Neuropsychological or neurocognitive tests provide information regarding the cognitive and emotional status of the concussed athlete. The development and availability of computerized testing platforms has allowed the application of baseline and follow-up testing models, and provide a more precise measurement of reaction time and processing speed. A combination of computerized assessment and a more expanded battery of tests may be a better approach to understanding the nature of the cognitive impact of sports concussion in youth athletes. This approach may be especially important for athletes with general risk factors and other potential modifiers or influencers on the cognitive performance data.
Neuropsychology is an applied science that is concerned with the behavioral expression of brain dysfunction. Although neurology and neurosurgery are focused primarily on the brain and its structural and nervous system integrity and functions, clinical neuropsychology focuses primarily on the mind, or how the brain interacts with the world. These cognitive, or neurocognitive, functions of the brain involve receptive and expressive functions, attention and concentration, and information processing, and the integrative functions of learning and memory and problem solving. Neurocognitive skills relate to how individuals track or select and acquire information, store and retrieve information, organize information for problem solving, and express or communicate. Emotions, and emotional functioning, have a bidirectional relationship with neurocognition, in that brain-based difficulties can cause emotional disturbance and emotional status can affect cognitive functioning.
Mild head injury or concussion is often characterized by cognitive symptoms in the form of attention or concentration problems, slowed processing, and/or memory difficulties. An individual may display minimal symptoms, and usually has a normal neurologic examination, but still has subtle changes in functioning; these differences from preinjury functioning may be observed by others and/or felt by the individual (“I don’t feel right” or “I don’t feel like myself”). In addition to the common physically based symptoms of sports concussions, such as headache, dizziness, balance problems, or sleep disturbance, subtle cognitive symptoms may be present, including reduced planning and ability to switch mental set, impaired memory and learning, reduced attention and ability to process information, and slowed reaction times and increased variability in response. The sports culture/context, and its influence on minimization of self-reported symptoms, created a need to evaluate cognitive functioning beyond the basic cognitive tests contained in a mental status examination or the reliance on self-reported cognitive functioning. Cognitive symptoms of concussion can persist beyond the resolution of major physical symptoms, and emotional symptoms from concussion can emerge as primary symptoms of head injury (eg, emotional lability or irritability) and/or reactive or secondary responses to symptoms or circumstances (eg, depression, discouragement or frustration with physical activity restriction, or interpersonal interaction changes). Increased risk of depression for those with mild traumatic brain injury has been found. This increased risk for depression extends to concussed athletes and has incorporated neuroimaging research; Chen and colleagues found that athletes with concussion with depressive symptoms showed neuroimaging patterns of activation and deactivation consistent with those found in clinical depression (ie, reduced activation in dorsolateral prefrontal cortex and striatum and attenuated deactivation in medial frontal and temporal regions).
Emergence of sports neuropsychology
The role of neuropsychology in a clinical setting can be to evaluate neurocognitive areas of functioning and relate the pattern of results to events (eg, traumatic brain injury), brain disease, and/or current level of functioning. These results can provide significant input to management and treatment of conditions. Neuropsychological assessments provide performance-based data (in contrast with self-report) that can document the level or degree of relative deficits and delineate areas of relative strength. Neuropsychology has played an important role in the understanding and evaluation of traumatic brain injury and its impact on adaptive functioning for many decades. The role of neuropsychology in mild traumatic brain injuries in sports, most often referred to as sports concussions, has created a growing field referred to as sports neuropsychology.
