Developmental Cognitive Neuroscience 4 (2013) 1628

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Developmental Cognitive Neuroscience

journal homepage: http://www.elsevier.com/locate/dcn

Preliminary data suggesting the efcacy of attention training for school-aged children with ADHD
Leanne Tamm a, , Jeffery N. Epstein a , James L. Peugh a , Paul A. Nakonezny b , Carroll W. Hughes b
a b

CCHMC, 3333 Burnet Avenue, ML 10006, Cincinnati, OH 45229, USA University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., MC 8589, Dallas, TX 75390-8589, USA

a r t i c l e

i n f o

a b s t r a c t
A pilot randomized clinical trial was conducted to examine the initial efcacy of Pay Attention!, an intervention training sustained, selective, alternating, and divided attention, in children diagnosed with Attention-Decit/Hyperactivity Disorder (ADHD). After a diagnostic and baseline evaluation, school-aged children with ADHD were randomized to receive 16 bi-weekly sessions of Pay Attention! (n = 54) or to a waitlist control group (n = 51). Participants completed an outcome evaluation approximately 12 weeks after their baseline evaluation. Results showed signicant treatment effects for parent and clinician ratings of ADHD symptoms, child self-report of ability to focus, and parent ratings of executive functioning. Child performance on neuropsychological tests showed signicant treatment-related improvement on strategic planning efciency, but no treatment effects were observed on other neuropsychological outcomes. Treatment effects were also not observed for teacher ratings of ADHD. These data add to a growing body of literature supporting effects of cognitive training on attention and behavior, however, additional research is warranted. 2012 Elsevier Ltd. All rights reserved.

Article history: Received 11 July 2012 Received in revised form 1 October 2012 Accepted 3 November 2012 Keywords: ADHD Attention training Cognitive training Executive functioning Intervention

1. Introduction Attention training, also known as cognitive training, is an intervention in which the various components of attention are viewed as skills that can be enhanced by training. Attention in this conceptualization is dened as the appropriate allocation of processing resources to relevant stimuli and is thought to comprise several sub-processes (Coull, 1998). Specically, attention can be fractionated into (1) attention orientation (direction of attention to a

Corresponding author at: Division of Behavioral Medicine and Clinical Psychology, Cincinnati Childrens Hospital Medical Center, 3333 Burnet Avenue, MLC 10006, Cincinnati, OH 45229, USA. Tel.: +1 513 803 3176; fax: +1 513 636 0755. E-mail addresses: leanne.tamm@cchmc.org (L. Tamm), jeff.epstein@cchmc.org (J.N. Epstein), james.peugh@cchmc.org (J.L. Peugh), paul.nakonezny@utsw.edu (P.A. Nakonezny), carroll.hughes@utsw.edu (C.W. Hughes). 1878-9293/$ see front matter 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dcn.2012.11.004

stimulus), (2) selective attention (prioritizing one stimulus in favor of another), (3) sustained attention (attending to one stimulus over time), and (4) divided attention (dividing attention between two plus stimuli) (Coull, 1998). These sub-processes are thought to be the building blocks underlying executive functioning and to have unique neuronal correlates (Coull, 1998). Theoretically, more efcient attentional sub-processes should give rise to enhanced executive processes (Paelecke-Habermann et al., 2005), such as inhibition, task management, planning, monitoring/working memory, and coding. Further, more efcient executive functioning should translate into improvements in behavior for example, improved inhibition might lead to better self-regulation. The rationale for attention training is based on the concept that efciency increases after repetitive practice of specic cognitive operations of attention (Posner and Raichle, 1994), theoretically because practice produces adaptations in the underlying neuroanatomical networks

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linked to these processes (Kerns et al., 1999). Initial neuroimaging research comparing brain activation before and after different forms of cognitive training supports this contention (Beauregard and Levesque, 2006; BrefczynskiLewis et al., 2007; Erickson et al., 2007; Kim et al., 2008; Thimm et al., 2006). Furthermore, controlled trials investigating the efcacy of attention training programs report gains in both trained and untrained assays of attention components such as sustained attention and executive function (Ethier et al., 1989; Finlayson et al., 1987; Gray and Robertson, 1989; Mateer and Mapou, 1996; Penkman, 2004; Sohlberg and Mateer, 1987; Thompson and Kerns, 1995). In the last decade, researchers have turned to investigate attention training as an intervention for Attention-Decit/Hyperactivity Disorder (ADHD) since ADHD involves impairment in attention and related executive functions. There is a growing literature providing support for attention training in individuals with ADHD (Epstein and Tsal, 2010; Kerns et al., 1999; Klingberg et al., 2002, 2005; OConnell et al., 2006; Semrud-Clikeman et al., 1999; Shalev et al., 2004; Tamm et al., 2007, 2010; Williams, 1989). These studies report improvements in the cognitive skill being trained directly but also improvements in untrained cognitive skills (Epstein and Tsal, 2010; Tamm et al., 2010; Williams, 1989), although effect sizes are typically small to moderate (Epstein and Tsal, 2010). Furthermore, studies of attention training in ADHD also provide initial support for improvements on untrained measures of attention and academic efciency (SemrudClikeman et al., 1999; Williams, 1989), as well as reductions (although not consistently) in teacher and parent ratings of ADHD symptoms (Kerns et al., 1999; Klingberg et al., 2005; Semrud-Clikeman et al., 1999; Shalev et al., 2004; Tamm et al., 2010; Thomson et al., 1984) and restlessness/head movements (Klingberg et al., 2002). There is also preliminary neuroimaging data to suggest that cognitive training impacts brain function in ADHD (Hoekzema et al., 2010, 2011). After 10 days of cognitive training, children with ADHD showed increases in orbitofrontal, superior frontal, middle temporal, and inferior frontal cortex on an inhibition task and increased cerebellar activity on an attentional task, while the control group showed no such activation differences (Hoekzema et al., 2010). Furthermore, these activation differences were complemented by focal volumetric gray matter increases in bilateral middle frontal cortex and right inferiorposterior cerebellum (Hoekzema et al., 2011). Taken together, these studies suggest that attention training is a promising treatment approach for ADHD. However, to date there have been few randomized clinical trials investigating attention training in ADHD. This is critical given that replication studies have not always been successful and, more critically, studies utilizing blinded evaluators do not always nd a positive effect for attention training. One potentially promising intervention is Pay Attention! (www.lapublishing.com), an intervention targeting sustained, selective, divided, and alternating attention, constructs which have been shown to be compromised in individuals with ADHD (Manly et al., 2001). A small randomized trial of the effects of Pay Attention! in seven

