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NeuroRehabilitation 34 (2014) 479–492 DOI:10.3233/NRE-141058 IOS Press

Neuroimaging and the school-based assessment of traumatic brain injury Paul B. Jantza,∗ and Erin D. Biglerb a Department

of Counseling, Leadership, Adult Education, and School Psychology, Texas State University, San Marcos, TX, USA b Brigham Young University, Salt Lake City, UT, USA

Abstract. Advanced neuroimaging contributes to a greater understanding of brain pathology following a traumatic brain injury (TBI) and has the ability to guide neurorehabilitation decisions. When integrated with the school-based psychoeducational assessment of a child with a TBI, neuroimaging can provide a different perspective when interpreting educational and behavioral variables relevant to school-based neurorehabilitation. School psychologists conducting traditional psychoeducational assessments of children with TBI seldom obtain and integrate neuroimaging, despite its availability. This article presents contextual information on the medical assessment of TBI, major types of neuroimaging, and networks of the brain. A case study illustrates the value of incorporating neuroimaging into the standard school-based psychoeducational evaluations of children with traumatic brain injury. Keywords: School psychologist, psychoeducational, TBI, neuroimaging, brain networks

1. Introduction For school-aged children who sustain a traumatic brain injury (TBI) it is axiomatic that their return to school and academic coursework becomes a real-world neurorehabilitation program (Glang et al., 2008; Marcantuono & Prigatano, 2008). However, most teachers have minimal exposure to the needs of children with TBI and likewise, school psychologists receive little formal training in assessing TBI or establishing school-based interventions for children with TBI (Jantz, Davies, & Bigler, in press). The need for school psychologists to become an integral part of the follow-up for children with TBI is highlighted by two recent studies with sobering statistics. Coronado et al. (2012) recently reported that US hospital, emergency department, outpatient department, ∗ Address for correspondence: Paul B. Jantz, Department of Counseling, Leadership, Adult Education, and School Psychology, 601 University Dr., ED 4033, Texas State University, San Marcos, TX 78666, USA. E-mail: [email protected].

and office-based physician data indicate that in 2009 approximately 3.5 million individuals sustained and survived a TBI. This figure is 1.9 million more than previous Centers for Disease Control and Prevention (CDC) estimates (Faul, Xu, Wald, & Coronado, 2010), which did not include data from outpatient facilities or doctor’s offices. Neither set of figures includes those who do not seek medical assistance. The CDC estimate indicates that approximately 43% of all TBIrelated emergency department visits/hospitalizations were children between the ages of 0–19, therefore it is reasonable to assume that at least 1.5 million of the approximately 3.5 million individuals in the Coronado et al. study were also between the ages of 0–19. In a study conducted in the province of Ontario, Canada that targeted children in grades 7–12 and assessed TBI prevalence, Ilie, Boak, Adlaf, Asbridge, and Cusimano (2013) report that 20% of all children reported a TBI. Within the year previous to taking the survey, 5.6% of these children reported having experienced a TBI. Taken together, the Coronado et al. and

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Ilie et al. studies suggest that in every classroom there is a good likelihood that a child with a TBI is present, yet for many of these children, given the lack of formal TBI-related training in assessment and intervention of teachers and school psychologists, it is likely that specific neurorehabilitation programs within the educational system that potentially could benefit the child are not being identified and/or implemented. School-based neurorehabilitation programs become more obvious for school-age children whose TBI requires hospitalization – because the need for neurorehabilitation continues long after the child’s integration back into school – or when they have obvious deficits such as hemiplegia, aphasia or some type of sensory deficit (Glang et al., 2008; Hawley, Ward, Magnay, & Mychalkiw, 2004). Although less obvious for children who sustain a mild TBI (mTBI), there is mounting evidence suggesting the need for ongoing school-based neurorehabilitation programs for some children with mTBI. Regardless of the injury severity level, when a school-aged child sustains a TBI and returns to school, at a minimum some form of spontaneous neurorehabilitation will automatically take place with the school environment and classroom becoming the rehabilitation program. While members of school-based multidisciplinary assessment and intervention teams do not typically think of their involvement with a child with a TBI as being in the realm of neurorehabilitation, if what they do were to occur in a hospital/medical setting it would be considered part of a broader neurorehabilitation plan. Therefore, it is clear that school-based assessment and intervention contribute significantly to the neurorehabilitation and follow-up of children with TBI within the school setting. School-based multidisciplinary intervention teams include school psychologists who provide a range of services, including psychoeducational assessment, that assist teams in implementing skill- and ability-based academic programs for children with TBI. Traditionally, a school psychologist’s typical psychoeducational assessment is comprised of standardized paper-and-pencil cognitive, achievement, emotional and behavioral testing and classroom observations (Merrell, Ervin, & Peacock, 2012). An important part of any psychoeducational assessment is that it purportedly provides objective characterization of cognitive and behavioral functioning of the child with information relevant for the classroom teacher (Domino & Domino, 2006; Merrell et al., 2012; Sattler, 2008). The master organ of cognition and behavior, of course, is the brain and psychoeducational assessment

