Brain Advance Access originally published online on July 16, 2009
Brain 2009 132(10):2850-2870; doi:10.1093/brain/awp181
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Impaired eye movements in post-concussion syndrome indicate suboptimal brain function beyond the influence of depression, malingering or intellectual ability
1 Department of Medicine, University of Otago, Christchurch, New Zealand 2 Van der Veer Institute for Parkinson's and Brain Research, Christchurch 8011, New Zealand 3 Department of Medical Physics & Bioengineering, Christchurch Hospital, New Zealand 4 Concussion Clinic, Brain Injury Rehabilitation Unit, Burwood Hospital, Christchurch, New Zealand 5 Department of Neurology, Christchurch Hospital, New Zealand
Correspondence to: Marcus H. Heitger, Van der Veer Institute for Parkinson's & Brain Research, 66 Stewart St. Christchurch 8011, New Zealand E-mail: marcus.heitger{at}otago.ac.nz
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.
Key Words: head injury; PCS; saccades; OSP; neuropsychological function
Abbreviations: ACC, Accident Compensation Corporation; ATI, absolute time index; BDI II, Beck Depression Inventory (2nd Ed.); D–KEFS, Delis–Kaplan Executive Function System; GCS, Glasgow Coma Scale; IRI, inter-response index; LOC, loss of consciousness; mCHI, mild closed head injury; OSP, oculomotor smooth pursuit; PCS, post-concussion syndrome; PTA, post-traumatic amnesia; PTSD, post-traumatic stress disorder; RAVLT, Rey Auditory Verbal Learning Test; RCFT, Rey Complex Figure Test; RHIFQ, Rivermead Head Injury Follow-up Questionnaire; RPSQ, Rivermead Post-concussion Symptoms Questionnaire; WAIS III, Wechsler Adult Intelligence Scale 3rd Edition; WMS III, Wechsler Memory Scale 3rd Edition; WTAR, Wechsler Test of Adult Reading
Received February 25, 2009. Revised April 30, 2009. Accepted May 25, 2009.