Preschool Inhibitory Control Predicts ADHD Group Status and Inhibitory Weakness in School

Preschool Inhibitory Control Predicts ADHD Group Status and Inhibitory Weakness in School Abstract Objective Discriminative utility of performance measures of inhibitory control was examined in preschool children with and without ADHD to determine whether performance measures added to diagnostic prediction and to prediction of informant-rated day-to-day executive function. Method Children ages 4–5 years (N = 105, 61% boys; 54 ADHD, medication-naïve) were assessed using performance measures (Auditory Continuous Performance Test for Preschoolers-Commission errors, Conflicting Motor Response Test, NEPSY Statue) and caregiver (parent, teacher) ratings of inhibition (Behavior Rating Inventory of Executive Function-Preschool version). Results Performance measures and parent and teacher reports of inhibitory control significantly and uniquely predicted ADHD group status; however, performance measures did not add to prediction of group status beyond parent reports. Performance measures did significantly predict classroom inhibitory control (teacher ratings), over and above parent reports of inhibitory control. Conclusions Performance measures of inhibitory control may be adequate predictors of ADHD status and good predictors of young children’s classroom inhibitory control, demonstrating utility as components of clinical assessments. Attention, Children and behavioral disorders, Developmental and learning disabilities, Executive functions, Assessment Inhibition is a critical construct in developmental psychopathology (Nigg, 2000) and an early developing and core element of executive control (Diamond, 2013). Inhibitory control is strongly associated with children’s social competence and externalizing behaviors (Nigg, Quamma, Greenberg, & Kusche, 1999), with specific deficits in inhibitory control considered a key component of the Attention-deficit/Hyperactivity Disorder (ADHD) phenotype (Barkley, 1997; Oosterlaan, Logan & Sergeant, 1998; Willcutt, Doyle, Nigg, Faraone & Pennington, 2005). As such, early identification of deficits in inhibitory control may help not only to predict adaptive outcomes but also to add value to clinical diagnosis of ADHD. A recent practice survey of pediatric neuropsychologists suggests that ADHD is the most common condition for which a neuropsychological evaluation is sought (Sweet, Benson, Nelson, & Moberg, 2015). Given this need for ADHD diagnostic clarification, early measures of inhibition may be particularly helpful in identifying younger children with ADHD as well as clarifying particular patterns of neuropsychological impairment in need of support. Emerging work suggests that deficient response inhibition in children with ADHD can be substantially improved via contingent reinforcement and stimulant medication (Rosch et al., 2016), suggesting that early identification of inhibitory control deficits may be helpful in identifying meaningful targets for remediation. There are a variety of methods that have been used to assess inhibitory control in children, including performance tasks of motor and cognitive inhibition as well as informant ratings of behavior. Caregiver ratings of adolescent inhibitory control have been shown to predict ADHD group status, while performance measures of the same construct appear to contribute little additional variance (Toplak et al., 2008). In preschool children specifically, prior research suggests that caregiver ratings of inhibitory control may hold the most discriminatory value when identifying ADHD in young children (Ezpeleta, Granero, Penelo, de la Osa, & Domenech, 2015; Skogan et al., 2015); ratings of inhibitory control accurately identified approximately 80% of a sample of preschool children with ADHD (Skogan et al., 2015). Unfortunately, much of the work examining associations among early performance measures and parent reported executive weaknesses has focused solely on continuous performance tasks rather than also considering performance on other measures of inhibition. A recent study found only a weak relationship between parent ratings and commission errors in preschoolers; no significant associations were identified between caregiver ratings of inhibition and other performance measures of impulsivity (perseverations, hit reaction time) (Çak, Çengel-Kültür, Gökler, Öktem & Taşkıran, 2017). Furthermore, parent ratings of executive behaviors failed to achieve incremental predictive accuracy for ADHD, over and above continuous performance tasks (Ezpeleta et al., 2015). The limited association between informant ratings and neuropsychological measures has been well documented in older children (e.g., McAuley, Chen, Goos, Schachar, & Crosbie, 2010), however, with both sources of clinical information important to neuropsychological assessment (e.g., Mahone, Slomine & Zabel, in press). Since behavioral ratings and performance measures of inhibitory control typically share only a modest proportion of variance, examination of the value of both sources of data regarding inhibitory control in early identification of ADHD may help guide clinical practice. Given the importance of early diagnosis and intervention, it remains to be determined whether performance measures show better predictive power at the preschool-age level. The purpose of the present study was to: (1) examine utility of performance measures of inhibitory control in preschool children as the basis for discriminating children with ADHD from typically developing children; and (2) contrast the prediction from performance measures with that of caregiver (parent, teacher) ratings of behavioral inhibition in characterizing ADHD diagnostic status. Because our research diagnostic groups were assigned, based in part upon caregiver report of ADHD symptomatology (per DSM-IV-TR), we hypothesized that performance measures of inhibitory control would be independently predictive of group membership, but that caregiver reports measures of day-to-day executive control would show stronger prediction of group status. Additionally, although the limited associations among performance measures and informant rating scales have been well documented, because study group membership was based upon caregiver report of symptomatology, we sought to determine whether the performance measures added to prediction of informant-rated day-to-day function outside the home (i.e., teacher ratings of inhibitory control), over and above parent reports of inhibitory control. METHODS Study Procedures Approval was granted by the hospital’s Institution Review Board. Participants were recruited from advertisements in the community, pediatricians’ offices, and local daycare centers, to participate in a longitudinal study of brain development. After description of the study, parents of participants signed written consent, and child participants provided verbal assent. Participants were initially screened via telephone interview with a parent to determine eligibility. Once enrolled, participants completed a neuropsychological assessment battery that included the cognitive, language, and inhibitory control measures. Parents (and teachers, if available) also completed behavior rating scales at the time of testing. Participants Inclusion and exclusion procedures Participants were excluded if they had any of the following, established via review of medical/developmental history, and/or by study screening assessment: (1) diagnosis of Intellectual Disability or Autism Spectrum Disorder; (2) known visual impairment; (3) treatment of any psychiatric disorder (other than ADHD) with psychotropic medications [for those with diagnosis of ADHD, treatment with stimulants was allowed, whereas children treated with other psychotropic medications were excluded]; (4) any history of DSM-IV Axis I diagnosis other than Oppositional Defiant Disorder or Adjustment Disorder; (5) neurological disorder (e.g., epilepsy, traumatic brain injury, tic disorder); (6) documented hearing loss ≥25 dB loss in either ear; (7) reported history of physical, sexual, or emotional abuse; (8) Full Scale IQ scores <80 (as determined by previous assessment or study screening assessment). In addition, children were excluded if there was a history of a Developmental Language Disorder (DLD) either determined during the initial phone screen, based on prior assessment (completed within 1 year of the current assessment), or determined during screening visit. DLD exclusion was made in deference to evidence that language impairments may influence development of inhibitory control, response preparation, and working memory—core features of ADHD (Hagberg, Miniscalco, & Gillberg, 2010). Diagnostic methods for the ADHD and control groups were adapted from the NIH Preschoolers with Attention-Deficit/Hyperactivity Disorder Treatment (PATS) Study (Kollins et al., 2006; Posner et al., 2007). For 4-year olds, diagnosis of ADHD was made using modified DSM-IV-TR criteria, based on parent report on the Diagnostic Interview Schedule for Children-Young Child (YC-DISC) (Lucas, Fisher, & Luby, 1998, 2008) or Diagnostic Interview for Children and Adolescents, Fourth Edition—DICA-IV (Reich, Welner, & Herjanic, 1997), depending on age, and the DSM-IV ADHD Scales (Scales L and M) of the Conners’ Parent Rating Scales-Revised (CPRS-R; Conners, 1997). The YC-DISC is a highly structured, computer-assisted diagnostic instrument that assesses common psychiatric disorders, as defined by DSM-IV, that present in young