Left-handedness in male schizophrenic patients is associated with increased impairment on the Luria-Nebraska neuropsychological battery

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Left-Handedness in Male Schizophrenic Patients Is Associated with Increased Impairment on the Luria-Nebraska Neuropsychological Battery William ~-). Faustman, James A. Moses, Jr., David L. Ringo, and John W. Newcomer*

Several studies suggest increased mixed and left-handedness in schizophrenia. This is of interest as early cerebral injury can result in increased left-handedness and some investigations have suggested a role for early developmental insult (e.g., birth complications) in schizophrenia. We administered the Luria-Nebraska Neuropsychological Battery (LNNB) to 24 left-handed male schizophrenic patients and a separate group of 24 right-handed schizophrenic patients who were age and education matched to the left-handed patients. The test protocol also was administered to 15 left-handed nonpsychiatric control subjects and 15 right-handed controls. Direct comparisons (t-test) of the left- to right-handed schizophrenics revealed that the left-handed patients showed significantly greater impairment on several LNNB measures sensitive to cognitive deficits in schizophrenia. There were no differences between left- and right-handed control subjects. A further 2 x 2 ANOVA pooling all subjects noted several significant interactions between handedness and diagnostic group. The findings suggest a unique interaction between left-handedness and neuropsychological impairment in schizophrenia and couM support a relationship between left-handedness, early cerebral insult, and cognitive deficits.

Schizophrenia may represent a disorder with multiple etiologies. Variables that may interact or indepe~.:lently contribute to the development of the disorder include obstetric and birth complications (Lewis and Murray 987) and prenatal viral infection (Mednick et al 1988). Neuroimaging studies have rel~eatedly elicited evidence for structural pathology (see Andreasen 1988, for a review), although the etiology of this finding remains obscure. Moreover, repeated works (see Levin et al 1989, for a review) using neuropsychological tests sensitive to cognitive impairment in neurologic samples have shown a high rate of cognitive impairment in schizophrenia. In general, there is growing acknowlFrom the Department of Psychiatry and Behavioral Sciences, Stanford Uniyersity School of Medicine, Stanford, California; and the Department of Veterans Affairs Medical Center, Polo Alto, California. *JW Newcomer is presently with the Department of Psychiah-y, Washington University School of Medicine, St. Louis, MO 63110. Address reprint requests to William O. Faustman, Ph.D., Psychology II6B, VA Medical Center, 3801 Miranda Ave., Polo Alto, CA 94304. Received September 20, 1990; revised March 1, 1991.

Published 1991 by Elsevier Science Publishing Company, Inc.

