JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY 2008, 30 (4), 410420

NCEN

Arithmetic performance in children with Tourette syndrome: Relative contribution of cognitive and attentional factors
Wendy Huckeba,1 Lynn Chapieski,2 Merrill Hiscock,3 and Daniel Glaze2
1 2

Arithmetic Performance in Tourette Syndrome

Private practice, Jenks, OK, USA Department of Pediatrics, Baylor College of Medicine, Houston, TX, USA 3 Department of Psychology and Center for Neuro-Engineering and Cognitive Science, University of Houston, Houston, TX, USA

The study addressed the issue of arithmetic deficiencies in children with Tourette syndrome (TS) as well as explanations for such deficiencies. A total of 47 children with TS were assigned to three subgroups based on a composite attention score from the Test of Variables of Attention (TOVA). These children, along with 17 normal controls between 8 and 16 years of age, were tested on standardized measures of IQ, attention, visuospatial ability, and arithmetic achievement. The children also were administered an experimental calculation task with two levels of structure. Children with TS scored below controls on tests of IQ, attention, and arithmetic achievement but not visuospatial ability. The TS subgroup with the greatest impairment of attention accounted for most of the differences in arithmetic achievement. Regression analysis, based on the 47 children with TS, indicated that IQ and TOVA scores were the best predictors of arithmetic achievement. Likewise, the experimental calculation task indicated that the poor performance of some children with TS could be attributed to deficient attention. Irrespective of structure, children in the TS subgroup with the greatest attentional impairment made more attention (but not visuospatial) errors than did controls on the experimental task. Thus, on both the standardized and the experimental tasks, poor arithmetic skill was found only in children with TS who had significant attentional deficits.

INTRODUCTION Tourette syndrome (TS) is a chronic movement disorder of childhood onset characterized by multiform motor and vocal tics, which wax and wane in severity. In addition to the tics, TS is often associated with cognitive, behavioral, and academic problems (Dooley, 2006; Gaze, Kepley, & Walkup, 2006). Inattention is an especially frequent complaint. In addition to subjective reports of inattention from individuals with TS and from teachers (Burd, Kerbeshian, Cook, Bornhoeft, & Fisher, 1988; Hornse, Banerjee, Zeitlin, & Robertson, 2001; Shady, Fulton, & Champion, 1988), the performance of individuals with TS on continuous performance tasks and other objective measures

has consistently demonstrated problems with inattention (Channon, Flynn, & Robertson, 1992; Gladstone et al., 1993; Harris et al., 1995; Stokes, Bawden, Camfield, Backman, & Dooley, 1990). Accordingly, many children with TS receive an additional diagnosis of attention-deficit/hyperactivity disorder (ADHD; Gaze et al., 2006). Children and adolescents with TS are at risk for general school problems and learning disabilities (Comings & Comings, 1990; Yeates & Bornstein, 1994). The academic skill that appears to be most commonly affected is arithmetic (Bornstein, Baker, Bazylewich, & Douglass, 1991; Brookshire, Butler, Ewing-Cobbs, & Fletcher, 1994; Dykens et al., 1990; Ferrari, Matthews, & Barabas, 1984). Arithmetic deficits may arise from difficulty in

The authors thank the Houston Tourette Syndrome Association, as well as the Southeast Texas Home School Association, for their assistance in recruiting participants. Address correspondence to Lynn Chapieski, Texas Childrens Hospital, 6621 Fannin, CC-1250, Houston, TX 77030, USA (E-mail: mlchapie@texaschildrenshospital.org).

2007 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business http://www.psypress.com/jcen DOI: 10.1080/13803390701494970