The application of neuropsychological approaches to sports concussions developed largely from the work of Barth and colleagues and the development of the Sports as a Laboratory Assessment Model (SLAM), which was oriented to using information from sports-related concussion to help inform the evaluation of mild head injury in the general population. In most clinical settings, clinical neuropsychological evaluations are in response to a brain trauma event and preinjury data are not available. Barth and colleagues used the sports environment and the opportunity to assess athletes before injury, thus creating the basis for the current approach to sports concussion that involves baseline testing and follow-up. The neuropsychological test batteries that have evolved from the early work of Barth and colleagues have been developed to evaluate areas of neurocognitive functioning most often affected by mild brain injury/concussion; these areas include attention/concentration; new learning; speeded problem solving, processing speed, and short-term memory; visual tracking; and balance testing, and these areas have been included in some evaluation approaches. Some neurocognitive test batteries add tests that assess areas that are not typically negatively affected by mild head injury and may serve as preinjury performance level estimates.
Comprehensive neuropsychological evaluations generally include a detailed clinical interview that not only explores the history of the present illness/injury but also history and background of the individual (social, educational, occupational, medical histories), review of available records, and neuropsychological testing to evaluate areas of cognitive functioning including intellectual functions, academic skills, attention and concentration, processing speed, learning, memory, psychomotor functions, and emotional functioning. This evaluation process provides an opportunity to observe individuals in their problem-solving efforts and make neurobehavioral observations. The neuropsychological report can describe the pattern and ranges of performance, and determine whether the pattern is consistent with the history of present illness and current symptoms. The neuropsychologist integrates the history, neurocognitive findings, medical data, and psychosocial-emotional factors and provides impressions regarding the individual’s current status, and may make recommendations for treatment planning.
In contrast with comprehensive clinical neuropsychological evaluations, sports concussion evaluations have generally focused on areas of functioning most often affected by concussion and are structured as neurocognitive screenings; having a preinjury or baseline performance level for comparison has emerged as the predominant paradigm. These evaluations are often administered sequentially (serial testing) to track neurocognitive status through the recovery phase; thus, alternate or multiple forms of tests are important to minimize the confounding of neurocognitive improvement and improvement caused by practice (or prior exposure) effects. Computerized neurocognitive testing for sports-related concussion solves the problem of alternate equivalent forms by generating multiple versions of subtests. However, although the content changes, the procedural practice effect (prior exposure to procedures and how the subtest works) remains.
Roles of Neuropsychological Evaluations in Sports Concussion
The roles of neuropsychological, or neurocognitive, evaluations in sports concussion have been seen in various ways, often seemingly dependent on the makeup of the expert group, as the sports concussion field has developed with time. The initial Concussion in Sports Group consensus statement promoted neuropsychological assessment as an important part of the evaluation of concussion protocol. This statement was followed by the second consensus statement, which described neuropsychological testing as being useful and important in the evaluation and management of complex concussions (which are contrasted with simple concussions, and relate to prolonged or slow recovery), and acknowledged the value of baseline and serial testing. The most recent consensus group statement recognized neuropsychological assessment as a useful tool in return-to-play decisions, and baseline testing, if possible, was again recommended. It was emphasized that neuropsychological assessment should not be seen as the “sole basis of management decisions, rather it should be seen as an aid to the clinical decision-making process in conjunction with a range of clinical domains and investigational results.” The essential aspect of this position regarding neuropsychological assessment is that it is but 1 data point among many that should be considered in concussion evaluation and management; this multidisciplinary approach, if possible, allows for the most comprehensive evaluation and management input for athletes as they recover.
The value of neuropsychological testing has been generally established in assessing or documenting cognitive problems emerging from sports-related concussion. Assessment strategies have varied from the traditional paper-and-pencil tests, to test batteries, to multiple options for computerized neurocognitive testing. Neurocognitive tasks are included in many of the brief sideline evaluations (eg, Standardized Assessment of Concussion [SAC ]), and assess orientation, auditory memory (immediate and delayed), concentration (digit span), and sequencing (months backward). These brief sideline evaluations provide a general view of functions and are not usually able to detect subtle changes in neurocognitive function emerging from concussion ; further, the sideline evaluators may not have a baseline performance level with which to compare an athlete’s postinjury performance level for memory or auditory attention tasks (eg, digit span). The sideline evaluation for concussion usually assesses symptoms and general responsiveness, postural stability and coordination, and the aforementioned brief cognitive functions, which usually provide current status information that informs clinical management decisions.