children with ADHD reported signicant benets of attention training in measures of sustained attention, executive functioning, and effortful processing compared to children in a video game control group (Kerns et al., 1999). However, the sample size for this study was small and participant diagnosis was not veried by the research team. We conducted an open trial of Pay Attention! with 23 children diagnosed with ADHD and showed effects on executive functioning measures (cognitive exibility, working memory, parent ratings), as well as improvements in ADHD symptomatology (Tamm et al., 2010). However, we did not utilize a control group as the primary emphasis was to determine feasibility of the intervention in a clinically diagnosed group and in our outpatient setting. The current trial was initiated to investigate if the Pay Attention! intervention was effective in improving trained and untrained executive functions as well as parent, teacher, and clinician ratings of attention and behavior when compared to a waitlist control group that did not receive the intervention. Consistent with the theoretical underpinnings of attention training, we hypothesized that by training attention (sustained, selective, divided, and alternating), we would see proximal treatment-related improvements in executive functioning and distal treatment-related improvements in attention and behavior (see Fig. 1). 2. Method The study was approved by the University of Texas, Southwestern Medical Center at Dallas Institutional Review Board and informed parental consent and participant assent were obtained from all participants prior to initiating any procedures. 2.1. Participants Participants (n = 132) were recruited from outpatient clinics at Childrens Medical Center at Dallas, the community, and Shelton School, a private school for learning differences; 105 participants were randomized (see Fig. 2, CONSORT diagram). Participants ranged in age from 7 to 15 years (M = 9.3, SD = 1.4) and were predominantly Caucasian. Demographic and baseline characteristics are presented in Table 1. Randomization was stratied by gender, ADHD subtype, and medication status. Participants were asked to maintain a stable medication status (i.e., continue taking medication as directed and not initiate new medication during the study). Exclusion criteria included the following: estimated full scale IQ < 85, history of head injury, history of prenatal drug exposure, diagnosis with other congenital or acquired neurological conditions, and participating in other non-pharmacological treatment interventions for ADHD (e.g., neurofeedback, cognitivebehavioral therapy, etc.). 2.2. Design and procedure Families meeting eligibility criteria by phone screen were invited to participate in a baseline evaluation.

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Proximal Outcomes Executive Functioning

(Working Memory, Cognitive Flexibility, Planning/Problem Solving, Response Inhibition, Metacognition as measured by subtests of the DKEFS, WISC, WJ-III, Quotient, and parent BRIEF ratings)

Attention Training
(Sustained, Selective, Alternating, Divided Attention as measured by TEA-Ch)

Distal Outcomes Behavior & Attention

(Inattention, HyperactivityImpulsivity, Impairment as measured by the SNAP, BASC, and CGI)

Fig. 1. Model of training targets and outcomes.

Assessed for eligibility (n = 132)

Enrollment

Excluded (n = 27) Not meeting inclusion criteria (n = 27)

Randomized (n = 105)

Allocated to intervention (n = 54)

Allocated to waitlist control (n = 51) Received allocated intervention (n = 51) Did not receive allocated intervention (n = 0)

Allocation

Received allocated intervention (n = 51) Did not receive allocated intervention (n = 3) Parent did not respond to calls to schedule intervention

Outcome

Attended Outcome (n = 45) Lost to follow up (n=6)

Attended Outcome (n = 46) Lost to follow up (n=5)

Fig. 2. CONSORT diagram.

L. Tamm et al. / Developmental Cognitive Neuroscience 4 (2013) 1628 Table 1 Demographic and baseline characteristics. Intervention (n = 54) Age (mean, SD) Race (n) Caucasian African American Hispanic Asian Mixed race Gender (n) Male Female ADHD subtype (n) Combined type Inattentive type Not otherwise specied Comorbid Dx (n) Oppositional deant disorder Anxiety disorders Elimination disorder Depressive disorders Learning disorder Medicated for ADHD (n) Estimated IQ (mean, SD) Intervention Sessions Attended (mean, SD) 9.1 (1.2) 40 (74%) 1 (1%) 7 (13%) 3 (6%) 3 (6%) 36 (66%) 18 (34%) 32 (59%) 21 (39%) 1 (2%) 1 (2%) 1 (2%) 6 (11%) 0 1 (2%) 35 (65%) 107.4 (11.5) 13.5 (3.2) Waitlist control (n = 51) 9.5 (1.5) 34 (67%) 4 (7%) 5 (10%) 2 (4%) 6 (12%)
2

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Statistical comparison t(103) = 1.29, n.s. 2 (4) = 3.7, n.s.

(1) = .05, n.s.

35 (69%) 16 (31%)
2

(2) = .003, n.s.

30 (59%) 20 (39%) 1 (2%) n/a 2 (4%) 4 (8%) 2 (4%) 1 (2%) 0 37 (73%) 105.9 (13.3) n/a

2 (1) = .73, n.s. t(100) = 0.63, n.s.

