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

Abstract

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.

Rapid number naming in chronic concussion: eye movements in the King–Devick test

“…Evidence supporting this interpretation has been demonstrated in standard, non‐KD, reflexive saccade (single saccade to a suddenly appearing visual target) paradigms in subacute concussion36 and in chronic postconcussive states,15, 16, 37 in which saccadic velocities were found to be no different than in controls. In fact, normal saccadic velocities following concussion are not a surprising result, as diffuse axonal injury rarely extends to the brainstem in mild traumatic brain injury 38.…”

“…It is estimated that more than half of the brain's pathways are linked to vision and eye movement control11; many of these areas are susceptible to injury by concussion, particularly the frontal and temporal lobes 12, 13. In this regard, the presence of abnormal eye movements has been shown to indicate sub‐optimal brain function in postconcussive states 14, 15, 16, 17, 18…”

Sports-Related Concussion: The Eyes Have It

“…Accordingly, reliable and validated testing strategies are necessary to insure timely detection and removal from play for individuals suspected of concussion. Vision and visual motor problems are commonly reported among athletes following concussion [7][8][9][10][11][12][13][14][15]. This is to be expected as it is estimated that approximately 50% of the brain is devoted to vision and visual motor processing [16].…”

“…In 2009, Heitger and colleagues reported on impaired eye movements among individuals with post-concussion syndrome (PCS) following mild closed head injury (mCHI) [12]. This study compared 36 PCS subjects with 36 individually matched controls (mCHI patients with similar severity of injury but with resolution of signs and symptoms) as a function of reflexive, anti-and self-paced saccades, memory-guided sequences and smooth pursuits [12].…”

“…This study compared 36 PCS subjects with 36 individually matched controls (mCHI patients with similar severity of injury but with resolution of signs and symptoms) as a function of reflexive, anti-and self-paced saccades, memory-guided sequences and smooth pursuits [12]. They found worse performance on anti-saccades, self-paced saccades, memoryguided sequences and smooth pursuits [12]. Furthermore, compared with neuropsychological tests, eye movement abnormalities were more likely to be related to PCS cases with high symptom load [12].…”