children. The DICA-IV is the parallel version of the computer-assisted, structured interview for older children and adolescents. In the present study, the DISC-YC was used for 4-year olds and the DICA-IV was used for 5-year olds. To be included in the ADHD group, symptoms must have been present for at least 6 months, and cross-situational impairment (defined as parent report of problems at home and with peers, as not all children were enrolled in school) was required. Additionally, children in the ADHD group were required to have T-scores ≥ 65 on one or both of the DSM-IV ADHD Scales (Scales L and M) of the CPRS-R. Once children met general entry/exclusion criteria above, they were included in the control group only if they did not meet categorical diagnostic criteria for ADHD on the YC-DISC or DICA-IV. Additionally, children in the control group were required to have T-scores ≤ 60 on the CPRS-R DSM-IV ADHD Scales. Measures Auditory Continuous Performance Test for Preschoolers (Mahone, Pillion, & Hiemenz, 2001) The Auditory Continuous Performance Test for Preschoolers (ACPT-P) is a computerized, auditory go/no-go task. Two presented auditory stimuli (dog bark, bell) are used as target and non-target respectively, with the child instructed to push the space bar only when a bark is heard. Duration of each stimulus is 690 ms, with a fixed inter-stimulus interval of 5,000 ms. A total of 18 targets and 15 non-targets are arranged randomly so that the child is presented four targets and 11 non-targets in the first half of the test, and 11 targets and four non-targets in the second half of the test. The total time of the test is approximately 5 min, with practice trials. The number of commission errors served as a measure of inhibitory control and the dependent variable of interest. Lower commission scores indicate greater behavioral inhibition. Due to the skewed nature of the ACPT-P Commission errors variable (skewness = 1.86; kurtosis = 2.99), the data were log transformed; following transformation, data fell within acceptable parameters (skewness = .294; kurtosis = −1.55). Conflicting motor response This task was adapted from the Luria-Christensen Battery (Christensen, 1975) and has been used to examine motor response inhibition deficits in children (Mahone et al., 2006). Children are told, “If I show you my finger, you show me your fist; if I show you my fist, you show me your finger.” The examiner presents each of the two gestures 12 times (for a total of 24 presentations) in random sequence, at a rate of one per second. Response inhibition is assessed through the total number of correct responses and errors. The dependent variable of interest was the number of correct responses made, with higher scores indicating greater behavioral inhibition. Conflicting Motor Response has been significantly correlated with other measures of motor control, such as Contralateral Motor Response (r = .52, p < .001), and NEPSY Statue (r = .23, p < .01) (Mahone et al., 2006). Statue (NEPSY-II; Korkman, Kirk, & Kemp, 2007) The Statue subtest is a measure of inhibition and motor persistence in which the child is asked to maintain a body position with eyes closed for 75 s, while inhibiting the impulse to respond to sound distractors. Reliability coefficients are .82 and .88 for ages 4 and 5, respectively. Errors made are converted to a norm-referenced scaled score, with higher scores indicating better behavioral inhibition. Behavior Rating Inventory of Executive Function-Preschool Version (Gioia, Epsy, & Isquith, 2003) The Behavior Rating Inventory of Executive Function-Preschool Version (BRIEF-P) is a rating scale for children ages 2–5 years designed to be completed by parents/caregivers or teachers that assesses executive behaviors in daily environments. Ratings of participants’ executive behavior were obtained from parents and from teachers when available (e.g., not all children were attending preschool or school programs). The BRIEF-P is organized into five clinical scales, with raw scores converted to age-referenced T-scores; the Inhibit scale served as the dependent variable of interest. Lower T-scores indicate caregiver ratings suggesting greater behavioral inhibition. Internal consistency and reliability for the Inhibit scale is good (α = .90 for parent report and α = .94 for teacher report). Published agreement between parent and teacher ratings on the Inhibit scale was weak; r = .25 (p < .01); however, the Inhibit scale is well-correlated with the ADHD-IV Hyperactivity-Impulsivity scale (r = .87 for parent report and r = .85 for teacher report, both p < .001). Conners’ Parent Rating Scales-Revised-Long Form (Conners, 1997) Dimensional ratings of ADHD symptom severity were obtained using the DSM-IV oriented scales from the Conners’ Parent Rating Scales-Revised-Long Form (CPRS-R), including Scale L (DSM-IV Inattentive) and Scale M (DSM-IV Hyperactive/Impulsive). Internal consistency for ages 3–5 on these scales ranged from .86 to .94. Clinical Evaluation of Language Functions-Preschool-2 (Wiig, Secord, & Semel, 2004) The Clinical Evaluation of Language Functions-Preschool-2 (CELF-P) is an individually administered, norm-referenced test developed to identify language and communication disorders in preschool children. Participants scoring <−1.5 SD on either the Receptive Language or Expressive Language Index of the CELF-P, or <−1.0 SD on both indices, were excluded. The CELF-P Core Language Index was used in analyses as measure of language competence. Wechsler Preschool and Primary Scale of Intelligence-Third Edition (Wechsler, 2002) The Wechsler Preschool and Primary Scale of Intelligence-Third Edition (WPPSI-III) is a widely used measure of early cognitive abilities. Although the Full Scale IQ score (FSIQ) was used in determining participant eligibility, the Verbal IQ (VIQ) and Performance IQ (PIQ) indices were used in analyses in order to minimize effects of processing speed when examining cognitive differences between groups. Data Analysis Plan Demographic variables were compared using one-way ANOVAs to assess differences between groups. Next, a series of logistic regressions examined each of the performance-based measures of inhibition (ACPT-P Commissions, Conflicting Motor Response Test, NEPSY-2 Statue), both with and without covariates of cognitive and language skills (WPPSI-III VIQ, WPPSI-III PIQ, and CELF-P Core Language Index), to determine whether performance measures of inhibitory control were individually predictive of ADHD group classification. Following these analyses, hierarchical logistic regression examined whether performance measures (as a group) added additional unique predictive value beyond BRIEF-P parent and teacher ratings. As a final step, an additional hierarchical linear regression examined whether the performance measures added to prediction of teacher ratings of classroom inhibitory control, over and above the contribution of parent ratings of the same construct. RESULTS The sample included 105 children, ages 4–5 years (M = 4.98, SD = 0.57), including 51 typically developing children (32 boys, 19 girls) and 54 children with clinical symptoms of ADHD (32 boys, 22 girls; see Table 1). None were prescribed stimulant medication at the time of participation, although several began treatment shortly afterward. The sample was predominantly Caucasian (84%), with an additional 11% of the sample identifying as African American. The remaining 5% identified as Asian (3%), multiple races (1%), and Other (1%). There were no significant group differences in the distribution of race (χ2(2) = 5.29, p = .259) or in VIQ, PIQ, or Core Language scores (Table 1). As anticipated, the ADHD group received significantly higher symptom ratings on the CPRS-R DSM-IV scales. Table 1. Participant demographics Control (n = 51) ADHD (n = 54) p Mean SD Mean SD Age 4.92 0.56 5.05 0.58 .262 CPRS-R DSM-IV Total 46.45 6.05 77.15 9.61 <.001 VIQ 113.33 14.11 111.55 12.84 .500 PIQ 106.14 16.62 108.43 15.96 .471 Core Language 106.28 11.47 106.35 10.31 .971 Commissions 0.745 1.21 2.35 2.92 <.001 Conflicting Motor 14.67 4.51 12.13 4.82 .006 Statue 9.61 3.31 6.63 4.09 <.001 Control (n = 51) ADHD (n = 54) p Mean SD Mean SD Age 4.92 0.56 5.05 0.58 .262 CPRS-R DSM-IV Total 46.45 6.05 77.15 9.61 <.001 VIQ 113.33 14.11 111.55 12.84 .500 PIQ 106.14 16.62 108.43 15.96 .471 Core Language 106.28 11.47 106.35 10.31 .971 Commissions 0.745 1.21 2.35 2.92 <.001 Conflicting Motor 14.67 4.51 12.13 4.82 .006 Statue 9.61 3.31 6.63 4.09 <.001 Note: CPRS-R = Conners’ Parent Rating Scale (N scale T-score); VIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Verbal IQ standard score; PIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Performance IQ standard score. Table 1. Participant demographics Control (n = 51) ADHD (n = 54) p Mean SD Mean SD Age 4.92 0.56 5.05 0.58 .262 CPRS-R DSM-IV Total 46.45 6.05 77.15 9.61 <.001 VIQ 113.33 14.11 111.55 12.84 .500 PIQ 106.14 16.62 108.43 15.96 .471 Core Language 106.28 11.47 106.35 10.31 .971 Commissions 0.745 1.21 2.35 2.92 <.001 Conflicting Motor 14.67 4.51 12.13 4.82 .006 Statue 9.61 3.31 6.63 4.09 <.001 Control (n = 51) ADHD (n = 54) p Mean SD Mean SD Age 4.92 0.56 5.05 0.58 .262 CPRS-R DSM-IV Total 46.45 6.05 77.15 9.61 <.001 VIQ 113.33 14.11 111.55 12.84 .500 PIQ 106.14 16.62 108.43 15.96 .471 Core Language 106.28 11.47 106.35 10.31 .971 Commissions 0.745 1.21 2.35 2.92 <.001 Conflicting Motor 14.67 4.51 12.13 4.82 .006 Statue 9.61 3.31 6.63 4.09 <.001 Note: CPRS-R = Conners’ Parent Rating Scale (N scale T-score); VIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Verbal IQ standard score; PIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Performance IQ standard score. Individual logistic regression analyses indicated that all three performance measures of inhibitory control significantly predicted ADHD group status in the expected directions (see Table 2). Of the three measures, Statue was most predictive of ADHD status, with performance on this task correctly classifying 68.6% of the typically developing children and 64.8% of the children in the ADHD group. ACPT-P Commission errors correctly classified typically developing and ADHD children at a rate of 58.8% and 61.1%, respectively, while performance on the Conflicting Motor Response task correctly identified 58.8% and 57.4%. Table 2. Prediction of group status from performance-based measures of inhibitory control Task Exp(Β) 95% CI Wald’s X2 p Commissions 2.193 1.25–3.84 7.531 .006 Conflicting Motor 0.889 0.82–0.97 6.908 .009 Statue 0.814 0.73–0.91 13.365 <.001 Task Exp(Β) 95% CI Wald’s X2 p Commissions 2.193 1.25–3.84 7.531 .006 Conflicting Motor 0.889 0.82–0.97 6.908 .009 Statue 0.814 0.73–0.91 13.365 <.001 Note: CI = confidence interval; Commissions (log transformed score). Table 2. Prediction of group status from performance-based measures of inhibitory control Task Exp(Β) 95% CI Wald’s X2 p Commissions 2.193 1.25–3.84 7.531 .006 Conflicting Motor 0.889 0.82–0.97 6.908 .009 Statue 0.814 0.73–0.91 13.365 <.001 Task Exp(Β) 95% CI Wald’s X2 p Commissions 2.193 1.25–3.84 7.531 .006 Conflicting Motor 0.889 0.82–0.97 6.908 .009 Statue 0.814 0.73–0.91 13.365 <.001 Note: CI = confidence interval; Commissions (log transformed score). Additionally, these models were examined again, including measures of intelligence (WPPSI-III VIQ and PIQ) and language (CELF-P Core Language) as covariates. As expected, IQ and language measures offered no significant unique additional predictive value in classifying children with ADHD symptoms versus typically developing children. Including these measures in the model, performance on two of three measures of inhibitory control continued to predict group membership (Table 3). Table 3. Prediction of group status from performance-based measures of inhibitory control, controlling for intelligence and language ability Exp(Β) 95% CI Wald’s X2 p Intelligence/Language measures  VIQ 0.973 0.93–1.01 1.685 .194  PIQ 1.012 0.99–1.04 0.749 .387  Core Language 1.018 0.97–1.07 0.454 .500 Inhibitory Control measures  Commissions 1.829 0.95–3.53 3.258 .071  Conflicting Motor .902 0.82–0.99 4.062 .044  Statue .857 0.76–0.97 6.255 .012 Exp(Β) 95% CI Wald’s X2 p Intelligence/Language measures  VIQ 0.973 0.93–1.01 1.685 .194  PIQ 1.012 0.99–1.04 0.749 .387  Core Language 1.018 0.97–1.07 0.454 .500 Inhibitory Control measures  Commissions 1.829 0.95–3.53 3.258 .071  Conflicting Motor .902 0.82–0.99 4.062 .044  Statue .857 0.76–0.97 6.255 .012 Note: CI = confidence interval; VIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Verbal IQ standard score; PIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Performance IQ standard score; Commissions (log transformed score). Table 3. Prediction of group status from performance-based measures of inhibitory control, controlling for intelligence and language ability Exp(Β) 95% CI Wald’s X2 p Intelligence/Language measures  VIQ 0.973 0.93–1.01 1.685 .194  PIQ 1.012 0.99–1.04 0.749 .387  Core Language 1.018 0.97–1.07 0.454 .500 Inhibitory Control measures  Commissions 1.829 0.95–3.53 3.258 .071  Conflicting Motor .902 0.82–0.99 4.062 .044  Statue .857 0.76–0.97 6.255 .012 Exp(Β) 95% CI Wald’s X2 p Intelligence/Language measures  VIQ 0.973 0.93–1.01 1.685 .194  PIQ 1.012 0.99–1.04 0.749 .387  Core Language 1.018 0.97–1.07 0.454 .500 Inhibitory Control measures  Commissions 1.829 0.95–3.53 3.258 .071  Conflicting Motor .902 0.82–0.99 4.062 .044  Statue .857 0.76–0.97 6.255 .012 Note: CI = confidence interval; VIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Verbal IQ standard score; PIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Performance IQ standard score; Commissions (log transformed score). Next, the BRIEF-P parent report Inhibit scale (T-score) was included as the first step in the logistic regression analysis to determine whether the performance measures, while predictive of group membership individually, added additional accuracy to group classification over and above parent report of day-to-day difficulties with inhibitory control. The parent report Inhibit scale significantly predicted group membership (OR = 1.287), and correctly classified 90.2% of typically developing children and 94.4% of children with ADHD. When the effect of performance measures of inhibitory control was assessed in combination with the parent rated Inhibit scale, the performance measures no longer had a significant affect on classification accuracy. Including both sets of measures, classification accuracy increased in the control group to 94.1%, but decreased for the ADHD group to 92.6%. Of the 105 children included in this analysis, 75 had teacher reported BRIEF-P measures available. The teacher-reported Inhibit scale (T-score) was independently significantly predictive of group status; however, when parent report of inhibition was also included in the model, the teacher report no longer significantly contributed to predictions of group status (see Table 4). As was the case with the BRIEF-P parent ratings, when both BRIEF-P parent and teacher ratings were included in the model, performance measures of inhibitory control no longer predicted group membership. Table 4. Prediction of group membership from caregiver ratings and performance-based measures of inhibitory control Exp(Β) 95% CI Wald’s X2 p Analysis 1  BRIEF-P parent Inhibit 1.287 1.16–1.43 21.304 <.001  Performance Measures   Commissions 2.737 0.64–11.70 1.845 .174   Conflicting Motor 0.861 0.68–1.09 1.582 .209   Statue 1.020 0.79–1.32 0.023 .879 Analysis 2  BRIEF-P parent Inhibit 1.235 1.11–1.38 13.841 <.001  BRIEF-P teacher Inhibit 1.054 0.98–1.13 2.232 .135  Performance Measures   Commissions 3.512 0.53–23.15 1.704 .192   Conflicting Motor 0.845 0.64–1.12 1.394 .238   Statue 0.994 0.76–1.31 0.002 .192 Exp(Β) 95% CI Wald’s X2 p Analysis 1  BRIEF-P parent Inhibit 1.287 1.16–1.43 21.304 <.001  Performance Measures   Commissions 2.737 0.64–11.70 1.845 .174   Conflicting Motor 0.861 0.68–1.09 1.582 .209   Statue 1.020 0.79–1.32 0.023 .879 Analysis 2  BRIEF-P parent Inhibit 1.235 1.11–1.38 13.841 <.001  BRIEF-P teacher Inhibit 1.054 0.98–1.13 2.232 .135  Performance Measures   Commissions 3.512 0.53–23.15 1.704 .192   Conflicting Motor 0.845 0.64–1.12 1.394 .238   Statue 0.994 0.76–1.31 0.002 .192 Note: BRIEF-P = Behavior Rating Inventory of Executive Function- Preschool Version; Commissions (log transformed score). Table 4. Prediction of group membership from caregiver ratings and performance-based measures of inhibitory control Exp(Β) 95% CI Wald’s X2 p Analysis 1  BRIEF-P parent Inhibit 1.287 1.16–1.43 21.304 <.001  Performance Measures   Commissions 2.737 0.64–11.70 1.845 .174   Conflicting Motor 0.861 0.68–1.09 1.582 .209   Statue 1.020 0.79–1.32 0.023 .879 Analysis 2  BRIEF-P parent Inhibit 1.235 1.11–1.38 13.841 <.001  BRIEF-P teacher Inhibit 1.054 0.98–1.13 2.232 .135  Performance Measures   Commissions 3.512 0.53–23.15 1.704 .192   Conflicting Motor 0.845 0.64–1.12 1.394 .238   Statue 0.994 0.76–1.31 0.002 .192 Exp(Β) 95% CI Wald’s X2 p Analysis 1  BRIEF-P parent Inhibit 1.287 1.16–1.43 21.304 <.001  Performance Measures   Commissions 2.737 0.64–11.70 1.845 .174   Conflicting Motor 0.861 0.68–1.09 1.582 .209   Statue 1.020 0.79–1.32 0.023 .879 Analysis 2  BRIEF-P parent Inhibit 1.235 1.11–1.38 13.841 <.001  BRIEF-P teacher Inhibit 1.054 0.98–1.13 2.232 .135  Performance Measures   Commissions 3.512 0.53–23.15 1.704 .192   Conflicting Motor 0.845 0.64–1.12 1.394 .238   Statue 0.994 0.76–1.31 0.002 .192 Note: BRIEF-P = Behavior Rating Inventory of Executive Function- Preschool Version; Commissions (log transformed score). As a final step examining a separate functional outcome, we examined whether the performance measures added to predictions of day-to-day inhibitory control as reported by teachers (Table 5). The performance measures as a group accounted for a substantial proportion of variance in teacher ratings of inhibitory control (R2 = .31, p < .001), suggesting that these measures do help to predict day-to-day affect in other settings outside the lab. Furthermore, even with parent ratings included in the model, two of the three performance measures (ACPT Commissions, β = .267, p = .004; Conflicting Motor, β = −.226, p = .013) remained significant predictors of classroom inhibitory control. Table 5. Prediction of teacher rated inhibitory control from performance-based measures of inhibitory control R2/ΔR2 β p Analysis 1  Performance measures .312 <.001   Commissions .329 .002   Conflicting Motor −.291 .006   Statue −.192 .076 Analysis 2  BRIEF-P parent Inhibit .382 <.001  Performance measures .126 .001   Commissions .267 .004   Conflicting Motor −.226 .013   Statue −.034 .725 R2/ΔR2 β p Analysis 1  Performance measures .312 <.001   Commissions .329 .002   Conflicting Motor −.291 .006   Statue −.192 .076 Analysis 2  BRIEF-P parent Inhibit .382 <.001  Performance measures .126 .001   Commissions .267 .004   Conflicting Motor −.226 .013   Statue −.034 .725 Note: BRIEF-P = Behavior Rating Inventory of Executive