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visuospatial processing. Data from a number of studies have indicated that TS is associated with poorly developed visuospatial skills (Como, 2001; Schultz et al., 1998) while studies with normal and math-disabled children have demonstrated the importance of spatial skills for arithmetic performance (McLeod & Crump, 1978; Rourke & Finlayson, 1978; Solan, 1987). Although a few researchers have suggested a possible link between weaknesses in visuospatial skills and the math problems commonly observed in individuals with TS (Brookshire et al., 1994; Incagnoli & Kane, 1983; Matthews, 1988), the actual relationship between these variables has not been established empirically. Another putative cause of arithmetic problems in individuals with TS is poor attention. Data collected by Abwender et al. (1996) identified a relationship between the presence of ADHD and general school problems in students with TS, and Matthews (1988) has suggested that poor math performance in students with TS may be due to inattention as well as visual-motor problems. Logue (1977) and Fletcher (2005) have proposed that attention and concentration are among the skills that underlie arithmetic performance. Inattention, for example, might result in careless errors such as misreading operation signs or skipping problems. Those careless errors may, in turn, interfere with performance in the classroom and on standardized tests. Researchers, in addition, have found that children with ADHD perform poorly on arithmetic tests and that, when their attentional problems are treated with stimulant medication, their math performance improves (BenedettoNasho & Tannock, 1999; Swanson et al., 1998). Other authors implicitly acknowledge the importance of attention by recommending the addition of structure within the classroom as a compensatory means for improving arithmetic performance in students with TS (Bauer & Shea, 1984; Harcherick, Carbonari, Shaywitz, Shaywitz, & Cohen, 1982). One way to evaluate the effect of inattention on arithmetic performance in children with TS is to compare the performance of children with and without a diagnosis of comorbid ADHD. However, in previous studies of children with TS, the additional diagnosis of ADHD has not consistently differentiated children with respect to their performance on tests of attention (De Groot, Yeates, Baker, & Bornstein, 1977; Harris et al., 1995; Mahone et al., 2002; Schuerholz, Singer, & Denkla, 1998). The results of a study by Sherman, Shepard, Joschko, and Freeman (1998) suggest that, even when groups of TS children with and

without ADHD can be differentiated on some measures of attention, children with TS only may still perform more poorly on measures of attention than do normal controls. There are fewer studies that have assessed the relationship between a diagnosis of ADHD and arithmetic skill in children with TS but the findings from those studies have been inconsistent as well (Dykens et al., 1990; Mahone et al., 2002). Consequently, we identified and classified children with attention problems on the basis of performance on a continuous performance test rather than by a diagnosis of ADHD. In the present study, children with TS were divided into three subgroups according to their performance on three measures of attention. Differences between each of the three TS subgroups and a group of normal controls were assessed using standardized measures of IQ, visuospatial skill, and math computation. Then, regression analyses were used to determine the relative contributions of IQ, attention, and visuospatial skill to math performance in the sample of children with TS. Finally, the same four groups of children participated in an experimental task in which calculation errors were categorized as attentional or visuospatial. The standardized testing addressed two specific research questions: (a) Do children with TS show deficiencies in any of the three realms that might be especially relevant to arithmeticthat is, general intellectual ability, visuospatial skill, and attentionand (b) what are the relative contributions of these three categories of ability to arithmetic performance? The experimental task provided information about the number of attentional and visuospatial errors made by children in the different subgroups. It also determined whether error rates would be decreased by adding structure to the task.

METHOD Participants The study involved 47 young people with TS and 17 nonclinical control participants. TS patients were recruited from a pediatric neurology outpatient clinic and the Houston Tourette Syndrome Association. Each child with TS was diagnosed by a neurologist. Each participant met the primary criteria for TS for the DSM-III-R (Diagnostic and Statistical Manual of Mental DisordersThird Edition, Revised; American Psychiatric Association, 1987): (a) multiple motor and one or more vocal tics have occurred at some time; (b) tics occur many times a day (usually in bouts), nearly every day, or intermittently for more than one year;

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(c) the anatomic location, number, frequency, complexity, and severity of the tics change over time; (d) onset is before age 21; and (e) the tics are not due to psychoactive substance intoxication or central nervous system disease. Children were not excluded if they had, or were suspected of having, comorbid conditions such as ADHD, obsessive-compulsive disorder (OCD), or learning disabilities. Control participants included children of hospital staff as well as volunteers obtained from a home-school association and local church groups. Children were excluded from the control group if there was any evidence of a previously diagnosed neurological disorder or learning disability. The TS group comprised 43 males and 4 females between the ages of 8 and 16 years (M = 11.6). The control group included 12 males and 5 females between the ages of 8 and 16 years (M = 10.7). Participants for the control group were selected so as to be comparable to the TS group with respect to age, socioeconomic status (SES), and gender. Group differences were assessed with either t tests or chi square. The two groups did not differ significantly in age, gender, ethnicity, or SES as assessed by the Hollingshead Four Factor Scale of Socioeconomic Status (Hollingshead, 1975). Table 1 summarizes the characteristics of the two groups. Children with TS were grouped according to mean z-scores from three scales of a continuous performance test, the Test of Variables of Attention (TOVA, Greenberg, 1990, 1993): omission errors, commission errors, and response time (latency). The high-attention subgroup (TS-HA) consisted of 17 children who scored no lower than one standard deviation below the normative mean for their age group. The middle-attention
TABLE 1 Demographic characteristics of control group and TS group Group Control (n = 17) 128.6 (28.0) 50.7 (16.1) 15 2 12 5 TS (n = 47) 138.9 (26.5) 46.5 (10.0) 45 2 43 4 ns

