA b Maryland Psychiatric Research Center and University of Maryland, Baltimore, MD, USA Received 16 April 1999; accepted for publication 14 June 1999
Abstract Deficits on verbal memory tasks, as well as on spatial and auditory working memory tasks, have been observed in schizophrenia patients. A useful strategy in the determination of the premorbid indicator status of specific cognitive and memory deficits observed in patients is to examine those persons at increased biological risk for schizophrenia (e.g. first-degree relatives), schizotypal personality disorder patients, and/or psychometrically identified schizotypes for comparable deficits, though perhaps less profound than those seen in actual patients. We examined verbal memory and auditory working memory functioning in 31 schizotypic and 26 normal control subjects from a large randomly ascertained non-clinical university population. Schizotypy status was determined psychometrically using the wellknown Perceptual Aberration Scale. Contrary to our theory-guided expectations, noteworthy deficits in verbal memory and auditory working memory were not observed in the schizotypic subjects and the two experimental groups did not differ significantly on any of the memory measures. These results were discussed in light of prior results obtained using the spatial delayed response task (i.e. spatial working memory) and Wisconsin Card Sorting Test performance on these same subjects. The theoretical implications of these findings are discussed in relation to the putative processes involved in the working memory system, as well as in relation to the schizotypy construct. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Auditory working memory; Memory; Recall; Schizophrenia; Schizotypal personality; Schizotypy; Verbal memory
1. Introduction Prior research has documented that schizophrenia patients reliably display evidence of a basic compromise in the ability to learn and retrieve new information (Saykin et al., 1991). Learning deficits have been documented in neuroleptic naive first episode samples, reducing concern that results * Corresponding author: Tel.: +1-617-495-9359; fax: +1-617-495-3728. E-mail address: [email protected] (M.F. Lenzenweger)
obtained from chronically treated populations simply reflect the potential negative impact of antipsychotic and anticholinergic medications on memory performance (e.g. Saykin et al., 1994). Deficits have been observed on both relatively effortful free recall tasks, as well as on tasks that make less of a demand on strategic encoding and retrieval processes, such as recognition and frequency estimation tasks (Gold et al., 1992). These behavioral findings have frequently been interpreted as implicating frontal and temporal lobe abnormalities, an inference consistent with neuroimaging and post mortem findings involving these regions
0920-9964/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S0 9 2 0 -9 9 6 4 ( 9 9 ) 0 0 12 1 - 8
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(Bogerts, 1997; Goldman-Rakic and Selemon, 1997). Direct evidence supporting this inference was found in a recent PET study that demonstrated that patents show abnormalities including frontal hyperactivity combined with a failure to augment hippocampal activity during memory retrieval (Heckers et al., 1998). Thus, there is reason to believe that disturbed memory function in schizophrenia is an indicator of one of the central neurobiological abnormalities of the disorder (Gold et al., 1992), though the possibility of a generalized deficit in schizophrenia should always be kept in mind as well. Another area of active inquiry in schizophrenia concerns the working memory system (Baddeley, 1986, 1998) and the potential relations between dysfunction in working memory and symptom development in the illness (Goldman-Rakic, 1994). Working memory may be thought of as a system for temporarily maintaining information in order that the information can be used subsequently to guide behavior (Baddeley, 1986, Baddeley, 1998). Park and Holzman (1992, 1993) have demonstrated the existence of spatial working memory deficits in both schizophrenia patients and their biological first-degree relatives. Gold et al. (1997) developed a task of working memory for the auditory modality and also found evidence of deficits on this measure of auditory working memory in schizophrenia patients. These data suggest that a deficit in working memory, assessed in two different modalities, may be an important feature of schizophrenia, and potentially in their relatives. Taken together, the available data on verbal memory and working memory in schizophrenia suggest that each of these memory systems is disrupted in the illness. Perhaps, more importantly, they further suggest the possibility that illumination of the pathology of these systems may hold promise for specifying those processes that may be important to the pathogenesis of schizophrenia, or at least some dimension of schizophrenia. One of the features of some of the memory data (e.g. auditory working memory) discussed thus far, however, is that these studies have been confined to the study of clinically affected cases, i.e. persons who have already expressed schizophrenia. The
