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Executive Functions After Pediatric Mild TraumaticBrain Injury: A Prospective Short-Term LongitudinalStudySarah Loher a , Simone T. Fatzer a & Claudia M. Roebers aa Department of Developmental Psychology , University of Bern , Bern , SwitzerlandPublished online: 23 Oct 2012.

To cite this article: Sarah Loher , Simone T. Fatzer & Claudia M. Roebers (2014) Executive Functions After Pediatric MildTraumatic Brain Injury: A Prospective Short-Term Longitudinal Study, Applied Neuropsychology: Child, 3:2, 103-114, DOI:10.1080/21622965.2012.716752

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APPLIED NEUROPSYCHOLOGY: CHILD, 3: 103–114, 2014Copyright © Taylor & Francis Group, LLCISSN: 2162-2965 print/2162-2973 onlineDOI: 10.1080/21622965.2012.716752

Executive Functions After Pediatric Mild Traumatic Brain Injury: A Prospective Short-Term Longitudinal Study

Sarah Loher, Simone T. Fatzer, and Claudia M. Roebers Department of Developmental Psychology, University of Bern, Bern, Switzerland

Traumatic brain injuries (TBIs) occur frequently in childhood and entail broad cognitive deficits, particularly in the domain of executive functions (EF). Concerning mild TBI (mTBI), only little empirical evidence is available on acute and postacute performance in EF. Given that EF are linked to school adaptation and achievement, even subtle deficits in performance may affect children’s academic careers. The present study assessed performance in the EF components of inhibition, working memory (WM), and switching in children after mTBI. Regarding both acute and postacute consequences, performance trajectories were measured in 13 patients aged between 5 and 10 years and 13 controls who were closely matched in terms of sex, age, and education. Performance in the EF components of inhibition, switching, and WM was assessed in a short-term longitudinal design at 2, 6, and 12 weeks after the mTBI. Results indicate subtle deficits after mTBI, which became apparent in the longitudinal trajectory in the EF components of switching and WM. Compared with controls, children who sustained mTBI displayed an inferior performance enhancement across testing sessions in the first 6 weeks after the injury in switching and WM, resulting in a delayed deficit in the EF component of WM 12 weeks after the injury. Results are interpreted as mTBI-related deficits that become evident in terms of an inability to profit from previous learning opportunities, a finding that is potentially important for children’s mastery of their daily lives.

Key words: children, executive functions, inhibition, mild traumatic brain injury, prospective longitudinal study, switching, working memory

Traumatic brain injury (TBI), resulting in a sudden acceleration–deceleration movement of the head caused by a mechanical force, is one of the most prevalent rea-sons for hospitalization in children and adolescents (Kirkwood et al., 2008). With an annual incidence of about 180 per 100,000 children, TBI calls for research efforts in this area (Altermatt, 2002; Kraus, 1995). Based on the level of functioning immediately after the injury, TBI is categorized as a mild, moderate, or severe injury. Empirical findings showed adverse outcomes after TBI both in cognitive (e.g., Dennis, Wilkinson, Koski, & Humphreys, 1995; Mandalis, Kinsella, Ong, & Anderson,

Address correspondence to Sarah Loher, Department of Devel-opmental Psychology, University of Bern, Muesmattstrasse 45, CH-3000 Bern 9, Switzerland. E-mail: sarah.loher@psy.unibe.ch

2007) and in social/behavioral domains (see Rosema, Crowe, & Anderson, 2012), with more severe injuries being associated with more adverse outcomes (dose–response relationship; e.g., Muscara, Catroppa, & Anderson, 2008). A recent interest of research has been drawn to the mild scope of head injuries (Menascu & MacGregor, 2007). Despite a high occurrence of mild TBI (mTBI) in childhood, there is little empirical research on acute and postacute neuropsychological conse-quences of pediatric mTBI, with the few existing find-ings being both heterogeneous and inconclusive (e.g., V. Anderson, Catroppa, Morse, Haritou, & Rosenfeld, 2001). The current study aims to provide insight into neuropsychological outcomes after sustained mTBI by assessing executive functions (EF) of pediatric patients shortly after the incident and in a short-term follow-up over 12 weeks.

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EF are important both for school and everyday life, and because they are related to frontal brain structures, they are an important focus of research, particularly in children after TBI. From a neuroanatomical perspective, frontal and temporal cerebral structures show a particu-lar vulnerability to TBI due to their proximity to bony structures of the anterior and middle fossa (Bigler, 2007; Menascu & MacGregor, 2007; Yeates, 2010b). Both dor-solateral and ventrolateral prefrontal structures are assumed to play a pivotal role in EF (P. J. Anderson, 2008; Diamond, 2006). EF are defined as an aggregation of interrelated higher-order cognitive functions (P. J. Anderson) involving the superordinate orchestration of a variety of components (Zelazo, Carlson, & Kesek, 2008). These self-regulatory processes are assumed to control thoughts and actions and aim to flexibly adapt to new and possibly more complex task demands (Miyake & Friedman, 2012). EF have also proven to play a crucial role in the context of school; both school readiness and school achievement have been predicted by EF (Blair & Razza, 2007; Roebers, Röthlisberger, Cimeli, Michel, & Neuenschwander, 2011), emphasizing the importance of their integrity in childhood.

