Marcus Heitger

Impaired eye movements in post-concussion syndrome indicate suboptimal brain function beyond the influence of depression, malingering or intellectual ability

Post-concussion syndrome (PCS) can affect up to 20%-30% of patients with mild closed head injury (mCHI), comprising incomplete recovery and debilitating persistence of post-concussional symptoms. Eye movements relate closely to the functional integrity of the injured brain and eye movement function is impaired post-acutely in mCHI. Here, we examined whether PCS patients continue to show disparities in eye movement function at 3-5 months following mCHI compared with patients with good recovery. We hypothesized that eye movements might provide sensitive and objective functional markers of ongoing cerebral impairment in PCS. We compared 36 PCS participants (adapted World Health Organization guidelines) and 36 individually matched controls (i.e. mCHI patients of similar injury severity but good recovery) on reflexive, anti- and self-paced saccades, memory-guided sequences and smooth pursuit. All completed neuropsychological testing and health status questionnaires. Mean time post-injury was 140 days in the PCS group and 163 days in the control group. The PCS group performed worse on anti-saccades, self-paced saccades, memory-guided sequences and smooth pursuit, suggesting problems in response inhibition, short-term spatial memory, motor-sequence programming, visuospatial processing and visual attention. This poorer oculomotor performance included several measures beyond conscious control, indicating that subcortical functionality in the PCS group was poorer than expected after mCHI. The PCS group had poorer neuropsychological function (memory, complex attention and executive function). Analysis of covariance showed oculomotor differences to be practically unaffected by group disparities in depression and estimated intellectual ability. Compared with neuropsychological tests, eye movements were more likely to be markedly impaired in PCS cases with high symptom load. Poorer eye movement function, and particularly poorer subcortical oculomotor function, correlated more with post-concussive symptom load and problems on activities of daily living whilst poorer neuropsychological function exhibited slightly better correlations with measures of mental health. Our findings that eye movement function in PCS does not follow the normal recovery path of eye movements after mCHI are indicative of ongoing cerebral impairment. Whilst oculomotor and neuropsychological tests partially overlapped in identifying impairment, eye movements showed additional dysfunction in motor/visuospatial areas, response inhibition, visual attention and subcortical function. Poorer subconscious oculomotor function in the PCS group supports the notion that PCS is not merely a psychological entity, but also has a biological substrate. Measurement of oculomotor function may be of value in PCS cases with a high symptom load but an otherwise unremarkable assessment profile. Routine oculomotor testing should be feasible in centres with existing access to this technology.

Motor deficits and recovery during the first year following mild closed head injury

Objective: This study examined motor impairments over 1 year following mild closed head injury (CHI). It is the first study to serially assess long-term oculomotor and upper-limb visuomotor function following mild head trauma. Methods: Thirty-seven patients with mild CHI and 37 matched controls were compared at 1 week, 3 months and 6 months and 31 available pairs at 12 months post-injury on measures of saccades, oculomotor smooth pursuit, upper-limb visuomotor function and neuropsychological performance. Symptomatic recovery was sampled using the Rivermead Postconcussion Symptoms Questionnaire. Results: At 1 week, the group with CHI reported high levels of post-concussional symptoms and exhibited prolonged saccade latencies, increased directional errors, decreased saccade accuracy and impaired fast sinusoidal smooth pursuit concomitant with increased arm movement reaction time, decreased arm movement speed and decreased motor accuracy on upper-limb visuomotor tracking tasks. Neuropsychological testing identified deficits only in verbal learning and speed of processing while attention, short-term/working memory and general cognitive performance were preserved. At 3 and 6 months, the group with CHI continued to show deficits on several oculomotor and upper-limb visuomotor measures in combination with some deficits on verbal learning and improved, yet abnormal, levels of post-concussional symptoms. At 12 months, the group with CHI had no cognitive impairment but residual deficits in eye and arm motor function and continued to show elevated levels of post-concussional symptoms. Conclusions: The findings indicate that multiple motor systems are measurably impaired up to 12 months following mild CHI and that instrumented motor assessment may provide sensitive and objective markers of cerebral dysfunction during recovery from mild head trauma independent of neuropsychological assessment and patient self-report.