findings permit making inferences about brain function. This is particularly true for children with TBI who are in need of neurorehabilitation acquired through special school assistance and accommodation after their injury. However, as pointed out by Millis (2009) “ . . . cognitive tests do not directly measure cognition: they measure behavior from which we make inferences about cognition” (p. 2409). This statement can be expanded to using cognitive and behavioral indices to make inferences about brain function, particularly abnormal brain function. If the results of a cognitive measure do not tap a particular dimension of underlying brain damage or dysfunction from TBI, their use may lead to incorrect inferences about the nature of the cognitive and/or behavioral deficit – especially if a conclusion about the absence of a brain injury effect was made because the measure was adequately performed. In addition, for effective neurorehabilitation to occur following TBI, it must be directly tied to the real-world competencies of the individual, something standardized testing does not do very well (Wilson, 2003). As Wilson notes, although standardized testing results may provide a “profile of a person’s cognitive strengths and weaknesses, they do not tell us a great deal about how people with neuropsychological deficits cope in everyday life” (p. 26). Part of making sense out of any psychoeducational assessment is integrating the clinical history with the objectivity of the assessment measures. At the beginning of the 21st Century there is a tremendous increase in diagnostic neuroimaging technology that is simply not being incorporated into the typical school-based psychoeducational assessment of the child with some form of acquired brain injury (ABI), which includes all TBIs that occur in childhood. Regardless of the etiology of the condition that lead to an ABI, it is likely that neuroimaging – often multiple types of brain scans – has been performed on the child and that information should be used by school psychologists. This is especially true for the child with a history of TBI. Traditional school-based approaches to the educational assessment of a child with TBI, regardless of the assessment model used or the outcome of the evaluation, ultimately results in a descriptive “paper profile” of the child. This typically takes the form of a psychoeducational report (written by the school psychologist) that summarizes information obtained from a variety of norm-based tests/assessments (e.g., cognitive measures, achievement measures), behavioral classroom observations, school records, medical records, neuropsychological reports, and interviews with relevant individuals; including the child. The final

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psychoeducational report is generally presumed by the school community to accurately represent the child’s educationally-based ability levels in the assessed areas. Unfortunately, it can also become gospel, rather than guidance; despite any caveats about inherent threats to reliability, validity, interpretability, and/or generalization. Once the school-based assessment process has been completed on a child with TBI, the culminating psychoeducational report plays an important role in determining whether or not the child meets qualifying criteria for special education services, as delineated in the Individuals with Disabilities Education Improvement Act (IDEIA 04; 2004). It also sets the tone for how the child will be viewed by teachers and administrators within the educational environment. That is, it becomes the means by which judgments and decisions are made about the degree to which a child appears to have recovered from his or her TBI and the basis for understanding any behavioral or academic irregularities; regardless of accuracy. Finally, should the child qualify for special education services, it will be used to guide school-based neurorehabilitation interventions deemed to be appropriate by the multidisciplinary team. Recently, an entire journal issue of NeuroRehabilitation (Vol. 31 (3), 2012) spoke to the advantages of advanced neuroimaging in the “greater understanding of brain pathology and . . . potential influence on rehabilitation outcome” (Wilde, Hunter, & Bigler, 2012a; p.223) and Stuss (2011), in discussing the future of cognitive neurorehabilitation, stated that “evolving new techniques of analyzing neural networks . . . allow assessment of specific aspects of brain plasticity” (p.759). Neuroimaging information provides an objective piece of clinical history and when properly integrated with the school-based psychoeducational assessment can make a distinct difference in understanding a TBI and its influence on educational and behavioral variables germane to neurorehabilitation in the schools. Neuroimaging information on the TBI child, including select images, is typically readily available and school psychologists should be incorporating this information into their standard psychoeducational evaluations of children with ABI/TBI; because it provides relevant information about potential brain regions affected by the injury. This becomes particularly relevant when brain injury disrupts social and emotional centers of the brain without necessarily adversely influencing brain regions that participate in more classic areas that psychoeducational testing is more sensitive to (i.e., academic performance, intellectual ability,

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perceptual motor functioning, memory and attention, language). The intent of this paper is to show from a neurorehabilitation standpoint, by way of a case study, that (a) without the integration of contemporary neuroimaging information, the traditional school-based psychoeducational assessment that tends to focus on cognitive test performance is limited in what it can accomplish when the TBI induces social-emotional changes, (b) in the era of neuroimaging, school-based educational assessment and neurorehabilitation programming for the TBI child may be enhanced by incorporating neuroimaging information, and (c) when objective structural damage is present, viewing neuroimages provides visually descriptive information and additional insight into understanding the influence that the brain injury has had on neurobehavioral and neurocognitive outcome in ways not derived from the traditional school psychologist-generated psychoeducational report. Recently an entire issue of NeuroRehabilitation was devoted to enhancing the role that neuroimaging findings may play in neurorehabilitation (see Wilde et al., 2012a). Although school psychology was not specifically dealt with in that issue, in a recent issue Bigler et al. (2013) reviewed neuroimaging findings in social outcome in school-aged children. Likewise, in this same cohort of children with TBI Dennis et al. (2013) examined TBI-related damage in five large-scale functional brain networks. The current study extends these observations to the role that neuroimaging may play in school-based neurorehabilitation in the post-discharge TBI child referred for psychoeducational assessment and congitive and behavioral intervention within the school. Contemporary neuroimaging methods utilized in neurorehabilitation have been overviewed by Wilde et al. (2012b) and likewise a variety of other reviews (Duhaime, Holshouser, Hunter, & Tong, 2012; Gean & Fischbein, 2010; Haacke et al., 2010) and will not be detailed in this case report. However, the issue of network disruption in TBI does require some review from the perspective of how neuroimaging assists in defining network damage.