subgroup (TS-MA) comprised 13 children whose scores fell between one and two standard deviations below the mean, and the low-attention subgroup (TS-LA) comprised 17 children with scores greater than two standard deviations below the mean. Characteristics of the three subgroups are summarized in Table 2. Participants who normally took stimulant medication did not take their medication the day of testing. A total of 25 TS patients were taking medications, other than a stimulant, for a behavioral disturbance or tics (e.g. clonidine or clomipramine). A total of 9 children were on a single medication, and 16 were on multiple medications. The remaining 22 patients were not taking any medications at the time of the study. Medicated and unmedicated children did not differ significantly on demographic variables, nor did they differ on any of the cognitive or academic variables selected for the study. However, significant differences were found on a tic inventory completed by parents, the Tourettes Syndrome Global Scale (Harcherick, Leckman, Detlor, & Cohen, 1984). The medicated children exhibited more severe symptomatology on three of the inventorys five scalesnamely, complex motor tics (p < .05), complex phonic tics (p < .01), and behavioral symptoms (p < .01). Medicated and unmedicated children did not differ with respect to simple motor or simple phonic tics. Psychometric instruments Childrens intellectual abilities were measured using the Hobby (1982) Split-Half Short Form of the Wechsler Intelligence Scale for Children Revised (WISC-R; Wechsler, 1974). Full Scale IQ, Verbal IQ, and Performance IQ were calculated
TABLE 2 Demographic and attentional characteristics of TS high-, middle-, and low-attention subgroups

Characteristic Agea SES Ethnicity Caucasian Other Gender Male Female

p Characteristic ns ns Agea SES TOVA compositeb

TS-HA (n = 17)

TS-MA (n = 13)

TS-LA (n = 17)

136.9 (26.9) 139.3 (32.8) 140.7 (22.0) ns 44.4 (11.4) 46.1 (10.3) 48.9 (8.3) ns 94.3 (7.2) 78.3 (4.7) 40.0 (23.3) .0001

Note. Standard deviations are shown in parentheses. TS = Tourette syndrome. SES = socioeconomic status as assessed by the Hollingshead Four Factor Scale of Socioeconomic Status. a In months.

Note. Standard deviations are shown in parentheses. TS-HA = Tourette syndrome, high-attention subgroup. TS-MA = Tourette syndrome, middle-attention subgroup. TS-LA = Tourette syndrome, low-attention subgroup. SES = socioeconomic status as assessed by the Hollingshead Four Factor Scale of Socioeconomic Status. TOVA = Test of Variables of Attention. a In months. bTOVA scores are represented as standard scores.

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using standard scoring procedures. The correlation between the WISC-R Full Scale IQ and the WISCR Split-Half Short Form Full Scale IQ is .97 for Hobbys (1982) normative sample and .96 for TS patients in a previous study (Bawden & Byrne, 1991). Visuospatial skills were measured using the Beery Visuomotor Integration test (VMI; Beery, 1982) and the Judgment of Line Orientation test (JLO; Benton, Hamsher, Varney, & Spreen, 1983). The Beery VMI requires the child to copy a series of geometric figures that are arranged in order of increasing complexity. The raw score (total number correct out of 24) was transformed to a standard score for the childs age group. The test retest reliability of the VMI is .81, and the splithalf reliability is .85. The JLO is a motor-free test on which children are required to match line segments having various spatial orientations to the reference line that appears in the same orientation. Raw scores (total number of correct items out of 30) were transformed to z-scores for each age level. Testretest reliability of the JLO is .90, and splithalf reliability is .91. Attention was assessed using a continuous performance task, the TOVA (Greenberg, 1990, 1993), a computer-based test that yields scores for omission and commission errors as well as response time and has been shown to be a valid laboratory measure of sustained attention (Barkley, 1990; Douglas, 1983; Halperin, 1991). TOVA stimuli consist of target and nontarget items that are presented randomly during a 22.5min interval. During the first half of the interval, the ratio of targets to nontargets is 1:3.5, which tends to induce omission errors (i.e., misses). The ratio of targets to nontargets is reversed during the second half of the interval, and this reversal tends to induce errors of commission (i.e., false positives). Raw scores were converted to z-scores on the basis of age-related norms. Arithmetic achievement was assessed using the Mathematics Computations subtest of the Kaufman Test of Educational Achievement (KTEA; Kaufman & Kaufman, 1985), a paper and pencil measure of math calculations. Each child started with an item specified for his or her grade level and continued until reaching a ceiling of five consecutive errors. Standard scores were used in the statistical analyses. Testretest reliability estimates from the normative data are .83 for Grades 16 and .92 for Grades 712. The effect of structure on childrens calculation was measured using Forms A and B of the Operations Scale from the KeyMathRevised Test (Connolly, 1988). Only the items from the Addition,