The use of neuropsychological testing for evaluation and management of sport-related concussion makes intuitive sense because it provides a measurement, or quantification, of cognitive function and emerges from a long history of application in brain injury evaluation. The inclusion of baseline testing in the testing protocol, as initially used by Barth and colleagues and now with other systems, provides each athlete with a nonconcussed comparison point. Evaluation of the changes in performance, and the pattern of changes for the different tests are the crucial analyses. Recognizing a decline as being significantly different (not occurring by chance or normal variability) and reliable measurement are the major challenges for the evaluator. The reliability, validity, sensitivity, and clinical usefulness of neuropsychological testing has been scrutinized and found by some to have not met criteria for clinical use. However, other research has provided some reliability and validity data that support neurocognitive testing ; the usage of reliable change indices is helpful in interpretation of the test data. Despite the ongoing need for more research regarding reliability and validity of measures with athlete populations, the use of neuropsychological or neurocognitive testing (within the baseline comparison protocol) has expanded and is a useful, important, and, in some contexts, a recommended or mandated aspect of concussion management.
Computer-Based Neurocognitive Testing
The development of computer-administered tests of cognitive functions grew out of the need to evaluate large numbers of athletes quickly and cost-efficiently; in contrast, traditional neuropsychological assessment requires more time and labor in terms of using a neuropsychologist. Computerized assessment also provides more exact measurement of reaction time and processing speed, both of which are important aspects in concussion-related performance changes. Lovell further suggested that the traditional approaches (noncomputer) limited the widespread use of neuropsychological assessment, especially at and below high school levels. Computer-based approaches have been used in youth athlete groups at all competitive ranges; however, hopes for expansion of involvement of neuropsychologists in sport settings have yet to be fulfilled. The various computerized neurocognitive assessment programs provide neurocognitive test data (scores or composite scores) that are subsequently interpreted for purposes of treatment planning and/or return-to-play decisions.
Although the administration of these computerized neurocognitive tests can be completed by an athletic trainer or someone trained in the administration and setup, it is the interpretation of the neurocognitive test data that has been variable. Echemendia and colleagues opine that, although baseline testing can be conducted by technicians with the supervision or guidance of a neuropsychologist, “post-injury assessment requires advanced neuropsychological expertise that is best provided by a clinical neuropsychologist.” They further suggest that interpretation responsibility may be seen in a medicolegal context and scope-of-practice issues can be raised. Despite the availability of hours of workshop training for nonneuropsychologists, the interpretation of computer-based neurocognitive tests is best completed by a trained, qualified neuropsychologist.
The complex factors that may affect neuropsychological test performance, specified by Collie and colleagues, include clinical (concussion/head injury, depression/anxiety/mood state, fatigue, use of drugs and alcohol, other medical or psychological conditions), methodological (testing situation, practice or learning effects, administrator expertise), test related (types of cognition assessed, availability of alternative forms, test reliability and/or repeatability, regression to the mean), statistical (metric properties, outcome variables such as reaction time and accuracy, statistical analysis used), and other (chance, random variability). It is the integration of these clinical and nonclinical factors with the individual test results that is the particular purview of neuropsychologists. Computerized programs that produce statistically determined results regarding return to baseline levels/ranges, or not returned to baseline, provide important information, but often provide an oversimplification of the complex system of cognitive functioning and the influence of other factors.
By virtue of their training and skill sets, neuropsychologists can provide “unique expertise in the assessment of cognitive functioning and post-injury neurocognitive and psychological assessment.” Moser and colleagues describe clinical neuropsychologists as uniquely qualified to translate test data into recommendations for clinical management; neuropsychological evaluation is recommended for use in the diagnosis, treatment, and management of sports-related concussion at all levels of play. Carr and Shunk detail training and qualifications of a sport neuropsychologist, suggesting that neuropsychologists should have additional training and specialization in the application of their clinical skills in the sports environment and with an athlete population. They emphasize the ethical responsibility of the psychologist to seek training to gain competency in this newly developing area.