2. Brain networking The human brain is organized into large-scale, interlinked, structural and functional networks that contain hundreds of brain regions and thousands of aggregate

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Fig. 1. Brain networks and hubs. Simplified illustration depicting the methods and steps that go into deriving networks of the brain. Using automated image analyses methods to identify traditional surface anatomy (two upper left images) along with subcortical (upper right images) regions of interest (ROI), various methods of size, volume and/or shape analyses may be used in establishing these regions of interest. Diffusion tensor imaging (DTI), including methods that establish white matter tracts of the brain, as shown in A (lower left) and combined traditional ROIs (B), show how pathways interconnect ROIs (C). From these, networks may be developed as shown in the lower right, where the largest hubs (large solid red circles - connected by thick blue lines) represent rich-club hubs that likely play the most vital ‘trafficking’ role in the pathway network. Smaller hubs have lesser roles in the network and minor nodes (smallest solid red circles) the least. Note in this network view that if damage occurred to one of the small nodes that minimal disruption to the network would occur. In contrast, because all regions throughout the brain have at least one direct connection to a rich-club hub a small lesion to a critical rich-club hub would result in major network disruption. Adapted with permission from van den Heuvel and Sporns (2011).

interconnecting white matter pathways (Sepulcre et al., 2012; van den Heuvel & Sporns, 2011). Three of these core networks appear to be intricately linked to higher cognitive function and dysfunction (e.g., working memory and attention, reward and motivation, self-referential mental activity, social processing) and major psychiatric and neurological disorders (e.g., depression, schizophrenia; Menon, 2011). These areas are the central executive network (CEN), the default mode network (DMN), and salience network (SE). Higher-level cognitive functions associated with the

CEN are control of attention and working memory, planning, and decision making. The (DMN) is a highly integrated system associated with self-related cognitive activity, including autobiographical, self-monitoring and social functions. The (SE) is involved in detecting and orienting to salient external stimuli and internal events. The CEN, DMN and SE in conjunction with two other neurocognitive networks (mentalizing network [MN]; mirror neuron empathy network [MNEN]) have been found to be involved in theory of mind (Bigler

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et al., 2013; Dennis et al., 2013). The MN is a social cognitive network that involves thinking about the mental states of others and oneself and the MNEN, also a social cognitive network, involves the ability to empathize and understand actions during didactic interactions. Central to the operation of these complex networks are cortical brain hubs that link widespread regions of the brain (Fig. 1). These cortical hubs are located in primary and secondary information processing areas of the brain, are thought to support the integration of high-level cognitive functions, and are believed to be responsible for maintaining efficient global brain communication (Colizza, Flammini, Serrano, & Vespignani, 2006; van den Heuvel & Sporns, 2011). In addition, it appears that some of the cortical hubs are more densely interconnected among themselves. These densely interconnected hubs have been referred to as “rich-clubs” (Colizza et al., 2006). Although rich-clubs are more highly interconnected with each other, they are also interconnected with other less densely connected hubs and brain regions. Failure of a hub within a rich-club or a large-scale neurocognitive network can have a significant effect on the degree of global communication efficiency of a brain region or network and possibly, overall brain communication. Thus, disruptions in rich-clubs or other less dense brain hubs result in disruption of function in “downstream” networks, which can lead to the propagation of dysfunctional downstream brain regions or networks over time (Menon, 2011). Damage to a brain region, hub, richclub, or the interconnecting pathways can also lead to a brain network behaving in an abnormal or untypical way. Because DTI is effective in revealing white matter tracts it has been used to reconstruct and map the richclub hubs and their interconnecting pathways combined with other MRI-based neuroimaging methods (Fig. 1; van den Heuvel & Sporns, 2011). This makes DTI a useful tool in the psychoeducational assessment of TBI as it allows the school psychologist to “look” at the scan and infer what specific hubs, nodes and networks are being affected by the injury; something that neuropsychological and psychological paper measures are not particularly well-suited to do. Furthermore, the combined use of DTI and other MRI neuroimaging allows the school psychologist to clearly “see” and fully understand the extensiveness of network disruptions following a TBI. This can be particularly helpful to school psychologists as they review and interpret the results of school-based psychoeducational assessments. DTI can also aide school psychologists in helping other

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school professionals appreciate the extent of a child’s TBI as they are “intuitive” to look at and see affected pathways.