Subtraction, Multiplication, and Division subscales were administered. Each subscale consists of 18 items requiring paper and pencil math calculations. Items from the subscales were combined in order of ascending difficulty within each of the two forms. Alternate assignment of items to Form A or Form B ensured that the two forms of the Operations Scale were comparable in overall difficulty. The two forms were then administered under structured and unstructured conditions as described below.

Procedures Each child was evaluated individually in a single testing session that required about two hours. The tests were administered by one of the authors (W.H.) who at the time was a doctoral student and had extensive experience administering psychological tests to children. With the exception of the Operations Scale from the KeyMath test, the various tests of intelligence, visuospatial skill, attention, and arithmetic achievement were administered according to standard clinical procedures. Each child completed both of the two equivalent forms of the KeyMath Operations Scale (Form A and Form B). One form was completed at the beginning of the testing session, and the other was completed at the end. The order in which the two forms were presented was counterbalanced within each group of children. Approximately half of the children within each combination of group and presentation order completed Form A with structured administration and Form B with unstructured administration. The other half completed Form B with structured administration and Form A with unstructured administration. Structured administration entailed five interventions: (a) the examiner sat at the table with the child as he or she worked; (b) the examiner gave instructions at the beginning of the test to work carefully, and watch for changes in the operations signs; (c) lines had been placed on the page to separate each problem from contiguous problems; (d) the operations sign of each problem was highlighted in yellow; and (e) after the child indicated that he or she had finished working, the examiner asked the child to check his or her work and to change any incorrect answers. Unstructured administration of the KeyMath scale required the child to work independently in the absence of specific verbal instructions from the examiner. The examiner was not present in the examination room while the child worked, the instruction to work carefully was omitted, and

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HUCKEBA ET AL. TABLE 3 Summary of results for control group and TS group Control group (n = 17) 116.0 (11.6) 117.8 (11.6) 118.5 (10.6) 81.6 (45.9) 108.4 (19.7) 118.6 (25.7) 102.9 (20.1) 95.2 (14.1) 102.7 (16.5) 113.4 (16.0)

the child was not told to check his or her work. The test contained neither lines separating problems nor highlighted operations signs. The time required to complete the scale and the time spent checking work in the structure condition were recorded by the experimenter. Analysis of KeyMath errors As no standard system for scoring calculation errors has been accepted universally, categories for KeyMath errors were developed by adopting aspects of systems previously described in the literature (e.g., Dowell, 1986; Strang & Rourke, 1985) and modifying them so as to capture parsimoniously the error types observed in the present data. For this study only two types of error were of primary interestattention and visuospatial errors. An error was considered attentional if a child skipped a problem or made a procedural error on a problem when the same skill had been demonstrated on a problem of similar type. This type of error is similar to the procedural slip described by Barnes et al. (2002). Misreading an operation sign was also considered an error of attention. An error was coded as visuospatial if the written solution was illegible or the error occurred because of misaligned or crowded numbers, number reversals, or directional confusion. Only items within the expected performance range for a child of a given age were of interest in the error analysis; errors occurring on items falling above that range were disregarded. RESULTS Preliminary analyses Prior to analyzing the data for the three TS subgroups, we computed a series of multivariate analyses of variance (MANOVAs) to compare the control group and the whole sample of children with TS on measures of IQ, attention, and visuospatial ability, respectively. Children with TS performed worse than controls on tests of IQ, F(2, 61) = 5.46, p < .01, and attention, F(3, 60) = 10.10, p < .0001, but not visuospatial ability, F < 1. Group means for each of the individual tests are shown in Table 3, along with means for the K-TEA. To assess the potentially confounding effect of tic severity on the cognitive and academic variables, we computed Pearson correlations between rated tic severity and each of the attention and cognitive measures. Tic severity was measured in terms of

Variablea Verbal IQ Performance IQ Full Scale IQ TOVA omissions TOVA commissions TOVA latency TOVA composite Beery VMI JLO K-TEA