ISSN/91/$0.00

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edgment that schizophrenia may in part represent a neurodevelopmental disorder with origins in prenatal development and birth complications. Linking patterns of biologic pathology to specific patient characterig:~,:s may help clarify the factors that underlie the disorder. One interesting subgrouping technique for schizophrenia research is to evaluate patterns and relationships of handedness. Several studies have suggested that the base rate of left-handedness is elevated in patients wi'd, schizophrenia. Gur (1977) noted an elevated rate of left-handedness in schizophrenic inpatients compared to a normal control sample. Nasrallah et al (1981) found that 17.8% of 84 male schizophrenics used the left hand for writing while 6.1% of a control group were left-handed. Oddy and Lobstein (1972) also suggested increased left-handedness among schizophrenic patients. Luchins et al (1979) found left-handedness to be associated with a milder form of schizophrenia. Shan-Ming et al (1985) noted than both ~ale and female schizophrenic patients showed increased left-handedness incidence ::elative to samples of manic-depressive patients. Hauser et al (1985) demonstrated ~'.:: ~:lore female than male schizophrenics are left-handed. Though Shimizu et al (1985) f~, :,d no increase in left-handedness in schizophrenia, there was an elevated rate of conv~::~ted right-handedness. Green et al (1989) performed a well-designed recent study that used a comprehensive test of handedness in 93 schizophrenic patients and 105 normal control subjects. The schizophrenic patients displayed a shift away from right-handedness ~ I towards mixed handedness. Other studies have examined the relationship between hanaedness in schizophrenia and presenting symptoms. Taylor et al (1982) found that ha~ *aess was generally unrelated to symptom presentation in 232 patients. Merrin ( 1 9 ~ j ~,~oted that among paranoid schizophrenic patients there was an association between left-handedness and inferior social competence. Ban" et al (1989) demonstrated that patients with a strong standard-dominance pattern may be more prone to developing tardive dyskinesia, while patients with more anomalous dominance were less prone to show tardive dyskinesia. However, other work (McCreadie et al 1982) suggested that mixed or left-handedness is linked with higher rates of tardive dyskinesia. Recent research evaluated the relationship between handedness and psychosis-proneness in over 7,000 college students (Chapman and Chapman 1987a). htt~restingly, there was an increase in ambilateral (mixed) handedness among subjects scoring high on self-report measures sensitive to psychosis-proneness. Severai studies have failed to note elevated rates of left-~,andedness in schizophrenia (e.g., Lishman and McMeekan 1976; Wahl 1976), yet a review of the literature shows that numerous published studies suggest increased mixed or left dominance in schizophrenia. The exact meaning of this finding is of interest. One intriguing explanation may be the observation that early cerebral injury may be associated with an increase in mixed or left-handedness (Kmsboume 1987). Accordingly, an increase in left-handedness may reflect a developmental neurologic insult to the normally dominant left hemisphere. An additional line of thinking suggests that schizophrenia may involve a specific disorder of the left hemisphere (Flor-Henry 1976; Abrams and Taylor 1979). Biological studies using neuroimaging and neuropsychologic measures have been used to further elucidate the importance of left-handedness in schizophrenia. Pearlson et al (1989) noted that a history of an abnormal birth delivery and the presence of lefthandedness were predictors of increased ventricle-brain ratio on computed tomography (CT) scans of schizophrenic outpatients. Katsanis and Iaeono (1989) examined CT scans

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and cognitive testing in 51 right-handed and 12 left-handed schizophrenic patients. Their left-handed patients showed significantly larger ventricle-brain ratios and tended to show greater impairment on a series of neuropsychological tests that included the Wisconsin Card Sorting Test and the Wechsler Adult Intelligence Scale-Revised. In an effort to expand and replicate these findings, we analyzed cognitive test performance in relatively large (n = 24 per group) samples of left- and right-handed schizophrenic patients. Patients were administered the Luria-Nebraska Neuropsychological Battery (LNNB), a broadscope measure of higher cortical functions that is sensitive to impairment in neurologic and psychiatric populations (Moses et al 1983). Methods ~rhe subjects were a total of 48 male schizophrenic patiems (24 each left- and righthanded) treated at the Department of Veterans Affairs Medical Center, Palo Alto, California. A total of 22 of the left-handed patients and 20 of the right-handed patients were studied during inpatient treatment whi[~ the remaining patients were studied as outpatients. The present study also included a sample of 30 male (15 each left- and right-handed) nonpsychiatric control subjects in order to test whether potential performance differences betv,een left- and right-handed individuals are unique to schizophrenia. Data were extracted from the database of the Psychological Assessment Unit in the Psychology Service at our medical center. Institutional review board approval has been granted for the research use of this database. This database contains testing results for patients referred for psychological testing from throughout the hospital (multiple inpatient units, outpatient clinics). Some patients in this database were referred for testing from a research unit (StanfortffVA Mental Health Clinical Research Center), while others represent routine clinical referrals from a broad array of psychiatric referral sources. All patients at our medical center who are referred for testing are routinely given the LNNB, so a selection bias based on what patients received this cognitive battery is unlikely. A review of this data base revealed a total of 24 left-handed patients with a diagnosis of schizophrenia. Handedness was determined by asking the patient which was the preferred hand for writing, with additional follow-up questioning regarding whether the patient had ever preferred to use the other hand. Patients who recalled ever changing the hand preference for writing were not included in the present analysis. The self-report of hand preference was confirmed by observing hand preference during the writing and drawing items of the LNNB. A comparison group of 24 right-handed, age- and education-matehed schizophrenics was formed. None of the schizophrenic patients had chart histories of significant head injury or other diagnosed neurologic disorder. The ethnic composition of the right-handed schizophrenic group was as follows: 19 white, 4 black, 1 Hispanic. The ethnic composition of the left-handed schizophrenic patients was 17 white, 5 black, 1 Asian, and 1 Hispanic. The 30 nonpsychiatdc controls consisted of a group of 15 left-handed subjects and an equal number of age- and education-matched right-handed participants. Control subjects were obtained from two sources. First, subjects were obtained from medical units at the Palo Alto VA Medical Center (n = 3 in right-handed control group, n = 12 in the lefthanded control group). These subjects had no central nervous system (CNS) involvement or condition that would directly interfere with performance on cognitive measures. Secondly, the nonpsychiatric subjects included a sample of community volunteers (n = 12