interpretation of data derived from patients is, of course, complicated and limited in terms of generalizability by the well-known third-variable confounds attending the study of expressed schizophrenia [i.e. deterioration, institutionalization, and motivation effects; see Lenzenweger (1998)]. More importantly, perhaps, one must be aware of the limited contribution data from expressed cases of the illness can make to the establishment and understanding of the premorbid indicators (or early expressions) of underlying liability for schizophrenia. This pattern of empirical relationships, as well as a desire to determine if memory deficits can be detected in non-psychotic, but schizotypic subjects, suggested a question for further study in research on schizotypy. The study of the schizotype, conceptualized as an alternative expression of schizophrenia liability, can be undertaken from three distinct vantage points. Namely, schizotypic subjects may be defined as (a) biological relatives of persons affected with schizophrenia, (b) those persons diagnosed with DSM-IV schizotypal personality disorder (PD), or (c) those persons who display deviance on a laboratory measure known to be associated with schizophrenia liability (e.g. psychometric measures) (Lenzenweger, 1994, 1998). Prior work focusing on either psychometrically identified [strategy (c)] or clinical [strategy (b)] schizotypes has been limited and characterized by the use of typically only one memory measure per study (LaPorte et al., 1994; Lyons et al., 1995; Voglmaier et al., 1997; Bergman et al., 1998), with no prior study examining multiple memory measures in the same clinical or psychometrically identified schizotypic subjects. Two studies have examined multiple memory measures in the biological relatives of schizophrenia patients [strategy (a)] (Cannon et al., 1994; Faraone et al., 1995). Upon testing with extensive neuropsychological test batteries, Faraone et al. (1995) found verbal memory deficits (i.e. logical memory for story material ) among the relatives of schizophrenia patients compared with controls, and Cannon et al. (1994) found the siblings of schizophrenia patients performed worse on verbal and spatial memory measures relative to controls. The incremental value of a study in which multiple memory systems
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were evaluated using multiple memory measures appeared noteworthy to the present investigators. The current study used the psychometric strategy [strategy (c), deviance on a laboratory measure] in detecting schizotypic persons and sought to determine whether such individuals would display evidence of both recall memory and auditory working memory deficits consistent with what has been observed in the study of schizophrenia patients. Furthermore, the subjects for the current study were also assessed on a measure of spatial working memory (Park et al., 1995), thus allowing for an important evaluation of relations among verbal recall, auditory working memory, and spatial working memory.
2. Method 2.1. Subjects Subjects for the present study were drawn from a randomly ascertained sample of first-year undergraduates at Cornell University who voluntarily completed a 250-item psychological inventory entitled ‘Attitudes, Feelings, and Experiences Questionnaire’ that included the Perceptual Aberration Scale (PAS; Chapman et al., 1978; see below for detail ). We chose this approach in order to maximize diversity within our pool of potential study subjects, as well as to minimize the effects of both subject self-selection factors and grouprelated test-taking attitudes often found in introductory psychology course-based sampling procedures. A total of 2000 individuals were initially selected at random from a university roster of all first-year students who entered during a recent fall semester (approximately 3000 students per year). A team of research assistants individually approached each of the potential study participants and asked them to voluntarily complete the psychological inventory noted above. The subjects were informed that their inventory responses would remain completely confidential and would be used for research purposes only. Study subjects were asked to complete the inventory within 48 h and the completed inventories were picked up by study staff in sealed
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envelopes. Of the 2000 potential subjects, 1684 (51.3% women, 48.7% men) completed the inventory. The response rate of 84.2% is consistent with representative sampling ( Kalton, 1983). To control for pseudo-random responding and invalid test-taking attitudes, a 14-item version of Jackson’s (1984) Infrequency Scale from his Personality Research Form was included in the 250-item screening inventory. Subjects scoring greater than three on the Infrequency Scale were dropped from the sample; 35 (2.1%) were excluded from our sample on this basis. Three additional subjects were dropped because of extensive missing data on the inventory. The final sample consisted of 1646 cases, from which two subject groups were composed for the experimental assessments described below. Separate group means and standard deviations for males and females on the PAS were computed and served as the basis for subject selection. Following Chapman and Chapman (1985), high PAS subjects were required to have scored at least 2.0 standard deviations above the group mean on the PAS, whereas normal controls were required to have scored no higher than 0.5 standard deviations above the group mean. Study subjects for each of the two groups were selected at random from the two sub-samples of subjects meeting the specified criteria. Testing was carried out blind to the group membership. A total of 26 (14 female) normal control subjects and 31 (16 female) high PAS subjects were tested. The proportions of male and female subjects across the two subject groups did not differ significantly [X2 (1, N=57)=0.03, p=n.s.]