The use of baseline testing has emerged as a crucial part of concussion management protocols, but the usefulness of this baseline model has been questioned ; psychometric and methodological issues are not at a level that justifies the implementation of a baseline testing system. Specifically, it is claimed that there are no studies showing that baseline testing reduces the duration of postconcussive symptoms, or the likelihood of repeat concussion, or the severity of symptoms or neurocognitive dysfunction after a second concussion, so the clinical use for return-to-play decisions is premature. Although these are important points regarding neurocognitive testing and its validity and sensitivity, the role for neurocognitive testing as one of many tools in clinical management and return-to-play decisions may not be fully appreciated. In addition to questions regarding the baseline model, some practitioners have believed that results from computerized testing do not add value beyond their own clinically informed decisions regarding return to play. Symptomatic athletes are generally not ready for return to play, regardless of their neurocognitive test results, so its added value for the return decision may be low; asymptomatic athletes (self-report) may or may not be ready for return to play and having some neurocognitive data describing their level of function (relative to a nonconcussed level) can be a helpful adjunct in return-to-play or management decisions. Poor, or below baseline, neurocognitive testing results, within the context of an asymptomatic report, at the least, will hopefully trigger additional consideration by the practitioner, especially if the athlete is also involved in school/academic activities. In some cases, the measurement, description, and tracking of the relative cognitive strengths and weaknesses and improvement for athletes during recovery can provide a helpful and adaptive perspective. Neurocognitive testing did show some degree of value-added benefits beyond self-report of symptoms, and may be helpful to the practitioner (especially with the involvement of a neuropsychologist) in detecting some of the subtle cognitive changes associated with concussion/mild traumatic brain injury that may not be within their specialty.
Randolph and others, in their discussions regarding baseline testing issues, suggest that baseline testing does not modify serious risks associated with sport-related concussion, noting that there “is no way that baseline testing could prevent a prolonged or atypical recovery, although in theory, baseline testing could help track recovery (presuming the tests were sufficiently reliable).” Although the evidence for baseline testing being able to modify risk or prevent serious outcomes in sports-related concussion is not available, the use of neuropsychological or neurocognitive testing to evaluate ongoing, prolonged, or atypical recovery is believed to be professionally prudent, with neuropsychologists being trained to integrate these data with the athlete’s history and potential risk factors.
Within a baseline neurocognitive testing and follow-up to concussion approach, the follow-up measures of functioning are of greatest use with a valid baseline comparison measure. Some athletes have been known to intentionally perform poorly on baseline to create a low comparison point to evaluate change on postconcussion follow-up; thus, any concussion-related cognitive decline may still be in their baseline range and suggest no cognitive residuals. Most athletes seem generally motivated to make a good effort at follow-up (which they perceive may help them be cleared to play), but some athletes have other issues or factors that affect their effort and performance. They may believe that they have to continue to display difficulties to support their injury, or they may be looking for an honorable or acceptable reason (eg, continuing to show ongoing symptoms) to discontinue participation, or other psychosocial factors may be involved. In some cases, youth athletes are able to access classroom or homework accommodations in school as long as they are experiencing concussion-related symptoms, which may relate to poor effort and performance on baseline or follow-up testing. Studies regarding baseline testing have revealed that psychological distress symptoms at the time of testing accounted for a significant amount of the baseline neurocognitive performance. This finding suggests the need for screening for psychological symptoms at baseline and follow-up concussion evaluations. Although it is intuitive to think of athletes being highly motivated individuals, their performances on neurocognitive testing can reflect variable effort; although they may display good effort on follow-up because it could affect return-to-play decisions, their baseline performances are often low and reflective of poor effort. Hunt and colleagues found that 11% of the high school athletes exerted poor effort and produced lowered or invalid neurocognitive performance on baseline testing, which could affect subsequent follow-up interpretation; the inclusion of an effort measure in a concussion assessment battery is recommended. For youth athletes, more frequent baseline testing is indicated, because the brain continues to develop and cognitively mature in adolescence. Some computer-based concussion programs recommend a new baseline yearly or every 2 years in youth athletes.