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Table 1. Demographic Characteristics of the Samples. Mean Values are Listed with Standard Deviations in Brackets. Schizophrenic patients

Age Age of Onset Education(years)

Non~mchiattic subjects

Left-handed n = 24

Right-handed n = 24

Left-handed n = 15

Right-handed n = 15

35.17 (9.38) 22.87 (6.44) 12.92(1.38)

35.96 (!0.30) 23.50 (3.86) 13.46 (1.25)

34.53 (11.25) -13.07 (3.73)

34.33 (12.21) -13.47 (2.87)

in right-handed control group, n = 3 in left-handed control group) who had no psychiatric or neurologic history and agreed to LNNB administration. All the control subjects were ethnically white. Diagnoses for the schizophrenic patients were obtained by a review of patient records by one of the investigators (JAM) in all cases. A subset of the total sample of schizophrenic patients also underwent a research diagnostic evaluation conducted at a clinical research center. The chart review showed that all patients met DSM-III criteria for schizophrenia except for one left-handed patient who was most recently studied and was diagnosed by DSM-IH-R criteria. A subset of the patients (13 of 24 fight-handed patients, 11 of 24 left-handed patients) also met Research Diagnostic Criteria [(RDC) Spitzer et al 1978] for schizophrenia. These patients were typically diagnosed based on a consensus of a clinical interview by a psychiatrist or psychologist and an independent interview by a trained research assistant/nurse using the Schedule for Affective Disorders and Schizophrenia (Endicott and Spitzer 1978). The remaining patients in the overall sample were not assessed using this procedure to obtain RDC diagnoses, as they represented clinical referrals to the Psychologies2 Assessment Unit. Table 1 displays demographic information for the samples. Left- and right-handed groups were closely matched for age and education, the two variables that most strongly influence level of performance on ~ e LNNB (Moses et al 1983). In addition, equal numbers of medicated (15 of 24) and treatment medication-free (9 of 24) schizophrenic patients were in the right- and left-handed schizophrenic patient groups. The LNNB was typically administered by one of the investigators (JAM) who has extensive testing experience with Lhis instrument. Performance was expressed in several ways consistent with other recent works using the LNNB (Faustman et al 1988; Faustman et al 1989). First, we examined the level of performance on the C2 (rhythm), CIO (memory), and CI 1 (intellectual processes) scales, as well as a mean of these three scales, a composite measure used in prior studies (Faustman et al 1988; Newcomer et al 1991). Prior work (Moses 1983; Faustman et al 1989) has noted that these three scales are sensitive to presence of cognitive impairment in schizophrenic samples. Research comparing schizophrenic to neurologic samples (Moses and Golden 1980) noted that both groups showed roughly equal levels of impairment on these three scales. We also used a global performance measure that represents the number of clinical scales, excluding C7 and C9 (writing and arithmetic) and including the S1 (pathognomonic) scale, that exceeded critical-level cutoff score. The critical level of the LNNB is an individualized, regression-based value computed from each subject's age and educational level (Moses et al 1983). We hypothesized a specific directional hypothesis that left-handed schizo-

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Table 2. Mean Values and Standard Deviations (in Parentheses) for the C2, CI0, and C11 (Rhythm, Memory, Intellectual Processes) LNNB Scales