. The mean ages of the high and low PAS subjects were 19.00 years (SD=0.52) and 18.96 years (SD=0.53) respectively. The mean PAS scores of the high and low PAS subjects were 19.77 (SD=6.35) and 0.77 (SD=0.99) respectively. There were no differences among the two groups in terms of agreement to participate in the study described below. Although the individuals contained in the pool of 1646 potential study subjects had been preselected initially for academic achievement (i.e. university admission), academic ability does not preclude a risk for psychopathology (see Stangler and Printz, 1980; Depue et al., 1989). The population from which the sample was drawn was most probably somewhat biased against particularly
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early-onset variants of severe psychopathology. However, one would not necessarily anticipate any diminution in the prevalence of schizophrenia spectrum-related personality disorders in the undergraduate population studied (Lenzenweger et al., 1997).
inventory used to measure depressive/dysphoric symptoms in the study subjects. The State–Trait Anxiety Inventory ( Form Y; Spielberger, 1983) is a well-known 40-item selfreport inventory was used to measure state and trait anxiety in the study subjects.
2.2. Schizotypy measure
2.4. Cognitive processing speed and general intellectual functioning measures
The PAS is the well-known 35-item true–false self-report measure of disturbances and distortions in perceptions of body image and of other objects (Chapman et al., 1978). It includes items like ‘Occasionally I have felt as though my body did not exist’ (keyed true) and ‘I have never felt that my arms or legs have momentarily grown in size’ (keyed false). Extensive literature reviews bearing on the reliability and validity of the PAS as schizotypy (or, perhaps more broadly, psychosisproneness) measures can be found elsewhere (Chapman et al., 1995; Edell, 1995; Lenzenweger, 1994, 1998). We chose the PAS for this study because of the importance attached to body-image and perceptual distortions in theoretical views of schizotypy (Rado, 1960; Meehl, 1964). Rado (1960, pp. 88, 90) viewed such distortions as deriving fundamentally from the putative proprioceptive (kinesthetic) diathesis hypothesized to be one of the two basic dimensions of pathology underlying schizotypal personality organization. Meehl (1964, pp. 24–27) identified body-image aberrations as a schizotypic sign in his ‘Manual’, which provides rich descriptions of the clinical manifestations of such phenomena. In addition to the work of Rado (1960) and Meehl (1964), perceptual and body-image distortions as phenomenological manifestations of schizophrenia (and other psychoses) have a long history in descriptive psychopathology, and this history has been reviewed extensively by Chapman et al. (1978). Therefore, as a measure of body image distortions and perceptual aberrations, we are suggesting that the PAS taps at least some of the symptoms of schizotypy. 2.3. Psychological state measures The Beck Depression Inventory (BDI; Beck et al., 1961) is a well-known 21-item self-report
A focal assessment of overall cognitive processing speed in the study subjects was done using the Digit Symbol subtest of the Wechsler Adult Intelligence Scale-Revised ( WAIS-R) ( Wechsler, 1981). In addition, every subject provided us with a formal release of information that allowed us to obtain their official Scholastic Aptitude Test (SAT ) scores, verbal and quantitative, from their Cornell University record. All participants were given the self-administered computerized screening version of the Diagnostic Interview Schedule (DIS-Screen; Robins et al., 1981) to assess lifetime presence of several psychopathological conditions, namely major depression– dysthymia, mania–hypomania, and schizophrenia– schizophreniform psychosis. No participant in either group met definite criteria for an affective disorder or schizophrenia–schizophreniform psychosis. 2.5. Procedures and memory tasks Potential study participants were contacted by telephone and were invited to participate voluntarily in a study of ‘Young Adult Development’ for which they would receive $50.00. A complex coding scheme was employed to disguise the group status of the subjects and all study staff were blind to a subject’s group membership throughout the study. The subjects completed the schizotypy, psychological state, and memory measures, along with other laboratory measures described in other reports (e.g. thought disorder, Coleman et al., 1996; antisaccade performance, O’Driscoll et al., 1998; working memory, Park et al., 1995). Subjects were tested in a quiet darkened room, the study measures were counterbalanced for administration order, and all subjects gave informed consent.