TS group (n = 47) 105.8 (14.3) 106.0 (14.6) 106.4 (13.7) 49.1 (61.8) 81.6 (37.6) 79.7 (30.5) 70.2 (28.0) 93.9 (13.0) 97.0 (16.5) 94.8 (17.2)

tb 2.64 3.01 3.30 2.26 3.68 4.69 4.42 0.37 0.22 3.9

p .01 .005 .005 .05 .0005 .0001 .0001 ns ns .0005

Note. Standard deviations are shown in parentheses. TS = Tourette syndrome. TOVA = Test of Variables of Attention. VMI = Visuomotor Integration test. JLO = Judgment of Line Orientation test. K-TEA = Kaufman Test of Educational Achievement. a All means are expressed as standard scores. bFor all t tests, df = 62.

the total score as well as each of the five subscales. Correlation coefficients ranged from .25 to +.34 with a median of +.03. None of the coefficients was significantly different from zero at p < .01. Analysis of variance (ANOVA) failed to reveal differences among the TS three subgroups on any measure of tic severity, p > .10. IQ and WISC-R subtest scores One-way ANOVAs were used to assess differences in WISC-R indices among the control, TSHA, TS-MA, and TS-LA children. For each of the dependent variables, when the analysis revealed a significant overall difference, we used Dunnetts t (Winer, 1971) to compare each of the TS subgroups with the control group. As shown in Table 4, the ANOVAs yielded significant overall differences for Verbal IQ, Performance IQ, and Full Scale IQ, and for scaled scores from the Vocabulary and Coding subtests. In all instances, the overall differences were attributable to lower averages for both the TS-MA and TS-LA subgroups than for the control participants. In no instance did scores for the TS-HA subgroup differ significantly from the corresponding scores for controls. To ensure that group differences on the principal dependent measures would reflect factors other than IQ differences between children with TS and controls, subsequent between-group tests were computed twice, once without adjustment for IQ and again using analysis of covariance (ANCOVA)

ARITHMETIC PERFORMANCE IN TOURETTE SYNDROME TABLE 4 Mean scores of control and TS high-, middle-, and low-attention subgroups on WISC-R test Group Indexa Verbal IQ Information Similarities Arithmetic Vocabulary Comprehension Digit Span Performance IQ Picture Completion Picture Arrangement Block Design Object Assembly Coding Full Scale IQ Control 116.0 (11.6) 13.5 (3.2) 14.4 (2.9) 11.6 (2.1) 12.4 (3.0) 11.9 (3.8) 10.6 (2.5) 117.8 (11.6) 12.6 (2.3) 13.5 (2.5) 11.9 (2.3) 13.5 (3.1) 11.8 (3.4) 118.5 (10.6) TS-HA 111.2 (15.4) 11.9 (3.0) 12.8 (3.7) 11.7 (3.4) 12.1 (3.3) 12.3 (2.3) 10.2 (2.3) 107.4 (17.4) 11.0 (2.1) 11.6 (3.3) 11.9 (3.1) 12.6 (3.5) 10.6 (4.5) 110.4 (16.8) TS-MA 102.8 (11.7) 11.2 (2.9) 11.2 (3.7) 10.5 (2.3) 9.5 (1.7) 10.8 (3.1) 9.2 (2.2) 104.0 (12.3) 11.1 (4.1) 12.1 (4.0) 10.4 (2.6) 11.9 (2.4) 8.3 (3.1) 103.5 (10.1) TS-LA 102.8 (14.1) 10.9 (3.2) 11.9 (3.2) 10.4 (3.0) 9.6 (2.7) 10.1 (3.0) 9.0 (2.0) 106.0 (13.7) 11.3 (3.3) 12.1 (3.1) 11.6 (3.2) 11.9 (3.1) 8.0 (3.0) 104.6 (12.3) Fb 3.82 2.22 2.62 0.99 4.77 1.76 1.94 3.08 1.07 1.18 0.90 0.90 4.27 4.54

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p .025 ns ns ns .005 ns ns .05 ns ns ns ns .01 .01

Note. Standard deviations are shown in parentheses. TS-HA = Tourette syndrome, high-attention subgroup. TS-MA = Tourette syndrome, middle-attention subgroup. TS-LA = Tourette syndrome, low-attention subgroup. a IQs are expressed as standard scores; subtest scores are expressed as scaled scores with means of 10 and standard deviations of 3. bFor all F-tests, df = 3, 60.

to adjust the dependent measure for the childs Full Scale IQ.