Concussion and mild head injury

A concussion is a physical injury to the head resulting in altered mental function, with expectation of recovery within 2–3 weeks. In a significant minority of cases the symptoms persist longer, thereby comprising a symptom complex commonly referred to as the “post concussion syndrome”, that is, one or more somatic (for example, headaches, dizziness), cognitive (for example, poor concentration, memory), or behavioural/affective (for example, irritability, mood swings) symptoms. Unfortunately, the referral of a patient with the possibility of post concussion syndrome to a busy neurology outpatient clinic can precipitate an inward sigh of reluctant resignation in even the most diligent neurologist or neurosurgeon. We know we are in for a potentially lengthy consultation—long on symptoms and short on signs. Moreover, the process can be convoluted and meandering, as unrewarding for the patient as it is unsatisfying for the clinician. It is important to acknowledge at the outset that there is a dearth of evidence-based knowledge of the underlying pathogenesis, and even less of the best management of post concussive symptoms. Thus, much of the information and advice in this article is empirical and based on expert and personal experience. The terminology surrounding trauma to the head confuses patients, doctors, and lay commentators alike. Terms such as concussion, mild head injury, mild TBI (traumatic brain injury), cerebral concussion, and post concussion syndrome are often used interchangeably to describe the physical injury itself as well as its immediate and later symptomatic consequences. There is in fact no commonly agreed definition of concussion, or whether it even differs from the term mild TBI. Our own working definition is that concussion is an acute trauma-induced change of mental function which generally lasts less than 24 hours (with or without preceding loss of consciousness) and associated with other symptoms (such as headaches and dizziness) which …

Mild traumatic brain injury and fatigue: A prospective longitudinal study

Primary objective: To examine fatigue prevalence, severity, predictors and co-variates over 6 months post-mild traumatic brain injury (MTBI). Research design: Longitudinal prospective study including 263 adults with MTBI. Procedures: Participants completed the Fatigue Severity Scale (FSS), Rivermead Post-concussion Symptoms Questionnaire (RPSQ), Hospital Anxiety and Depression Scale (HADS) and the Short Form 36 Health Survey-Version 2 (SF-36v2). Complete data were available for 159 participants. Key measures; prevalence—RPSQ Item 6: severity—FSS. The effect of time on fatigue prevalence and severity was examined using ANOVA. Multiple regression analysis identified statistically significant covariates. Main outcomes and results: Post-MTBI fatigue prevalence was 68%, 38% and 34% at 1 week, 3 and 6 months, respectively. There was a strong effect for time over the first 3 months and moderate-to-high correlations between fatigue prevalence and severity. Early fatigue strongly predicted later fatigue; depression, but not anxiety was a predictor. Fatigue was seen as laziness by family or friends in 30% of cases. Conclusions: Post-MTBI fatigue is a persistent post-concussion symptom, exacerbated by depression but not anxiety. It diminishes in the first 3 months and then becomes relatively stable, suggesting the optimum intervention placement is at 3 months or more post-MTBI.

A new approach to predicting postconcussion syndrome after mild traumatic brain injury based upon eye movement function

Following on from our earlier findings of a close relationship between motor function and outcome after mild traumatic brain injury (mTBI), this study examined whether it might be possible to predict poor recovery in the form of postconcussion syndrome (PCS) based upon early eye and arm motor function. Within 1 week post-injury, we assessed 37 mTBI patients on measures of saccades, oculomotor smooth pursuit, upper-limb visuomotor function, neuropsychological status, and self-reported health condition. At 3 months, 8 patients met the criteria for PCS. Using discriminant function analyses, we examined whether this future PCS-group could be identified prospectively based on motor function, neuropsychological status, and self-reported health condition at 1 week post-injury. Early eye movement function was the most effective in distinguishing between PCS and non-PCS patients, achieving a sensitivity and specificity of 100% in the present sample. This was followed by self-reported early health condition (sensitivity: 87%, specificity: 97%), early upper-limb motor performance (87%, 97%), neuropsychological function (62%, 100%), and age, gender, education and clinical measures of trauma severity (37%, 87%). Leave-one-out validation analyses confirmed eye movements as the most robust discriminator (sensitivity: 62%, specificity: 97%). Assessment of eye movement function after mTBI may contribute to a prospective identification of patients who develop PCS, supporting the targeting of early health-care intervention.

Saccade sequences as markers for cerebral dysfunction following mild closed head injury

Diffuse axonal injury caused by mild closed head injury (CHI) is likely to affect the neural networks concerned with the planning and execution of sequences of memory-guided saccades. Thirty subjects with mild CHI and thirty controls were tested on 2- and 3-step sequences of memory-guided saccades. CHI subjects showed more directional errors, larger position errors, and hypermetria of primary saccades and final eye position. No deficits were seen in temporal accuracy (timing and rhythm). These results suggest that computerized tests of saccade sequences can provide sensitive markers of cerebral dysfunction after mild CHI.