Function- Preschool Version; Commissions (log transformed score). Table 5. Prediction of teacher rated inhibitory control from performance-based measures of inhibitory control R2/ΔR2 β p Analysis 1  Performance measures .312 <.001   Commissions .329 .002   Conflicting Motor −.291 .006   Statue −.192 .076 Analysis 2  BRIEF-P parent Inhibit .382 <.001  Performance measures .126 .001   Commissions .267 .004   Conflicting Motor −.226 .013   Statue −.034 .725 R2/ΔR2 β p Analysis 1  Performance measures .312 <.001   Commissions .329 .002   Conflicting Motor −.291 .006   Statue −.192 .076 Analysis 2  BRIEF-P parent Inhibit .382 <.001  Performance measures .126 .001   Commissions .267 .004   Conflicting Motor −.226 .013   Statue −.034 .725 Note: BRIEF-P = Behavior Rating Inventory of Executive Function- Preschool Version; Commissions (log transformed score). Discussion The present findings suggest that performance-based neuropsychological measures of inhibition designed for preschoolers do help discriminate between children with and without ADHD, and remain significant predictors of group status even after controlling for cognitive and language abilities. Furthermore, parent reports (based on rating scales) of day-to-day behavioral inhibition also predict group status; however, when informant reports are entered first in the model, performance measures no longer add significantly to this prediction. Likewise, with parent report of behavioral inhibition entered first in the model, teacher reports of classroom behavioral inhibition also do not add to prediction of group status. However, in contrast to prior findings describing limited associations between performance measures of executive function and day-to-day function as measured by rating scales (e.g., McAuley et al., 2010), performance measures of inhibition added significantly to prediction of teacher ratings of young children’s classroom inhibitory control – even after inclusion of parent ratings in the model. These data suggest that, by themselves, performance measures of inhibitory control may be generally adequate predictors of ADHD status and somewhat stronger predictors of cross-setting behavioral control in preschool-aged children, and therefore have some utility as components of clinical assessments. Moreover, different aspects of inhibitory control show differential trajectories of development throughout childhood (Best & Miller, 2010; Dempster, 1993; Rothbart & Bates, 1998), potentially related to the protracted development of the multiple underlying brain systems supporting inhibitory control (e.g., anterior cingulate, lateral and orbital prefrontal cortex, basal ganglia). Notably, however, performance measures of inhibitory control have been shown to predict both concurrent and later ADHD symptomatology (Martel et al., 2007; Oosterlaan et al., 1998; Pennington & Ozonoff, 1996), mood symptoms (Kertz, Belden, Tillman & Luby, 2016), as well as important academic skills such as math (Allan, Hume, Allan, Farrington, & Lonigan, 2014; Blair & Razza, 2007) and language (Blair & Razza, 2007). As such, performance measures have the potential to add clinical value to assessments of preschool-age children in terms of predicting need for intervention and forecasting a variety of critical outcomes, especially considering the association between these early performance measures and informant ratings of day-to-day function. Given the importance of early intervention as a means of minimizing developmental psychopathology and the substantial later costs associated with preschool ADHD (Chorozoglou, Smith, Koerting, Thompson, Sayal & Sonuga-Barke, 2015), early identification of children at highest risk for poorer outcomes is a priority for developmental and pediatric neuropsychological evaluations and should take advantage of a multi-modal approach. Further work is needed to clarify the most effective and predictive methods for assessing multiple aspects of early inhibitory control. Current ADHD diagnostic criteria require informant ratings of symptomatology; in the present study, parent reports of ADHD symptoms on the CPRS-R were used in conjunction with structured parent psychiatric interview for group assignments, consistent with methodology modified from the PATS studies (Kollins et al., 2006; Posner et al., 2007). In considering the prediction of group status from the BRIEF-P, findings are limited somewhat by similarity of item content of the BRIEF-P Inhibit scale and the CPRS-R scale M (DSM-IV hyperactivity-impulsivity) in this age group; item-level examination suggests a substantial overlap of six items between the CPRS-R M scale and the 10-item BRIEF-P Inhibit scale. In this sample, these two scales are highly correlated (r = .91), although parent and teacher ratings on the BRIEF-P are not as strongly correlated with each other (i.e., r = .28 and .31, for controls and ADHD, respectively). As such, the present observation that parent ratings on the BRIEF-P are most predictive of group membership (which was based in part on parent ratings of ADHD symptoms on the CPRS-R) is not surprising. Nevertheless, performance measures remain important in the overall clinical assessment and prediction of risk, since preschoolers’ behavior can be variable and setting- or context-dependent. In other words, performance during the in-clinic neuropsychological assessment may potentially map more closely onto behavior in other more structured settings, such as that of the classroom, as well as onto later academic achievement (Dekker, Ziermans, Spruijt & Swaab, 2017). There is a large body of work highlighting the (often modest) associations between performance-based measures of executive function and informant ratings of executive control behavior in daily settings (e.g., see McAuley et al., 2010 for a review). However, in the present study, performance measures did help to predict behavior in other settings, accounting for 31% of the variance in teacher BRIEF-P Inhibit scores. Findings should also be considered in light of the sampling criteria used. Specifically, children with a variety of identified comorbidities or neurologic disorders were excluded from the study, which may have contributed to the lack of intellectual or language score differences between groups. As such, findings may not entirely generalize to the more common comorbid presentation of children with ADHD symptomatology. In addition, exclusion of comorbidities may have also contributed to the high IQ scores in the ADHD group (Waber et al., 2007); the relatively high cognitive level of both groups may limit generalizability of findings to other samples of young children with emerging symptoms of ADHD, particularly those with comorbidities likely to lower observed IQ scores. However, at the same time, it is important to note that exclusion of comorbidities allows for greater understanding of ADHD-specific impacts upon performance. Furthermore, participants (in the ADHD group) were selected based upon early emerging symptoms of the disorder, thus differences may exist between those children with symptoms already evident in preschool versus the larger population of youth whose symptoms only appear evident later in development. Notably, diagnostic classification over the preschool to early school-age time period may be unstable (Chacko, Wakschlag, Hill, Danis, & Espy, 2009) and we do not know how many of those within the ADHD group will still meet diagnostic criteria at later assessments and thus prove “true positives” in terms of early diagnostic accuracy. However, there is also evidence for stability of early diagnoses of ADHD, in that 89% of the preschoolers in the PATS sample continued to meet criteria for ADHD at 6 year follow-up (Riddle et al., 2013). Given that onset during early childhood is associated with significant long-term costs (Chorozoglou et al., 2015), early identification and appropriate intervention appear critical. As such, comprehensive assessment that reaches beyond rating scales is important for identifying affect of symptoms on functioning and potential targets for intervention (Pritchard, Nigro, Jacobson, & Mahone, 2011). The present study adds to the existing evidence for inhibitory deficits in young children with ADHD and suggests that performance measures of inhibitory control – in isolation – are predictive of both current ADHD diagnostic status and functional real-life outcomes such as classroom inhibition. Given that the evidence for prediction of later symptoms and functional impairment from early performance measures of inhibition is mixed at present (e.g., Nigg et al., 1999; Sjowall, Bohlin, Rydell, & Thorell, 2016; van Lieshout et al., 2017), further work is needed to clarify the nature of associations among specific early executive skills and later functional outcomes. Given the proposed central nature of inhibitory deficits to ADHD (Barkley, 2006; Oosterlaan et al., 1998; Willcutt et al., 2005), longitudinal examination of the development of inhibitory control in children with ADHD may help to clarify the nature of the inhibitory deficits over time and their potentially changing relation to functional outcomes. Funding A portion of this study was presented at the annual meeting of the International Neuropsychological Society in New Orleans, LA, February 4, 2017. Supported by R01 HD068425, U54 HD079123, UL1 RR025005 and the Johns Hopkins Brain Science Institute. 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Preschool Inhibitory Control Predicts ADHD Group Status and Inhibitory Weakness in School