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2.6. Memory tasks 2.6.1. Verbal memory (recall) measures Each subject received three trials of a 38 word list for immediate recall and a delayed recall trial that followed approximately 20 min after the third recall trial. The word list was adapted from those used in Gold et al. (1992). The lists were composed of five exemplars from each of six taxonomic categories that were constructed so that related items never appeared consecutively. The first and last four items on the list were drawn from eight other taxonomic categories so that primacy and recency items were not semantically related to other list items. 2.6.2. Letter–number (LN) span task The LN span task, developed by Gold et al. (1997), involves the auditory presentation by an examiner of a mixed series of alternating numbers and letters. The task has been conceptualized as a test of auditory working memory (Gold et al., 1997). The subject is asked to respond by first saying the numbers in order from the smallest to largest, followed by saying the letters in alphabetical order. For example, a subject would hear ‘w7t4’, and the correct answer is ‘47tw’. Following a series of practice trials, the test involves four trials at each string length, beginning with twoitem strings (such as ‘m3’) and proceeding up to seven-item strings (such as ‘c7g4q1s’) for a total of 24 items. The total number of correct responses is then computed out of a possible total of 24. The test is terminated when a subject fails all four trials at any one string length. The internal consistency of the LN span is high (a=0.85) and, in terms of criterion validity, the LN span association with prominent neuropsychological and cognitive measures, among schizophrenia patients, appears robust, even when the effects of IQ and general memory ability are removed (Gold et al., 1997). 2.6.3. Preliminary pilot evaluation of memory measures In order to ensure that both the verbal memory and LN span tasks were sufficiently difficult for the undergraduate subjects to be tested in the current study, a pilot study was undertaken involv-
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ing 27 randomly selected university undergraduate students. Each of the 27 students completed both the verbal memory and LN span tasks, counterbalanced for order of administration, and an examination of the means and distributions for the tasks revealed that the student subjects, as a group, were not performing at or near the ceiling on any of the measures. These data may be made available upon request. 2.6.4. Statistical analysis The verbal memory trials, four total, were scored simply as the total number of correct items recalled. These data were analyzed using a repeated measures analysis of variance (ANOVA) approach, with one between-subjects factor (group, two-levels) and one within-subjects factor (trial, three-levels). The fourth trial of the verbal memory measure was treated as a separate measure of delayed recall. For the LN span, two performance scores were computed. The first was the total number of correct trials achieved, out of 24 possible, and the second was the highest string length attained, where at least one item of that string length was passed. Correlational analyses were conducted using the Pearson product-moment correlation coefficient. Effect-size estimates were computed as per Cohen (1988); for the ANOVA analyses the effect size is reported as partial g2 and for the t-test, Cohen’s d is used.
