Distinct Patterns of Everyday Executive Function Problems Distinguish Children With Tourette Syndrome From Children With ADHD or Autism Spectrum Disorders

Abstract

Objective: The aim is to investigate the everyday executive function (EF) in children with Tourette syndrome (TS), Inattentive or Combined presentations of ADHD (ADHD-I/ADHD-C), autism spectrum disorders (ASD), and typically developing children (TDC). Method: Nineteen TS, 33 ADHD-C, 43 ADHD-I, 34 ASD, and 50 TDC participated (8-17 years). Parents completed the Behavior Rating Inventory of Executive Function (BRIEF). Results: TS, ADHD-C, ADHD-I, or ASD were rated with significantly more regulation problems on all scales compared with TDC. Considerable overlap of symptoms between clinical groups made differentiation difficult on individual scales. Scale configurations showed children with TS to have more problems with emotional control (EC) than cognitive flexibility in relation to children with ASD, more problems with EC than inhibitory control in relation to ADHD-C, and more problems with EC than planning/organizing in relation to ADHD-I. Conclusion: Paired BRIEF scales dissociated EF problems in children with TS from children with ADHD-C, ADHD-I, or ASD. Clinical relevance is discussed.

Keywords

Tourette syndrome ADHD autism spectrum disorders executive function EF behaviors

Introduction

Tourette syndrome (TS) is a neurodevelopmental disorder characterized by motor and phonic tics persisting for a minimum of 1 year (Plessen, 2013). Whereas the diagnostic criteria are restricted to the presence of chronic tics, executive function (EF) problems affecting everyday attentional, behavioral, and emotional control (EC) are associated with the disorder and often represent the most debilitating aspect of the condition (Carter et al., 2000; Singer, 2005). As many as 70% of patients with TS in clinical settings report experiencing problems with emotional outbursts (Budman, Rockmore, Stokes, & Sossin, 2003), and emotional problems tend to increase during childhood for children with TS (Hoekstra, Lundervold, Lie, Gillberg, & Plessen, 2013). Problems regulating emotions present more frequently in children than in adults, are more problematic for children than for adults, and are common reasons for psychiatric referral in children with TS (Budman, Bruun, Park, Lesser, & Olson, 2000).

There is general agreement that adaptive control of behavior depends on intact EF (Jurado & Rosselli, 2007), which refers to the top-down, mental processes involved in monitoring, regulating, and mediating cognition, emotions, and behavior (Diamond, 2013; Zelazo & Cunningham, 2007). Impaired EF is, however, not only a characteristic feature of TS but is also associated with a wide range of neurodevelopmental disorders including ADHD and autism spectrum disorders (ASD; Geurts, de Vries, & van den Bergh, 2014; Hill, 2004a, 2004b; Mahone, Koth, Cutting, Singer, & Denckla, 2001; Wåhlstedt, Thorell, & Bohlin, 2008). Emerging evidence indicates a pathogenic association and a phenomenological overlap among these three childhood-onset disorders (Clarke, Lee, & Eapen, 2012; Freeman & Tourette Syndrome International Database Consortium, 2007; Roessner, Becker, Banaschewski, Freeman, & Rothenberger, 2007). Despite indications of an overlap of symptoms, however, few studies have compared everyday EF problems in children with TS to children with other common neurodevelopmental disorders. Obtaining a more distinct characterization of EF problems in children with TS might improve treatment prospects for this disorder.

Self-regulatory abilities needed for adaptive functioning in everyday situations are commonly measured using EF rating scales (Gioia, Isquith, Guy, & Kenworthy, 2000a). Whereas performance tests assessing EF show significant impairment in only half of children with a diagnosis of ADHD compared with typically developing children (TDC; Willcutt, Doyle, Nigg, Faraone, & Pennington, 2005), scales assessing EF are elevated in the majority of children with ADHD (McAuley, Chen, Goos, Schachar, & Crosbie, 2010; Toplak, Bucciarelli, Jain, & Tannock, 2009; Toplak, West, & Stanovich, 2013). EF assessment scales have strong associations with neurological bases of EF (Isquith, Roth, & Gioia, 2013), leading some to suggest that rating scales of EF may be the preferred method of detecting clinical conditions with EF problems (Barkley, 2012). The Behavior Rating Inventory of Executive Function (BRIEF) assesses children’s behavior in natural settings and provides a measure of fundamental cognitive, emotional, and behavioral regulatory processes (Gioia, Isquith, Guy, & Kenworthy, 2000b). The rating scale is completed by a parent or teacher and provides eight non-overlapping scales reflecting commonly agreed upon domains of EF behaviors: Inhibit, Shift, EC, Working Memory, Initiate, Plan/Organize, Organization of Materials, and Monitor, which are combined to form three broad classifications of executive functioning—Behavioral Regulation, Metacognition, and the Global Executive Composite. Research applying the BRIEF indicates that, relative to TDC, the rating scale is sensitive in detecting behavior difficulties in children with TS (Mahone et al., 2002), ADHD (McCandless & O’Laughlin, 2007; Toplak et al., 2009), and ASD (Gilotty, Kenworthy, Sirian, Black, & Wagner, 2002; Kenworthy et al., 2005).