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Abstract

Abstract Objective Discriminative utility of performance measures of inhibitory control was examined in preschool children with and without ADHD to determine whether performance measures added to diagnostic prediction and to prediction of informant-rated day-to-day executive function. Method Children ages 4–5 years (N = 105, 61% boys; 54 ADHD, medication-naïve) were assessed using performance measures (Auditory Continuous Performance Test for Preschoolers-Commission errors, Conflicting Motor Response Test, NEPSY Statue) and caregiver (parent, teacher) ratings of inhibition (Behavior Rating Inventory of Executive Function-Preschool version). Results Performance measures and parent and teacher reports of inhibitory control significantly and uniquely predicted ADHD group status; however, performance measures did not add to prediction of group status beyond parent reports. Performance measures did significantly predict classroom inhibitory control (teacher ratings), over and above parent reports of inhibitory control. Conclusions Performance measures of inhibitory control may be adequate predictors of ADHD status and good predictors of young children’s classroom inhibitory control, demonstrating utility as components of clinical assessments. Attention, Children and behavioral disorders, Developmental and learning disabilities, Executive functions, Assessment Inhibition is a critical construct in developmental psychopathology (Nigg, 2000) and an early developing and core element of executive control (Diamond, 2013). Inhibitory control is strongly associated with children’s social competence and externalizing behaviors (Nigg, Quamma, Greenberg, & Kusche, 1999), with specific deficits in inhibitory control considered a key component of the Attention-deficit/Hyperactivity Disorder (ADHD) phenotype (Barkley, 1997; Oosterlaan, Logan & Sergeant, 1998; Willcutt, Doyle, Nigg, Faraone & Pennington, 2005). As such, early identification of deficits in inhibitory control may help not only to predict adaptive outcomes but also to add value to clinical diagnosis of ADHD. A recent practice survey of pediatric neuropsychologists suggests that ADHD is the most common condition for which a neuropsychological evaluation is sought (Sweet, Benson, Nelson, & Moberg, 2015). Given this need for ADHD diagnostic clarification, early measures of inhibition may be particularly helpful in identifying younger children with ADHD as well as clarifying particular patterns of neuropsychological impairment in need of support. Emerging work suggests that deficient response inhibition in children with ADHD can be substantially improved via contingent reinforcement and stimulant medication (Rosch et al., 2016), suggesting that early identification of inhibitory control deficits may be helpful in identifying meaningful targets for remediation. There are a variety of methods that have been used to assess inhibitory control in children, including performance tasks of motor and cognitive inhibition as well as informant ratings of behavior. Caregiver ratings of adolescent inhibitory control have been shown to predict ADHD group status, while performance measures of the same construct appear to contribute little additional variance (Toplak et al., 2008). In preschool children specifically, prior research suggests that caregiver ratings of inhibitory control may hold the most discriminatory value when identifying ADHD in young children (Ezpeleta, Granero, Penelo, de la Osa, & Domenech, 2015; Skogan et al., 2015); ratings of inhibitory control accurately identified approximately 80% of a sample of preschool children with ADHD (Skogan et al., 2015). Unfortunately, much of the work examining associations among early performance measures and parent reported executive weaknesses has focused solely on continuous performance tasks rather than also considering performance on other measures of inhibition. A recent study found only a weak relationship between parent ratings and commission errors in preschoolers; no significant associations were identified between caregiver ratings of inhibition and other performance measures of impulsivity (perseverations, hit reaction time) (Çak, Çengel-Kültür, Gökler, Öktem & Taşkıran, 2017). Furthermore, parent ratings of executive behaviors failed to achieve incremental predictive accuracy for ADHD, over and above continuous performance tasks (Ezpeleta et al., 2015). The limited association between informant ratings and neuropsychological measures has been well documented in older children (e.g., McAuley, Chen, Goos, Schachar, & Crosbie, 2010), however, with both sources of clinical information important to neuropsychological assessment (e.g., Mahone, Slomine & Zabel, in press). Since behavioral ratings and performance measures of inhibitory control typically share only a modest proportion of variance, examination of the value of both sources of data regarding inhibitory control in early identification of ADHD may help guide clinical practice. Given the importance of early diagnosis and intervention, it remains to be determined whether performance measures show better predictive power at the preschool-age level. The purpose of the present study was to: (1) examine utility of performance measures of inhibitory control in preschool children as the basis for discriminating children with ADHD from typically developing children; and (2) contrast the prediction from performance measures with that of caregiver (parent, teacher) ratings of behavioral inhibition in characterizing ADHD diagnostic status. Because our research diagnostic groups were assigned, based in part upon caregiver report of ADHD symptomatology (per DSM-IV-TR), we hypothesized that performance measures of inhibitory control would be independently predictive of group membership, but that caregiver reports measures of day-to-day executive control would show stronger prediction of group status. Additionally, although the limited associations among performance measures and informant rating scales have been well documented, because study group membership was based upon caregiver report of symptomatology, we sought to determine whether the performance measures added to prediction of informant-rated day-to-day function outside the home (i.e., teacher ratings of inhibitory control), over and above parent reports of inhibitory control. METHODS Study Procedures Approval was granted by the hospital’s Institution Review Board. Participants were recruited from advertisements in the community, pediatricians’ offices, and local daycare centers, to participate in a longitudinal study of brain development. After description of the study, parents of participants signed written consent, and child participants provided verbal assent. Participants were initially screened via telephone interview with a parent to determine eligibility. Once enrolled, participants completed a neuropsychological assessment battery that included the cognitive, language, and inhibitory control measures. Parents (and teachers, if available) also completed behavior rating scales at the time of testing. Participants Inclusion and exclusion procedures Participants were excluded if they had any of the following, established via review of medical/developmental history, and/or by study screening assessment: (1) diagnosis of Intellectual Disability or Autism Spectrum Disorder; (2) known visual impairment; (3) treatment of any psychiatric disorder (other than ADHD) with psychotropic medications [for those with diagnosis of ADHD, treatment with stimulants was allowed, whereas children treated with other psychotropic medications were excluded]; (4) any history of DSM-IV Axis I diagnosis other than Oppositional Defiant Disorder or Adjustment Disorder; (5) neurological disorder (e.g., epilepsy, traumatic brain injury, tic disorder); (6) documented hearing loss ≥25 dB loss in either ear; (7) reported history of physical, sexual, or emotional abuse; (8) Full Scale IQ scores <80 (as determined by previous assessment or study screening assessment). In addition, children were excluded if there was a history of a Developmental Language Disorder (DLD) either determined during the initial phone screen, based on prior assessment (completed within 1 year of the current assessment), or determined during screening visit. DLD exclusion was made in deference to evidence that language impairments may influence development of inhibitory control, response preparation, and working memory—core features of ADHD (Hagberg, Miniscalco, & Gillberg, 2010). Diagnostic methods for the ADHD and control groups were adapted from the NIH Preschoolers with Attention-Deficit/Hyperactivity Disorder Treatment (PATS) Study (Kollins et al., 2006; Posner et al., 2007). For 4-year olds, diagnosis of ADHD was made using modified DSM-IV-TR criteria, based on parent report on the Diagnostic Interview Schedule for Children-Young Child (YC-DISC) (Lucas, Fisher, & Luby, 1998, 2008) or Diagnostic Interview for Children and Adolescents, Fourth Edition—DICA-IV (Reich, Welner, & Herjanic, 1997), depending on age, and the DSM-IV ADHD Scales (Scales L and M) of the Conners’ Parent Rating Scales-Revised (CPRS-R; Conners, 1997). The YC-DISC is a highly structured, computer-assisted diagnostic instrument that assesses common psychiatric disorders, as defined by DSM-IV, that present in young children. The DICA-IV is the parallel version of the computer-assisted, structured interview