A semi-structured clinical interview, the Kiddie-SADSPresent and Lifetime Version or K-SADS-PL (Kaufman et al., 1997), was conducted with the primary caregiver, and with the child/adolescent separately, to determine ADHD diagnosis. Information regarding family functioning, family psychiatric history, and developmental and medical histories was also collected. In addition, the clinical interviewers provided ratings of ADHD on the Swanson, Nolan, and Pelham DSM-IV ADHD rating scale (SNAP-IV) based on the interviews, and impairment/functioning using the Clinical Global Impressions (CGI) rating scale. Parents completed several rating scales assessing attention, executive function, and behavior, and participants were administered several tests assessing a variety of executive functions including planning, behavioral inhibition, visualspatial abilities, and working memory. Following the baseline evaluation, participants were randomized to either receive the intervention or to a waitlist control group. Participants randomized to the intervention attended twice-weekly 30-min sessions for 8 consecutive weeks (for a total of 16 sessions). Individuals randomized to the waitlist control condition were asked to not begin any new treatment for ADHD during the wait period and were offered the opportunity to receive the intervention at the end of the wait period. All participants and their parents were invited to attend an outcome evaluation. There was variability between subjects as to how long it took them to complete the 16 treatment sessions due to parent and interventionist schedules; thus we opted to re-test all participants on the same schedule (i.e., 12 weeks after baseline). During the outcome evaluation, parents and children were re-interviewed using the K-SADS-PL, clinicians completed SNAP-IV and CGI improvement ratings, and participants completed the same battery of executive functioning measures as at baseline. Parents were also given a packet of ratings to give to teachers to complete at baseline and outcome, although few teachers returned

the forms (n = 33 at baseline and n = 27 at outcome for the intervention group; n = 25 at baseline and n = 27 at outcome for the waitlist control group). 2.3. Intervention The Pay Attention! materials are designed to train sustained, selective, alternating, and divided attention using visual and auditory stimuli. The visual stimuli include a set of cards depicting drawings of children and adults that can be distinguished by various features including age, gender, hair color, and other physical qualities; and a set of home layouts that include several rooms with objects that can be sorted by color, shape, and other characteristics. The auditory stimuli include lists of words played on a CD with the participant required to press a buzzer whenever a specic word is heard. The tasks become progressively more difcult (e.g., a distracting overlay is placed over the visual stimuli, a distracting sound is played during task completion, or participants are asked to complete two tasks simultaneously). All participants completed an initial session to establish performance levels and orient them to the materials. Participants then progressed through the four modules, beginning with the simplest sustained attention tasks. After criterion was reached (e.g., gains in speed while maintaining overall accuracy), the next module was started. Not all participants completed all four modules since they progressed at different rates, although the majority completed at least the sustained and selective attention modules. Participants were given immediate feedback regarding their performance and interventionists spent time each session discussing how the targeted attentional skill could be applied in a home or school setting. Pay Attention! is designed to be exibly delivered so that the interventionist can tailor the treatment to the specic needs of the participant. Parents were also provided with reading materials about the attention skills being trained

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and met with the child and interventionist for a few minutes after each session to discuss the activities practiced at each session, which skill was being trained, and how parents could support the childs implementation of the skill in home and school activities. 2.4. Measures 2.4.1. Rating scales Swanson, Nolan, and Pelham (SNAP-IV) DSM-IV ADHD Rating Scale (Swanson, 1992): Clinicians (based on parent and child interview), parents and teachers rated how well each ADHD symptom described the child on a four point Likert scale (0 = not at all, 1 = just a little, 2 = quite a bit, 3 = very much). We examined average scores for Inattention symptoms and Hyperactivity/Impulsivity symptoms. Although psychometric properties have not been investigated for the SNAP-IV, adequate reliability and validity has been established for similar DSM-IV checklists [e.g., ADHD Rating Scale-IV (DuPaul et al., 1998)]. Behavioral Assessment System for Children, Second Edition (BASC-II) (Reynolds and Kamphaus, 2004): Parents and teachers completed the BASC-II describing a variety of behaviors. For analytic purposes, we analyzed subscales relevant to ADHD (i.e., Externalizing, Hyperactivity, Attention Problems and Behavioral Symptoms Index). The scale has been demonstrated to have adequate reliability and validity (Reynolds and Kamphaus, 2004). Clinical Global Impressions (CGI) (Leon et al., 1993): Un-blinded clinicians rated the severity of the childs impairment related to ADHD at baseline and outcome on an 7-point scale ranging from Not At All Ill to Very Severely Ill, and the level of improvement at outcome on an 7-point Likert scale ranging from Very Much Improved to Very Much Worse (4 being no change). The scale has adequate reliability and validity (Leon et al., 1993). Attentional Control Scale (ATTC) (Derryberry and Reed, 2002): Participants rated themselves on their ability to focus and shift their attention on the ATTC. The ATTC consists of 20 items that are rated on a four-point Likert scale from 1 (almost never) to 4 (always). The ATTC yields two primary scales (attention shifting and attention focusing). This measure was added later in the study, and thus was only available for 20 participants. Analyses of content, internal and construct validity as well as reliability provided evidence of the scales signicant convergent and discriminant validity (Fajkowska and Derryberry, 2010). Behavior Rating Inventory of Executive Function (BRIEF) (Gioia et al., 2000): Parents and teachers completed this rating scale assessing executive function behaviors in the home and school environments, yielding T-scores on several subscales, including Inhibit, Shift, Working Memory, Emotion Regulation, Organization, Planning, Initiate, Monitor, Behavioral Regulation Index, Metacognitive Index, and a General Executive Composite. The scale has adequate reliability and validity (Gioia et al., 2000).