In a study comparing everyday EF behavior in children with TS with and without comorbid ADHD to children with ADHD on the BRIEF, the children with only TS were rated as less impaired than the children with ADHD or with TS + ADHD on scales measuring behavioral inhibition and working memory and on the Metacognition Index, Behavioral Regulation Index, and Global Executive Composite (Mahone et al., 2002). In the previously mentioned study, the authors recommended distinguishing between Inattentive (ADHD-I) and Combined (ADHD-C) presentations of ADHD in future studies using the BRIEF. The presentations ADHD-I and ADHD-C are by many considered distinct disorders (Milich, Balentine, & Lynam, 2001), and the common tendency to group children with these two presentations together when examining difficulties risks ignoring the unique underlying profile of difficulties associated with children with ADHD-C compared to children with ADHD-I (Diamond, 2005; Milich et al., 2001). Several studies administering the BRIEF in children with ADHD have discriminated between ADHD-C and ADHD-I. Two studies reported the Inhibit scale to be useful in distinguishing the more severe inhibitory impairment characteristics of children with ADHD-C from less severe impairment in children with ADHD-I in two studies (Gioia et al., 2000b; Skogli, Egeland, Andersen, Hovik, & Oie, 2014). In a separate study, the results on the Behavior Regulation Index indicated more severe behavior regulation problems in children with ADHD-C compared to children with ADHD-I (McCandless & O’Laughlin, 2007). To our knowledge, no studies have compared children with TS to these two subgroups of ADHD on a rating scale assessing everyday EF behavior. Consistent with the literature, however, children with TS likely exhibit comparatively more problems controlling emotional responses (Budman et al., 2003), whereas children with ADHD-C have more problems inhibiting impulsive actions (McCandless & O’Laughlin, 2007) and children with ADHD-I are less able to organize and execute planned activities (Diamond, 2005).

ASD is a term encompassing children with autism, Asperger’s syndrome (AS), or Pervasive Developmental Disorder–Not Otherwise Specified (PDD-NOS). Evidence for executive dysfunction in ASD is high and is associated with the social and cognitive difficulties observed in these children (Geurts et al., 2014; Happé, Booth, Charlton, & Hughes, 2006; Pennington & Ozonoff, 1996). A study comparing children with ASD to children with ADHD-C and ADHD-I on the BRIEF reported more severe behavior regulation difficulties for the ASD group compared to both ADHD subgroups (Semrud-Clikeman, Walkowiak, Wilkinson, & Butcher, 2010). Another study reported the ASD group to be distinguishable by more severe impairment in cognitive flexibility as measured on the BRIEF Shift scale, whereas the ADHD-C group was unique in the frequency and severity of inhibitory deficits (Gioia, Isquith, Kenworthy, & Barton, 2002). An extensive review concludes that the severity and pattern of EF deficits are distinct for ASD and ADHD, with larger effect sizes being associated with impaired cognitive flexibility in ASD than for any other executive dysfunction measured in ADHD or TS (Kenworthy, Yerys, Anthony, & Wallace, 2008; Pennington & Ozonoff, 1996).

In sum, the existing literature suggests that different EF-related behavior characteristics are associated with the common neurodevelopmental disorders such as TS, ADHD-C, ADHD-I, and ASD. Despite examples of individual scales in the BRIEF identifying behavior characteristics associated with some disorders, the general picture is that individual scales and indexes alone cannot be used to differentiate between diagnoses (Gioia et al., 2002). In most rating scales, measuring an overarching psychological construct thought to be composed of distinguishable sub-processes will be sensitive to the general effect of severity. The severity dimension, which is the rationale for computing sum scores for cognitive constructs, provides good power to differentiate between clinical participants and TDC. Yet, analyzing the severity of disturbances is seldom sufficient to discriminate between clinical groups. For this, we need qualitative analyses of profiles. Children with TS, ASD, ADHD-I, or ADHD-C, for example, are expected to be rated as having more difficulties in regulating their emotions than their typically developing peers. However, whereas parents of children with TS report EC difficulties to be the most problematic behavioral symptom (Budman et al., 2003; Dooley, Brna, & Gordon, 1999), research has not identified such difficulties to be the most problematic behavioral deficit in children with ASD, ADHD-I, or ADHD-C. Nevertheless, participants with ASD, ADHD-I, or ADHD-C score more impaired than TDC on the EC scale on the BRIEF (Gilotty et al., 2002; McCandless & O’Laughlin, 2007). Higher scores reflect a higher level of impairment on the BRIEF. A high score on the EC scale, however, may merely reflect the level of severity of EF disturbance, as will be the case when other scales are also scored high, or even higher than the participants’ EC score. Level of severity may differ both within and between clinical groups. By contrasting the EC scale score with another strategic scale score, however, we can control for the severity effect. For example, participants with ASD are considered to be characterized by cognitive inflexibility (Corbett, Constantine, Hendren, Rocke, & Ozonoff, 2009), whereas participants with TS are expected to exhibit a relatively smaller impairment in this domain. A plausible hypothesis would then be that while both groups can have somewhat elevated ratings on many BRIEF scales, a relatively higher EC score in the context of a relatively lower Shift score would be more typical of children with TS in comparison with participants with ASD; and a relatively higher Shift score in the context of a relatively lower EC score would be more typical of children with ASD in comparison with participants with TS. By applying this strategic analysis approach, two scales based on highly characteristic behavior patterns associated with the conditions are chosen rather than looking for an overall pattern among all eight BRIEF scales.

Similarly, evidence from factor and cluster analytic studies in children with ADHD suggests that ADHD-C is more characterized by a lack of inhibitory control whereas ADHD-I is more characterized by sluggish, disorganized behavior (Diamond, 2005; Milich et al., 2001). Symptoms of disinhibition and disorganization in children with TS are most often associated with a comorbid ADHD diagnosis. Thus, we might expect that a high EC score in the context of a relatively lower Inhibit score would characterize children with TS compared to a low EC score but a high Inhibit score in children with ADHD-C. Similarly, a high EC score in the context of a lower Plan/Organize score would characterize TS, compared to a low EC score but high Plan/Organize score in children diagnosed with ADHD-I. The current practice of interpreting BRIEF results already makes use of this strategic qualitative process approach, for example, high Working Memory impairment and less severe impairment in Inhibition are indications of ADHD-I rather than ADHD-C (Gioia & Isquith, 2001). Accordingly, when trying to differentiate between the two ADHD subtype diagnoses, two scales may be considered strategic, whereas the other six scales may be less uniquely relevant.