3. Results The means and standard deviations for the verbal memory and auditory working memory tasks are contained in Table 1. The repeated measures ANOVA for the verbal memory task revealed a significant main effect for trial [F(2, 110)=46.08, p<0.001; effect size (partial g2)=0.46 ], but neither the main effect for group [F(1, 55)=0.002, p= 0.96; effect size (partial g2)=0.000] or the group by list interaction [F(2, 110)=0.35, p=0.71; effectsize (partial g2)=0.006 ] were statistically significant. A t-test comparison of the two groups on the delayed recall trial of the verbal memory task
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Table 1 Means and standard deviations for the verbal memory and auditory working memory measuresa Schizotype (n=31)
Controls (n=26)
Mean
SD
Mean
SD
higher levels of state-anxiety ( p<0.001), traitanxiety ( p<0.001), and dysphoric (BDI ) features ( p<0.001) relative to controls. However, none of the memory indexes was correlated significantly with state-anxiety, trait-anxiety, or depression scores (all p>0.20).1
Verbal recall Trial 1 Trial 2 Trial 3 Delay trial
15.29 19.58 21.65 25.58
5.32 5.19 5.76 4.63
14.73 19.35 22.27 24.58
3.40 5.05 6.84 5.15
3.2. Relations with spatial working memory (delayed response task; DRT) and Wisconsin Card Sorting Test (WCST) performance (Park et al., 1995)
LN span Total correct Longest string
18.16 6.45
2.44 0.62
18.88 6.62
2.53 0.57
Measure
a The final trial of the verbal memory task was a delayed recall trial (delay trial ), whereas trials 1, 2 and 3 were immediate recall. Values for the verbal recall trials are the total number of words correctly recalled out of a possible 38. Longest string indicates the longest string length at which at least one item on the LN span was passed correctly.
was non-significant [t(55)=0.78, p<0.44; d= 0.20]. For the LN span, the two groups performed virtually identically for both the total number of correct responses and the longest string achieved. For the total correct on the LN span [t(55)=1.10, p=0.278; d=0.29] and for the longest string achieved [t(55)=1.03, p=0.310; d=0.29]. With respect to the relations between the LN span and performance on the four verbal memory trials, there were no statistically significant correlations between with the LN span total score or LN span longest string achieved score and any of the four verbal memory trials. 3.1. Intellectual functioning and psychological state analyses In terms of general intellectual functioning, the schizotypic subjects did not differ significantly from the controls on either the SAT Quantitative ( p>0.80) or SAT Verbal ( p>0.52) scores. With respect to speed of processing, there was a nonsignificant trend for the schizotypic subjects to have lower digit symbol raw scores [t(55)=1.71, p<0.10]. As would be expected, based on model of Meehl (1990), schizotypic subjects did display
As noted above, the subjects in this study were also evaluated for performance on a DRT known to assess spatial working memory, as well as on the WCST ( Heaton, 1981) (Park et al., 1995). Park et al. (1995) found that the schizotypic subjects in this sample displayed significantly lower accuracy on the spatial working memory task, as well as an increase in the failure to maintain set ( FMS) variable on the WCST. The availability of these data presented the opportunity to examine auditory working memory in relation to spatial working memory and WCST performance in the same subjects. The DRT accuracy score was minimally related to the LN span total score (r=0.09), whereas DRT performance was significantly associated with the longest string achieved on the LN span (r=0.32, p<0.02, two-tailed ). The LN span total score was correlated with the WCST FMS score (r=−0.20, p<0.15, two-tailed ); LN span longest string achieved was correlated with the FMS score (r=−0.13, p<0.33). We note also that the LN span total score was correlated 0.25 ( p<0.07, two-tailed ) with the WCST categories completed score; LN span longest string achieved was correlated 0.13 ( p<0.35, two-tailed ) with the WCST categories completed score.
4. Discussion The primary results of this study reveal that schizotypic subjects, selected on the basis of 1 The psychological state data both across the groups and in relation to the memory indexes have been presented in summary form. The complete set of means, standard deviations, t-tests, correlations, and associated p-values may be requested from the authors.