for older children and adolescents. In the present study, the DISC-YC was used for 4-year olds and the DICA-IV was used for 5-year olds. To be included in the ADHD group, symptoms must have been present for at least 6 months, and cross-situational impairment (defined as parent report of problems at home and with peers, as not all children were enrolled in school) was required. Additionally, children in the ADHD group were required to have T-scores ≥ 65 on one or both of the DSM-IV ADHD Scales (Scales L and M) of the CPRS-R. Once children met general entry/exclusion criteria above, they were included in the control group only if they did not meet categorical diagnostic criteria for ADHD on the YC-DISC or DICA-IV. Additionally, children in the control group were required to have T-scores ≤ 60 on the CPRS-R DSM-IV ADHD Scales. Measures Auditory Continuous Performance Test for Preschoolers (Mahone, Pillion, & Hiemenz, 2001) The Auditory Continuous Performance Test for Preschoolers (ACPT-P) is a computerized, auditory go/no-go task. Two presented auditory stimuli (dog bark, bell) are used as target and non-target respectively, with the child instructed to push the space bar only when a bark is heard. Duration of each stimulus is 690 ms, with a fixed inter-stimulus interval of 5,000 ms. A total of 18 targets and 15 non-targets are arranged randomly so that the child is presented four targets and 11 non-targets in the first half of the test, and 11 targets and four non-targets in the second half of the test. The total time of the test is approximately 5 min, with practice trials. The number of commission errors served as a measure of inhibitory control and the dependent variable of interest. Lower commission scores indicate greater behavioral inhibition. Due to the skewed nature of the ACPT-P Commission errors variable (skewness = 1.86; kurtosis = 2.99), the data were log transformed; following transformation, data fell within acceptable parameters (skewness = .294; kurtosis = −1.55). Conflicting motor response This task was adapted from the Luria-Christensen Battery (Christensen, 1975) and has been used to examine motor response inhibition deficits in children (Mahone et al., 2006). Children are told, “If I show you my finger, you show me your fist; if I show you my fist, you show me your finger.” The examiner presents each of the two gestures 12 times (for a total of 24 presentations) in random sequence, at a rate of one per second. Response inhibition is assessed through the total number of correct responses and errors. The dependent variable of interest was the number of correct responses made, with higher scores indicating greater behavioral inhibition. Conflicting Motor Response has been significantly correlated with other measures of motor control, such as Contralateral Motor Response (r = .52, p < .001), and NEPSY Statue (r = .23, p < .01) (Mahone et al., 2006). Statue (NEPSY-II; Korkman, Kirk, & Kemp, 2007) The Statue subtest is a measure of inhibition and motor persistence in which the child is asked to maintain a body position with eyes closed for 75 s, while inhibiting the impulse to respond to sound distractors. Reliability coefficients are .82 and .88 for ages 4 and 5, respectively. Errors made are converted to a norm-referenced scaled score, with higher scores indicating better behavioral inhibition. Behavior Rating Inventory of Executive Function-Preschool Version (Gioia, Epsy, & Isquith, 2003) The Behavior Rating Inventory of Executive Function-Preschool Version (BRIEF-P) is a rating scale for children ages 2–5 years designed to be completed by parents/caregivers or teachers that assesses executive behaviors in daily environments. Ratings of participants’ executive behavior were obtained from parents and from teachers when available (e.g., not all children were attending preschool or school programs). The BRIEF-P is organized into five clinical scales, with raw scores converted to age-referenced T-scores; the Inhibit scale served as the dependent variable of interest. Lower T-scores indicate caregiver ratings suggesting greater behavioral inhibition. Internal consistency and reliability for the Inhibit scale is good (α = .90 for parent report and α = .94 for teacher report). Published agreement between parent and teacher ratings on the Inhibit scale was weak; r = .25 (p < .01); however, the Inhibit scale is well-correlated with the ADHD-IV Hyperactivity-Impulsivity scale (r = .87 for parent report and r = .85 for teacher report, both p < .001). Conners’ Parent Rating Scales-Revised-Long Form (Conners, 1997) Dimensional ratings of ADHD symptom severity were obtained using the DSM-IV oriented scales from the Conners’ Parent Rating Scales-Revised-Long Form (CPRS-R), including Scale L (DSM-IV Inattentive) and Scale M (DSM-IV Hyperactive/Impulsive). Internal consistency for ages 3–5 on these scales ranged from .86 to .94. Clinical Evaluation of Language Functions-Preschool-2 (Wiig, Secord, & Semel, 2004) The Clinical Evaluation of Language Functions-Preschool-2 (CELF-P) is an individually administered, norm-referenced test developed to identify language and communication disorders in preschool children. Participants scoring <−1.5 SD on either the Receptive Language or Expressive Language Index of the CELF-P, or <−1.0 SD on both indices, were excluded. The CELF-P Core Language Index was used in analyses as measure of language competence. Wechsler Preschool and Primary Scale of Intelligence-Third Edition (Wechsler, 2002) The Wechsler Preschool and Primary Scale of Intelligence-Third Edition (WPPSI-III) is a widely used measure of early cognitive abilities. Although the Full Scale IQ score (FSIQ) was used in determining participant eligibility, the Verbal IQ (VIQ) and Performance IQ (PIQ) indices were used in analyses in order to minimize effects of processing speed when examining cognitive differences between groups. Data Analysis Plan Demographic variables were compared using one-way ANOVAs to assess differences between groups. Next, a series of logistic regressions examined each of the performance-based measures of inhibition (ACPT-P Commissions, Conflicting Motor Response Test, NEPSY-2 Statue), both with and without covariates of cognitive and language skills (WPPSI-III VIQ, WPPSI-III PIQ, and CELF-P Core Language Index), to determine whether performance measures of inhibitory control were individually predictive of ADHD group classification. Following these analyses, hierarchical logistic regression examined whether performance measures (as a group) added additional unique predictive value beyond BRIEF-P parent and teacher ratings. As a final step, an additional hierarchical linear regression examined whether the performance measures added to prediction of teacher ratings of classroom inhibitory control, over and above the contribution of parent ratings of the same construct. RESULTS The sample included 105 children, ages 4–5 years (M = 4.98, SD = 0.57), including 51 typically developing children (32 boys, 19 girls) and 54 children with clinical symptoms of ADHD (32 boys, 22 girls; see Table 1). None were prescribed stimulant medication at the time of participation, although several began treatment shortly afterward. The sample was predominantly Caucasian (84%), with an additional 11% of the sample identifying as African American. The remaining 5% identified as Asian (3%), multiple races (1%), and Other (1%). There were no significant group differences in the distribution of race (χ2(2) = 5.29, p = .259) or in VIQ, PIQ, or Core Language scores (Table 1). As anticipated, the ADHD group received significantly higher symptom ratings on the CPRS-R DSM-IV scales. Table 1. Participant demographics Control (n = 51) ADHD (n = 54) p Mean SD Mean SD Age 4.92 0.56 5.05 0.58 .262 CPRS-R DSM-IV Total 46.45 6.05 77.15 9.61 <.001 VIQ 113.33 14.11 111.55 12.84 .500 PIQ 106.14 16.62 108.43 15.96 .471 Core Language 106.28 11.47 106.35 10.31 .971 Commissions 0.745 1.21 2.35 2.92 <.001 Conflicting Motor 14.67 4.51 12.13 4.82 .006 Statue 9.61 3.31 6.63 4.09 <.001 Control (n = 51) ADHD (n = 54) p Mean SD Mean SD Age 4.92 0.56 5.05 0.58 .262 CPRS-R DSM-IV Total 46.45 6.05 77.15 9.61 <.001 VIQ 113.33 14.11 111.55 12.84 .500 PIQ 106.14 16.62 108.43 15.96 .471 Core Language 106.28 11.47 106.35 10.31 .971 Commissions 0.745 1.21 2.35 2.92 <.001 Conflicting Motor 14.67 4.51 12.13 4.82 .006 Statue 9.61 3.31 6.63 4.09 <.001 Note: CPRS-R = Conners’ Parent Rating Scale (N scale T-score); VIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Verbal IQ standard score; PIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Performance IQ standard score. Table 1. Participant demographics Control (n = 51) ADHD (n = 54) p Mean SD Mean SD Age 4.92 0.56 5.05 0.58 .262 CPRS-R DSM-IV Total 46.45 6.05 77.15 9.61 <.001 VIQ 113.33 14.11 111.55 12.84 .500 PIQ 106.14 16.62 108.43 15.96 .471 Core Language 106.28 11.47 106.35 10.31 .971 Commissions 0.745 1.21 2.35 2.92 <.001 Conflicting Motor 14.67 4.51 12.13 4.82 .006 Statue 9.61 3.31 6.63 4.09 <.001 Control (n = 51) ADHD (n = 54) p Mean SD Mean SD Age 4.92 0.56 5.05 0.58 .262 CPRS-R DSM-IV Total 46.45 6.05 77.15 9.61 <.001 VIQ 113.33 14.11 111.55 12.84 .500 PIQ 106.14 16.62 108.43 15.96 .471 Core Language 106.28 11.47 106.35 10.31 .971 Commissions 0.745 1.21 2.35 2.92 <.001 Conflicting Motor 14.67 4.51 12.13 4.82 .006 Statue 9.61 3.31 6.63 4.09 <.001 Note: CPRS-R = Conners’ Parent Rating Scale (N scale T-score); VIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Verbal IQ standard score; PIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Performance IQ standard score. Individual logistic regression analyses indicated that all three performance measures of inhibitory control significantly predicted ADHD group status in the expected directions (see Table 2). Of the three measures, Statue was most predictive of ADHD status, with performance on this task correctly classifying 68.6% of the typically developing children and 64.8% of the children in the ADHD group. ACPT-P Commission errors correctly classified typically developing and ADHD children at a rate of 58.8% and 61.1%, respectively, while performance on the Conflicting Motor Response task correctly identified 58.8% and 57.4%. Table 2. Prediction of group status from performance-based measures of inhibitory control Task Exp(Β) 95% CI Wald’s X2 p Commissions 2.193 1.25–3.84 7.531 .006 Conflicting Motor 0.889 0.82–0.97 6.908 .009 Statue 0.814 0.73–0.91 13.365 <.001 Task Exp(Β) 95% CI Wald’s X2 p Commissions 2.193 1.25–3.84 7.531 .006 Conflicting Motor 0.889 0.82–0.97 6.908 .009 Statue 0.814 0.73–0.91 13.365 <.001 Note: CI = confidence interval; Commissions (log transformed score). Table 2. Prediction of group status from performance-based measures of inhibitory control Task Exp(Β) 95% CI Wald’s X2 p Commissions 2.193 1.25–3.84 7.531 .006 Conflicting Motor 0.889 0.82–0.97 6.908 .009 Statue 0.814 0.73–0.91 13.365 <.001 Task Exp(Β) 95% CI Wald’s X2 p Commissions 2.193 1.25–3.84 7.531 .006 Conflicting Motor 0.889 0.82–0.97 6.908 .009 Statue 0.814 0.73–0.91 13.365 <.001 Note: CI = confidence interval; Commissions (log transformed score). Additionally, these models were examined again, including measures of intelligence (WPPSI-III VIQ and PIQ) and language (CELF-P Core Language) as covariates. As expected, IQ and language measures offered no significant unique additional predictive value in classifying children with ADHD symptoms versus typically developing children. Including these measures in the model, performance on two of three measures of inhibitory control continued to predict group membership (Table 3). Table 3. Prediction of group status from performance-based measures of inhibitory control, controlling for intelligence and language ability Exp(Β) 95% CI Wald’s X2 p Intelligence/Language measures  VIQ 0.973 0.93–1.01 1.685 .194  PIQ 1.012 0.99–1.04 0.749 .387  Core Language 1.018 0.97–1.07 0.454 .500 Inhibitory Control measures  Commissions 1.829 0.95–3.53 3.258 .071  Conflicting Motor .902 0.82–0.99 4.062 .044  Statue .857 0.76–0.97 6.255 .012 Exp(Β) 95% CI Wald’s X2 p Intelligence/Language measures  VIQ 0.973 0.93–1.01 1.685 .194  PIQ 1.012 0.99–1.04 0.749 .387  Core Language 1.018 0.97–1.07 0.454 .500 Inhibitory Control measures  Commissions 1.829 0.95–3.53 3.258 .071  Conflicting Motor .902 0.82–0.99 4.062 .044  Statue .857 0.76–0.97 6.255 .012 Note: CI = confidence interval; VIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Verbal IQ standard score; PIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Performance IQ standard score; Commissions (log transformed score). Table 3. Prediction of group status from performance-based measures of inhibitory control, controlling for intelligence and language ability Exp(Β) 95% CI Wald’s X2 p Intelligence/Language measures  VIQ 0.973 0.93–1.01 1.685 .194  PIQ 1.012 0.99–1.04 0.749 .387  Core Language 1.018 0.97–1.07 0.454 .500 Inhibitory Control measures  Commissions 1.829 0.95–3.53 3.258 .071  Conflicting Motor .902 0.82–0.99 4.062 .044  Statue .857 0.76–0.97 6.255 .012 Exp(Β) 95% CI Wald’s X2 p Intelligence/Language measures  VIQ 0.973 0.93–1.01 1.685 .194  PIQ 1.012 0.99–1.04 0.749 .387  Core Language 1.018 0.97–1.07 0.454 .500 Inhibitory Control measures  Commissions 1.829 0.95–3.53 3.258 .071  Conflicting Motor .902 0.82–0.99 4.062 .044  Statue .857 0.76–0.97 6.255 .012 Note: CI = confidence interval; VIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Verbal IQ standard score; PIQ = Wechsler Preschool and Primary Scale of Intelligence, Third Edition, Performance IQ standard score; Commissions (log transformed score). Next, the BRIEF-P parent report Inhibit scale (T-score) was included as the first step in the logistic regression analysis to determine whether the performance measures, while predictive of group membership individually, added additional accuracy to group classification over and above parent report of day-to-day difficulties with inhibitory control. The parent report Inhibit scale significantly predicted group membership (OR = 1.287), and correctly classified 90.2% of typically developing children and 94.4% of children with ADHD. When the effect of performance measures of inhibitory control was assessed in combination with the parent rated Inhibit scale, the performance measures no longer had a significant affect on classification accuracy. Including both sets of measures, classification accuracy increased in the control group to 94.1%, but decreased for the ADHD group to 92.6%. Of the 105 children included in this analysis, 75 had teacher reported BRIEF-P measures available. The teacher-reported Inhibit scale (T-score) was independently significantly predictive of group status; however, when parent report of inhibition was also included in the model, the teacher report no longer significantly contributed to predictions of group status (see Table 4). As was the case with the BRIEF-P parent ratings, when both BRIEF-P parent and teacher ratings were included in the model, performance measures of inhibitory control no longer predicted group membership. Table 4. Prediction of group membership from caregiver ratings and performance-based measures of inhibitory control Exp(Β) 95% CI Wald’s X2 p Analysis 1  BRIEF-P parent Inhibit 1.287 1.16–1.43 21.304 <.001  Performance Measures   Commissions 2.737 0.64–11.70 1.845 .174   Conflicting Motor 0.861 0.68–1.09 1.582 .209   Statue 1.020 0.79–1.32 0.023 .879 Analysis 2  BRIEF-P parent Inhibit 1.235 1.11–1.38 13.841 <.001  BRIEF-P teacher Inhibit 1.054 0.98–1.13 2.232 .135  Performance Measures   Commissions 3.512 0.53–23.15 1.704 .192   Conflicting Motor 0.845 0.64–1.12 1.394 .238   Statue 0.994 0.76–1.31 0.002 .192 Exp(Β) 95% CI Wald’s X2 p Analysis 1  BRIEF-P parent Inhibit 1.287 1.16–1.43 21.304 <.001  Performance Measures   Commissions 2.737 0.64–11.70 1.845 .174   Conflicting Motor 0.861 0.68–1.09 1.582 .209   Statue 1.020 0.79–1.32 0.023 .879 Analysis 2  BRIEF-P parent Inhibit 1.235 1.11–1.38 13.841 <.001  BRIEF-P teacher Inhibit 1.054 0.98–1.13 2.232 .135  Performance Measures   Commissions 3.512 0.53–23.15 1.704 .192   Conflicting Motor 0.845 0.64–1.12 1.394 .238   Statue 0.994 0.76–1.31 0.002 .192 Note: BRIEF-P = Behavior Rating Inventory of Executive Function- Preschool Version; Commissions (log transformed score). Table 4. Prediction of group membership from caregiver ratings and performance-based measures of inhibitory control Exp(Β) 95% CI Wald’s X2 p Analysis 1  BRIEF-P parent Inhibit 1.287 1.16–1.43 21.304 <.001  Performance Measures   Commissions 2.737 0.64–11.70 1.845 .174   Conflicting Motor 0.861 0.68–1.09 1.582 .209   Statue 1.020 0.79–1.32 0.023 .879 Analysis 2  BRIEF-P parent Inhibit 1.235 1.11–1.38 13.841 <.001  BRIEF-P teacher Inhibit 1.054 0.98–1.13 2.232 .135  Performance Measures   Commissions 3.512 0.53–23.15 1.704 .192   Conflicting Motor 0.845 0.64–1.12 1.394 .238   Statue 0.994 0.76–1.31 0.002 .192 Exp(Β) 95% CI Wald’s X2 p Analysis 1  BRIEF-P parent Inhibit 1.287 1.16–1.43 21.304 <.001  Performance Measures   Commissions 2.737 0.64–11.70 1.845 .174   Conflicting Motor 0.861 0.68–1.09 1.582 .209   Statue 1.020 0.79–1.32 0.023 .879 Analysis 2  BRIEF-P parent Inhibit 1.235 1.11–1.38 13.841 <.001  BRIEF-P teacher Inhibit 1.054 0.98–1.13 2.232 .135  Performance Measures   Commissions 3.512 0.53–23.15 1.704 .192   Conflicting Motor 0.845 0.64–1.12 1.394 .238   Statue 0.994 0.76–1.31 0.002 .192 Note: BRIEF-P = Behavior Rating Inventory of Executive Function- Preschool Version; Commissions (log transformed score). As a final step examining a separate functional outcome, we examined whether the performance measures added to predictions of day-to-day inhibitory control as reported by teachers (Table 5). The performance measures as a group accounted for a substantial proportion of variance in teacher ratings of inhibitory control (R2 = .31, p < .001), suggesting that these measures do help to predict day-to-day affect in other settings outside the lab. Furthermore, even with parent ratings included in the model, two of the three performance measures (ACPT Commissions, β = .267, p = .004; Conflicting Motor, β = −.226, p = .013) remained significant predictors of classroom inhibitory control. Table 5. Prediction of teacher rated inhibitory control from performance-based measures of inhibitory control R2/ΔR2 β p Analysis 1  Performance measures .312 <.001   Commissions .329 .002   Conflicting Motor −.291 .006   Statue −.192 .076 Analysis 2  BRIEF-P parent Inhibit .382 <.001  Performance measures .126 .001   Commissions .267 .004   Conflicting Motor −.226 .013   Statue −.034 .725 R2/ΔR2 β p Analysis 1  Performance measures .312 <.001   Commissions .329 .002   Conflicting Motor −.291 .006   Statue −.192 .076 Analysis 2  BRIEF-P parent Inhibit .382 <.001  Performance measures .126 .001   Commissions .267 .004   Conflicting Motor −.226 .013   Statue −.034 .725 Note: BRIEF-P = Behavior Rating Inventory of Executive Function- Preschool Version; Commissions (log transformed score). Table 5. Prediction