The aim of the current study is to identify everyday EF behavior that may distinguish children with TS from TDC and children with ADHD-C, ADHD-I, or ASD. Two primary hypotheses were explored. First, a review of the EF literature indicates that children with TS may exhibit deficits in EF behavior regardless of the co-occurrence of comorbidities. In terms of the severity of EF disturbances, we expect parents of children with TS to report more severe problems on all scales and general indices of EF behavior compared with the TDC group. We also predict that neither overall severity nor severity of impairment on individual scales will be sufficient to discriminate between the clinical groups. Second, we expect that applying strategic qualitative profile analyses may differentiate the TS participants from the children with ASD, ADHD-C, or ADHD-I, who are also characterized by clinically impaired EF behavior. We predict that a scale configuration consisting of the scales EC and Shift will differentiate between TS and ASD, the EC and Inhibit scales will differentiate the TS from the ADHD-C and, the EC and Plan/Organize will discriminate between the TS and the ADHD-I groups. A more accurate characterization of problem behaviors associated with TS beyond tics should improve treatment outcome by providing better information for more targeted interventions. To investigate whether a parent report of executive behaviors can provide such information for a small, but relatively typical clinical sample of first-referral children with TS, we test whether differences in group averages apply to individual scale classifications. We thus classify each participant as to displaying the expected configuration of EC versus Shift/Inhibit/Plan/Organize pattern and compare the frequency of each pattern in the clinical groups.

Method

Participants

The sample consisted of 179 children between 8 and 17 years (19 with TS, 33 with ADHD-C, 43 with ADHD-I, 34 with ASD, and 50 TDC). All clinical participants were first-time referrals to the Child and Adolescent Mental Health Centres in Innlandet Hospital Trust (IHT) in Norway. The TDC were recruited from local schools and received a gift certificate worth NOK 200 for participating. The participants in the groups did not differ significantly in age. Only 5 of the 179 participants were of a different ethnic background than the majority, who were ethnic Norwegian. Demographic and clinical characteristics are presented in Table 1. Four of the participants were receiving medication for behavior problems at the time of assessment (2 children with TS: low dose of Quetiapine and Ariprirazole, respectively; 2 children with ADHD: low dose of Risperidone and Quetiapine, respectively). None of the other participants were on medication during the 6 months prior to testing, nor upon testing, as most of the participants were first-time referrals to child health services. Six of the children with TS had co-occurring ADHD (3 with ADHD-I and 3 with ADHD-C) and 4 with comorbid ASD, which is a common rate for this population (Robertson, Eapen, & Cavanna, 2009). Two of the children with TS had co-occurring Oppositional Defiant Disorder (ODD) and 1 had Obsessive–Compulsive Disorder. More details about the TS group are available in (Hovik, Plessen, Skogli, Andersen, & Øie, 2016). In the ADHD groups, comorbid ODD was evident in 22.3% of the participants with ADHD-C and 2.3% of the ADHD-I participants. (More details about the ADHD group are available in Skogli, Teicher, Andersen, Hovik, & Øie, 2013.) Of the children in the ASD group, 27 were diagnosed with AS and 7 with PDD-NOS. None of the participants in this group met the diagnostic criteria for Autistic Disorder. More details about this group are available in Andersen, Hovik, Skogli, Egeland, and Øie (2013). Parents were asked in the diagnostic interview whether their child had a learning disability. The following percentage of parents in each category responded affirmatively that their child had a reading/writing disability: 2% of TS, 33% of ADHD-C, 53% of ADHD-I, 4% of ASD, and 0% of TDC. The following percentage of parents in each category reported that their child had math difficulties: 2% of TS, 33% of ADHD-C, 35% of ADHD-I, 2% of ASD, and 0% of TDC.

Table 1.

Demographic Characteristics: Means and Standard Deviations for the Five Groups.

Variable	TS (n = 19)	ADHD-C (n = 33)	ADHD-I (n = 43)	ASD (n = 34)	TDC (n = 50)	Group comparison		Post hoc^a
Variable	TS (n = 19)	ADHD-C (n = 33)	ADHD-I (n = 43)	ASD (n = 34)	TDC (n = 50)	F/χ²	p	Post hoc^a
Age (years)	11.8 (2.2)	11.6 (2.1)	11.6 (1.9)	11.9 (2.3)	11.6 (2.0)	0.1	ns
Gender (male/female)	16/3	20/13	20/23	28/6	32/18	14.9	<.01
Mother’s education (years)	12.2 (2.4)	12.6 (2.3)	13.1 (1.9)	13.0 (2.6)	14.6 (2.4)	6.0	<.01	All clinical groups < TDC
Full Scale IQ (WASI)	101.9 (15.2)	96.8 (13.8)	94.2 (15.2)	98.2 (18.6)	103.8 (12.9)	2.7	<.05	ADHD-I < TDC
Inattention^b	13.7 (8.9)	16.6 (5.8)	14.8 (5.2)	12.5 (5.7)	1.6 (1.9)	54.9	<.01	TDC < All clinical groups
Hyperactivity/Impulsivity^b	11.9 (6.7)	13.6 (5.6)	6.7 (5.2)	7.8 (6.3)	0.9 (1.3)	37.5	<.01	TDC < ADHD-I and ASD < TS and ADHD-C
CBCL–Total Problems	65.0 (8.8)	62.9 (8.0)	60.3 (8.1)	64.1 (9.6)	37.9 (8.7)	74.5	<.01	All clinical groups < TDC

Note. TS = Tourette syndrome; ADHD-C = ADHD–combined; ADHD-I = ADHD–inattentive; ASD = autism spectrum disorders; TDC = typically developing children; WASI = Wechsler Abbreviated Scale of Intelligence; CBCL = Child Behavior Checklist.