As an umbrella term, EF comprise a variety of cogni-tive components. In adults, Miyake, Friedman, Emerson, Witzki, and Howerter (2000) investigated the internal structure of EF by means of a confirmatory factor analy-sis and found evidence for a hierarchical construct with three separable yet interconnected core components: working memory (WM)/updating, inhibition, and switching/shifting. Although these components tend to be even more closely interrelated in young normative samples, the assumption of three distinguishable processes is widely accepted and has proven to be fruitful for research approaches in children (Lehto, Juujärvi, Kooistra, & Pulkkinen, 2003; Rose, Feldman, & Jankowski, 2011). According to Miyake and colleagues, the ability to con-tinuously maintain and specifically update or manipulate newly acquired memory contents denotes the process of WM (Davidson, Amso, Anderson, & Diamond, 2006; Schmid, Zoelch, & Roebers, 2008). Inhibition is defined as the ability to successfully suppress prepotent or domi-nant stimuli, information, impulses, or knowledge con-tents that are irrelevant to current task demands (Mazuka, Jincho, & Oishi, 2009; Miyake et al.). Switching refers to the ability to flexibly switch between rules, tasks, or mental sets (Mazuka et al.; Miyake et al.). As the process of switching requires the combination of the active main-tenance of task goals (WM) and the suppression of pre-viously active mind sets (inhibition), this EF component is assumed to comprise particularly high levels of com-plexity (Diamond, 2006).

Development of EF is protracted and stretches from infancy across childhood and into adolescence. Thereby, some components display an adult level of functioning in

early adolescence (Zelazo et al., in press; Zelazo & Carlson, 2012; Zelazo & Müller, 2002), whereas full functionality is not reached until late adolescence (Huizinga, Dolan, & van der Molen, 2006). However, marked developmental progression is observable in child-hood with switching, WM, and certain inhibition pro-cesses (e.g., Stroop task) showing distinct improvements in the early primary school years (Diamond, 2006). Therefore, regarding EF development, the time frame from 5 to 10 years has been moved in the central focus of researchers, practitioners, and policymakers. This time frame of marked developmental progression is of partic-ular importance after pediatric acquired brain injuries, as the injury happens at a time when the development of these brain structures is still ongoing. Although brain structures themselves thus may not be impaired initially after mTBI and performance typically does not appear to be deficient, a disruption of the subsequent development may nevertheless occur even after mTBI (V. Anderson, Catroppa, Morse, Haritou, & Rosenfeld, 2005; Dennis et al., 1995). This possibility is explored in the present study.

As mentioned earlier, EF have repeatedly shown a pro-nounced vulnerability to pediatric TBI, particularly after moderate and severe injuries. In the following section, existing empirical findings on EF deficits after moderate and severe TBI will briefly be summarized. Evidence on sequelae after pediatric mTBI, the central focus of the present article, will then be summarized in the subsequent sections. Most empirical research on neuropsychological consequences after pediatric TBI focused on the patients’ performance in the domain of WM. Despite method-ological variations across studies, moderate-to-severe TBI was consistently associated with greater WM dys-function, which was found both in performance measures and in parental reports (Conklin, Salorio, & Slomine, 2008; Slovarp, Azuma, & Lapointe, 2012), and seemed to persist even years after the injury (Levin et al., 2002). With respect to ongoing WM development in children, there is an indication of a dose–response relationship between severity of the initial trauma and the long-term WM developmental outcome (V. Anderson, Catroppa, Rosenfeld, Haritou, & Morse, 2000). Similar results have been obtained in the EF components of inhibition and switching, with inhibitory performance being inversely related to the severity of the injury (Gerrard-Morris et al., 2010; Sesma, Slomine, Ding, & McCarthy, 2008) and persisting at least 1 year after severe TBI (Levin, Hanten, Zhang, Swank, & Hunter, 2004). As for the EF component of switching, empirical findings indicate a similar but less pronounced pattern of deficits with injury-related deficits appearing either in accuracy (ACC; Gerrard-Morris et al., 2010; Slomine et al., 2002) or in an increase in reaction time (RT), pointing to slower pro-cessing speed (V. Anderson & Catroppa, 2005).

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Turning to studies addressing consequences of mild injuries, mTBI shall briefly be defined as follows: mTBI refers to the mildest range of closed-head trauma and comprises about 80% to 90% of all TBI cases (Menascu & MacGregor, 2007). The most exhaustive definition was established by the American Congress of Rehabilitation Medicine (ACRM, 1993) and includes at least one of the following symptoms: initial Glasgow Coma Scale score of 13 to 15, loss of consciousness of 30 minutes or less, loss of memory not exceeding 24 hours, alteration in mental state, or focal neurological deficits (possibly transient).

Compared with empirical findings after moderate-to-severe TBI where clear severity-related deficits were found, EF performance after mTBI has rarely been studied despite the high prevalence. Several studies that assessed performance deficits after moderate-to-severe TBI also included children with mTBI but did not compare the patients’ performance with an appropriate control group. Although these studies allow insight into different pat-terns of deficits after mTBI compared with severe TBI, the question of relative deficits after mTBI (performance of children after mTBI compared with children without brain injury) remains unanswered (see Yeates, 2010b). Therefore, in the following literature review, we only included studies that compared the level of performance after mTBI to appropriate controls.