Although computerized baseline and follow-up neurocognitive testing has provided a response to the issues of the high number of athletes to be tested, relative cost and time, and alternate test forms, the computer-based approach has significant limitations regarding the information obtained. Specifically, the computer-based approach provides no information regarding auditory processing or verbal-auditory memory, because it is all visually presented; information regarding auditory processing or auditory attention can be particularly important for youth athletes and the impact on school or classroom performance and functioning. The computer-based evaluations provide data based on visual recognition memory, not recall memory; this is of note because recognition memory is more likely to be preserved in mild traumatic brain injury and recall memory more likely to be affected. Recognition memory tasks involve identifying stimuli from presented choices, recall memory tasks involve generating the stimuli from memory. In contrast with traditional face-to-face testing, computerized testing provides no neurobehavioral observational data regarding problem-solving efforts, distractibility, expressive or receptive language, motor skills, or emotional responses.
The hybrid model described by Echemendia involves the combination of computer and traditional face-to-face testing. In this way, the important reaction time data and general cognitive efficiency (speed vs accuracy) is used from the computerized testing, and the memory, problem-solving, and neurobehavioral observations can be used from the face-to-face testing. This hybrid approach may be particularly useful with athletes with certain risk factors, such as preexisting learning disabilities or attention-deficit/hyperactivity disorder, history of migraine headache, prior brain/head trauma, illnesses or diseases that may have compromised neurocognitive functioning, and psychiatric/psychological disorders. The expanded battery of neurocognitive tests may give the practitioner additional information to use in the description of the athlete’s current status and any return-to-play decision or treatment planning.
Pediatric and Adolescent Sport Concussion Management
Sport concussion issues specific to pediatric and adolescent athlete populations center on concussion management issues for these athletes being distinct from adult athletes and call for a more conservative approach. Children are believed to have increased susceptibility to concussion and potentially worse neuropsychological outcomes based on their neurodevelopmental status, including incomplete myelination of brain axons, greater head/body ratio, and thinner cranial bones. With the primary research emphasis being on college or professional athlete concussions and concussion management, Kirkwood and colleagues describe pediatric sport-related concussed athletes as “an oft-neglected population.” As the epidemiology of postconcussion symptoms is researched and described, youth sport concussion is becoming seen as a growing health concern. An 11-year prospective study of high school concussion incidence found that the rate increased across all 12 sports studied, with the concussion rate increasing 4.2-fold, reflecting a 15.5% annual increase.
Most practitioners dealing with sports-related concussion or mild traumatic brain injury acknowledge that having some form of neurocognitive or neuropsychological test data to supplement other medical, physiologic, or historical data is helpful in the clinical management of these athletes. Neurocognitive test data are generally not believed to be a stand-alone measure for return-to-play decisions, but are among several data points to be considered. Similarly, patient self-report of the absence of postconcussion symptoms or a normal balance performance should not solely be relied on to determine return-to-play status. In many concussion management programs, a multidisciplinary or interdisciplinary team approach is used. Uniquely, neuropsychologists can provide the team, program, or physician managing youth concussions with (1) age-normed data regarding neurocognitive functioning, (2) recommendations regarding potentially important issues related to academic functioning, and (3) assessment of social-emotional functioning or psychosocial issues that have affected functioning levels. In addition, neuropsychologists can interface, if needed, with parents and school regarding ongoing concussion issues. The neuropsychological evaluation integrates the physical, cognitive, and emotional aspects of sports-related concussions, and considers alternative explanations and factors symptoms persist.