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Comparison of athletes with concussion and healthy athletes on optokinetic and reaction time parameters
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Oculomotor tests in concussion commonly show impairment in smooth pursuit and saccadic function. Honing in on the systems likely to be affected by concussion will streamline use of oculomotor function as a supplemental diagnostic and prognostic tool, as well as improve our understanding of the pathophysiology of concussion.
Purpose:...
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Mild traumatic brain injury (mTBI), or concussion, occurs following a direct or indirect force to the head that causes a change in brain function. Many neurological signs and symptoms of mTBI can be subtle and transient, and some can persist beyond the usual recovery timeframe, such as balance, cognitive or sensory disturbance that may pre-dispose...
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... Concussed individuals often complain of oculomotor symptoms, including blurred vision, convergence insufficiency, difficulty reading, diplopia, headaches, difficulty tracking a moving target, general asthenopia (eye strain), dizziness, nausea, and problems scanning visual information [3,4] which can be explained by the fact that concussion may disrupt the underlying neurophysiology of oculomotor functions [5]. In particular, mTBI may be a leading cause of clinically impaired smooth pursuit and saccadic eye movements [6]. ...
Eye-tracking techniques have gained widespread application in various fields including research on the visual system, neurosciences, psychology, and human-computer interaction, with emerging clinical implications. In this preliminary phase of our study, we introduce a pilot test of innovative virtual reality technology designed for tracking head and eye movements among healthy individuals. This tool was developed to assess the presence of mild traumatic brain injury (mTBI), given the frequent association of oculomotor function deficits with such injuries. Alongside eye-tracking, we also integrated fMRI due to the complementary nature of these techniques, offering insights into both neural activation patterns and behavioural responses, thereby providing a comprehensive understanding of oculomotor function. We used fMRI with tasks evaluating oculomotor functions: Smooth Pursuit (SP), Saccades, Anti-Saccades, and Optokinetic Nystagmus (OKN). Prior to the scanning, the testing with a system of VR goggles with integrated eye and head tracking was used where subjects performed the same tasks as those used in fMRI. 31 healthy adult controls (HCs) were tested with the purpose of identifying brain regions associated with these tasks and collecting preliminary norms for later comparison with concussed subjects. HCs’ fMRI results showed following peak activation regions: SP–cuneus, superior parietal lobule, paracentral lobule, inferior parietal lobule (IPL), cerebellartonsil (CT); Saccades–middle frontal gyrus (MFG), postcentral gyrus, medial frontal gyrus; Anti-saccades—precuneus, IPL, MFG; OKN—middle temporal gyrus, ACC, postcentral gyrus, MFG, CT. These results demonstrated brain regions associated with the performance on oculomotor tasks in healthy controls and most of the highlighted areas are corresponding with those affected in concussion. This suggests that the involvement of brain areas susceptible to mTBI in implementing oculomotor evaluation, taken together with commonly reported oculomotor difficulties post-concussion, may lead to finding objective biomarkers using eye-tracking tasks.
... When evaluated at the group level, recent studies have shown that measurements of both saccades and smooth pursuits can differentiate between subjects with mTBI and age-matched controls [62]. One study, including 28 college athletes within 72 h of diagnosed concussion and 87 healthy control athletes, found that concussion was associated with significantly increased saccadic latency and reduced saccadic accuracy when measured with VOG [63]. This study also observed that vertical smooth pursuit was more abnormal than horizontal movement in concussed individuals. ...
... One specific subtype of nystagmoid eye movement that has been investigated for its association with concussion is prolonged optokinetic after-nystagmus (OKAN) [63,66,73]. Optokinetic nystagmus (OKN) is a physiologically normal reflexive eye movement driven by rotating motion in the visual field [69]. ...
Mitigating the substantial public health impact of concussion is a particularly difficult challenge. This is partly because concussion is a highly prevalent condition, and diagnosis is predominantly symptom-based. Much of contemporary concussion management relies on symptom interpretation and accurate reporting by patients. These types of reports may be influenced by a variety of factors for each individual, such as preexisting mental health conditions, headache disorders, and sleep conditions, among other factors. This can all be contributory to non-specific and potentially misleading clinical manifestations in the aftermath of a concussion. This review aimed to conduct an examination of the existing literature on emerging approaches for objectively evaluating potential concussion, as well as to highlight current gaps in understanding where further research is necessary. Objective assessments of visual and ocular motor concussion symptoms, specialized imaging techniques, and tissue-based concentrations of specific biomarkers have all shown promise for specifically characterizing diffuse brain injuries, and will be important to the future of concussion diagnosis and management. The consolidation of these approaches into a comprehensive examination progression will be the next horizon for increased precision in concussion diagnosis and treatment.