Empirical findings assessing the performance in the EF component of WM after pediatric mTBI were reported to be mixed. On the one hand, there are many studies that revealed mTBI-related performance deficits. Therein, Scherwath and colleagues (2011) found objecti-fiable deficits in verbal WM (digit span) with an increased percentage of children after mTBI displaying WM deficits 2 months after the injury compared with healthy controls. Further evidence for mTBI-related WM deficits was provided in a study by Catale, Marique, Closset, and Meulemans (2009). The authors compared WM perfor-mance of 6- to 11-year-old children after sustained mTBI to matched controls (along with attentional performance and inhibition) 1 year after the injury. WM performance (n-back task) was found to be impaired, with deficits observable even 1 year after mTBI. These results are in line with deficits that were reported in parent-rated ques-tionnaires evaluating EF in everyday situations in chil-dren between 7 and 15 years of age at 3 months and 12 months after mTBI (Behavior-Rating Inventory of Executive Function [BRIEF]; Sesma et al., 2008). The authors thus suggested WM is particularly sensitive to mTBI at least within the first year after the injury with no substantial recovery over time. As these two latter studies reported EF deficits in the postacute phase (3 months up to 1 year), they leave the question regarding short-term performance trajectories in the acute phase after mTBI open. Further indications of subtle rather than gross

neuropsychological disturbances after mTBI were found in terms of diverging brain activation patterns in children after sustained mTBI compared with controls in a com-plex task combining WM and inhibitory aspects (Krivitzky, Roebuck-Spencer, Roth, Blackstone, & Johnson, 2011). In contrast, no WM differences were found between children with mTBI and uninjured con-trols in ecologically valid tests of everyday memory (V. Anderson et al., 2001). However, as these tests aim to assess memory functions in an ecologically valid manner (e.g., story recall, spatial learning), they are hardly com-parable to classic WM tests (e.g., n-back tasks or complex span tasks). No mTBI-related deficits were observed in a visual n-back task in children who sustained an mTBI at least 2 years before the study (Levin et al., 2002). Therefore, findings regarding the EF component of WM indicate for the most part that this function may be subtly disrupted after mTBI, with deficits being observable even a year after the injury but possibly becoming weaker in the 2nd year after the injury. However, empirical evidence of the trajectory of performance-based measures in WM shortly after the mTBI is still inconclusive.

Regarding the EF domain of inhibition, empirical find-ings indicate few, if any, deficits after mTBI. Concerned with inhibitory performance in the aforementioned study by Catale and colleagues (2009), a go/no-go test revealed marginally significant performance differences in respect of ACC, but the patients’ performance did not differ from that of controls regarding RT. This finding thus indicates that children after mTBI tended to make more mistakes without slowing down their speed of response. Additionally, an indication of subtle inhibitory deficits was found in a study assessing EF based on a parent-rated questionnaire (BRIEF; Sesma et al., 2008). Even though the authors did not find clinically relevant inhibi-tory deficits, they did find small but significant differ-ences in parental reports of inhibitory performance between children after mTBI and controls. Parent ratings are undoubtedly a particularly sensitive and ecologically valid indicator of deficits, as parents rate their children’s behavior in everyday situations. At the same time, the objectivity of this assessment may be questioned in this context, particularly as it cannot be ruled out that the parents’ knowledge about their children’s injury may bias their ratings.

Compared with WM, there are fewer empirical find-ings concerning the level of performance after mTBI in the EF component of switching. While switching perfor-mance has been found to be deficient in children after severe TBI, switching performance of mTBI patients aged 3 to 6 years and 11 months did not differ signifi-cantly from the performance of orthopedic-injured con-trols (Gerrard-Morris et al., 2010). These findings are in line with results of parent-rated EF performance, obtained by the BRIEF by Sesma et al. (2008), which

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found no switching deficits shortly after pediatric mTBI. However, while performance improved over time, perfor-mance of children with mTBI remained stable or deterio-rated, indicating that a normative learning effect may be absent after mTBI. The discrepancy between behavioral data, as assessed in the study by Gerrard-Morris and col-leagues, and parent-rated EF as in the BRIEF may point to a fundamental difference of these measurements, which is of particular importance in the context of mTBI. Thereby, as stated, the BRIEF seems to be sensitive to deficits in everyday life. In contrast, behavioral measures (as applied in the study by Gerrard-Morris et al.) assess EF in highly artificial, structured situations, allowing for an assessment of these functions that is as accurate and as pure as possible. The structured assess ment session, how-ever, neglects the complexity of everyday life situations. Thus, in these very structured situations, subtle EF defi-cits may be covered and only become apparent in highly complex everyday situations, emphasizing the utmost importance of behavioral measures that have proven to be sensitive. A different picture emerges if considering subjective reports of symptoms rather than performance-based measures or parental reports of EF. Possibly related to the aforementioned inferior performance enhance-ment across assessment sessions that was found in chil-dren after mTBI in parent-rated EF performance (e.g., Sesma et al.), children after mTBI are frequently described by their parents as being forgetful, inattentive, and as seeming to process slower than before the accident. These subjectively reported symptoms are referred to as post-concussive symptoms (PCS), encompassing somatic (e.g., headache, fatigue), affective (e.g., disinhibition), as well as cognitive symptoms (e.g., inattention, forget-fulness; Yeates, 2010a; Yeates et al., 1999). There is some evidence of PCS being specific to mTBI (Sroufe et al., 2010), with children after mTBI displaying diverging developmental trajectories of PCS compared with injured controls without mTBI (Yeates et al., 2009).