Fisher’s Least Significant Difference.

ADHD rating scale IV.

Ethics Statement

Parents and children (12 years and older) signed consent forms before participating in the study. The study was approved in advance by the Regional Committee for Medical Research Ethics in Eastern Norway (REK-Øst), and by the Privacy protection ombudsman for research at IHT. The study was conducted in accordance with the Helsinki Declaration of the World Medical Assembly.

Procedures

Exclusion criteria were premature birth (<36 weeks), neurological disorder, estimated full scale IQ < 70, or previous stimulant treatment. Diagnostic assessments were based on interviews conducted by experienced psychologists or clinical educational therapists of participants and parents separately using the Schedule for Affective Disorders and Schizophrenia for School-Age Children/Present and Lifetime version–2009 (K-SADS-PL; Kaufman et al., 1997). Good to excellent validity and reliability have been reported for the K-SADS-PL (Kaufman et al., 1997; Kim et al., 2004). The 2009 version used in the project includes the supplement for ASD. The results from the K-SADS-PL interviews and supporting information were reviewed independently by the supervising senior clinician who is a specialized psychologist in neurodevelopmental disorders (M.Ø.). Disagreements were discussed in meetings with all the clinicians present to arrive at a “best estimate” Diagnostic and Statistical Manual of Mental Disorders (4th ed.; DSM-IV; American Psychiatric Association [APA], 1994) consensus (Gargaro, Rinehart, Bradshaw, Tonge, & Sheppard, 2011). The diagnostic evaluations were supplemented with information provided in self-report forms completed by the parent or parents: the Yale Global Tic Severity Scale (YGTSS; Leckman et al., 1989), the ADHD Rating Scale–IV (DuPaul, Power, Anastopoulos, & Reid, 1998), the Autism Spectrum Screening Questionnaire (ASSQ; Ehlers, Gillberg, & Wing, 1999; Posserud, Lundervold, & Gillberg, 2009), and Child Behavior Checklist (CBCL; Achenbach & Rescorla, 2001). Normative data from the ASSQ (Ehlers et al., 1999), the ADHD Rating Scale–IV manual (DuPaul et al., 1998), and T-scores above 65 on the syndrome and DSM-oriented scales in CBCL (Achenbach & Rescorla, 2001) were applied to assess clinical significance. Information from teachers about the child’s school functioning (academic, social, and emotional competencies) is mandatory on referral to IHT and was available to the clinicians. If both parents could not report on K-SADS-PL and rating scales together, information from mothers was used. When information on the K-SADS-PL was not consistent with rating scales, information from K-SADS-PL was emphasized in the assessment. All diagnoses had to fulfill Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev.; DSM-IV-TR; APA, 2000) criteria. TDC were also screened in interviews (child and parent separately) for any psychiatric condition fulfilling DSM-IV criteria, as well as head injuries involving loss of consciousness or known dyslexia.

Participants were part of a larger research project investigating cognitive, emotional, and behavioral development in children and adolescents with neuropsychiatric disorders. The data for the current study were collected for the children with TS, ADHD-C, ADHD-I, ASD, and TDC as part of a standard clinical neuropsychological evaluation.

Measure of EF Behavior

One or both parents of each child completed the parent version of the BRIEF (Gioia et al., 2000b). The BRIEF for children and adolescents aged 5 to 18 years includes 86-item parent and teacher forms that allow professionals to assess everyday EFs in the home and school environments (Gioia et al., 2000b). The rating instrument is composed of eight clinical scales, two broad indices, and one overall score. The current study used the Norwegian version of the parent-rating form, which has shown high internal consistency (Cronbach’s α = .76-.92; Fallmyr & Egeland, 2011) and similar levels to that reported for the English version (.80-.98; Gioia et al., 2000b). Evidence of construct validity for the instrument has been demonstrated by convergent and discriminant analyses with several established behavior and attention rating scales (Gioia et al., 2000b; Isquith et al., 2013). The representativeness of the American norms for healthy control children in English speaking countries and Europe has been examined in several studies. No normative differences have been shown in English speaking countries (Roth, Erdodi, McCulloch, & Isquith, 2014). In a study involving forty-eight 10-year-olds in Norway rated with the children’s version of the BRIEF, the Norwegian TDC were rated at similar levels to the American norm sample (Fallmyr & Egeland, 2011). Small numerical differences were registered, however, in favor of the Norwegian 10-year-olds scoring at a less impaired level than the American norms. A study in the Netherlands with 847 healthy children (ages 5-18) rated on the children’s version of the BRIEF reported the Dutch TDC to be rated significantly less impaired compared with the American normative sample (Huizinga & Smidts, 2010). The Dutch study indicated a particular discrepancy compared with the American norms in performance ratings for the older TDC (i.e., 9-18 years), but not the younger TDC (i.e., 5-8 years). The clinical range in the current study is based on the mean value for the 50 Norwegian TDC in the study. We have applied the same criteria for clinical cutoff rates as in the original manual (Gioia et al., 2000b). Higher T-scores on the BRIEF indicate a higher degree of impairment.