2.4.2. Neuropsychological measures Test of Everyday Attention for Children (TEA-Ch) The TEA-Ch is an objective measure of attention (Manly et al., 2001). The battery has alternate forms (A and B) to allow for re-test. Subtests utilized for this study included: Sky Search, Score!, Creature Counting, Sky Search DT, Score DT, and Code Transmission. The TEA-Ch was designed to more directly assess sustained, alternating, selective, and divided attention constructs while at the same time, minimizing demands on memory, reasoning, task comprehension, motor speed, verbal ability, and perceptual ability (Manly et al., 2001). Thus, the TEA-Ch tasks more directly map onto the constructs being trained in Pay Attention! and was included as an assessment of whether the intervention was successful in training the desired target (and thus was only collected for the intervention group). Form A of the TEA-Ch has adequate reliability although Form B is not as well established; validity studies are lacking (Strauss et al., 2006). Wechsler Intelligence Scale for Children Fourth Edition (WISC-IV) (Wechsler, 2004): Matrix Reasoning (uid reasoning/cognitive exibility), Digit Span and Letter Number Sequencing (working memory). Vocabulary and Block Design were administered to provide an estimate of Full Scale IQ (Sattler and Dumont, 2004) at baseline only. Psychometric properties for this measure are well established (Wechsler, 2004). Woodcock Johnson Tests of Achievement Third Edition (WJ-III) (Woodcock et al., 2001): Understanding Directions (auditory working memory, listening comprehension). The subtest has high reliability (>.8) (Woodcock et al., 2001). DelisKaplan Executive Functioning System (D-KEFS) (Delis et al., 2001): Tower Test (problem solving) and Color-Word Interference (CWI; inhibition/cognitive exibility). Additional measures generated from the Tower subtest include Mean First Move Time (initial planning time as measured by the time spent planning the rst move), Time Per Move Ratio (overall planning time as measured by the time spent planning all moves subsequent to the rst move), Move Accuracy Ratio (accuracy and planning efciency of problem solving strategy as measured by the total number of moves), and Rule Violations Per Item Ratio (establishing and maintaining cognitive set as measured by the number of rule violations). Reliability of the DKEFS subtests is in the moderate to high range and validity has been established with a number of executive functioning measures (Delis et al., 2004). Quotient ADHD system The Quotient is a continuous performance test assessing a participants ability to pay attention which also objectively measures a patients ability to sit still (Sumner, 2010). Children are asked to press a button each time they see an eight-sided star but to withhold their response to ve-sided stars. A motion-tracking device directed at sensors on the ankles and forehead records movement simultaneously with performance of the task. Variables analyzed included omission errors (percentage of missed targets), commission errors (percentage of inaccurate responses to non-targets), latency (average amount of time to respond

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correctly), and variability (variation in response time to the correct target). Reliability and validity for this measure has not yet been established, although the task is very similar to the Connors Continuous Performance Test which has adequate reliability and validity (Conners and Jeff, 1999). 2.5. Analytic strategy Demographic and baseline clinical characteristics of the two groups were reported using mean (SD) for continuous variables and frequency (percentage) for categorical variables. To identify any differences between the characteristics of the 2 groups, we used the 2-independent sample t test for continuous variables and the 2 test for categorical variables. As a manipulation check of whether the Pay Attention! intervention impacted sustained, selective, divided, and/or alternating attention, we conducted repeated measures ANOVAs in SPSS for each of the 6 subtests administered of the TEA-Ch (note, alternate forms were used for this measure) for the intervention group only; this measure was not available for the waitlist control group. To address whether the intervention improved behavioral and executive functioning ratings, and child performance on executive function tasks, multivariate and univariate generalized estimating equation (GEE) analyses were performed to test for signicant mean differences between the treatment intervention and waitlist control groups at outcome using baseline scores and participant age (for non-normed measures, e.g., SNAP-IV, CGI) as control covariates (e.g., Feldon et al., 2011). The baseline scores were included as covariates to address potential group differences at baseline contributing to the pattern of ndings at outcome. Multivariate GEE analyses were used to test for group mean differences among correlated subtests from the same response variable measure (e.g., BRIEF subscales), while univariate GEE analyses were used to test for mean differences among summative subscales or total scores from a response variable measure separately to avoid collinearity (e.g., BRIEF Index scores). These GEE analyses were conducted using Mplus version 6.12 (Muthn and Muthn, 19982010) to: (a) handle missing data via maximum likelihood estimation assuming missing at random (MAR) (e.g., Enders, 2010), (b) test for signicant response variable mean differences directly using the Model Constraint and New commands, and (c) ensure that analysis assumptions of homogeneity of covariance matrices and homogeneity of covariate regression slopes were met by imposing the necessary parameter estimate constraints prior to analysis. Testing for group differences on the ATTC attention focusing and attention shifting scales was done via separate analyses of covariance in SPSS (baseline scores and age were entered as covariates) due to the reduced sample size (N = 20) available for those analyses. Given the number of response variable mean difference computations involved, the false discovery rate procedure (Benjamini and Hochberg, 1995) was used to ensure that no more than 5% of the total number of signicant ndings reported represent Type-I errors. The false discovery rate has been shown to produce fewer