Taken together, in the field of research regarding EF after mTBI, many questions still remain unanswered. Both parent-rated assessments and performance-based measures vary, depending on the EF component. Thereby, several studies revealed subtle deficits in WM (Catale et al., 2009; Scherwath et al., 2011; Sesma et al., 2008), and the modest empirical evidence in inhibition indicates at most minimal mTBI-related deficits (Catale et al.; Sesma et al.). In switching, both parental reports and performance-based measures reported no initial deficits (Gerrard-Morris et al., 2010; Sesma et al.), with parent ratings indicating an increase in switching difficulties within the 1st year after mTBI.

Based on the assumption that mTBI-related deficits tend to be subtle, particularly sensitive assessment instru-ments are needed to detect potential deficits. Moreover, as previous studies mostly targeted a rather long-time

horizon (e.g., Catale et al., 2009; Gerrard-Morris et al., 2010; Levin et al., 2002), empirical findings concerning the performance trajectory within the first few weeks after the mTBI are still lacking. It is of particular importance that, to the best of our knowledge, there is no existing study that has assessed EF following a theoretically and empirically established model of EF, as previous studies rather focused on single components of EF (e.g., Catale et al.; Levin et al., 2002).

With the present study, we aimed to contribute to more and detailed insights into EF performance after pediatric mTBI shortly after the accident and also regarding short-term developmental trajectories. Consideration of included EF components ensued, strictly theory-driven, following the model by Miyake and colleagues (2000). The selection of the EF tasks was made based on the tasks’ sensitivity to changes, confirmed in normative samples (e.g., Fatzer & Roebers, 2012; Michel & Roebers, 2008; Roebers et al., 2011; Roebers, Schmid, & Roderer, 2010). We explored potential EF performance differences between children with sustained mTBI and controls (matched in terms of sex, age, and education) at an initial assessment session 2 weeks after the injury. Furthermore, we aimed to examine the short-term longitudinal trajectories of EF dimensions (up to 12 weeks) in terms of either a recovery (in the case of indications of initial deficits in EF components) or in terms of potential inferior performance enhancements in the longitudinal trajectory (absent learning effect) if no ini-tial performance deficits were observable initially.

METHOD

Participants

Participants were recruited between November 2009 and December 2010 from different emergency departments of pediatric hospitals in Switzerland. Ethical consent for the study was obtained by the local ethics committees. Parents of patients within an age range of 5 to 10 years with a medical diagnosis of mTBI were informed about the current study by the responsible local hospital per-sonnel. Fifteen parents of patients who met inclusion cri-teria consented to participate (written consent). Thereafter, these parents were informed about the study in detail by the project coordinator by telephone where-upon all parents confirmed their child’s participation in the study and were scheduled for a first assessment ses-sion in the first 2 weeks after the injury (M = 13.6 days; SD = 4.1). Parents of one patient decided to withdraw from participation after the first assessment due to time needed for the study. For each patient, an uninjured child carefully matched in terms of age, sex, and education was recruited either in local schools or by personal contact. Highest levels of parental education (5-point scale) did

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not differ between patients and controls: for maternal education, t(23) = –0.88, p = .39 (mTBI, M = 2.46, SD = 1.3; controls, M = 2.92, SD = 1.2); for paternal edu-cation, t(24) = –1.28, p = .21 (mTBI, M = 3.15, SD = 1.35; controls, M = 3.86, SD = 1.41). Controls were tested fol-lowing exactly the same procedure as the patients for an estimation of practice effects due to multiple assessments. One patient and his corresponding control had to be excluded from analyses due to several missing data. Classification of the severity of the TBI was obtained according to medical case notes, and additional informa-tion was provided by parents. Descriptive statistics of patients and controls are shown in Table 1.

The definition of mTBI according to the ACRM (1993) was chosen as the main inclusion criterion comprising patients with at least one of the following symptoms: loss of consciousness, loss of memory immediately before or after the accident, alterations in mental state at the time of the accident, or focal neurological deficits. Moreover, the loss of consciousness must not exceed 30 minutes, the Glasgow Coma Scale score had to be rated in a range

between 13 and 15, and the loss of memory had to be resolved within 24 hours after the accident. As exclusion criteria, neurological, psychiatric, or (neuro-) develop-mental disorders (including attention-deficit hyperactivity disorder) were considered as was a documented history of previous relevant brain injuries. No participant had to be excluded according to these criteria.

All patients had been hospitalized for 1 to 3 days, fol-lowing the respective hospital routine for the treatment of mTBI. Furthermore, patients received pain medication if necessary and had been instructed to avoid visual stimu-lation from television and computers and also to avoid physical activity for 3 to 10 days (depending on the spe-cific guidelines of the hospital).

Procedure

A short-term longitudinal design with three assessments was realized. Testing sessions were scheduled 2 (T1), 6 (T2), and 12 (T3) weeks after the injury to assess acute as well as postacute sequelae of the mTBI. For controls, the temporal distance between assessment sessions was matched as closely as possible to that of the patients. Task order was either sequentially (Sequence A) or counterbal-anced (Sequence B) within patients but always parallel between patients and corresponding controls across test-ing sessions (either ABA or BAB). At the first assessment, a short parental interview was conducted and included information about the accident, family background, the parents’ educational attainment, and the child’s medical history. This information was used for a careful matching procedure of controls to patients. Thereafter, the child was tested individually in two 30-minutes sessions with a short break in between to prevent fatigue. After comple-tion of all tasks, children received a small gift.