Scale Classifications

Based on the earlier mentioned research on behavior characteristics of the clinical groups, pairs of clinical scales were strategically selected to investigate their ability to differentiate between TS and other clinical groups. In the analyses comparing the TS and ADHD-C group, the EC and Inhibit scales were used. For the TS and ADHD-I group comparison, the EC and Plan/Organize scales were applied. In the TS and ASD comparison, the EC and Shift scales were analyzed. Table 2 provides an overview of the percentage of children in each clinical category scoring in the clinical range on the specific scales.

Table 2.

Percentage of Children in the Various Groups Rated in the Clinical Range^a on Each Scale.

	TS (n = 19)	ADHD-C (n = 33)	ADHD-I (n = 43)	ASD (n = 34)	TDC (n = 50)
BRIEF Scales
Inhibit	78%	88%	65%	79%	10%
Shift	78%	67%	67%	91%	8%
Emotional Control	94%	79%	84%	85%	8%
Initiate	67%	76%	77%	77%	10%
Working Memory	78%	94%	98%	85%	12%
Plan/Organize	78%	94%	95%	85%	10%
Organization of Materials	50%	73%	51%	47%	6%
Monitor	83%	94%	88%	94%	8%
BRIEF Indexes
Behavior Regulation Index^b	83%	88%	84%	91%	10%
Metacognition Index^c	89%	94%	95%	94%	10%
Global Executive Composite^d	89%	97%	95%	94%	10%

Note. TS = Tourette syndrome; ADHD-C = ADHD–combined; ADHD-I = ADHD–inattentive; ASD = autism spectrum disorders; TDC = typically developing children; BRIEF = Behavior Rating Inventory of Executive Function.

Clinical range is defined as a score higher than 1.5 SD above the mean value for the TDC.

Inhibit, Shift, and Emotional Control.

Initiate, Working Memory, Plan/Organize, Organization of Materials, and Monitor.

All eight clinical scales.

Data Analyses

Data analyses were conducted using the statistical package IBM SPSS Statistics for Windows, version 18.0 (SPSS, Inc., Chicago, Illinois). Demographic characteristics were investigated using the chi-square test for independence (nominal variables) and ANOVA (continuous variables) followed up by post hoc tests for group comparisons when appropriate.

Ratings on the individual scales and indices on the BRIEF data were analyzed with ANOVAs and post hoc analyses including a Bonferroni correction to account for multiple comparisons. Repeated-measures ANOVAs were conducted on each pair of scales to compare the parent ratings of the children with TS with each of the other clinical groups. To compare the frequencies of the expected scale patterns within each clinical group, a categorical variable was derived for each pair by subtracting the score on the paired scale from the EC scale, that is, EC scale minus Shift scale. A positive number was labeled “1” indicating a higher level of EC compared with the paired scale, and a negative number was labeled “2” indicating the opposite. A chi-square test for independence was then conducted for each pair to examine rates of classification into diagnostic groups.

Results

A one-way between-groups multivariate ANCOVA was performed to investigate overall everyday EF problems in the participants. The eight subscales and three composite scales on the BRIEF were entered as the dependent variables. The independent variable was group, and the covariates were gender and mother’s education level. There was a statistically significant difference between the TDC and each of the clinical groups on all of the combined dependent variables, F(44, 622) = 8.03, p ≤ .001, Wilks’s Lambda = .18, $η_{p}^{2}$ = .35. Gender was not significantly related, whereas mother’s education did show a significant interaction. ANOVAs with post hoc comparisons including a Bonferroni correction to account for multiple comparisons revealed that parent ratings on the BRIEF were consistently significantly higher on all clinical scales and indexes for each of the clinical groups compared with the TDC. This finding suggests a higher level of global EF impairment in children with clinical diagnoses (see Table 3 for overview). In the ANOVAs examining individual scales, the entire TS group and ADHD-C group were rated as significantly more impaired than the ADHD-I and ASD groups on the Inhibit scale, and the ASD group was rated as significantly more impaired than the ADHD-I/ADHD-C groups on the Shift scale.

Table 3.

Results on BRIEF Scales and Indexes: Means, Standard Deviations, and MANCOVA With Post Hoc Group Comparisons (Including Bonferroni Correction to Account for Multiple Comparisons).

Variable	TS (n = 19)	ADHD-C (n = 33)	ADHD-I (n = 43)	ASD (n = 34)	TDC (n = 50)	Group comparison		η²	Post hoc*
Variable	TS (n = 19)	ADHD-C (n = 33)	ADHD-I (n = 43)	ASD (n = 34)	TDC (n = 50)	F	p	η²	Post hoc*
Inhibit	65 (14.3)	67 (14.9)	55 (11.8)	59 (15.1)	42 (3.4)	F(4, 173) = 25.8	<.001	.37	TDC < ADHD-I and ASD < TS and ADHD-C
Shift	62 (15.2)	59 (13.9)	55 (10.5)	68 (14.0)	41 (4.9)	F(4, 173) = 32.6	<.001	.43	TDC < ADHD-I and ADHD-C < ASD TDC < TS
Emotional Control	65 (12.8)	61 (15.7)	59 (12.7)	61 (13.3)	41 (4.3)	F(4, 173) = 26.6	<.001	.38	TDC < all clinical groups
Initiate	60 (12.1)	61 (11.6)	59 (11.7)	59 (11.0)	41 (6.7)	F(4, 173) = 30.8	<.001	.42	TDC < all clinical groups
Working Memory	65 (15.8)	70 (11.3)	69 (8.6)	65 (12.3)	42 (4.6)	F(4, 173) = 61.3	<.001	.59	TDC < all clinical groups
Plan/Organize	59 (14.2)	66 (10.0)	65 (9.5)	62 (11.4)	41 (4.9)	F(4, 173) = 50.6	<.001	.54	TDC < all clinical groups
Organization of Materials	52 (13.0)	59 (10.2)	55 (11.4)	54 (11.8)	42 (7.6)	F(4, 173) = 17.6	<.001	.29	TDC < all clinical groups
Monitor	61 (13.2)	65 (11.7)	59 (11.6)	63 (12.7)	39 (5.6)	F(4, 173) = 43.8	<.001	.50	TDC < all clinical groups
Behavior Regulation Index^a	66 (14.2)	64 (15.6)	57 (10.8)	64 (13.2)	40 (4.0)	F(4, 172) = 36.0	<.001	.46	TDC < all clinical groups
Metacognition Index^b	61 (14.3)	68 (12.2)	64 (9.6)	62 (10.8)	40 (5.2)	F(4, 173) = 56.8	<.001	.57	TDC < all clinical groups
Global Executive Composite^c	64 (14.2)	68 (13.5)	62 (10.2)	64 (11.6)	39 (4.9)	F(4, 173) = 54.2	<.001	.56	TDC < all clinical groups