... Manual Reaction Time (MRT) protocols are widely used to study interactions between perceptual, cognitive, emotional, and motor functions (Cardoso et al., 2021;Green et al., 2020;Mahon et al., 2018;Portugal et al., 2020). Some of these protocols have also been applied in the sporting context exploring different perspectives, to study cognitive specialization (Bhattacharya et al., 2022;Giglia et al., 2011;Janicijevic & Garcia-Ramos, 2022;Kasper et al., 2012), executive functions in high-performance athletes (Causer et al., 2011;Ervilha et al., 2020;Yongtawee et al., 2022), to evaluate cognitive changes related to exercise effects (Silveira et al., 2021), concussions (Cochrane et al., 2019), and other applications (Conde et al., 2018;Shahmoradi et al., 2022). ...
Manual Reaction Time measures have been widely used to study interactions between perceptual, cognitive, and motor functions. The Stimulus–Response Compatibility is a phenomenon characterized through faster Manual Reaction Times when stimuli and response locations coincide (correspondent condition) than when they are on different sides (noncorrespondent condition). The present study adapted a protocol to study if the Stimulus–Response Compatibility effect can be detected during a virtual combat simulation. Twenty-seven participants were instructed to defend themselves by clicking a key in order to block the presented punch. Videos of two fighters were used, granting two types of basic strokes: the back fist , a punch performed with the dorsal part of the fighter’s hand, starting at the opposite side to which it is directed; and the hook punch, performed with a clenched fist starting and finishing ipsilaterally. The Manual Reaction Times were different between the correspondent and noncorrespondent conditions, F (1, 26) = 9.925; p < .004; η ² = .276, with an Stimulus–Response Compatibility effect of 72 ms. Errors were also different, F (1, 26) = 23.199; p < .001; η ² = .472, between the correspondent (13%) and the noncorrespondent conditions (23%). The study concluded that spatial codes presented at the beginning of the punch movement perception substantially influenced the response execution.
... The disparity in findings may in part be explained by differences in time since onset of injury, injury severity, and definitions of abnormality which often differ between studies. Recently, Cochrane et al. (45) observed increased saccadic latency and decreased accuracy in athletes who suffered concussions compared to non-concussed athletes, but there was no group difference in horizontal smooth pursuit. Convergence insufficiency has been associated with blast-related TBI [e.g., (46)]; however, versional eye movement was not assessed in the current study. ...
The purpose of this study was to examine vestibular and balance function in individuals with chronic dizziness associated with mTBI/blast. A prospective case-control study design was used to examine ocular motor, vestibular function, and postural stability in veterans with symptoms of dizziness and/or imbalance following an mTBI or blast exposure (n = 77) and a healthy control group (n = 32). Significant group differences were observed for saccadic accuracy, VOR gain during slow harmonic acceleration at 0.01 Hz, cervical vestibular evoked myogenic potentials asymmetry ratio, composite equilibrium score on the sensory organization test, total Dynamic Gait Index score, and gait. The frequency of test abnormalities in participants with mTBI/blast ranged from 0 to 70% across vestibular, ocular motor, and balance/gait testing, with the most frequent abnormalities occurring on tests of balance and gait function. Seventy-two percent of the mTBI/blast participants had abnormal findings on one or more of the balance and gait tests. Vestibular test abnormalities occurred in ~34% of the individuals with chronic dizziness and mTBI/blast, and abnormalities occurred more frequently for measures of otolith organ function (25% for cVEMP and 18% for oVEMP) than for measures of hSCC function (8% for SHA and 6% for caloric test). Abnormal ocular motor function occurred in 18% of the mTBI/blast group. These findings support the need for comprehensive vestibular and balance assessment in individuals with dizziness following mTBI/blast-related injury.
... There are limited studies examining female populations in mTBI and nearly all studies evaluating ocular motor measures with cohorts inclusive of females did not perform a subgroup analysis or compare results between genders (Balaban et al., 2016;Cochrane et al., 2019;DiCesare et al., 2017;Heitger et al., 2004Heitger et al., , 2006Heitger et al., , 2007Heitger et al., , 2008Heitger et al., , 2009Howell et al., 2018;Kelly et al., 2019;Maruta et al., 2013;Maruta et al., 2017;Maruta, Palacios, et al., 2016;Maruta et al., 2018;Murray et al., 2014;Webb et al., 2018;Wetzel et al., 2018). This is an important consideration, as mTBI incidence is greater in females for gender-comparable sports (Covassin et al., 2016;Dick, 2009;Gessel et al., 2007;Lincoln et al., 2011;Marar et al., 2012). ...