Attention ANOVA and ANCOVA were computed for standard scores representing errors of omission, errors of commission, and log-transformed response latency from the TOVA. Full Scale IQ served as the covariate for each ANCOVA. The mean TOVA scores are displayed in Table 5. The analyses for errors of omission yielded a significant group effect irrespective of whether scores were adjusted for IQ: F(3, 60) = 11.99, p < .0001, for ANOVA, and F(3, 59) = 10.35, p < .0001, for ANCOVA. However, Dunnetts t indicated that

only the TS-LA subgroup differed significantly from the control group, p < .01. The results were similar for errors of commission, in which ANOVA yielded F(3, 60) = 11.89, p < .0001, and ANCOVA yielded F(3, 59) = 13.91, p < .0001. Again the only TS subgroup that differed significantly from the control group was the TS-LA subgroup, p < .01. Analysis of response latency also yielded a significant overall difference among groups: F(3, 60) = 10.60, p < .0001, for ANOVA, and F(3, 59) = 8.32, p < .0001, for ANCOVA. For this dependent variable, Dunnetts t indicated that each of the three TS subgroups responded more slowly than controls, p < .01. Thus, children with TS performed worse than controls on all three TOVA variables but, with the exception of response latency, only the TS subgroup with the lowest TOVA composite scores

TABLE 5 Mean TOVA scores of control and TS high-, middle-, and low-attention subgroups Group TOVA variablea Omissions Commissions Latency Composite Control 81.6 (45.9) 108.4 (19.7) 118.6 (25.7) 102.9 (20.1) TS-HA 90.2 (22.8) 102.9 (10.4) 89.6 (19.7) 94.2 (7.2) TS-MA 59.0 (45.7) 89.2 (24.3) 86.5 (36.6) 78.2 (4.6) TS-LA 0.5 (67.0) 54.5 (47.0) 64.7 (30.0) 39.9 (23.3) Fb 48.53 9.49 8.26 48.87 p .0001 .005 .01 .0001

Note. Standard deviations are shown in parentheses. TS-HA = Tourette syndrome, high-attention subgroup. TS-MA = Tourette syndrome, middle-attention subgroup. TS-LA = Tourette syndrome, low-attention subgroup. TOVA = Test of Variables of Attention. a All means are expressed as standard scores. bFor all F-tests, df = 3, 60.

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differed significantly from the control group. None of the three ANCOVAs showed a strong relationship between TOVA measures and Full Scale IQ. Only in the analysis for errors of commission did IQ account for a significant proportion of the variance, F(1, 59) = 4.17, p < .05. Visuospatial ability

yielded a somewhat attenuated effect, F(3, 59) = 3.74, p < .05, which was accounted for primarily by the control versus TS-LA contrast, p < .01. The ANCOVA revealed a strong effect for the covariatethat is, a strong association between K-TEA and Full Scale IQ, F(1, 59) = 21.44, p < .0001. Prediction of arithmetic achievement

After conversion to standard scores based on norms for each age level, data from the JLO and Beery VMI were analyzed in separate one-way ANOVAs and ANCOVAs. Neither of the two ANOVAs yielded a statistically significant effect, p > .20, and the results remained nonsignificant after adjustment for IQ. Both ANCOVAs yielded significant effects for the covariatethat is, an association between JLO scores and Full Scale IQ, F(1, 59) = 5.49, p < .05, and between Beery VMI scores and Full Scale IQ, F(1, 59) = 11.41, p < .005. The Pearson correlation between VMI and JLO scores was .32, p < .01. Arithmetic achievement Each groups mean standard score from the KTEA test is shown in Figure 1. These scores were analyzed in a one-way ANOVA as well as an ANCOVA with Full Scale IQ as the covariate. ANOVA yielded a significant effect, F(3, 60) = 7.94, p < .001, which is largely attributable to differences between the control group and the TS-LA subgroup, p < .01, and between the control group and the TS-MA subgroup, p < .01. No significant difference was found between the control group and the TS-HA group. ANCOVA

The degree to which IQ, attention, and visuospatial measures predict K-TEA scores was assessed with a stepwise multiple regression analysis for the TS group only. The predictor variablesFull Scale IQ, JLO, Beery VMI, TOVA omission errors, TOVA commission errors, and TOVA latency entered the equation only if they met the F-to-enter criterion of 4.0. The results of the regression analysis are presented in Table 6. Full Scale IQ accounted for the greatest proportion of explained variance in KTEA scores. The second predictor to enter the equation was TOVA latency, which accounted for an additional 9.0% of the variance. Two additional predictor variables met the F-to-enter criterion. TOVA omission errors accounted for 5.8% of the variance in K-TEA performance, and the JLO score accounted for another 5.2%. The total proportion of variance in K-TEA scores accounted for by the full model was 53.3%. Calculation errors Completion time and checking time Prior to analyzing errors, we examined the time required to complete the KeyMath items under structured and unstructured testing conditions.
TABLE 6 Prediction of K-TEA scores from performance on IQ, attention, and visuospatial tests (TS group only) Predictor variable Full Scale IQ TOVA latency TOVA omissions JLO Model R2 .33 .42 .48 .53 R2 increment .33 .09 .06 .05 Variable F 22.44 6.86 4.82 4.68