3. Case study Every day, professionals working in public schools make judgments about child behavior. Some judgments are based on data obtained from standardized test scores while others are based on general observational comparisons to same-age peers. Judgments about children with TBI are no different, however, those judgments based on general observation of physical appearance often take precedence over more reliable information (e.g., informant report). That is, if physical signs such as scarring or motor impairment are absent, or easily overlooked, then the child may be judged to have “fully recovered” from his or her TBI because outwardly they appear “normal”, despite informant report to the contrary. This is due, in part, to the fact that intrinsic to human nature is the tendency to judge others by their outward appearance and allow those judgments to influence decisions in other areas. In qualitative research this is known as the halo effect (Thorndike, 1920) and it is well documented. In the majority of TBI cases, injury consequences, or the extent of recovery, do not manifest in readily observable physical signs, nor can either be determined by observation alone. This is because the areas that, if damaged, result in physical signs (e.g., paralysis) constitute a very small percentage of the total area of the brain and the chances of injury to these specific areas (relative to other brain areas) are significantly low. In addition, scarring, if present, can often be covered by makeup, hair, or clothing (hats). Consequently, to all outward appearances, a child with a TBI will generally appear to be either unaffected by the TBI or fully recovered. Therefore, when judgments are made based solely on appearance, and there is lack of evidence to the contrary, the observer will likely perceive the child as being unaffected by the TBI and, unfortunately, misattribute TBI-related behavior to other causes (e.g., volition) and hold the child to a higher level of behavioral expectation. The following case presents a young adolescent with a severe TBI who, in the absence of outward physical abnormalities, language impairment, or noticeable limitation in cognitive ability demonstrated significant social-emotional and behavioral difficulties related to the disruption of interconnected frontal lobe networks.

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By combining neuroimaging of this child with available cognitive, behavioral, and academic test results, this case illustrates how, on paper and to the uninformed observer – including teachers and school counselors – the consequences of a TBI can appear to be unconnected to observed behavior, how the TBI-related behaviors could easily be misattributed to other causes, and how neuroimages can assist school psychologists and other educational professionals by providing a more complete description and additional insight into understanding how structural damage may influence the neurobehavioral and neurocognitive outcome in ways not derived from the traditional school psychologist-generated psychoeducational report 3.1. Medical background The adolescent was a 13-year-old, 8th grade male who sustained a severe TBI as a result of a high-speed, multi-car accident at the age of 11. Although appropriately restrained he was nonetheless struck in the head, sustaining a penetrating injury to the right frontal area. To the casual observer he lacked any readily noticeable physical characteristics (e.g., motor deficits) that might indicate he had been in a serious accident, or sustained a substantial TBI, and he had grown his hair fashionably long to hide indications of surgery, a subtle skull defect, and injury scarring. There was nothing unusual whatsoever about his speech, with normal prosody and flow of oral communication. Likewise, outward mannerism were entirely age-appropriate. When injured he was unconscious throughout extrication and loading onto the medical evacuation helicopter. In route to the hospital, while restrained on a backboard, he remained unconscious, but began making unintelligible sounds, and became combative. Upon arrival in the emergency department he was intubated and an intracranial pressure monitor was placed. He continued to be combative, make unintelligible sounds, and his GCS score was 7; indicating a severe TBI. He remained unconscious for three days. The admitting diagnosis was: severe closed head injury with contusion and traumatic injury to the right orbit. Nine days post-injury he was discharged from the hospital with the following diagnosis: right frontal bone and skull fracture, right frontal epidural hematoma, bilateral temporal contusion, mild diffuse subarachnoid hemorrhage, right-side diffuse axonal injury, right medial and right orbital roof fracture, and left external auditory canal fracture. One month post-injury he was diagnosed with Attention Deficit Hyperactivity Disor-

der (ADHD) secondary to TBI and prescribed stimulant medication. 3.2. Neuroimaging DOI CT scans revealed evidence of a small right-sided temporal epidural hematoma, early uncal herniation, right-side diffuse axonal injury, edema in the right temporal lobe, and a right-side depressed fracture of the orbital roof. A clinical MRI sequence (T1, T2, GRE, FLAIR) conducted four days post-injury revealed significant and extensive contusional injury of the right frontal lobe and right temporal lobe; right-side epidural and subdural hematoma, evidence of subarachnoid hemorrhage, and right-side shear injury affecting the splenium of the corpus callosum. A CT taken 23 days post-injury revealed right frontal-temporal encephalomalacia (generalized brain tissue softening). A clinical MRI sequence (T1, T2, GRE, FLAIR) taken 10 months post-injury (Fig. 2) revealed mild to moderate bilateral hippocampal atrophy, more severe on the right; multiple frontal areas of abnormal signal intensity indicative of hemorrhagic contusions and/or shearing injury, significantly greater on the right, with associated encephalomalacia, also more severe on the right; abnormal signal intensity involving the region of the olfactory bulbs, more severe on the right; significant decrease in corpus callosum fiber tracts frontally, more severe on the right, and chronic sinusitis. 3.3. Emotional and psychosocial behavior Two years post-injury the adolescent required substantial direct parental supervision due to significant difficulties with impulsivity; over-reaction to minor problems; ongoing unawareness of dangerous situations; a continued inability to assess, identify or manage emergency situations; significant ongoing difficulty getting along with demanding siblings; and combativeness. Emotionally, he was prone to extreme mood lability (bouts of hysterical crying, angry outbursts, excessive irritability) and intense periods of acute onset anxiety or fear. Socially, despite repeated effort on his part he was unable to make and maintain friendships because he was perceived as being overbearing, immature, and “strange.” He continually made sexually inappropriate comments about female peers and was the victim of teasing and bullying by male peers. Compared to same-age peers, his mother’s ratings of his behavior two years post-injury on a normative measure used to help assess Attention Deficit Hyperactivity