Material

The selection of the applied EF tasks was made theory-driven and consisted of different tasks aiming to cover three core EF components of inhibition, shifting, and WM according to Miyake et al. (2000). Computerized tests were all programmed and run using E-Prime (Version 2.0) on a laptop. Responses were recorded employing two external response buttons, which were connected with a serial response box assessing ACC and RT. A schematic illustration of two examples of comput-erized tasks can be found in Figure 1.

Inhibition. Inhibition was assessed using a flanker task (aimed at assessing inhibitory performance of motor responses) and a fruit/vegetable Stroop task (covering the inhibition process of interference control). In the flanker task (child-friendly adaptation of the flanker task by Eriksen & Eriksen, 1974), the child was instructed to

TABLE 1 Participant Characteristics

Group

mTBI Controls

T1

N 13a 13a

Age at T1 in months, M (SD) 86.9 (14.4) 88.9 (15.9) Age range in months at T1

(min to max)61–114 60–116

Males, n (%) 7 (54) 7 (54) Age at injury in months (SD) 86.5 (14.6) — Time lag between injury and

T1 in days (SD)13.6 (4.1) —

GCS initial M (SD) 14.62 (0.7) — Posttraumatic amnesia 0–60 minutes (n) 6 — >60 minutes <24 hours (n) 3 — Loss of Consciousness 0–30 minutes (n) 5 — >30 minutes (n) 0 —T2

Age at T2 in months, M (SD)

87.9 (14.4) 89.7 (16.1)

Age range in months at T2 (min to max)

62–115 60–117

Time lag between T1 and T2 in days (SD)

29.92 (5.82) 27.77 (3.81)

T3

Age at T3 in months, M (SD) 89.3 (14.6) 91.0 (16.0) Age range in months at T3

(min to max)63–117 62–118

Time lag between T2 and T3 in days (SD)

44.5 (6.8) 45.8 (6.6)

an = 12 for the flexibility task due to missing data from one patient.

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respond as quickly and as accurately as possible to the orientation of a centrically presented stimulus (fish) while ignoring flanking stimuli (either fish or starfish; Michel & Roebers, 2008; Roebers & Kauer, 2009; Roebers et al., 2010). If the fish in the center of the screen pointed to the left side, the child had to press the left response button with the left hand regardless of the orientation of the flanking stimuli. By contrast, if the centrically presented fish was oriented to the right side, the child had to press the response button on the right side. Different conditions (fish alone, fish with flanking starfish, fish with flanking fish aligned [congruent condition], and fish with flanking fish opposed [incongruent condition]) were assumed to contain increasing inhibitory demands (see Figure 1a). After an instruction trial and 8 practice trials, two test blocks consisting of 36 trials each were carried out. Within a trial, an interstimulus interval, varying randomly between 800 ms and 1,400 ms, was presented, followed by a fixation cross, presented for 100 ms. Thereafter, another interval (500 ms) then was followed by the stimulus, which was presented for

1,000 ms at most or until the child pressed a button. A flanker inhibition composite score consisting of RTs and ACCs of incongruent trials (based on the scoring algorithm applied by Zelazo et al., in press), reflecting the ability of inhibitory control of motor responses, served as a dependent variable.

To assess the inhibition process of interference control, the fruit/vegetable Stroop task, an adapted and child-friendly version of the fruit Stroop task, was used (Archibald & Kerns, 1999; Roebers et al., 2011). Here, the child was pre-sented with four pages, printed with 25 items each. Squares, colored in yellow, blue, red, or green, were printed on the first page. The child was asked to name the colors, one after another, as quickly as possible. The next page consisted of fruits and vegetables (banana, strawberry, plum, and salad), which were colored in the same colors as the squares before, followed by a page consisting of the same fruits and vegeta-bles, printed in black and white. The last page was printed with incorrectly colored fruits and vegetables (e.g., blue banana). The child was asked to name the correct colors of the fruits and vegetables (e.g., yellow for banana) while ignor-ing the depicted color (e.g., blue in the case of the banana). Interference control was used as a dependent measure apply-ing the formula of Archibald and Kerns, with smaller units (seconds) indicating better resistance to stimulus incompati-bility and thus enhanced performance in interference control.

Working Memory. For the assessment of WM, a complex span task was administered (Fatzer & Roebers, 2012; Schmid et al., 2008). Children were presented with bisyllabic objects (colored in either blue or red) on a computer screen one after another (e.g., blue football, red pencil, and red airplane). Depending on the color of the object, children had to press an external response button for each presented object. Response buttons were placed next to the laptop keyboard on the left and the right sides and were marked with an underlying paper circle (blue or red). In addition, children were instructed to memorize the presented items. As a classic WM task, children had to memorize the presented items (storage) while continuously judging the color of the presented items (manipulation). The objects were presented for 1,500 ms, and a blank screen was presented after the stimulus allowing the children to take as much time as they needed for the ongoing task (pressing the button according to the color). At the end of a trial, a washtub was presented, and the child was asked to retrieve the memorized objects of the respective trial in the correct order. The task started with a span length of two objects immediately after three practice trials. Children had to complete six trials per span, and span length was increased by one if ACC was at least 50%. Trials were scored as correct if the child mentioned all objects of a span, irrespective of their order of presentation. Total number of correct trials was used as dependent variable.