Arithmetic Achievement and Full Scale IQ 140 120 Standard Score 100 80 60 40 20 0 Control TS-HA TS-MA TS-LA
Note. All F-values for regression models are statistically significant at p < .0001. All F-values for individual predictor variables are statistically significant at p < .05. K-TEA = Kaufman Test of Educational Achievement. TS = Tourette syndrome. TOVA = Test of Variables of Attention. JLO = Judgment of Line Orientation test.
K-TEA FSIQ

Model F 22.44 16.11 13.28 11.98

Figure 1. Mean score from the K-TEA Mathematics Computations subtest, relative to Full Scale IQ, for the control group and each of the three attention subgroups (high, middle, and low) of children with Tourette syndrome. Error bars indicate one standard error of the mean.

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A Group Structure ANOVA for logarithmtransformed completion time yielded no significant main effects and no significant interaction. Structure had very little influence on the completion time of either the children with TS or the controls. An analysis of log-transformed time spent checking work in the structured condition also failed to reveal a significant difference among groups. Errors Although each of the ANOVAs for calculation errors was followed by an ANCOVA in which Full Scale IQ was used as a covariable, none of the ANCOVA results substantially altered the ANOVA results. Consequently, only the ANOVA results are reported. An initial Group Structure ANOVA was performed on total errors, which included errors that could not be classified as either attentional or visuospatial. The ANOVA yielded significant main effects for group, F(3, 59) = 15.17, p < .0001. Dunnetts t indicated that control children made fewer errors than did children in either the TS-LA (p < .01) or the TS-MA (p < .05) subgroups. The difference between controls and children in the TS-HA subgroup was not significant. Neither the effect for structure nor the interaction was statistically significant. A 4 2 2 (Group Structure Error Category) ANOVA was computed to evaluate group differences in attention errors and visuospatial errors. The ANOVA yielded significant main effects for group, F(3, 60) = 8.89, p < .0001, and error category, F(1, 60) = 92.44, p < .0001, as well as a significant Group Error Category interaction, F(3, 60) = 5.06, p < .005. As shown in Figure 2, children with TS made more errors than did children in the

control group, and both groups made more attention errors than visuospatial errors. The interaction reflected a greater difference between groups in number of attention errors relative to visuospatial errors. Simple main effect analyses indicated that differences among groups were significant for attention errors, F(3, 60) = 8.98, p < .0001, but not for visuospatial errors, p > .20. Comparisons between the control group and each of the TS subgroups using Dunnetts t indicated that only the low-attention subgroup (TS-LA) made significantly more attention errors than did controls, p < .01. The manipulation of structure did not have a significant effect on the results.

DISCUSSION When considered together, the results of the psychometric and experimental parts of the study both support the conclusion that the TS sample as a whole is impaired in written calculation ability. Thus, the findings corroborate earlier reports (Bornstein et al., 1991; Dykens et al., 1990; Ferrari et al., 1984; Incagnoli & Kane, 1983; Yeates & Bornstein, 1994). Moreover, both aspects of the study implicate general intellectual ability and attention, but not visuospatial abilities, as attributes that are closely associated with calculation scores and the majority of classifiable calculation errors. One might argue that the two putative cognitive factorsIQ and attentionare themselves highly correlated. The largest mean difference between TS and control groups on the WISC-R was obtained from the Coding subtest, which demands a high level of concentration. On the other hand, none of the three TOVA indices was strongly correlated with Full Scale IQ. Consequently, it appears that IQ and attention, at least for the present sample of children and as measured by the WISC-R and TOVA, respectively, are largely independent of each other. A related issue concerns the relative importance of the three TOVA scales in differentiating groups and in predicting arithmetic performance. It was response time and, to a lesser degree, commission and omission errors that differentiated children with TS from controls. Moreover, response time was the TOVA variable that proved to be most closely associated with arithmetic performance in the TS group. Likewise, in predicting attention errors made on KeyMath items during the experimental phase of the study, TOVA response time again proved to be one of the useful variables. In the latter instance, however, TOVA omission errors made an additional contribution to the prediction

Errors Categorized by Content Analysis

12 Mean Number of Errors 10 8 6 4 2 0 Control TS-HA TS-MA

Attention Visuospatial

TS-LA

Figure 2. Mean number of attention and visuospatial errors made by children with Tourette syndrome and by controls as they performed calculation items from the KeyMath test. Error bars indicate one standard error of the mean (SEM).