Type-I errors than per-comparison critical alpha corrections, and has been shown to better maintain statistical power compared to experiment-wise critical alpha corrections (Benjamini and Hochberg, 1995; Maxwell and Delaney, 2004). The p-values listed in Tables 24 are those generated from the false discovery rate procedure and are thus labeled corrected p-value. We also report effect sizes which can be particularly illuminating when there is limited power (e.g., teacher ratings, child self-report ratings), and where one wants to compare them with other research in the literature. Cohens d effect size estimates were computed for all group mean differences. Finally, additional analyses were conducted to investigate if there were any moderators of treatment response after controlling for baseline score variation. Specically, for each response variable, separate treatment group by (1) age, (2) gender, (3) IQ, (4) ADHD subtype, and (5) medication status interaction variables were computed and tested for signicance. Results of these analyses were also corrected for Type-1 error ination via the false discovery rate procedure. 3. Results 3.1. Manipulation check Compared to their pre-intervention performance, the group that received intervention improved signicantly on the TEA-Ch Score!, Sky Search Completion Time and Attention (combined accuracy and timing score), and Creature Counting Completion Time after the intervention (Table 2). 3.2. Parent, clinician, and teacher behavioral ratings Parents and clinicians reported signicantly fewer ADHD symptoms on the SNAP-IV Inattention and Hyperactivity/Impulsivity ratings for the intervention group compared to the waitlist control group (Table 3). On the BASC-II, parents rated children in the intervention group as having fewer Attention Problems compared to the waitlist control group. Teacher ratings were not signicant for the SNAP-IV or BASC-II. Clinician ratings on the CGI indicated lower severity and greater improvement for the intervention group than the waitlist control group. Participants rated themselves as having signicantly improved ability to focus their attention [F(3, 19) = 6.6, p < .05, Cohens d = 1.11] and shift their attention [F(3, 19) = 5.5, p < .05, Cohens d = .51] on the ATTC. Examination of effect sizes revealed that teachers were also reporting reductions in Hyperactivity/Impulsivity ratings (medium effect) for the intervention group compared to the control group. On the BASC-II, both parents and teachers reported improvements on the Externalizing, Hyperactivity, and Behavioral Symptoms Index, and teachers reported improvements on the Attention Problems subscale, for the intervention group compared to the control group. These effect sizes ranged from small to large (Table 3).

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Table 2 Intervention group results on Test of Everyday Attention for Children (TEA-Ch). Pre-intervention Mean (SD) Sustained attention/divided attention Score! Sky Search Dual Task Score Dual Task Code Transmission Selective attention Sky Search Accuracy Sky Search Completion Time Sky Search Attention (combined accuracy/time) Alternating attention Creature Counting Accuracy Creature Counting Completion Time
* **

Post-intervention Mean (SD) 8.6 (3.3) 7.8 (3.8) 9.2 (3.5) 8.1 (3.3) 10.5 (2.6) 10.1 (2.7) 9.9 (2.7) 9.9 (2.8) 9.8 (3.0)

Corrected p

7.2 (2.4) 7.0 (4.0) 8.8 (3.4) 7.6 (2.8) 10.2 (3.1) 8.8 (2.3) 8.9 (2.9) 9.3 (3.3) 8.5 (2.6)

8.02 .06 .47 1.31 .57 12.3 5.5 .73 9.4

.007** .80 .50 .26 .46 .001** .024* .39 .004**

p < .05. p < .01.

3.3. Parent and teacher ratings of executive functioning Signicant improvements were reported by parents for all the BRIEF subscales, with the exception of Inhibit (trend for improvement) and Emotion Regulation for the intervention group compared to the waitlist control group (Table 4). In contrast, no signicant effect of treatment was observed for any subscale on the teacher BRIEF ratings. Examination of effect sizes for the teacher ratings revealed improvements for the intervention group compared to the waitlist control group on the teacher rated BRIEF Shift, Emotion Regulation, Initiate, Working Memory subscales, and Behavioral Regulation Index, and a decrement (moderate effect size) for Organization (Table 4), though none of these effects reached statistical signicance. 3.4. Child measures of neuropsychological functioning Children in the intervention group performed signicantly better than the waitlist control group on the DKEFS Tower Time per Move Ratio (Table 5). No other significant differences between the intervention and waitlist control group were observed on the other neuropsychological measures. Examination of effect sizes revealed a small effect favoring the intervention group on the DKEFS Inhibition, DKEFS Inhibition/Switching Errors, DKEFS Tower Mean First Move Time, DKEFS Tower Move Accuracy Ratio, WISC-IV Matrix Reasoning, Quotient Latency, Quotient Variability, and WJIII Understanding Directions measures, but these did not reach statistical signicance. The intervention group also made more errors of omission on the Quotient compared to the waitlist control group. 3.5. Potential treatment moderators There were no signicant interactions between group and IQ, ADHD subtype, medication status, or gender. However, we observed an interaction between age and group on the BRIEF Shift subscale (b = 3.33, Wald Z = 3.26, p < .01), BRIEF Behavioral Regulation Index (b = 1.95, Wald Z = 2.67, p < .01), and the CGI Severity rating (b = .23, Wald Z = 2.56,

p < .01) at outcome. For all three interactions, older members of the treatment group had lower scores on those response variables.

4. Discussion The results of this pilot randomized clinical trial of Pay Attention! in children with ADHD suggest that the intervention was successful in impacting attentional sub-processes targeted by training (i.e., we observed improvement on tasks assessing aspects of sustained, selective, divided and alternating attention like visual detection, response speed, etc.). Further, our data show that the intervention improved ADHD symptomatology by parent and clinician report, reduced impairment by clinician report, improved executive functioning including inhibition, shifting, planning, and self-monitoring by parent report, improved child self-report of ability to focus and shift attention, and improved child performance on a task measuring planning efciency. Although non-signicant, examination of effect sizes revealed small to moderate improvements for the intervention group on teacher ADHD and executive function (Shift, Emotion Regulation, Initiate, and Working Memory) ratings, and child performance on executive function measures of inhibition, planning, comprehension and memory of verbal instructions, cognitive exibility, and response latency. As with other studies, these promising ndings are tempered by the fact that we did not have blinded evaluators, parents may have been affected by expectancy bias or Hawthorne Effect, and the vast majority of the most objective measures administered to both groups (child neuropsychological tests) were not statistically signicant despite having small to moderate effect sizes. Further, teacher ratings were not signicant. Although not statistically signicant in most cases, the direction of group means were, however, generally consistent with those of the previous small randomized clinical trial of Pay Attention! (Kerns et al., 1999) which reported gains on measures of planning, sustained auditory attention, sustained visual attention, behavioral inhibition/executive function/selective attention, and academic efciency. There was also a trend observed for improved teacher ADHD ratings. In this trial, which utilized different