Mild traumatic brain injury (mTBI), commonly known as concussion, is a complex neurobehavioral phenomenon affecting six in 1000 people globally each year. Symptoms last between days and years as microstructural damage to axons and neurometabolic changes result in brain network disruption. There is no clinically available objective biomarker to diagnose the severity of injury or monitor recovery. However, emerging evidence suggests eye movement dysfunction (e.g., saccades and smooth pursuits) in patients with mTBI. Patients with a higher symptom burden and prolonged recovery time following injury may show higher degrees of eye movement dysfunction. Likewise, recent advances in magnetic resonance imaging (MRI) have revealed both white matter tract damage and functional network alterations in mTBI patients, which involve areas responsible for the ocular motor control. This scoping review is presented in three sections: Section 1 explores the anatomical control of eye movements to aid the reader with interpreting the discussion in subsequent sections. Section 2 examines the relationship between abnormal MRI findings and eye tracking after mTBI based on the available evidence. Finally, Section 3 communicates gaps in our knowledge about MRI and eye tracking, which should be addressed in order to substantiate this emerging field. This review aims to scientifically resolve the correlation between eye movement dysfunction in mTBI with advanced neuroimaging. Included are the neuroanatomical basis of eye movement control, novel MRI correlations to eye tracking measures in mTBI patients, and areas requiring future research.
... Oculomotor assessment following TBI generally includes an evaluation of smooth pursuit eye movements and fixation, vergence and accommodation and saccades [154]. Poorer oculomotor function is correlated with more symptoms post-TBI and difficulties with everyday activities [155,156]. ...
Traumatic Brain Injury (TBI) is a major global public health problem. Neurological damage from TBI may be mild, moderate, or severe and occurs both immediately at the time of impact (primary injury) and continues to evolve afterwards (secondary injury). In mild (m)TBI, common symptoms are headaches, dizziness and fatigue. Visual impairment is especially prevalent. Insomnia, attentional deficits and memory problems often occur. Neuroimaging methods for the management of TBI include computed tomography and magnetic resonance imaging. The location and the extent of injuries determine the motor and/or sensory deficits that result. Parietal lobe damage can lead to deficits in sensorimotor function, memory, and attention span. The processing of visual information may be disrupted, with consequences such as poor hand-eye coordination and balance. TBI may cause lesions in the occipital or parietal lobe that leave the TBI patient with incomplete homonymous hemianopia. Overall, TBI can interfere with everyday life by compromising the ability to work, sleep, drive, read, communicate and perform numerous activities previously taken for granted. Treatment and rehabilitation options available to TBI sufferers are inadequate and there is a pressing need for new ways to help these patients to optimize their functioning and maintain productivity and participation in life activities, family and community.
... 2,3 Similarly, deficiencies in saccadic eye movements, vestibulo-ocular reflex (VOR), and visual motion sensitivity (VMS) are all associated with concussion. [4][5][6][7] It is also well-established that light sensitivity can be enhanced after concussion 8 and thus is a standard question on concussion symptom inventories. [9][10][11] Visually evoked effects offer an intriguing avenue for concussion assessment-including evaluations that extend beyond effects localized to the eye. ...
Increased sensitivity to light is common following concussion. Viewing a flickering light can also produce uncomfortable somatic sensations like nausea or headache. Here we examined effects evoked by viewing a patterned, flickering screen in a cohort of 81 uninjured youth athletes and 84 concussed youth. We used Multiple correspondence analysis and identified two primary dimensions of variation: the presence or absence of visually evoked effects, and variation in the tendency to manifest effects that localized to the eyes (e.g., eye watering), versus more generalized neurologic effects (e.g., headache). Based on these two primary dimensions, we grouped participants into three categories of evoked symptomatology: no effects, eye-predominant effects, and brain-predominant effects. A similar proportion of participants reported eye-predominant effects in the uninjured (33.3%) and concussed (32.1%) groups. By contrast, participants who experienced brain-predominant effects were almost entirely from the concussed group (1.2% of uninjured, 35.7% of concussed). The presence of brain-predominant effects was associated with a higher concussion symptom burden and reduced performance on visio-vestibular tasks. Our findings indicate that the experience of negative constitutional, somatic sensations in response to a dynamic visual stimulus is a salient marker of concussion and is indicative of more severe concussion symptomatology. We speculate that differences in visually evoked effects reflect varying levels of activation of the trigeminal nociceptive system.
... Vision and oculomotor assessment using eye-tracking devices, saccadometers, and electrooculography are also used to assess mTBI and concussion [93][94][95][96][97][98][99] . This method correlates with concussion symptoms in children and adults and has promising utility as a rapid, objective, and non-invasive aid for diagnosis. ...