FIGURE 1 Schematic illustration of trials of two computerized tasks (flanker task [a], cognitive flexibility task [b]).

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Switching. Switching was assessed employing a cognitive flexibility task. Two representatives (fish) of different categories (unicolored vs. multicolored) were presented on a screen simultaneously—a unicolored fish on the one side and a multicolored fish on the other side (see also Figure 1b; Fatzer & Roebers, 2012; Michel & Roebers, 2008; Roebers & Kauer, 2009; Roebers et al., 2011). The child was told to feed the fish while alternating between the unicolored and the multicolored family of fish. The side of presentation of the fish varied, following a predetermined pseudorandomized pattern. Therefore, the child had to hold in mind the relevant response dimension (unicolored/multicolored) while pressing the response button on the side of the target stimulus. As the task encourages a predominant response pattern of changing response sides (left–right–left), nonswitch trials referred to trials with changing response side (e.g., right–left), whereas trials with switching response sets (set-switch trials) were defined as trials with unchanging response sides in consecutive trials (e.g., left–left). Because set-switch trials require the individual to abandon the predominant pattern of response, demands on switching performance are highest in this condition. After an instruction trial and 10 practice trials, two test blocks were conducted consisting of 23 trials each with a short break in between. Within a trial, the stimulus (unicolored and multicolored fish) was presented after an interstimulus interval, varying randomly between 300 ms and 700 ms. The stimulus remained on the screen until the child responded. An auditory signal was presented if the child responded incorrectly. In the trial thereafter, the target stimulus was encircled. As dependent variable, a switching composite score (RTs and ACCs of set-switch trials) was calculated analogous to the flanker inhibition composite score (based on the scoring algorithm applied by Zelazo et al., in press), reflecting the ability to steadily switch response dimensions according to the current task demand.

Speed of Information Processing. Processing speed was assessed with a computerized RT task, where the child was asked to respond to a centrically presented stimulus as quickly as possible (Kail, 1991; Roebers & Kauer, 2009; Schmid et al., 2008). Here, a fish and a fisherman were presented simultaneously on the screen. The child was told that the fisherman intended to catch the fish and it was the child’s task to help the fish escape from the fisherman. There were 6 practice trials, followed by 16 test trials. Within a trial, after an interstimulus interval that varied randomly between 1,600 and 3,000 ms, the stimulus was presented for no longer than 1,500 ms or until the child responded. Mean RT was used as the dependent variable.

RESULTS

For each EF task, a mixed analysis of variance (ANOVA) with time as a within-subjects factor (T1, T2, and T3) and

group as a between-subjects factor (children with sus-tained mTBI and controls) was calculated to estimate improvements of performance relative to the initial level of performance. Partial eta2 values (ηp

2) are reported as an estimation of the effect size. No differences were observed between groups in terms of age, sex, and educa-tion due to the matched control design; these variables were therefore not included as covariates. Because speed of information processing did not differ between groups, F(1, 24) = 0.02, ηp

2 = .001, p = .88, nor did it differ across time, F(2, 48) = 0.42, ηp

2 = .02, p = .66, processing speed was not included in the analyses.

Inhibition

In terms of inhibitory performance of motor responses (flanker inhibition composite score, see Figure 2), a mixed ANOVA revealed a significant main effect of time, F(2, 48) = 7.98, ηp

2 = .25, p = .00 (T1 < T3), but neither the dif-ference between groups, F(1, 24) = 0.05, ηp

2 = 0, p = .82, nor the interaction between time and group, F(2, 48) = 0.3, ηp

2 = .01, p = .74, was found to be significant. In terms of interference control, measured with the fruit/vegetable Stroop task, a mixed ANOVA did not reveal any differ-ences between patients and controls: time, F(2, 48) = 1.59, ηp

2 = .06, p = .21; group, F(1, 24) = 0.06, ηp2 = 0, p = .81;

time × group, F(2, 48) = 0.44, ηp2 = .02, p = .65.

Switching

Figure 3 shows performance in the cognitive flexibility task. There was a significant main effect of time, F(2, 40) = 30.76, ηp

2 = .61, p = .00 (T1 < T2/T3), which was fur-ther qualified by an interaction between group and time, F(2, 40) = 3.47, ηp

2 = .15, p = .04. Tests of within-subject contrasts revealed that this interaction was attributable to an inferior performance enhancement between T1 and T2

in children with mTBI compared with controls. Overall,

FIGURE 2 Inhibition Composite Score (consisting of ACC and RT) of incongruent trials (and standard errors of the mean) in the flanker task as a function of time (T1, T2, and T3) and group (children with mTBI vs. controls).

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there were no group differences observable between patients and controls, F(1, 20) = 0, ηp

2 = 0, p = .98. Moreover, post-hoc comparisons did not reveal any dif-ferences between both groups at any time point.