Table 3 Group differences at outcome: parent, clinician and teacher behavior ratings. L. Tamm et al. / Developmental Cognitive Neuroscience 4 (2013) 1628 Intervention Mean (SD) Baseline SNAP-IV Inattention P Hyperactivity/Impulsivity P Inattention C Hyperactivity/Impulsivity C InattentionT Hyperactivity/Impulsivity T BASC-II Externalizing P Behavioral Symptoms IndexP Hyperactivity P Attention Problems P Externalizing T Behavioral Symptoms Index T Hyperactivity T Attention Problems T CGI Severity Improvement 2.13 (0.5) 1.30 (0.7) 2.37 (0.4) 1.60 (0.6) 1.96 (0.7) 1.62 (1.0) 54.52 (9.4) 57.26 (9.8) 59.87 (12.1) 65.06 (7.7) 60.64 (11.1) 65.30 (10.6) 66.79 (14.1) 65.12 (5.8) 4.33 (0.5) n/a Waitlist Mean (SD) Baseline 2.14 (0.5) 1.42 (0.8) 2.42 (0.4) 1.58 (0.7) 1.46 (0.8) 0.94 (0.8) 56.47 (10.1) 59.24 (9.2) 63.24 (12.9) 67.90 (5.4) 50.52 (7.7) 55.04 (9.0) 54.78 (12.2) 58.35 (8.4) 4.35 (0.5) n/a Intervention Mean (SD) Outcome 1.42 (0.5) 0.93 (0.6) 1.84 (0.5) 1.27 (0.6) 1.84 (.6) 1.35 (0.9) 51.83 (9.1) 53.67 (10.2) 54.50 (9.6) 60.21 (8.3) 57.97 (10.3) 61.00 (8.4) 63.83 (14.5) 62.97 (6.1) 3.51 (0.9) 2.80 (0.8) Waitlist Mean (SD) Outcome 2.15 (0.5) 1.30 (0.7) 2.39 (0.5) 1.51 (0.7) 1.68 (0.7) 1.18 (0.9) 54.96 (10.6) 57.8 (9.8) 60.43 (13.7) 66.00 (7.4) 54.77 (10.3) 58.72 (11.7) 60.67 (14.6) 62.78 (8.1) 4.19 (0.6) 3.66 (0.8) Wald Z Corrected p Cohens d

7.42 3.19 6.85 3.44 0.20 1.23 1.21 1.56 2.13 3.00 1.72 0.94 1.37 1.39 5.45 5.54

<.001 .007 <.001 .003 .98 .37 .37 .29 .10 .01 .21 .53 .33 .32 <.001 <.001

1.65 L 0.65 M 1.41 L 0.68 M 0.07 0.49 M 0.25S 0.35 S 0.46 M 0.66 M 0.66 M 0.33 S 0.78 L 0.33 S 1.04 L 1.14 L

Note: S = small effect size (.2.4); M = medium effect size (.5.8); L = large effect size (>.8) (Cohen, 1992); SNAP-IV = Swanson, Nolan, and Pelham ADHD Rating Scale; BASC-II = Behavioral Assessment System for Children, Second Edition; CGI = Clinician Global Impairment rating; P = parent; T = teacher; C = clinician.

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Table 4 Group differences at outcome: parent and teacher ratings of executive functioning. Intervention Mean (SD) Baseline BRIEF parent Inhibit Shift Emotion Regulation Initiate Working Memory Planning Organization Monitor Behavioral Regulation Index Metacognitive Index General Executive Composite BRIEF teacher Inhibit Shift Emotion Regulation Initiate Working Memory Planning Organization Monitor Behavioral Regulation Index Metacognitive Index General Executive Composite 60.34 (12.4) 56.92 (11.6) 52.13 (10.8) 61.83 (10.1) 70.02 (8.3) 66.85 (10.0) 60.60 (9.1) 60.83 (9.8) 57.26 (10.7) 67.15 (8.9) 64.19 (8.8) 69.29 (16.7) 61.76 (11.9) 60.21 (11.9) 65.85 (10.8) 73.32 (14.6) 68.29 (12.5) 66.65 (18.3) 69.79 (13.0) 65.76 (12.6) 70.97 (13.7) 70.47 (13.2) Waitlist Mean (SD) Baseline 63.00 (14.0) 56.66 (13.0) 53.54 (11.0) 60.26 (9.2) 71.68 (7.4) 66.88 (9.9) 62.14 (8.7) 63.06 (9.1) 58.94 (11.8) 68.00 (7.9) 65.64 (8.9) 64.76 (19.9) 61.42 (13.5) 55.80(12.0) 67.16 (11.1) 72.60 (14.9) 66.92 (10.9) 67.08 (19.1) 65.04 (16.0) 62.79 (15.6) 69.60 (13.5) 68.87 (14.7) Intervention Mean (SD) Outcome 56.31 (11.9) 52.08 (9.0) 49.04 (10.0) 53.94 (11.2) 61.17 (10.3) 58.69 (11.4) 56.23 (10.3) 54.98 (10.0) 52.83 (10.3) 58.71 (10.5) 56.85 (10.1) 70.24 (19.0) 59.93 (11.4) 61.52 (15.5) 65.10 (10.4) 70.45 (11.7) 67.55 (11.6) 70.69 (16.7) 69.14 (12.7) 66.07 (15.5) 70.41 (11.5) 70.24 (12.3) Waitlist Mean (SD) Outcome 62.32 (14.0) 56.98 (13.1) 52.68 (12.9) 60.26 (8.1) 71.30 (8.2) 67.02 (10.1) 61.00 (8.7) 61.83 (11.3) 58.45 (12.5) 67.45 (8.9) 65.06 (9.9) 67.35 (20.7) 61.29 (19.1) 57.52 (17.7) 67.35 (10.8) 72.19 (12.5) 68.12 (12.6) 66.38 (20.9) 66.69 (17.4) 62.96 (19.6) 70.64 (14.8) 68.91 (17.6) Wald Z Corrected p Cohens d L. Tamm et al. / Developmental Cognitive Neuroscience 4 (2013) 1628