Note. BRIEF = Behavior Rating Inventory of Executive Function; TS = Tourette syndrome; ADHD-C = ADHD–combined; ADHD-I = ADHD–inattentive; ASD = autism spectrum disorders; TDC = typically developing children.

Inhibit, Shift, and Emotional Control.

Initiate, Working Memory, Plan/Organize, Organization of Materials, and Monitor.

All eight clinical scales.

p < .05 with Bonferroni correction for multiple comparisons.

EF ratings for the TS children without a co-occurring ADHD condition were compared with those for the TDC in ANOVAs with post hoc comparisons (including a Bonferroni correction to account for multiple comparisons) to see whether it was the co-occurring ADHD that was responsible for the higher impairment ratings. The same higher pattern of EF dysfunction was found for the TS children without comorbid ADHD compared to the TDC with the exception of the Organization of Materials scale for which there was no longer a difference between groups. In these follow-up analyses, the TS-only group also showed significantly lower impairment compared with the ADHD-C group on the Plan/Organize and Organization of Materials scales and the Metacognition Index, whereas the TS-only group was rated lower on the Plan/Organize scale than was the ADHD-I group.

The entire TS group was compared in Repeated Measures ANOVAs with each of the other clinical groups on pairs of scales selected based on the a priori hypotheses. For the first comparison of scale pairs, the entire TS and ASD groups were compared on the EC and Shift scales. A mixed between–within subjects analysis revealed a significant interaction between ratings on the two scales and group, Wilks’s Lambda = .84, F(1, 50) = 9.5, p < .01, $η_{p}^{2}$ = .16. There was no significant main effect, however, indicating similar levels of severity on the two scales. Figure 1 shows the interaction, with the entire TS group rated as substantially higher on the EC scale than the Shift scale and the ASD group showing the reverse pattern. The mixed between–within subjects analysis comparing the EC and Inhibit scale ratings for all the children with TS and those with ADHD-C again revealed a significant interaction between the two scales and group, Wilks’s Lambda = .92, F(1, 49) = 4.4, p < .05, $η_{p}^{2}$ = .08, and no main effects. Again, no main effect is a reflection of similar levels of severity on the two scales. The entire TS group was rated relatively higher on EC, whereas the ADHD-C group was rated relatively higher on inhibitory control. For the final comparison, the mixed model analysis revealed a significant interaction between the entire TS and ADHD-I groups and ratings on the EC and Plan/Organize, Wilks’s Lambda = .83, F(1, 59) = 12.5, p < .01, $η_{p}^{2}$ .18, with no main effects. Again, the results indicate similar levels of severity on this pair of scales. Children with TS were rated as having greater difficulties on the EC scale than on the Plan/Organize scale, whereas children with ADHD-I showed the opposite pattern. IQ and gender did not explain significant variance when entered as covariates in the above analyses. The analyses were repeated after removing the six children in the TS group who were also diagnosed with comorbid ADHD. In each instance, this resulted in a stronger interaction effect. Figure 1 presents a visual depiction of the strategic pair comparisons with the TS-only children (i.e., excluding the children with comorbid TS and ADHD or ASD).

Figure 1.

Comparing EF behavior on strategic scale classifications for TS compared with ADHD-C, ADHD-I, and ASD, respectively.

The chi-square test for independence (with Yates Continuity Correction) indicated a significant association between all three pair classifications. The TS children with comorbid ADHD-I, ADHD-C, or ASD were excluded in the analyses to avoid the possible confounding effect of co-occurring disorders on the results. A significant association was found between diagnosis and high/low on the EC and Shift scales for the TS-only and ASD children, χ²(1, n = 44) = 7.8, p < .01, phi = .48. Of the children with TS only, 70% had a higher score on the EC scale compared with the Shift scale, and of the children with ASD, 83% had a higher score on the Shift scale compared with the EC scale. Significant associations were also revealed between diagnosis and high/low on the EC and Inhibit scales for the TS-only and ADHD-C children, χ²(1, n = 43) = 4.3, p < .05, phi = −.37, and diagnosis and high/low on the EC and Plan/Organize scales for the TS-only and ADHD-I children, χ²(1, n = 53) = 4.4, p < .05, phi = −.34. Among the children with ADHD-C, 73% had a higher score on the Inhibit scale compared with the score on the EC scale, and 70% of the children with TS only had a higher score on the EC scale compared with the Inhibit scale. On the scale classification comparing EC with Plan/Organize scales, 63% children with ADHD-I had a higher score on the Plan/Organize scales compared with the score on the EC, whereas 80% of the TS-only children had a higher score on the EC scale compared with the score on the Plan/Organize scale.