Schizophrenicpatients LNNB measure

Left-handed

C2 (Rhythm) CI0 (Memory) CI 1 (Intellectual Processes) Mean of C2/CI0/CI 1 LNNBGIobal

63.50 (18.16) 63.67 (16.84) 62.96 (15.53) ¢~3.37 (13.66) 3.13 (2.74)

Right-handed 54.33 53.37 56.42 54.71 2.29

(17.87)* (13.80)* (12.96) (12.70)* (2.12)

Nonpsychiauic controls Left-ha~ed 47.93 42.93 46.80 45.89 0.87

(17.41) (10.12) (10.03) (8.98) (1.36)

Right-handed 40.13 (10.45) 44.20 (9.56) 44.87 (11.37) 43.07 (8.39) 0.27 (0.59)

A mean for the three scales represents a composite index of the measures. LNNB Global represents the number of clinical scales (excluding C7 & C9--writing & arithmetic) in addition to file Sl (patlmgnomonic) scale that exceeded critical cutoff levels for each patient. LNNB scales are expressed as T-scores; higher scmus indicate greater deficits since the test is scored for errors. Schizop~nic samples are n -- 24 in each of right- and left-handed groups. Nonpsycbiatric controls consist of two groups of 15 vatients each. ~ 2 × 2 ANOVA analysis (see text) supported an interaction between diagnos~c group membership and handedness for the C2 measure and the mean of the C2/CI0/CI! measures. *p < 0.05, based on one-tail~ t-rest comparison of left- versus rigbt-lmaded patients within each group.

phrenic patients, but not controls, would show greater deficits (higher scores, as the LNNB is scored for errors) than their right-handed counterparts. Data were analyzed by means of t-tests contrasting left and right-handed patients within each diagnostic group as well as e 2 x 2 ANOVA that pooled all patients. Results The results of the analysis are displayed in Table 2. T-test comparisons of the leftand right-handed schizophrenic patients showed that among the left-handers there was significandy greater impairment, on the C2 (rhythm) and C10 (memory) sc~es, as well as on the mea~i of the C2-CI0--CII scales. The C2-C10-4211 average is a commonly used index of L~,q~IB perfota~ace in schizophrenic samples (e.g., Faustman et al 1988), as these scales are particularly sensitive to cognitive deficit in schizophrenia (Fanstman et al 1989). There were no significant differences between the global levels (i.e., number of scales abo~e critical level) for the left- and righ~-handed schizophrenic groups. Performance levels for the LNNB measures were quite similar for left.- and righthanded nonpsych~,ic controls. Using the t-test comparisons, none of the measures showed a trend t~:ward~ group differences between left- and right-handed controls. Further statistical analysis involved a 2 x 2 analysis of variance ANOVA (main effects = handedness & diagnostic group) for each of the variables examined. A.highly significant main effect (p < 0.001) was obtained for diagnostic group membership for all variables, suggesting that for all measures the schizophrenic patients were more impaired when compared to nonpsychiatric controls. A significant (F = 4.93, p < 0.05) main effect for handedness was obtained for the C10 (memory) variable. Several significant two-way interactions were obtained in the ANOVA, supporting a unique interaction between handedness and diagnostic group. First, a significant interaction (F = 4.46, p < 0.05) was obteOned for the LNNB summary measure consisting of the mean of the C2 (rhythm), C1G (memory), and CI 1 (intellectual processes) scales. A significant interaction (F = 4.75, p < 0.05) was also noted for the C2 (rhytlh-n) variable. Interaction effects for the other meastaes were as follows: C10 (memory) F = 2.04, p = 0.16; Cl I