2.33 3.06 1.84 4.72 5.29 4.65 2.50 3.37 3.00 5.17 4.79 0.37 0.49 0.81 0.80 0.71 0.18 1.54 0.12 0.58 0.21 0.05

.06 .009 .18 <.001 <.001 <.001 .04 .004 .01 <.001 <.001 .91 .82 .60 .60 .66 .98 .29 .98 .76 .98 .98

0.51 M 0.63 M 0.38 S 0.98 L 1.16 L 1.00 L 0.53 M 0.70 M 0.63 M 1.13 L 1.03 L 0.12 0.15 S 0.23 S 0.20 S 0.20 S 0.05 0.52 M 0.03 0.22 S 0.07 0.02

Note: S = small effect size (.2.4); M = medium effect size (.5.8); L = large effect size (>.8); BRIEF = Behavior Rating Inventory of Executive Function.

Table 5 Group differences at outcome: child performance on executive functioning measures. Intervention Mean (SD) Baseline DKEFS Color Word Interference Inhibition Scaled Score Inhibition/Switching Scaled Score Inhibition Errors Inhibition/Switching Errors DKEFS Tower Tower Scaled Score Tower Mean First Move Time Tower Time Per Move Ratio Tower Move Accuracy Ratio Tower Rule Violations Per Item WJ-III Understanding Directions WISC-IV Matrix Reasoning Digit Span Letter Number Sequencing Quotient Omission Errors Commission Errors Latency Variability 9.88 (3.0) 10.43 (2.7) 9.19 (2.6) 9.71 (2.9) 10.04 (2.4) 12.35 (1.5) 10.89 (1.9) 7.46 (3.0) 9.65 (2.1) 101.70 (10.1) 10.56 (2.4) 10.63 (2.4) 10.15 (2.7) 13.07 (14.4) 34.68 (20.4) 508.2 (89.8) 206.7 (85.2) Waitlist Mean (SD) Baseline 9.96 (3.0) 10.41 (2.9) 9.88 (3.7) 9.98 (3.4) 10.51 (2.7) 12.35 (1.3) 11.29 (1.7) 8.27 (2.6) 9.39 (2.5) 102.1 (11.9) 11.51 (2.5) 10.30 (3.0) 9.68 (3.3) 10.17 (11.3) 29.07 (16.7) 519.9 (82.6) 189.8 (71.5) Intervention Mean (SD) Outcome 11.56 (2.7) 11.31 (2.2) 10.33 (2.4) 11.83 (13.4) 11.53 (2.6) 13.12 (1.0) 12.80 (1.1) 7.73 (3.0) 10.82 (1.1) 106.20 (10.8) 11.51 (3.1) 10.69 (2.4) 10.47 (2.9) 16.2 (19.1) 24.34 (21.1) 568.6 (86.8) 219.4 (99.3) Waitlist Mean (SD) Outcome 10.98 (2.5) 11.17 (2.6) 10.45 (2.6) 10.3 (2.7) 11.57 (2.0) 12.85 (0.9) 12.36 (1.2) 7.13 (2.6) 10.8 (1.0) 103.3 (13.1) 11.51 (2.8) 10.26 (3.1) 10.04 (2.9) 10.27 (12.4) 21.00 (17.2) 558.3 (108.5) 192.0 (72.5) Wald Z Corrected p Cohens d L. Tamm et al. / Developmental Cognitive Neuroscience 4 (2013) 1628

1.24 0.14 0.01 0.79 0.28 1.4 2.61 1.26 0.05 1.79 1.43 0.24 0.05 1.43 0.14 1.19 1.21

.37 .98 .99 .60 .97 .32 .03 .37 .98 .19 .32 .98 .98 .32 .98 .37 .37

0.25 S 0.03 0.01 0.17 S 0.06 0.29 S 0.55 M 0.28 S 0.01 0.35 S 0.30 S 0.05 0.01 0.29 S 0.03 0.23 S 0.26 S

Note: WISC-IV = Wechsler Intelligence Scale for Children, Fourth Edition; WJ-III = Woodcock Johnson Tests of Achievement, Third Edition; DKEFS = DelisKaplan Executive Functioning System.

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assessment instruments, we also showed signicant improvements on planning efciency, and non-signicant gains in behavioral inhibition/executive function/selective attention, and auditory attention/memory. It should be noted that Kerns (Kerns et al., 1999) utilized raw scores in her analyses to address issues related to not being able to detect treatment effects due to a child remaining in the same normative group and to detect a childs own gains compared to their own performance. We opted to use scaled scores allowing us better ability to compare the current results to those on the open trial which utilized the same measures. The ndings from our RCT are also essentially consistent with attention, behavior, and executive functioning improvements we observed in our open trial (Tamm et al., 2010). While we did not replicate our previous ndings of signicantly improved cognitive exibility on the DKEFS Inhibition/Switching subtest with the Pay Attention! intervention (Tamm et al., 2010), we did observe greater improvement on the WISC Matrix Reasoning and DKEFS Inhibition subscales for the intervention group compared to the waitlist group (small effects). Thus, we still see evidence of enhanced uid reasoning or cognitive exibility with Pay Attention! which may not have achieved signicance due to the relatively small sample size. The improvement in these domains, if replicated in future studies, is clinically relevant for individuals diagnosed with ADHD who have neuropsychological decits in these constructs which are associated with impaired brain functioning (Tamm and Juranek, 2012). Despite signicant improvements on parent ratings of working memory, improvements on child working memory subtests were not observed. There was, however, a small, non-signicant effect of treatment on the WJ-III Understanding Directions subtest which does involve a working memory component in that it requires listening and mapping a series of sequential directions onto the mental structure under construction and maintaining the sequence in immediate awareness until a new directive changes the sequence (Gernsbacher, 1991). It may be that Pay Attention! improves listening abilities and selective attention more than the construct of working memory. Analysis of processing variables necessary for DKEFS Tower subtest completion revealed a signicant effect on the Time Per Move Ratio. The Time Per Move Ratio represents the mean amount of time that was spent on each move it is a ratio of the total number of seconds spent solving a problem relative to the total number of moves used for that problem (Yochim et al., 2009). Interestingly, the intervention group also signicantly improved on the TEA-Ch subtests involving timing (Sky Search, Creature Counting), which, taken together with small nonsignicant improvements on Mean First Move Time (speed) and increased latency (i.e., slowing) on the Quotient continuous performance subtest, suggests that one impact of Pay Attention! training is on the childs efciency and timing. Certainly, the intervention itself included a signicant focus on timing, with children encouraged to improve speed and efciency for each subsequent administration of the various tasks. This nding, if replicated, could have signicant implications for reducing impairment in ADHD, since