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Fig. 2. Clinical MRI axial sequence (T1, T2, FLAIR, GRE, DTI) taken 10 months post-injury with corresponding 3-D reconstruction. When image reconstruction is presented in 3-D juxtaposed to the clinical MRI, the images are not in radiological orientation, so left is on left in viewing the image. Depending on the MRI sequence, the amount of visible damage varies. Damage to the right frontal white matter is clearly evident in the T1 image (compare prominent dark region on right to vibrant light gray white matter tracts on left). Focal damage to right frontal brain tissue (from the penetrating head injury) appears white in the T2 image and black in the FLAIR image. The black dots in the right frontal area of the GRE indicate hemosiderin left over from prior hemorrhagic contusions and/or shearing injury, also visible as black dots in corresponding areas of the FLAIR image. The corresponding 3-D axial image on the right top further demonstrates the extent of damage to the frontal area - in this 3-D image, the red represents the focal encephalomalacia, the flesh color represents the white matter abnormalities on the FLAIR sequence, and the yellow depicts the aggregate regions of hemosiderin deposition. The 3-D oblique image on the right top illustrates focal atrophy of the entire frontal lobe when compared/contrasted to the left frontal oblique (bottom image). The duller color in the right frontal area of the axial DTI image on the bottom left and the sagittal 3-D DTI image on the bottom right indicate severe disruption to the white matter tracks and corresponding brain networks. On DTI, warm colors (orange-red) represent lateral projecting fiber tracts, green are anterior to posterior and blues are vertically oriented tracts. The color-code for the DTI tractography in the axial DTI image on the bottom left and the sagittal 3-D DTI on the right bottom image are the same. Note the significantly enlarged ventricle on the right-side of the T1, T2, & FLAIR images, indicative of increased volume loss of brain tissue affecting the entire hemisphere. In instead of the SWI sequence in Fig. 1, this child underwent a standard GRE sequence, which also shows hemosiderin.

Deficit (Connors’ Parent Rating Scales – Revised: Long form [CPRS-RL], Connors, 1997) resulted in ten out of thirteen significantly clinically elevated T-scores. Compared to same-age peers, the adolescent’s ratings of his own behaviors on a self-report version of a similar measure (Conners-Wells’ Adolescent Self-Report Scale – Long Form [CASS-L], Conners et al., 1997) resulted in one borderline clinically elevated score. Additionally, his self-ratings on a normative measure of depression, anxiety, anger, disruptive behavior and self-concept (Beck Youth Inventories, 2nd ed. [BYI-2]; Beck, Beck, Jolly, & Steer, 2005) resulted in only one borderline clinically elevated scale (see Table 1). 3.4. School behavior and academic progress The adolescent experienced significant behavioral difficulties at school, which resulted in multiple

referrals to the principal’s office for disciplinary action. Difficulties included failing to comply with school rules (tardy to class, running or yelling in the halls), talking back to teachers, arriving late to school, and getting into physical and verbal fights with peers. He had his bus privileges revoked for not following safety discipline rules (getting out of seat while the bus was moving, yelling out windows at pedestrians). Other observed difficulties included significant forgetfulness (e.g., forgetting to take school supplies and assignments to class, forgetting after school activities), disorganization, difficulties with concentration, and difficulties planning enough time to complete assignments. Parents reported they had to organize his homework for him and monitor his study time, which often became a source of conflict between them. School records two years post-injury indicated that the majority of obtained grades (tests, work

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Table 1 Results of emotional and psychosocial behavior rating scales 24 months post injury T-score Parent CPRS-RL Oppositional Cognitive Problems – Inattention Hyperactivity Anxious-Shy Perfectionism Social Problems Psychosomatic ADHD Index Restless Impulsive Emotional Lability DSM-IV Inattentive DSM-IV Hyperactive/Impulsive DSM-IV Total Student CASS-L Family Problems Emotional Problems Conduct Problems Cognitive Problems Inattention Anger Control Problems Hyperactivity ADHD Index DSM-IV Inattentive DSM-IV Hyperactive/Impulsive DSM-IV Total BYI-2 Self-concept Anxiety Depression Anger Disruptive Behavior

63 71 83 90 57 90 54 71 74 67 72 70 73

58 60 56 59 61 53 63 54 59 57 43 60 56 59 57

CPRS-RL = Conners’ Parent Rating Scale – Revised Long Form (Connors, 1997). CASS-L = Conners-Wells’ Adolescent Self-Report Scale - Long Form (Connors et al., 1997). BYI-2 = Beck Youth Inventories - Second Edition (Beck, Beck, Jolly, & Steer, 2005).

samples, and report cards) were B’s and C’s (74%), with a few A’s (17%) and a few F’s (10%); indicating a decline compared to A’s and B’s the previous year. 3.5. Adaptive behavior On a normative measure of functional skills necessary for daily living (Adaptive Behavior Assessment System, 2nd, (Harrison & Oakland, 2003) the adolescent’s parents reported significant concerns about independent levels of functioning because they perceived him as na¨ive; gullible; unaware of his cognitive, social, and emotional deficits; and unable to understand the consequences of his actions (e.g., the risks involved with forgetting to turn off the stove). They also believed he was incapable of living alone because they perceived him as having severe deficits in the skills