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of attention errors. There is some evidence that response time has more temporal stability than do errors of omission or commission (Llorente et al., 2001). Slow response times presumably reflect deficient arousal or readiness to respond, which may be one of the most salient characteristics of children with TS who also have attention difficulties. Without exception, the arithmetic deficiencies observed in children with TS can be attributed to the TS subgroups with poor attentionthat is, with TOVA composite scores more than one standard deviation below average. As one would expect if inattention were a major contributing factor to arithmetic difficulty, the subgroup with the most impaired attention was the subgroup that consistently showed the most deficient arithmetic performance. The converse is especially clear in the present data: Children with diagnoses of TS whose attention skills (i.e., TOVA composite scores) lie within one standard deviation of the population average do not differ significantly from controls in any facet of their arithmetic ability. Perhaps this is the most important conclusion to be drawn from our findings. This outcome provides strong support for the position that TS per se does not entail an arithmetic disability or calculation impairment of any kind. Because much of the previous literature has overlooked the effects of medication, we included both medicated and unmedicated TS patients and compared those two subgroups on all our psychometric measures. Apart from the greater severity of certain tic and behavioral symptoms, as reported on the Tic Symptom Checklist, no significant differences between subgroups were found. In fact, as indicated in the Method section, the medicated and unmedicated patients were indistinguishable on all measures except the checklist. The manipulation of structure warrants a comment. Even though added structure failed to have a significant effect on error rates, we would not conclude that structure is never of benefit. Perhaps the structure manipulation could have been enhanced by more active involvement of the adult in the room. Periodic verbal reminders to pay attention, for example, might have had a more pronounced effect. Finally, this study illustrates how objective measures of attention may be used to define subgroups in future research into the neuropsychological and behavioral characteristics of children with TS. Children with TS frequently are diagnosed with comorbid disorders ranging from ADHD and OCD to various learning disabilities. Even if the additional diagnoses are appropriate in most instances, they are based largely on subjective evidence and may be influenced by extraneous factors such as family socioeconomic status. Because they

are regarded as categorical (all-or-none) characteristics, the diagnoses are not ideal for research purposes. As illustrated by the present findings, attention problems are not simply present or absent; attention problems manifest themselves in various degrees of severity that can be quantified objectively. In addition, categorizing children on the basis of multiple disorders greatly increases the difficulty of selecting participants as well as the difficulty of interpreting the findings. By selecting children on the basis of the primary diagnosisthat is, Tourette syndromeand then measuring the specific attribute of interestfor example, performance on an objective measure of attentionit is possible to isolate the effect of that attribute on the dependent variables of interest while avoiding the complexity associated with multiple diagnoses. This strategy for defining and measuring attention may also prove to be useful for neuroimaging studies, in which classification according to multiple diagnostic categories has led to contradictory findings regarding the localization of the neurological abnormality in TS (cf. Braun et al., 1993; Chase, Geoffrey, Gillespie, & Burrows, 1986; George et al., 1992; Leckman et al., 1997; Riddle, Rasmusson, Woods, & Hoffer, 1992; Stoetter et al., 1992). Activation of the frontal lobes, for example, is not a categorical variable. Frontal activation patterns in individuals with TS may be abnormal to various degrees, and the degree of abnormality may covary with degree to which the individual is unable to deploy attention adaptively. If that covariance is to be demonstrated consistently, attention difficulty must be represented as a continuously distributed variable. In conclusion, the present research helps to clarify the underlying basis for the math problems that are frequently reported in children with TS. As a group, the children in our study with TS performed more poorly on measures of calculation than did normal controls. In this respect, our findings substantiate previous reports and clinical observations of arithmetic deficiencies in this population. Our study, however, clearly shows that the degree of arithmetic disability is correlated with the degree of attentional deficit as indexed by the continuous performance test. Children with TS who showed no evidence of attention problems were indistinguishable from controls in their arithmetic performance. Whereas a diagnosis of TS carries with it a heightened risk for calculation problems, that risk exists only for an identifiable subset of this population.
Original manuscript received 13 December 2006 Revised manuscript accepted 31 May 2007 First published online 12 September 2007

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