Multi-modal biomarkers (e.g., imaging, blood-based, physiological) of unique traumatic brain injury (TBI) endophenotypes are necessary to guide the development of personalized and targeted therapies for TBI. Optimal biomarkers will be specific, sensitive, rapidly and easily accessed, minimally invasive, cost effective, and bidirectionally translatable for clinical and research use. For both uses, understanding how TBI biomarkers change over time is critical to reliably identify appropriate time windows for an intervention as the injury evolves. Biomarkers that enable researchers and clinicians to identify cellular injury and monitor clinical improvement, inflection, arrest, or deterioration in a patient's clinical trajectory are needed for precision healthcare. Prognostic biomarkers that reliably predict outcomes and recovery windows to assess neurodegenerative change and guide decisions for return to play or duty are also important. TBI biomarkers that fill these needs will transform clinical practice and could reduce the patient's risk for long-term symptoms and lasting deficits. This article summarizes biomarkers currently under investigation and outlines necessary steps to achieve short- and long-term goals, including how biomarkers can advance TBI treatment and improve care for patients with TBI.
... As an example, dynamic pupillary responses are increased in children following concussion, and have been proposed as an objective biomarker 2,3 . Similarly, deficiencies in saccadic eye movements, vestibulo-ocular reflex (VOR), and visual motion sensitivity (VMS) are all associated with concussion [4][5][6][7] . ...
Increased sensitivity to light is common following concussion. Viewing a flickering light can also produce uncomfortable somatic sensations like nausea or headache. Here we examined effects evoked by viewing a patterned, flickering screen in a cohort of 81 uninjured youth athletes and 84 youth with concussion. We used exploratory factor analysis and identified two primary dimensions of variation: the presence or absence of visually evoked effects, and variation in the tendency to manifest effects that localized to the eyes (e.g., eye watering), versus more generalized neurologic symptoms (e.g., headache). Based on these two primary dimensions, we grouped participants into three categories of evoked symptomatology: no effects, eye-predominant effects, and brain-predominant effects. A similar proportion of participants reported eye-predominant effects in the uninjured (33.3%) and concussion (32.1%) groups. By contrast, participants who experienced brain-predominant effects were almost entirely from the concussion group (1.2% of uninjured, 35.7% of concussed). The presence of brain-predominant effects was associated with a higher concussion symptom burden and reduced performance on visio-vestibular tasks. Our findings indicate that the experience of negative constitutional, somatic sensations in response to a dynamic visual stimulus is a salient marker of concussion and is indicative of more severe concussion symptomatology. We speculate that differences in visually evoked effects reflect varying levels of activation of the trigeminal nociceptive system.
... Most studies of saccades in concussions show that simple visually guided saccades are unaffected (i.e., not slowed), thus indicating that the immediate premotor structures in the brainstem that drive saccades are typically unaffected in acute concussion and chronic symptomatic states after concussion [40][41][42][43][44][45][46]. The exception to simple visually guided saccades being unaffected is the finding of in-creased saccadic latency (time between visual stimulus presentation and initiation of a saccade) for visually guided saccades in hyper-acute concussion, a finding which quickly resolves [47,48]. In keeping with studies largely showing normal visually guided saccades, saccade speeds have been shown to be normal during KD testing post-concussion, as well [26]. ...
(1) Background: The King-Devick (KD) rapid number naming test is sensitive for concussion diagnosis, with increased test time from baseline as the outcome measure. Eye tracking during KD performance in concussed individuals shows an association between inter-saccadic interval (ISI) (the time between saccades) prolongation and prolonged testing time. This pilot study retrospectively assesses the relation between ISI prolongation during KD testing and cognitive performance in persistently-symptomatic individuals post-concussion. (2) Results: Fourteen participants (median age 34 years; 6 women) with prior neuropsychological assessment and KD testing with eye tracking were included. KD test times (72.6 ± 20.7 s) and median ISI (379.1 ± 199.1 msec) were prolonged compared to published normative values. Greater ISI prolongation was associated with lower scores for processing speed (WAIS-IV Coding, r = 0.72, p = 0.0017), attention/working memory (Trails Making A, r = −0.65, p = 0.006) (Digit Span Forward, r = 0.57, p = −0.017) (Digit Span Backward, r= −0.55, p = 0.021) (Digit Span Total, r = −0.74, p = 0.001), and executive function (Stroop Color Word Interference, r = −0.8, p = 0.0003). (3) Conclusions: This pilot study provides preliminary evidence suggesting that cognitive dysfunction may be associated with prolonged ISI and KD test times in concussion.