Table 2 Results of adaptive behavior 24 months post-injury ABAS-II

SS

Com CoUe FA HL Lei SC

4 2 10 1 4 5

SS SD Soc GAC Con So Pr

1 1 62 72 64 54

Adaptive Behavior Assessment System II (ABAS II; Harrison & Oakland, 2003): Com = Communication; CoUs = Community Use = FA: Functional Academics; HL = Home Living; Lei = Leisure; SC = Self Care; SD = Self Direction; Soc = Social; GAC = General Adaptive Composite; Con = Conceptual; So = Social; Pr = Practical. Table 3 Results of cognitive and academic measures over time WISC-IV Five months post-injury VCI PRI WMI PSI FSIQ RIAS 19 months post-injury VIX NIX CMX CIX WISC-IV 24 months post-injury VCI PRI WMI PSI FSIQ

SS

WJ-III ACH

SS

128 110 97 97 114 SS

PC AP RF MF WF WJ-III ACH

113 118 128 102 126 SS

SS

PC AP RF MF WF WJ-III ACH

109 114 122 106 125 SS

119 102 97 94 106

PC AP RF MF WF

110 113 129 100 126

124 105 104 115

CAS

SS

PCS SmPC AC ScPC FSIQ

112 115 109 114 117

Wechsler Intelligence Scale for Children – Fourth Ed. (WISCIV; Wechsler, 2003): VCI = Verbal Comprehension Index; PRI = Perceptual Reasoning Index; WMI = Working Memory Index; PCI = Processing Speed Index; FSIQ = Full Scale IQ. Reynolds Intelligence Assessment System (RIAS; Reynolds & Kamphaus,2003): VIX = Verbal Intelligence Index; NIX = Nonverbal Intelligence Index; CMX = Composite Memory Index; CIX = Composite Intelligence Index; Cognitive Assessment System (CAS; Das, & Naglieri, 1997): PCS = Planning Composite Score; SmPC = Simultaneous Processing Composite; AC = Attention Composite; ScPC = Successive Processing Composite; FSIQ = Full Scale IQ. Woodcock-Johnson III-Tests of Achievement (WJ-III ACH; Woodcock, MMcGrew, & Mather, 2001): PC = Passage Comprehension; AP = Applied Problems; RF = Reading Fluency; MF = Math Fluency; WF = Writing Fluency.

required to effectively communicate, use community resources, take care of the home environment, remain safe and healthy, engage in leisure activities, care for himself, or engage in necessary self-directing behaviors (see Table 2).

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Table 4 Results of neurological assessment 24 months post-injury WCST Categories Set Failures Trials to First Perseverations D-KEFS TMT Scanning N Sequencing L Sequencing Switching M Speed DFT Filled Empty Switching Total Correct Perseverations Set Loss VFT Letter Category Cat Switching Total Switching Perseverations Set Loss

FTT >16% >16% >16% T 51

SS 10 SS 12 SS 12 SS 13 SS 13 SS 5 SS 6 SS 7 SS 5 SS 12 SS 9 SS 10 SS 15 SS 14 SS 14 SS 3 SS 13

GPBT

R-Hand L-Hand

T 60 T 55

CVLT-C Trial 1 Trial 5 Total Learning Learning Slope List B Proactive Interference SDF Recall SDC Recall LDF Recall LDC Recall Semantic Cluster Serial Cluster Recognition Hits Total Intrusions Total Perseverations Primacy Middle Recency

Z 0.5 Z −0.5 T 56 Z −1.0 Z 2.5 Z 2.0 Z 0.5 Z 1.5 Z 1.0 Z 1.5 Z 1.0 Z −0.5 Z 0.5 Z −0.5 Z 0.0 Z 0.5 Z −0.5 Z 0.0

R-Hand L-Hand

T 60 T 55

RCFTRT Immediate Delayed Recognition Copy Time False Positive True Negative

T 45 T 39 T 58 16% >16% >16%

TOMM Trial 1 Trail 2 Retention

48 50 50

Wisconsin Card Sorting Test (WCST; Grant & Berg, 1948; Milner, 1963; Heaton, 1981; Heaton, Chelune, Talley, Kay, & Curtis, 1993). Finger Tapping Test (FTT; Reitan, 1969). Grooved Pegboard Test (GPBT; Matthews & Klove, 1964). Delis-Kaplan Executive Function System (D-KEFS; Delis, Kramer & Kaplan, 2001) TMT = Trail Making Test; DFT = Design Fluency Test; VFT = Verbal Fluency Test. California Verbal Learning Test – Children’s Version (CVLT-C; Delis, Kramer, Kaplan, & Omer, 1994) SDF Recall = Short Delay Free Recall; SDC Recall = Short Delay Cued Recall; LDF = Long Delay Free Recall; LDC Recall = Long Delay Cued Recall. Rey Complex Figure Test and Recognition Trial (RCFTRT; Meyers & Meyers, 1996). Test of Memory Malingering (TOMM; Tombaugh, 1996).