Discussion

Confirming our first hypothesis, the TS group was rated as more impaired on all BRIEF scales compared with the TDC. With the exception of the Organization of Materials scale, this finding was sustained after excluding the TS children with co-occurring ADHD from the analyses. Children with TS were rated as having clinically significant EF difficulties in the everyday environment regardless of whether or not they were also diagnosed with comorbid ADHD. This finding contrasts with an earlier study that found that children with TS without ADHD were rated more similarly to TDC on measures of executive dysfunction on the BRIEF (Mahone et al., 2002). A number of differences in the TS participants between the two studies may explain the contrasting findings. First, the participants in the current study were first-time referrals for TS, whereas the children with TS in the study by Mahone et al. (2002) were already diagnosed patients in treatment. Being in treatment may have reduced the level of symptom reporting in the earlier study, whereas the need for treatment by the specialist health services at the time of testing in the present study may have resulted in a tendency for parents to report higher levels of symptoms. Second, the mean age in the current study is somewhat older (almost 12 years) than in the Mahone study (10 years). Developmental factors involved in the executive regulation processes might play a role in the reporting of behavioral difficulties. Regardless, our findings of no difference between the children with TS without comorbid ADHD and the TDC on the Organization of Materials scale emphasize the need to discriminate between TS with and without comorbid ADHD in future studies examining difficulties in EF behaviors.

In the overall comparison between clinical groups, the ratings on individual scales showed the TS and ADHD-C groups to be more impaired than the ADHD-I and ASD groups on the Inhibit scale, and the ASD group to be more impaired on the Shift scale compared with the ADHD-I and ADHD-C groups. The global analysis did not discriminate between the clinical categories. The general picture is that children in the clinical groups were rated by their parents as exhibiting higher levels of EF problems in a range of everyday situations compared with TDC. These findings provide evidence supporting the idea that there is considerable overlap of EF behavioral problems in children with neurodevelopmental disorders.

In our second hypothesis, we predicted that strategic pairs of scales could discriminate between TS and other diagnostic categories. The first scale comparison tested whether the EC and Shift scales could differentiate between children with TS and children with ASD. Whereas behavioral rigidity and cognitive inflexibility across functional domains characterize ASD and distinguish this group from children with TS (Geurts, Corbett, & Solomon, 2009; Ozonoff, Strayer, McMahon, & Filloux, 1994), differences in EC between the two groups are less clear. A study comparing children with ASD with TDC found the former to have elevated scores on all Behavioral Regulation scales on the BRIEF, with the strongest effect size for the Shift scale (Semrud-Clikeman, Walkowiak, Wilkinson, & Christopher, 2010). The analyses in our study confirmed the prediction that the groups of children with TS and ASD would have dissociable ratings when comparing the groups on the EC and Shift scales, with the TS group rated relatively higher on the EC subscale and the ASD lower, and the opposite pattern for ratings on the Shift subscale.

The second scale classification tested whether the EC and Inhibit scales could discriminate between the TS and ADHD-C groups. Both TS and ADHD-C are disorders characterized by excess motor activity (Leckman, 2002), but with widely varying criteria for diagnosis depending on whether the symptoms involve tics or restlessness. Both disorders are presumed to be symptomatic of anomalous basal ganglia-thalamo-cortical loops involving regions of the prefrontal cortex thought to mediate EF (Denckla & Reiss, 1997). Children with TS only are thought to have a different social-emotional profile than those with TS + ADHD (Carter et al., 2000), however, and thus the emotional salience of behaviors in the TS and ADHD-C group may be somewhat different. Emotional outbursts are reported to be particularly common in clinically referred children with TS (Budman et al., 2000), and are not necessarily related to symptoms of hyperactivity (Singer & Rosenberg, 1989). Yet, some studies report aggressive behavior (e.g., swearing, throwing, punching) in children with TS to be associated with the co-occurrence of ADHD (Stephens & Sandor, 1999). In our analyses, the EC and Inhibit scales dissociated between children with TS and children with ADHD-C, with the former exhibiting more problems regulating emotions and the latter group exhibiting relatively more difficulties inhibiting impulsive behaviors. These findings remained after controlling for both IQ and gender.

The third comparison tested the ability of the EC and Plan/Organize scales to discriminate between children with TS and children with ADHD-I. A previous study comparing children with ADHD-I and ADHD-C on the BRIEF concluded that metacognitive difficulties better characterize children with ADHD-I, whereas behavior regulation difficulties better characterized children with ADHD-C (Gioia et al., 2002). Although Working Memory is a metacognitive process considered to be a core deficit in children with ADHD-I (Diamond, 2005), it is a common impairment in children with neurodevelopmental disorders as well (Alloway & Gathercole, 2006). It may therefore be well-suited for differentiating ADHD-I from normal performance, but not for differentiating ADHD-I from other neurodevelopmental disorders. The metacognitive scale Plan/Organize was chosen for this scale classification to contrast the often disorganized behavior associated with ADHD-I with the relatively better metacognitive skills associated with TS (Mahone et al., 2002). In our analyses, a dissociation on the EC and Plan/Organize scales distinguished children with TS from children with ADHD-I. Children with TS were more elevated on the EC scale, whereas children with ADHD-I were more elevated on the Plan/Organize scale. These findings also held after controlling for IQ and gender.