of teacher rated inhibitory control from performance-based measures of inhibitory control R2/ΔR2 β p Analysis 1  Performance measures .312 <.001   Commissions .329 .002   Conflicting Motor −.291 .006   Statue −.192 .076 Analysis 2  BRIEF-P parent Inhibit .382 <.001  Performance measures .126 .001   Commissions .267 .004   Conflicting Motor −.226 .013   Statue −.034 .725 R2/ΔR2 β p Analysis 1  Performance measures .312 <.001   Commissions .329 .002   Conflicting Motor −.291 .006   Statue −.192 .076 Analysis 2  BRIEF-P parent Inhibit .382 <.001  Performance measures .126 .001   Commissions .267 .004   Conflicting Motor −.226 .013   Statue −.034 .725 Note: BRIEF-P = Behavior Rating Inventory of Executive Function- Preschool Version; Commissions (log transformed score). Discussion The present findings suggest that performance-based neuropsychological measures of inhibition designed for preschoolers do help discriminate between children with and without ADHD, and remain significant predictors of group status even after controlling for cognitive and language abilities. Furthermore, parent reports (based on rating scales) of day-to-day behavioral inhibition also predict group status; however, when informant reports are entered first in the model, performance measures no longer add significantly to this prediction. Likewise, with parent report of behavioral inhibition entered first in the model, teacher reports of classroom behavioral inhibition also do not add to prediction of group status. However, in contrast to prior findings describing limited associations between performance measures of executive function and day-to-day function as measured by rating scales (e.g., McAuley et al., 2010), performance measures of inhibition added significantly to prediction of teacher ratings of young children’s classroom inhibitory control – even after inclusion of parent ratings in the model. These data suggest that, by themselves, performance measures of inhibitory control may be generally adequate predictors of ADHD status and somewhat stronger predictors of cross-setting behavioral control in preschool-aged children, and therefore have some utility as components of clinical assessments. Moreover, different aspects of inhibitory control show differential trajectories of development throughout childhood (Best & Miller, 2010; Dempster, 1993; Rothbart & Bates, 1998), potentially related to the protracted development of the multiple underlying brain systems supporting inhibitory control (e.g., anterior cingulate, lateral and orbital prefrontal cortex, basal ganglia). Notably, however, performance measures of inhibitory control have been shown to predict both concurrent and later ADHD symptomatology (Martel et al., 2007; Oosterlaan et al., 1998; Pennington & Ozonoff, 1996), mood symptoms (Kertz, Belden, Tillman & Luby, 2016), as well as important academic skills such as math (Allan, Hume, Allan, Farrington, & Lonigan, 2014; Blair & Razza, 2007) and language (Blair & Razza, 2007). As such, performance measures have the potential to add clinical value to assessments of preschool-age children in terms of predicting need for intervention and forecasting a variety of critical outcomes, especially considering the association between these early performance measures and informant ratings of day-to-day function. Given the importance of early intervention as a means of minimizing developmental psychopathology and the substantial later costs associated with preschool ADHD (Chorozoglou, Smith, Koerting, Thompson, Sayal & Sonuga-Barke, 2015), early identification of children at highest risk for poorer outcomes is a priority for developmental and pediatric neuropsychological evaluations and should take advantage of a multi-modal approach. Further work is needed to clarify the most effective and predictive methods for assessing multiple aspects of early inhibitory control. Current ADHD diagnostic criteria require informant ratings of symptomatology; in the present study, parent reports of ADHD symptoms on the CPRS-R were used in conjunction with structured parent psychiatric interview for group assignments, consistent with methodology modified from the PATS studies (Kollins et al., 2006; Posner et al., 2007). In considering the prediction of group status from the BRIEF-P, findings are limited somewhat by similarity of item content of the BRIEF-P Inhibit scale and the CPRS-R scale M (DSM-IV hyperactivity-impulsivity) in this age group; item-level examination suggests a substantial overlap of six items between the CPRS-R M scale and the 10-item BRIEF-P Inhibit scale. In this sample, these two scales are highly correlated (r = .91), although parent and teacher ratings on the BRIEF-P are not as strongly correlated with each other (i.e., r = .28 and .31, for controls and ADHD, respectively). As such, the present observation that parent ratings on the BRIEF-P are most predictive of group membership (which was based in part on parent ratings of ADHD symptoms on the CPRS-R) is not surprising. Nevertheless, performance measures remain important in the overall clinical assessment and prediction of risk, since preschoolers’ behavior can be variable and setting- or context-dependent. In other words, performance during the in-clinic neuropsychological assessment may potentially map more closely onto behavior in other more structured settings, such as that of the classroom, as well as onto later academic achievement (Dekker, Ziermans, Spruijt & Swaab, 2017). There is a large body of work highlighting the (often modest) associations between performance-based measures of executive function and informant ratings of executive control behavior in daily settings (e.g., see McAuley et al., 2010 for a review). However, in the present study, performance measures did help to predict behavior in other settings, accounting for 31% of the variance in teacher BRIEF-P Inhibit scores. Findings should also be considered in light of the sampling criteria used. Specifically, children with a variety of identified comorbidities or neurologic disorders were excluded from the study, which may have contributed to the lack of intellectual or language score differences between groups. As such, findings may not entirely generalize to the more common comorbid presentation of children with ADHD symptomatology. In addition, exclusion of comorbidities may have also contributed to the high IQ scores in the ADHD group (Waber et al., 2007); the relatively high cognitive level of both groups may limit generalizability of findings to other samples of young children with emerging symptoms of ADHD, particularly those with comorbidities likely to lower observed IQ scores. However, at the same time, it is important to note that exclusion of comorbidities allows for greater understanding of ADHD-specific impacts upon performance. Furthermore, participants (in the ADHD group) were selected based upon early emerging symptoms of the disorder, thus differences may exist between those children with symptoms already evident in preschool versus the larger population of youth whose symptoms only appear evident later in development. Notably, diagnostic classification over the preschool to early school-age time period may be unstable (Chacko, Wakschlag, Hill, Danis, & Espy, 2009) and we do not know how many of those within the ADHD group will still meet diagnostic criteria at later assessments and thus prove “true positives” in terms of early diagnostic accuracy. However, there is also evidence for stability of early diagnoses of ADHD, in that 89% of the preschoolers in the PATS sample continued to meet criteria for ADHD at 6 year follow-up (Riddle et al., 2013). Given that onset during early childhood is associated with significant long-term costs (Chorozoglou et al., 2015), early identification and appropriate intervention appear critical. As such, comprehensive assessment that reaches beyond rating scales is important for identifying affect of symptoms on functioning and potential targets for intervention (Pritchard, Nigro, Jacobson, & Mahone, 2011). The present study adds to the existing evidence for inhibitory deficits in young children with ADHD and suggests that performance measures of inhibitory control – in isolation – are predictive of both current ADHD diagnostic status and functional real-life outcomes such as classroom inhibition. Given that the evidence for prediction of later symptoms and functional impairment from early performance measures of inhibition is mixed at present (e.g., Nigg et al., 1999; Sjowall, Bohlin, Rydell, & Thorell, 2016; van Lieshout et al., 2017), further work is needed to clarify the nature of associations among specific early executive skills and later functional outcomes. Given the proposed central nature of inhibitory deficits to ADHD (Barkley, 2006; Oosterlaan et al., 1998; Willcutt et al., 2005), longitudinal examination of the development of inhibitory control in children with ADHD may help to clarify the nature of the inhibitory deficits over time and their potentially changing relation to functional outcomes. Funding A portion of this study was presented at the annual meeting of the International Neuropsychological Society in New Orleans, LA, February 4, 2017. Supported by R01 HD068425, U54 HD079123, UL1 RR025005 and the Johns Hopkins Brain Science Institute. 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Archives of Clinical NeuropsychologyOxford University Press

Published: Dec 26, 2017

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