3.6. Cognitive and academic ability

3.8. Interpersonal communication

Cognitive and academic ability was measured three times within a 19 month period: five months post-injury, 19 months post-injury, and 24 months post-injury. Relevant results are reported in Table 2. Results of standardized cognitive assessment instruments showed a steady decline in cognitive functioning over a 14-month period with scales measuring overall cognitive ability dropping from high average performance to average performance. Overall scores on standardized measures of academic performance during the same time period remained relatively consistent with scores ranging from average to superior.

Communicatively the adolescent engaged in grammatically correct conversations with simplistic sentences that were generally lacking in abstract content. Despite adequate conversational comprehension skills, he demonstrated poor conversational reciprocity, had significant difficulty taking the perspective of others, interrupted frequently, and maintained little eye contact – all essential to of theory of mind.

3.7. Neuropsychological The results of neuropsychological testing twenty four months post-injury (Table 4) revealed mild to moderate impairments in executive function, visual memory retrieval, visuomotor integration, and psychomotor speed (left more affected than right hand).

3.9. Self-perception Despite the perceptions of others, the adolescent perceived that behaviorally any problems or issues he may have been experiencing were not of a significant nature. That is, he stated that as far as he was concerned, things were “okay.” He also felt that he was not picked on, singled out, nor bullied at school. He believed that he had a circle of friends; including a best friend, when in fact, he had neither. Despite academic performance at

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school falling mostly in the B and C range, he stated he disliked every aspect of school and would rather stay at home and play computer video games. 4. Discussion This case presents a 13-year-old adolescent who sustained a severe TBI with prominent social difficulties, emotional and behavioral sequelae, mild to moderate difficulties in executive functioning, and significant impairments with theory of mind – but minimal to no “cognitive” deficits as shown by traditional psychoeducational assessment. If neuroimaging information was excluded, and the results of this adolescent’s psychoeducational paper profile were considered outside of the context of a TBI, strictly at face value, and from a purely academic perspective the overall results would not raise alarm among the educational community. That is, with the majority of his academic grades falling within the average to above average range, this adolescent would not, on the basis of academic performance alone, be brought to the attention of school-based academic performance evaluation team members. Furthermore, his cognitive performance profile would not compromise his ability to perform at an adequate (passing) academic level. Behaviorally, the ADHD assessment results would adequately “explain” his current behavioral difficulties and his deficits related to theory of mind (e.g. difficulty taking the perspective of others) would be considered to be due to poor social skills. In addition, many of his behaviors, such as fluctuating academic progress, conflict over homework, mood lability, and angry outbursts/irritability would be common among adolescents in this age group. Without the history of TBI combined with the neuroimaging findings, explanations of behavioral problems could all be framed with purportedly non-TBI-related neurologic conditions. When taken within the context of a TBI, without the integration of neuroimaging, the neuropsychological test results and psychoeducational paper profile produced by cognitive, academic, and behavioral testing would support a diagnosis of ADHD secondary to sustaining a severe brain injury. That is, impulsivity and inattention would be perceived to be at the root of this adolescent’s academic variability and behavioral difficulties – accounted for by TBI-induced deficits in executive functioning resulting from focal damage to the right anterior frontal lobe. In addition, many of his emotional behaviors (e.g., intense periods of acute onset anxiety or fear) and social behaviors (e.g., oppositional behavior) could potentially be relegated to what

in DSM-V (American Psychiatric Association, 2013) parlance would be an “adjustment disorder.” Without the neuroimaging, explanations of behavioral problems could easily be limited to mild to moderately severe executive functioning deficits (e.g., impulsivity and perseveration, nonverbal mental rigidity), ADHD, and non-neurologic psychological trauma. Integrating neuroimaging provides a much different profile of this adolescent. As already noted, the multimodality approach to neuroimaging with the summary images in Fig. 2 reveal the true extent of widespread damage beyond the focal penetrating injury. The four vertical axial images on the right side of Fig. 3 (obtained at a different level than those in Fig. 2) show that while the frontal lesion is unmistakably large (four images on right), it is not just the frontal lesion that is a problem, but it is how the focal frontal damage disrupts the entire network functioning of the brain. In addition to showing the focal injury to the right inferior frontal lobe (white arrows), Fig. 3 reveals that the entire right frontal lobe is compromised, there is diffuse damage to the brain, and there is a generalized disruption of white matter fiber tracts. It also reveals the degree to which significant disruption of the brain networks connecting the anterior aspect of the corpus callosum, superior longitudinal fasciculus, anterior corona radiata, occipotofrontal fasciculus, arcuate fasciculus, uncinate fascicles, and the anterior commissure has occurred. From a brain network perspective, inferences can be made from Figs. 1, 2, and 3 that critical so-called “richclub” hub damage has occurred involving connections and networks involved in theory of mind (e.g., prefrontal cortex – CEN, DMN, MN networks; superior temporal sulcus – MN network, dorsolateral prefrontal cortex – CEN network; hippocampal formation – DMN network; orbitofrontal cortex – SE network). Without integrating this adolescent’s neuroimaging into the psychoeducational assessment process, it is easy for school psychologists and multidisciplinary team members to unintentionally, albeit understandably, underreport the full extent of the neurological sequelae of this adolescent’s TBI. That is, without the benefit of examining neuroimaging, it is easy to miss the full extent of the social-cognitive network damage. Although the school psychologist’s psychoeducational assessment report would include a summary of medical and neuropsychological information, and state that a penetrating head injury has led to a severe TBI with right focal frontal damage, this information would be limiting – unfortunately, right focal frontal damage does not necessarily imply that the social-cognitive network is