Working Memory

In the complex span task (see Figure 4), a mixed ANOVA revealed a significant effect of time, F(2, 48) = 12.93, ηp

2 = .35, p = .00 (T1 < T2/T3), which was qualified by a significant time × group interaction, F(2, 48) = 5.66, ηp

2 = .19, p = .01. As was the case in the switching task, this interaction was attributable to an inferior perfor-mance enhancement between T1 and T2 in patients, compared with controls. The main effect of group was not significant, F(1, 24) = 0.56, ηp

2 = .02, p = .46. Post-hoc comparisons of time points revealed no differences between both groups at T1, t(24) = 0.66, p = .51, and T2, t(24) = –0.90, p = .38, but they revealed a significant group difference at T3 (mTBI < controls) indicating that the inferior performance enhancement led to small but mea-surable performance deficits over the course of the study, t(24) = –2.29, p = .04.

DISCUSSION

Although the relation between severe TBI and EF deficits has been demonstrated reliably through several studies both in adults and in children, empirical evidence con-cerning outcomes after mTBI in terms of EF is inconsis-tent and inconclusive, especially in pediatric samples. Nevertheless, both subjective complaints of PCS (Sroufe et al., 2010; Yeates et al., 1999) and functional magnetic resonance imaging (fMRI) results of diverging activation patterns after pediatric mTBI compared with healthy con-trols (Krivitzky et al., 2011) may count as indications of subtle deficits after pediatric mTBI, calling for particu-larly sensitive performance assessments. The present study aimed to investigate the initial level and the trajectory of EF in pediatric patients in a short-term longitudinal design (2, 6, and 12 weeks after mTBI). Performance of patients was compared to healthy controls, who were indi-vidually matched in terms of sex, age, and education. Despite a very small sample size, subtle deficits were observed in children after mTBI, which manifested in an inferior performance enhancement across assessment ses-sions in the EF components of switching and WM.

Comparing the performance of children after mTBI to controls initially and in the short-term longitudinal trajec-tory revealed differing results across EF components. In the EF component of inhibition, the present study did not reveal mTBI-related deficits. Although performance remained stable across assessment sessions in the process of interference control, both groups equally improved their performance in terms of inhibition of motor responses over time, which may be interpreted as a learning effect due to multiple testing. With respect to switching, performance enhancements were observable, particularly between 2 and 6 weeks after the injury, which may also be interpreted as a learning effect. However, this learning effect was less pro-nounced in children with mTBI compared with controls. In the EF component of WM, the present study again revealed diminished performance improvements between T1 and T2 in patients after sustained mTBI indicating that patients did not benefit from a previous administration of the tests in the same extent as healthy controls, resulting in subtle but measurable performance deficits 12 weeks after the injury. These deficits are assumed to be attributable to the injury, confirming findings that suggest that WM may be particu-larly sensitive to mTBI (Catale et al., 2009; Sesma et al., 2008). Our results are in line with results obtained with fMRI techniques (Krivitzky et al., 2011) indicating subtle mTBI-related deficits in the allocation of resources in com-plex EF tasks.

The finding that mTBI-related performance impair-ments did not manifest themselves initially after the injury but became apparent later on in longitudinal tra-jectories corresponds to one of the suggested scenarios. A similar performance trajectory in terms of a lack of an

FIGURE 4 Working Memory: mean number of correct trials (and standard errors of the mean) in the complex span task as a function of time (T1, T2, and T3) and group (children with mTBI vs. controls).

FIGURE 3 Switching Composite Score (consisting of ACC and RT) of set-switch trials (and standard errors of the mean) in the cognitive flexibility task as a function of time (T1, T2, and T3) and group (children with mTBI vs. controls).

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expected performance improvement over time as found in our study has also been documented in parental reports of switching performance (Sesma et al., 2008). Moreover, the issue of whether mTBI may affect ongoing develop-ment has already been raised previously by Dennis and colleagues (1995) outlining that effects of a head injury may occur developmentally time-lagged due to disrup-tions of the ongoing development. Our results, revealing that children after mTBI did not benefit from the repeated administration of a task whereas controls showed a per-formance enhancement over time both in WM and switching, count as further evidence for the assumption of a disruption of the ongoing development (Dennis et al.). In this context, our results add to the literature suggesting that consequences of mTBI in terms of switch-ing and WM may primarily consist of a lack of practice effect rather than manifesting themselves as substantial initial deficits. Considering children’s everyday life in school, this lack of performance improvement through practice may be significant as school activities often rely on repeated practice of newly acquired complex cognitive operations and children with mTBI may thus face a dis-advantage in such situations. However, regarding the small effect sizes of our results, it is questionable if these obviously small performance deficits manifest in every-day life.

One might argue that these performance deficits possi-bly underlie or relate to the deficits that are reported by parental ratings, stating that their children tend to be more forgetful and easily distracted after mTBI (e.g., PCS or BRIEF). Future research may therefore include both reported measures and sensitive performance-based assess-ments to disentangle associations and diversities among processes that are assessed with these different measure-ment instruments. As potential interrelations may shed light on the impact of even subtle EF deficits in everyday life, this question still remains unanswered.

A further arising question refers to the EF components that seemed to be affected by mTBI. Our study was based on the assumption of a three-factorial model of EF, with inhibition, WM, and switching being interrelated but separable subcomponents of EF (Miyake et al., 2000). Regarding the EF components of WM and switching, developmental progression is known to continue during the grade-school years (Diamond, 2006), whereas inhibi-tory skills are assumed to be relatively well developed at the age of 5 years (Davidson et al., 2006; Diamond). This faster developmental trajectory of inhibition may poten-tially act as a protective factor, preventing mTBI-related inhibitory performance deficits in children beyond the age of 5. From this perspective, the injury may have inter-rupted ongoing development in the EF components of WM and switching in our sample. Undoubtedly, more evidence in support of this hypothetical interpretation is needed.