Accurate identification of EF deficits is relevant not only for diagnosis but, perhaps more so, for prognosis because children with differing EF profiles will likely respond differently to interventions (Semrud-Clikeman, Walkowiak, Wilkinson, & Christopher, 2010). Important differences in outcome from treatment, for example, were shown for children with ADHD-C and ADHD-I who underwent the same general treatment for ADHD (Pfiffner et al., 2007), suggesting the need for accurate identification of behavior profiles even in quite similar psychopathologies. This study indicates that about three out of four children with TS have more problems controlling their emotions than with inhibition, mental flexibility, and planning/organizing abilities, whereas only about one in four children with ASD or ADHD-C have more problems controlling their emotions than with mental flexibility and inhibition, respectively. A failure to detect emotional dysregulation could represent a failure to address a potentially serious source of distress for children with TS and their families in their everyday lives. Some argue that a focus on specific EF difficulties rather than on diagnosis would provide a better basis for clinical treatment in any event (Pelham, 2001). Undoubtedly, obtaining a more accurate and detailed characterization of the executive difficulties of a child referred for treatment for his or her challenges in daily life will provide a better basis on which to design a tailored treatment program aimed at alleviating such difficulties. A better characterization of EF difficulties associated with neurodevelopmental disorders examined in the current study may provide a better understanding of the similarities and differences in behavioral impairment in these childhood-onset disorders and thereby improve treatment prospects in general as well.

This study had several strengths and weaknesses. The group of children with TS is rather small, several of the children with TS had comorbid disorders, and the groups span a rather large age range. Future studies should attempt to remedy these limitations by focusing on specific developmental stages related to EC, better controlling for co-existing disorders, and matching the clinical groups by age, IQ, and mother’s education. A more comprehensive accounting for symptoms of inattention and hyperactivity/impulsivity in the TS and ADHD-C groups should also be considerations addressed in future studies, as the symptom levels are similar in the two groups in the current study. Whereas small sample size and comorbid conditions increase the risk of Type II errors, significant findings with such a group indicate that the results may be clinically useful. The division into ADHD-C and ADHD-I subgroups is a strength (Mahone et al., 2002), as is the absence of medication use in all but two of the children with TS.

Conclusion

The present study indicates that parents of children with TS who were referred for treatment reported significant difficulties with EF in the everyday environment compared with TDC irrespective of co-occurring conditions. While there was considerable overlap in reported EF problems in children with TS, ADHD-C, ADHD-I and ASD, comparison of ratings on select scales helped distinguish between children with TS and children with ADHD-C, ADHD-I, or ASD. This suggests that children with a range of common developmental disorders show EF difficulties in general, but that there may be more specific characteristics in everyday EF for select groups. Specifically, children with TS were shown to have relatively more problems with EC than cognitive flexibility in relation to children with ASD, more problems with EC than inhibitory control in relation to children with ADHD-C, and more problems with EC than planning/organizing compared with the children with ADHD-I. The approach of using strategic scale classifications to differentiate clinical groups represents a promising first step for the more discriminate use of rating scales in differentiating EF difficulties. Identifying the specific deficit in EF for individual children may guide treatment toward more targeted interventions versus a global omnibus EF rating or intervention.

Footnotes

Declaration of Conflicting Interests

The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: The co-authors Gerard Gioia and Peter K. Isquith maintain financial interest in the Behavior Rating Inventory of Executive Function (BRIEF) as developers of the instrument. The first author and other co-authors declare no conflict of interest with respect to the authorship or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The project has received financial support from Innlandet Hospital Trust (IHT), Norway (Grant 150207) and the Regional Resource Center for Autism, ADHD, Tourette’s syndrome (TS), and Narcolepsy, Oslo University Hospital, Norway (Grant 150182).

Author Biographies

Kjell Tore Hovik, MA, is a clinical psychologist and PhD student at the Department of Psychology at the University of Oslo. In collaboration with the Innlandet Hospital Trust, Division Mental Health, his research focuses on the regulation of congition, emotion, and behavior in children and adolescents with neurodevelopmental disorders.

Jens Egeland, PhD, is a clinical neuropsychologist and professor at the Department of Psychology, University of Oslo. He is director of research in the Division of Mental Health and Addiction in Vestfold Hospital Trust, Norway. His research interest is in neurocognition related to ADHD and schizophrenia, as well as methodological issues related to neuropsychological tests and assessments.

Peter K. Isquith, PhD, is a licensed psychologist with specialty in developmental neuropsychology. He is assistant professor in psychiatry at the Geisel School of Medicine at Dartmouth College.

Gerard Gioia, PhD, is a pediatric neuropsychologist and the chief of the Division of Pediatric Neuropsychology at Children’s National Medical Center. He is professor of Pediatrics and Psychiatry at the George Washington University School of Medicine. His research includes examination of the executive functions, as well as outcomes of mild traumatic brain injury in children. He is coauthor of a variety of assessment instruments including the Behavior Rating Inventory of Executive Function.

Erik Winther Skogli, PhD, is a clinical psychologist. In collaboration with the Innlandet Hospital Trust, Division Mental Health, his research interests include the development of cognitive and emotional regulation in children and adolescents with ADHD.

Per Normann Andersen, MA in Special Education, has worked 20 years in child and adolescent psychiatry assessing and treating neuropsychiatric disorders. He is currently a PhD student at the Department of Psychology, University of Oslo, and is conducting research at the Innlandet Hospital Trust, Division Mental Health. His research interests include emotional and cognitive impairments in children with Autistic Spectrum Disorders.

Merete Øie, PhD, is a clinical neuropsychologist and professor at the Department of Psychology, University of Oslo, and a research adviser at the Innlandet Hospital Trust, Division Mental Health. Her research interests include neuropsychological functions in ADHD and other neuropsychiatric disorders.

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