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Fig. 3. All images are in the anatomical view (right side of the image is the right side of the brain). The series of three smoothed diffusion axial images on the top left illustrate tracts color-coded as visualized at the base of the brain at the axial level at the midbrain (first image on left), at the level of the thalamus and III-ventricle (middle image) and at the level of the lateral ventricle (right). Using the color-coded tracts and comparing where the focal pathologies are in the MRI sequences on the right, when superimposed it is clearly evident that white matter tracks connecting rich hubs and networks of the brain have been damaged (compare to the illustration from van den Heuvel and Sporns, 2011, Fig. 3).

damaged. In addition, information provided in neuroradiology reports and medical discharge summaries does not make inferences about the effects of damaged areas of the brain on behavior, it merely describes the damage. By viewing neuroimaging, the extent of the structural damage and pathway disruption becomes quite evident, as does the fact that much of the psychological, psychoeducational, and neuropsychological testing falls short of assessing the extent of damage.

Although this adolescent’s psychoeducational assessment report would state that he had sustained a severe TBI, had mild to moderate deficits in executive functioning, and was taking stimulant medication for ADHD, without the benefit of integrating neuroimaging this information would fall short of providing sufficient neurorehabilitation information. By integrating neuroimaging into the psychoeducational evaluation of this adolescent, the ramifications of his injury are more

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concretely appreciated. That is, this is more than a case of TBI-induced ADHD and a lack of social skills, it is a developing brain that has been significantly compromised by a severe injury. In this case study, neuroimaging would help the school psychologist, and the school-based assessment team, appreciate the true extent of this adolescent’s injury and it would assist them in the appropriate planning of extensive, ongoing, real-world-based neurorehabilitation services and educational support. That is to say, in addition to developing neurorehabilitation efforts focusing on executive functioning (e.g., visual memory retrieval, visuomotor integration, and psychomotor speed) and ADHD (e.g., impulsivity, hyperactivity, inattention and disorganization), neurorehabilitation would also focus on social-cognitive deficits (e.g., social and interpersonal communication, interaction in the school and home environments, development of self-direction in life, and awareness of self-care, leisure, health and safety needs).This would in turn help reduce the potential long-term neurological, educational, and neuropsychiatric negative sequelae associated with his injury. That is, because of the extent of the frontal lobe damage and the disruption to social-cognitive brain networks, this adolescent would likely continue to have significant problems associated with impulse control, poor judgment, and impaired executive decisionmaking (ADHD) – all important neurological skills needed to function successfully in the real-world. He would also likely experience significant difficulty as a result of his poor ability to predict how others would act based on his own impaired ability to think about the mental states of himself and others, and then use that information to understand what others know (theory of mind). Therefore, he would have the potential for major psychiatric disorders, including depression, anxiety disorder, and substance abuse in his future. In addition, integrating neuroimaging would help the school psychologist and school-based assessment team realize they would need to plan for this adolescent’s ongoing neurorehabilitation post-high school; with this level of structural damage, this adolescent would have a reduced likelihood for educational achievement and attainment, as well as ability to sustain employability.

readily available with very sophisticated image presentation formats that show invaluable objective clinical information that can be integrated into the neurorehabilitation planning for children with ABI. School psychologists are well positioned within the schoolbased assessment process to obtain and integrate neuroimaging information when assessing children with ABI. If the school psychologist’s psychoeducational assessment of a child with ABI is to be optimally informative to the neurorehabilitation of children in educational settings, it not only must provide an accurate, objective characterization of cognitive and behavioral functioning, but it must also include all relevant information that may offer insight about potential change in function. Neuroimaging provides an objective piece of clinical history, which when integrated with a school psychologist’s psychoeducational assessment can, make a distinct difference in understanding ABI and its influence on educational and behavioral variables germane to neurorehabilitation in the schools. In the case of a child with a history of TBI, neuroimaging can provide the school psychologist with a level of understanding that is not fully appreciated by traditional approaches to school-based assessment. Unfortunately, school psychologists are not trained to regularly incorporate diagnostic neuroimaging into the typical psychoeducational assessment of a child with a TBI, even though neuroimaging is frequently done as part of a medical assessment and it is usually easily available upon request. Because school personnel place significant emphasis on the information contained within a TBI psychoeducational report, and because this report drives all subsequent neurorehabilitation decisions, it is imperative that the conclusions drawn from the contents of that report be correct. Integrating objective clinical neuroimaging results into the psychoeducational evaluation of a child with TBI is a means by which school psychologists can increase the usefulness of a psychoeducational report and improve neurorehabilitation decisions and outcomes. Since neuroimaging information is often readily available, especially in children with moderateto-severe TBI, its use in the psychoeducational process is recommended.

5. Summary

Declaration of interest

At the beginning of the 21st century not only is advanced neuroimaging available to neurorehabilitation specialists and school psychologists, it is becoming

Dr. Bigler co-directs a neuropsychological assessment laboratory and may be asked to render expert testimony concerning TBI. No other potential conflict

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