RECOVERY IN THE FIRST YEAR AFTER MILD HEAD INJURY: DIVERGENCE OF SYMPTOM STATUS AND SELF-PERCEIVED QUALITY OF LIFE

OBJECTIVE To examine self-perceived health status during the first year following mild closed head injury. METHODS At 1 week, and at 3, 6 and 12 months post-injury, 37 patients with mild closed head injury completed written versions of the Rivermead Post-Concussion Symptoms Questionnaire (RPSQ), the Rivermead Head-Injury Follow-up Questionnaire (RHIFQ) and the SF-36 Health Survey. Thirty-seven controls provided baselines for the SF-36 and the RPSQ. RESULTS The 3 questionnaires conveyed differing impressions of recovery. On the RPSQ, the patients exhibited ongoing symptomatic complaints and higher scores compared with controls. The RHIFQ conveyed a better recovery in terms of everyday function. The SF-36 showed the best recovery, with the mild closed head injury group achieving normal scores at 3, 6 and 12 months. Regression analyses indicated an influence of IQ, but not of age, education, or clinical measures of injury severity, on long-term health status. CONCLUSION Recovery after mild closed head injury can involve a dichotomy of persistent post-concussional symptoms but relatively normal functionality and quality of life. In addition to indicating an influence of IQ on perception of recovery in mild closed head injury, our findings demonstrate that the nature of self-report questionnaires considerably influences the picture of recovery. This emphasizes the importance of methods unaffected by IQ and self-evaluative accuracy in the assessment of mild closed head injury.

Mild head injury—a close relationship between motor function at 1 week post-injury and overall recovery at 3 and 6 months

Based on previous findings of impaired eye and arm motor control after mild closed head injury (CHI), this study examined whether early eye and arm motor function, and the level of post-injury cerebral dysfunction manifested in motor control, relates systematically to recovery at 3 and 6 months after mild CHI. At 1 week post-injury, we assessed oculomotor function, upper-limb visuomotor performance, and cognitive status in 37 mild CHI patients. Re-examination at 3 and 6 months determined outcome in terms of postconcussional symptoms and performance of everyday tasks, as assessed by the Rivermead Postconcussion Symptoms Questionnaire, the Rivermead Head Injury Follow-up Questionnaire and the SF-36 Health Survey. We then examined the association of early motor function, cognitive status and self-reported health condition with outcome using linear regression. Motor-based regression models explained a high proportion of the variance in outcome (70-89%), with motor function at 1 week being more closely related to outcome at 3 and 6 months than early psychometric assessment (13-32%) or self-reported health status (54-79%). These motor-based models incorporated subcortical/subconscious motor functions alongside motor functions that are subject to volitional control and are primarily mediated by frontal, parietal and temporal cortical brain regions. Early assessment of eye and arm motor function may help in improving accuracy of outcome prediction after mild CHI. Such assessment may assist in the better targeting of early health care intervention and help decrease head-trauma-related morbidity and rehabilitation costs.

The impact of mild closed head injury on involuntary saccadic adaptation: Evidence for the preservation of implicit motor learning

Objective: Mild closed head injury (CHI) can impair performance on volitional saccades (fast eye movements), with poorer saccade accuracy being one of the principal deficits. Assessing a patient group with known deficits of volitional saccades, the authors investigated whether mild CHI similarly impairs the implicit adaptation of visually-guided (reflexive) saccades, an important process which maintains saccadic accuracy. Methods: Within 2 weeks following mild CHI, 30 patients and 30 matched controls were compared on a computerized paradigm, which artificially induced saccadic adaptation. In response to an initial stimulus, subjects made a saccade during which the stimulus was displaced centripetally causing the initial (primary) saccade to be inaccurate. While these intra-saccadic changes remained unnoticed by the subjects, the displacements gradually caused adaptive saccadic hypometria. Results: No differences in adaptation were found between the CHI group and the controls (F(1, 29) = 0.51, p = 0.48). This finding indicates that mild CHI does not impair implicit reflexive saccade adaptation and suggests that cerebellar function and functions of deeper brain structures such as the thalamus, superior colliculus and the basal ganglia may be largely preserved following mild CHI. The current results support the notion that the profile of oculomotor function after mild CHI reflects a centripetal gradient of impairment and relates closely to the functional integrity of the injured brain.

Measurement of eye and arm movement deficits following mild closed head injury

Diffuse axonal injury caused by mild closed head injury (CHI) is likely to damage the extensive neural networks concerned with oculomotor and visuomotor control. We hypothesized that infrared oculography and computerized tests of visuomotor function would be able to measure the resulting motor deficits. We compared 37 patients with mainly mild closed head injury (CHI, 36 mild and 1 moderate) and 37 controls (matched for age, gender, years of education) at 1 week, 3 months and 6 months post injury on measures of saccades, oculomotor smooth pursuit, and upper-limb visuomotor function. At 1 week, the CHI group demonstrated prolonged saccade latencies, increased directional errors and decreased saccade accuracy in combination with increased arm movement reaction time, decreased arm movement speed, and decreased motor accuracy in the visuomotor tests. Fast oculomotor smooth pursuit was mildly impaired. At 3 months, several oculomotor and visuomotor deficits remained. At 6 months, no deficits were found on any of the motor tests. Our results show that multiple motor systems can be impaired up to several months following mild CHI. These findings indicate that quantitative tests of oculomotor and upper-limb visuomotor function can provide sensitive markers of neurophysiological dysfunction and supports the possible use of such tests to supplement patient assessment following non-severe CHI.