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psychometric deviance on the PAS, do not differ from control subjects on measures of verbal recall memory and auditory working memory. The effect sizes associated with group membership in relation to recall memory were essentially zero, whereas the effect sizes for the LN span were larger, though still small by accepted standards (Cohen, 1988). In order to place the LN span findings into a more readily understood context, in order to detect the effect that we observed for the LN span correct with 80% power and to have it be significant at the 0.05 level would have required 188 subjects in each subject group (376 total ). Clearly, neither verbal recall memory or auditory working memory appear to be associated with psychometrically identified schizotypes. The failure to find subtle verbal memory and/or auditory working memory deficits in the schizotypes is inconsistent with the memory literature for schizophrenia patients, which suggests verbal memory (Gold et al., 1992) and auditory working memory (Gold et al., 1997) deficits are present in clinically affected individuals. Our findings are especially interesting in light of the fact that positive, but not negative, symptoms are most closely related to auditory processing deficits in schizophrenia (Strauss, 1993) and one might arguably consider the PAS to assess a positive symptom-like form of phenomenology. Moreover, the failure to find differences between the schizotypes and controls on the two memory tasks is generally inconsistent with the prevailing pattern of results in the schizotypy research area, wherein the modal finding in such studies is that schizotypes do usually differ from controls on a task of interest and schizotypic performance is usually consistent with, albeit in attenuated form, deficits seen in schizophrenia patients (see Lenzenweger, 1998). The challenge to us, therefore, has been to try to understand our results for the verbal memory and auditory working memory measures and extract meaning and direction from them. Our findings for auditory working memory provide us with an interesting pattern of results when combined with those reported previously by Park et al. (1995) using the same subjects. Whereas the schizotypes in this study did display a significant difference from normal controls on the DRT task,
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which is suggested to be a measure of visual– spatial working memory, the same subjects did not display a deficit on a task of auditory working memory (LN span). Moreover, for those subjects who completed both the LN span and the DRT, the performance accuracy on the DRT was not correlated with overall accuracy on the LN span, but it was correlated with the longest string passed successfully on the LN span. Performance on the LN span was uncorrelated with the FMS variable from the WCST, which was also completed by these same subjects. At a minimum, this general pattern of results suggests less of a connection (or diminished association) between the LN span and the other measures putatively involved with working memory assessed in the visual modality (i.e. the DRT and WCST ). In attempting to better understand our current results, we have considered the following possibilities: namely modality-based differences across tasks, the processes tapped by the measures under consideration, differences in the progressive impairment of memory systems, and the nature of psychometrically assessed schizotypy. First, regarding the modality-based differences issue, it is clearly evident that the aspect of working memory tapped by the DRT (Park et al., 1995) is fundamentally involved with the visual processing nature of the task. The visual–spatial DRT may involve activation of the so-called visuo-spatial sketchpad in the tripartite model of working memory suggested by Baddeley (1994), whereas the LN span may involve the activation of the so-called phonological loop of the tripartite working memory system. In this view, one might argue that our results suggest that the psychometrically identified schizotypes have a modality specific working memory deficit, which involves the visual– spatial sketchpad (or channel ) but not the phonological loop. A complication in this view, however, concerns the fact that both the DRT and LN span are sufficiently demanding tasks and, presumably, they both should make demands on (or involve) the ‘central executive,’ which is argued to subserve the coordination, manipulation, and updating of contents in the working memory slave sub-systems (Baddeley, 1998). It strikes us as somewhat odd to think that the central executive could function