Beyond the earlier-discussed ongoing developmental progression in switching and WM across the grade-school period, switching tasks present high challenges insofar as they require the individual to deactivate a previous response pattern to master the current task demands (Cragg & Chevalier, 2012; Davidson et al., 2006; Diamond, 2006). Similarly, our WM task contains a high level of complexity as it requires the individual to hold newly required memory content in mind while continu-ously manipulating these items (Garon, Bryson, & Smith, 2008). If the pattern of results was categorized according to the task complexity, our findings suggest that mTBI may lead to subtly limited resources as becomes evident in more complex tasks. Our results therefore indicate that children with mTBI were perfectly able to solve “easy” inhibitory tasks and to improve their performance to an expected extent. However, in more complex tasks, their resources were shown to be limited insofar as the task did not become easier despite multiple implementations. Support for this complexity-dependent interpretation comes from an adult study in which mTBI deficits were only found under more complex executive task demands (Bohnen, Jolles, & Twijnstra, 1992).

A new theoretical framework offers another possible yet speculative explanation. Based on the assumption that EF cannot be assessed purely, Miyake and Friedman (2012) recently introduced the unity/diversity framework. Using a latent variable approach, they evaluated common underlying variance as well as component-specific variance of an EF battery in adults, resulting in three underlying processes: common EF, WM-specific, and switching-specific abilities. Following these assumptions, our results possibly suggest that the common EF processes seemed to be spared by the mTBI while subtle disturbances were found in the longitudinal trajectory of the EF-specific WM and switching factors. Regarding our small sample size, this explanation may rather be considered as a vague assumption. Future research exploring EF after mTBI with larger samples that allow a latent modeling approach is indicated to further clarify mTBI-specific deficits in particular EF components.

There are some limitations of the study that ought to be mentioned at this point. First, due to our approach aiming to apply strict theory-based inclusion criteria, our sample size was small. However, by means of the applied closely matched control design, conclusions can be drawn despite the small sample, which can be regarded as a merit of our study. A larger sample size would thus possibly confirm our findings of WM deficits and addi-tionally reveal significant mTBI-related performance deficits in switching as well. Alternatively, however, different patterns of results may emerge. Second, the present data cannot determine whether the relative per-formance deficit in patients with mTBI reflect an absent practice effect or point to an interrupted development.

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Therefore, further studies are needed to evaluate the integrity or deficiency of EF and their development, par-ticularly in the context of mTBI. Third, even though we were able to demonstrate mTBI-related performance deficits in the longitudinal trajectory, the time horizon of 12 weeks between injury and T3 was relatively short. Particularly because our study revealed deficits that were not apparent initially but that emerged in the longitudi-nal trajectory in some core components of EF, it may be crucial to trace these functions in a longer term (e.g., 6 months, 1 year) to assess if the gap between patients and controls may be diminished or, in contrary, may enlarge. Therefore, the inclusion of additional long-term follow-up assessments would yield further clarification concern-ing very long-term consequences. Fourth, we applied a control group consisting of carefully matched controls. As one might argue, patients with, for example, orthope-dic injuries would constitute a more appropriate control group as they share the experience of being hospitalized. However, we follow the assumption that this experience per se is not especially critical and thus only contributes to the interpersonal variance of subjective experiences with sex, age, and education being much more crucial for performance, legitimating our matched case-control design. Fifth, IQ has not been assessed in the present study and could therefore not be controlled for. Sixth, as attention may not be intact even after mTBI, the assess-ment of attentional functions would be important as attention is known to be essential for the perception and processing of incoming information (Dennis et al., 1995). Thus, the stated inability to profit from previous learning sessions may potentially be moderated by defi-cits in the attentional system. Further examination of both the interplay and differences between EF and atten-tion after mTBI would be of particular importance in future studies.

To conclude, despite a small sample size, our study revealed subtle irregularities in performance after pedi-atric mTBI, which became evident in the longitudinal performance trajectories in the EF components of switching and WM in the course of the first 12 weeks after mTBI, whereas no adverse consequences of the accident were found for inhibition. More specifically, while performance enhancements over time were observed in healthy controls in the EF components of switching and WM in the first 6 weeks after the injury, inferior performance enhancements were observable in children after a sustained mTBI, leading to measurable performance deficits 12 weeks after the injury in the component of WM. Our results thus suggest mTBI-spe-cific limitations of cognitive resources after pediatric mTBI, which become apparent in terms of an inability to profit from previous learning opportunities in more complex EF tasks—a finding that is potentially impor-tant for children`s mastery of their daily lives.

ACKNOWLEDGEMENTS

We would like to give thanks to participating children and their parents, to Dr. Glock, Dr. Bruhin-Feichter, Dr. Trötschler, Dr. Keller, Dr. Liniger, Dr. Bittel, to the administrative services who helped us to establish contact with patients, and to Martina Studer, and Manuela Spiess, who supported us in the data collection. Many thanks also to R. Bühlmann, to P. Cimeli, to N. Destan, and to R. Neuenschwander for helpful comments on the manuscript.

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