recent research suggests that individuals with ADHD have specic decits in timing functions which are postulated to be closely associated with impulsiveness, dened as premature, impatient and delay averse with associated lack of temporal foresight (Hart et al., 2012; Zelaznik et al., 2012). Analyses investigating potential treatment moderators were not signicant for gender, IQ, medication status, or ADHD subtype. Age interacted with group on two parentrated variables (BRIEF Shift and Behavioral Regulation Index) and one clinician-rated variable (CGI) but not with any of the child neuropsychological variables. We controlled for age in the primary analyses for the CGI but not for the BRIEF which is an age-normed measure. It is tempting to conclude that older children may have beneted more from the intervention, but given that this effect was observed on so few variables, it may be that these few variables are more sensitive to the effects of maturation. One of the issues with psychosocial interventions which has not received much attention in the literature is whether treatment can have emanative (Whalen et al., 1985) or unintended negative effects. It is often assumed that behavioral or cognitive interventions are either benign or have no impact, versus potentially negatively impacting outcomes. Although the ndings were not statistically signicant, there was a small effect for the intervention group to make more errors of omission on the Quotient continuous performance task and a moderate non-signicant effect for the intervention group to be rated as less organized by teachers than the waitlist control group. Thus, it appears that despite potentially improving inhibition and planning efciency, the Pay Attention! intervention might be having an unintended negative effect in that the child might be slowing too much and therefore failing to respond quickly enough resulting in somewhat increased errors of omission again, this effect was not statistically signicant but warrants attention. Replication is necessary, given the large number of statistical tests and possibility of chance ndings. There are a number of strengths to this study including that it is amongst the largest randomized clinical trials investigating attention training in ADHD. However, the sample size was still relatively limited, at least for detecting effects on the neuropsychological variables. It should be noted that when we did a post hoc power analysis to examine what sample size would be needed to reject the null hypothesis for the neuropsychological measures, necessary sample sizes were much larger than our sample size (e.g., DKEFS Inhibition, N = 314; WISC-IV Matrix Reasoning, N = 178). The use of a waitlist control group and the resulting lack of blinding to condition could have resulted in a Hawthorne effect or inated ratings by parent, child, and clinician; replication is necessary with an attention control group. Another limitation was the relative lack of teacher data (approximately 50% of the sample had teacher data available for outcome). Finally, we observed signicant variability on some outcome variables suggesting the possibility that participants differed in their response to treatment. Further work is necessary to investigate individual differences in response to treatment and to identify potential moderators.

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Overall, our study adds to the growing body of literature suggesting cognitive training may improve executive function and behavior in children with ADHD. However, before Pay Attention! can be considered for use in clinical settings additional research is needed. The optimal design would be an RCT which includes a larger sample of, ideally un-medicated, children with ADHD, blinded evaluators, a control group that is designed to reduce expectancy biases, more teacher ratings, and tests that are selected to measure both proximal (areas trained) and distal (generalization to functional impairment) gains. Nonetheless, our results suggest that Pay Attention! did improve sustained, selective, and alternating attention directly, and specically timing efciency. Further, it may be effective in reducing ADHD symptoms as well as improving parental ratings of executive functioning. Effect size examination reveals small although non-signicant improvements on teacher ratings (small n) and child neuropsychological measures of executive functioning including planning, cognitive exibility, inhibition, auditory working memory, and response latency/variability. Caution is warranted, however, given the large number of statistical comparisons conducted. Conict of interest All authors declare that there are no actual or potential conicts of interest including any nancial, personal or other relationships with other people or organizations within 3 years of beginning the submitted work that could inappropriately inuence, or be perceived to inuence, their work. The funding sources did not have a role in study design, collection, analysis and interpretation of data, writing of the manuscript, nor the decision to submit the article for publication. Acknowledgements This research project was supported in part by the National Center for Research Resources, National Institutes of Health Grant Number UL1 RR024982. Its contents are solely the responsibility of the authors and do not necessarily represent the ofcial views of the NIH. Additional funding for the project was provided by a gift from the Sparrow Foundation for the Center for Advanced ADHD Research, Treatment, and Education (CAARTE). We gratefully acknowledge the Pay Attention! interventionists, Aleksandra Foxwell, Jarrette Moore, Lauren Smith, Jeanne Rintelmann, Amanda Gray, Laure Ames, Maryanne Hetrick, Amy Rollo, Cathy Bass, Ana Arenivas, Deidre Edwards, Sarah Swart, Shelley Williamson, Gina Bolanos, and Kyle Clayton, and Conrad Barnes for his data management. We also thank Joyce Pickering, Hum.D. for her support and the use of space at the Shelton School. We appreciate the families who participated in the evaluations and intervention. References
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