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effectively for an auditory working memory task, but function ineffectively for visuo-spatial information (i.e. DRT ) in the same people. How then to best understand these data? One could consider the possibility that the two tasks (DRT versus LN span) each represent one of two types of working memory task, that is a task that requires storage, maintenance, and evaluation of representations (i.e. ‘maintenance’ tasks) versus those that also require manipulation and updating of the contents of working memory (i.e. ‘maintenance+’ tasks) (see Schacter et al., 1999). From this standpoint, we might suggest that schizotypes have reliable deficits on the first type of working memory task (operationalized as the DRT ), but do not have deficits on the second type of working memory task (operationalized as the LN span). However, from this standpoint, it is somewhat difficult to conceptualize poor performance on a task that requires only maintenance functioning (e.g. DRT ), but uncompromised performance on a task that calls for maintenance plus manipulation functioning (e.g. LN span) in the same schizotypic subjects. Alternatively, one could also consider the possibility that central executive processes could be impaired on a modality specific basis. An alternative speculation regarding these results would rely on the concept of disinhibition, which has enjoyed increasing prominence in discussions of cognitive deficits in schizophrenia (e.g. Park et al., 1996; O’Driscoll et al., 1998). Other data from these same subjects is consistent with disinhibition as a characteristic of the psychometric schizotypes in terms of their functioning on neurocognitive tasks that require intact inhibitory functioning and are processed through the visual modality. For example, in this sample of subjects the psychometric schizotypes reveal increased tendency to lose set on the WCST, increased antisaccade errors, and poorer smooth pursuit eye tracking (O’Driscoll et al., 1998). Therefore, one might differentiate the processes tapped respectively by the DRT and the LN span. One could consider that possibility that performance on the visual–spatial DRT is actually better conceptualized as an index of disinhibition. That is, the DRT involves holding target information over a filled delay, perhaps providing for greater opportunity
for distraction, drift, or interference from prior trials. The LN span, on the other hand, involves discrete trials and no delay period, allowing for less involvement of disinhibitory effects. A third alternative to consider would involve the point in the developmental progression of the putative schizophrenia-related process observed in these subjects in relation to auditory working memory and verbal memory. It may be, perhaps, that one might only see auditory working memory and verbal (semantic) memory deficits after a clinical illness began to express itself in a more definitive manner. That is, perhaps auditory working memory and verbal (semantic) memory deficits are most noted only once an illness has begun to unfold in patients. If, however, one were to detect such deficits in the non-psychotic biological relatives of schizophrenia patients, then such evidence would tend to argue against this view. Verbal memory deficits (i.e. logical memory for story material ) have been found among the relatives of schizophrenia patients (Cannon et al., 1994; Faraone et al., 1995), and auditory working memory deficits have yet to be studied in firstdegree biological relatives of schizophrenia patients. Therefore, data are not yet available from relatives to address directly the verbal and auditory working memory measures used in this study. Finally, we must consider the possibility that psychometrically assessed schizotypy does not overlap perfectly with the construct of schizophrenia liability. It could very well be the case that the construct defined by psychometric schizotypy, at least insofar as it is assessed with the PAS, does not capture all aspects of schizophrenia liability. Thus, psychometric schizotypy is but an imperfect measurement of the true latent construct of schizophrenia liability. It is also conceivable that the PAS possesses some appreciable measure of validity with respect to underlying schizophrenia liability, as indicated by the multitude of findings on high PAS subjects that are highly comparable to what is observed in clinical schizophrenia patients [see Lenzenweger (1998) for review], yet the scale generates an admixture of true-positive cases for schizophrenia liability as well as false-positive cases whose PAS scores are not reflective of genuine schizotypy. In the absence of a gold standard for
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schizophrenia liability (e.g. a gene or genes), such a conjecture is difficult to evaluate empirically. The weight of the evidence from prior studies using the PAS, however, is against this particular explanation of the results obtained (see Lenzenweger, 1998). In summary, the present study did not find evidence of verbal memory or auditory working memory deficits in psychometrically identified schizotypes. The effect-size estimates, particularly for the verbal memory measures, suggest the absence of group differences on the memory measures was not due to unduly small groups; moreover, the sample sizes used in this study were comparable to those used consistently in this line of research. We have offered several alternative interpretations of these data in relation to other data we have available on the same subjects. This study has provided us with additional useful information regarding schizotypy and may best be viewed for its heuristic value.
Acknowledgements We thank Daniel Schacter, Ph.D., for his helpful comments regarding working memory. We also thank Michael Raulin, Ph.D., and an anonymous reviewer for their helpful comments on an earlier version of this article.
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