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(intellectual processes) F = 1.94, p = 0.17; Global (scales exceeding critical levels) F = 2.29, p = 0.13. Discussion The present study generally supports the notion that left-handedness may be an important marker for subgrouping schizophrenic patients. In the t-test analysis the left-handed schizophrenic patients demonstrated significantly greater impairment on the C2-ClOCII LNNB scales used in prior schizophrenia research (Fanstman et al 1988). These LNNB measures reflect a dimension of attention, information encoding and processing, and memorial functions (Moses et al 1983). Using a 2 x 2 ANOVA analysis we also noted a significant interaction for the C2-CI0-CI1 summary measure. The failure to note a difference between left- and right-handed schizophrenic groups on the LNNB global measure may have been due to variance restriction problems, as global scores tend to group from 0 to 3 for most patients. Using the direct t-test analyses, left-handed nonpsychiatric controls did not differ from right-handed controls, suggesting that the findings in schizophrenia were not due to left-handedness alone but .rather to an interaction between schizophrenia and left-handedness. The ANOVA results offer some further support for this conclusion. The present findings provide a replication and extension of similar results of Katsanis and Iacono (1989). One could speculate that our results complement prior works that demonsUate an increase in cognitive deficit in schizophrenic samples (see Levin et al 1989, for a review). As noted above, there is growing evidence that some forms of schizophrenia may be related to prenatal insult or birth injury (Mednick et al 1988; Lewis and Murray 1987). One potential outcome of early cerebral insult is an increase in mixed dominance and left-handedness. Multiple prior works have succx~sfully shown an increase in left-handedness in schizophrenia. The finding that left-handedness in schizophrenia is associated with greater cognitive impairment could lend support to a potential relationship between left-handedness, early cerebral insult, and increased level of neuropsychological deficits. Unfortunately, we did not have research data available on the incidence of birth injuries or obstetric complications in our patients. Further research in this area would benefit by adding such measures. In addition, further work would benefit from the use of nonschizophrenic psychiatric reference groups (e.g., mood disorder patients) to evaluate handedness differences. The current study may contain certain methodological shortcomings. We had sufficient numbers of only male patients to perform an analysis, so we are unable to generalize whether these findings extend to women. The nonpsychiatric control groups represented a mix of medical patients and community volunteers. A more homogenous group of noopsychiatric patients would have been preferable. However, we feel that it is legitimate to pool these different samples, as they represent nonschizophrenic samples who in all probability lack the elevated potential risk factors (e.g., prenatal and birth-related insult) that one could speculate as being present in producing the differences found in the schizophrenic patients. Further limitat20ns of the present study include the diagnostic and handedness assessment procedures. Standmdized research diagnostic procedures to obtain RDC diagnoses were only performed in approximately half of the patients in each handedness group, while a review of patient records was used for all the patients. Though chart records nmy not yield optimal research diagnoses, some work (i'?lcGlashan 1984) suggests that they

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can offer usable diagnostic information. Furthermore, it should be noted that VA schizophrenic samples usually contain chronic patients with well-documented histories who have records for multiple prior hospitalizations. Accordingly, the use of record review procedures appears to have validity. The current study contained a mixture of patients tested on and off neuroleptie medications, though each schizophrenic patient group contained an equal number of such patients. We screened for handedness using self-report with follow-up observation of writing preference during LNNB administration. Recent studies using more sophisticated handedness assessment (e.g., Green et al 1989) procedures (e.g., assessment of mixed-handedness) have demonstrated superior subgrouping and evaluation strategies. Unfortunately, we were not able to assess the degree of mixedhandedness in our patients. It should be noted, however, that some work (Chapman and Chapman 1987b) suggests that hand writing preference usually identifies handedness correctly. Despite the aforementioned limitations of the present study, we see no manner in which these methodological issues would introduce systematic bias that would question the strength or direction of the current findings. It is worth noting that some researchers have questioned the validity of the LNNB primarily on theoretical grounds (for a review please see Moses and Maruish 1989; Moses and Maruish 1990). However, in recent years there has been a growing research literature demonstrating that the LNNB is a reliable (Moses and Maruish 1987) and valid (Moses and Maruish 1988a, 1988b, 1988c) measure of a broad range of higher cortical functions in neurologic and psychiatric samples. Moreover, as a standardized battery with known psyd~ometric properties the LNNB provides substantial research advantages in terms of replicability and objective interpretability. Supported in part by MH30854fromthe NationalInstituteof MentalHealthto the Stanford/VAMentalHealth Clinical ResearchCenterand fundsfromthe Departmentof Veterans AffairsMedicalResearchOffice.

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