Review The neuro-ophthalmology of head trauma Rachel E Ventura, Laura J Balcer, Steven L Galetta Lancet Neurol 2014; 13: 1006–16 Traumatic brain injury (TBI) is a major cause of morbidity and mortality. Concussion, a form of mild TBI, might be Department of Neurology, associated with long-term neurological symptoms. The eff ects of TBI and concussion are not restricted to cognition New York University School of and balance. TBI can also aff ect multiple aspects of vision; mild TBI frequently leads to disruptions in visual Medicine, New York, NY, USA functioning, while moderate or severe TBI often causes structural lesions. In patients with mild TBI, there might be (R E Ventura MD, Prof L J Balcer MD, Prof abnormalities in saccades, pursuit, convergence, accommodation, and vestibulo-ocular refl ex. Moderate and severe S L Galetta MD) TBI might additionally lead to ocular motor palsies, optic neuropathies, and orbital pathologies. Vision-based testing Correspondence to: is vital in the management of all forms of TBI and provides a sensitive approach for sideline or post-injury concussion Dr Steven L Galetta, Department screening. One sideline test, the King-Devick test, uses rapid number naming and has been tested in multiple athlete of Neurology, New York cohorts. University School of Medicine, New York, NY 10016, USA [email protected] Introduction particular of eye movements, needs coordination of Traumatic brain injury (TBI) is increasingly recognised as refl exive and voluntary activity, including frontoparietal a major cause of morbidity and mortality worldwide, with circuits and subcortical nuclei;15 these pathways are estimates of its incidence ranging from 106 to 790 per vulnerable to injury in mild to severe TBI. 100 000 people per year.1,2 Because around half of the circuits in the brain are involved in vision, many aspects of Defi cits in visual function in mild TBI the visual system are vulnerable to moderate, severe, or Saccades, antisaccades, and cognitive function mild TBI.3 Not surprisingly, a wide range of visual Saccadic eye movements involve a wide variety of complaints might follow head trauma, including cognitive processes and fi ndings from several studies photophobia, double vision, blurred vision, loss of vision, have shown abnormalities in saccade generation after all and visual processing problems. The topic of sports forms of brain trauma. The generation of saccades concussion, a mild form of TBI, has received a lot of media involves weighing aspects of the stimulus as well as attention as a result of increased recognition of potential processes incorporating goals and intentions.16 long-term deleterious eff ects of repeated concussive Visuospatial information is relayed from the occipital events, such as depression, altered cognition, and lobe and then processed in the posterior parietal cortex. neurodegenerative diseases (eg, chronic traumatic Saccades can then be refl exively generated from the encephalopathy and Alzheimer’s disease).4,5 Improvement parietal eye fi eld or intentionally generated in the frontal of the ways in which we screen for concussion is eye fi eld.16,17 The dorsolateral prefrontal cortex plays a part imperative, particularly since objective fi ndings can be in inhibition of refl exive saccades, in prediction of when subtle and athletes often under-report their symptoms.6 anticipatory saccades are needed, and in short-term Examination of the integrity of the visual system helps to spatial memory18 (table 1, fi gure 1). One frequently used both screen and monitor the recovery of patients with TBI. test to assess executive function is the assessment of antisaccades. Antisaccades are examined by having the TBI and concussion patient try to look away from a stimulus; this action TBI can be classifi ed as mild, moderate, or severe. needs inhibition of refl exive saccades and generation of Concussion is the most common form of TBI in a subset voluntary saccades. Saccades can also be used to test for of patients classifi ed as having mild TBI7–9 (see panel 1 for memory (eg, with the memory-guided saccade test) or to defi nitions).The diff erences between combat-related and assess attention (eg, with the gap-saccade test; panel 2). civilian TBI have not fully been elucidated, although it In a study in patients with mild TBI within 10 days of should be noted that mechanisms of blast-related head their injury, antisaccades were assessed with video- injury are complex and might include other injuries oculography and found to be impaired, with prolonged related to burns, toxic inhalation, and radiation exposure. saccadic latencies, high directional errors, and poor Many clinical features of post-concussive syndrome spatial accuracy, although simple refl exive saccades were mirror those of frontal and temporal lobe syndromes, normal.19 These patients also had impairments in including problems with executive function and memory-guided saccades.19,20 This work was then diffi culties with attention, memory, and concentration,10 extended to patients who had post-concussive syndrome and frontal and temporal lobe damage has been shown in with symptoms 3–5 months after their injury in neuropathological11 and imaging12 studies. Investigators comparison with patients who had good recovery. Those of studies using diff usion tensor imaging (DTI) to assess with post-concussive syndrome did worse in microstructural white matter changes in mild TBI antisaccades, in memory-guided saccades, and in a self- identifi ed a high prevalence of injury in the frontal lobes, paced saccade test in which patients were instructed to corpus callosum, and corona radiata, and diff usely in look back and forth between two points as rapidly as deep white matter.13,14 The cognitive control of vision, in possible.21 Kraus and colleagues22 identifi ed similar 1006 www.thelancet.com/neurology Vol 13 October 2014 Review results in patients with chronic TBI of duration greater than 6 months, and showed that eye movements were Panel 1: Glossary of terms more sensitive than neuropsychological testing for Concussion persisting neurological abnormalities in these patients. A traumatically induced transient disruption of brain function;9 a subset of mild traumatic Drew and colleagues23 noted that patients with acute brain injury. mild TBI had defi cits in a gap saccade test, in which the patient fi xates on one target and then has to orientate to Mild traumatic brain injury a peripheral target after a variable amount of time. The Traumatic brain injury has been deemed mild when there is a normal CT, Glasgow coma patients with mild TBI had longer saccadic reaction scale score (GCS) of 13–15, loss of consciousness of less than 30 min, alteration of mental 8 times compared with healthy controls when the state of less than 24 h, and post-traumatic amnesia for less than 24 h. temporal gap between the initial target and the new Accommodation target was short but not when it was long, which is The process by which the eye changes the shape of the lens to maintain focus on an object consistent with abnormalities in disengagement of as its distance varies. attention. Patients with mild TBI with acute or chronic Accommodative amplitude symptoms, therefore, seem to have impairments in Reciprocal of the focal length in metres. It can be subjectively measured by correcting for executive function, attention, and memory that can be distance vision and then having the subject move a near reading card towards the eyes associated with impaired saccadic function.19–23 Defi cits until the text is no longer in focus, then measuring the reciprocal of the distance in in subcortical visual pathway function were also seen as metres. Alternatively, the card could be initially placed close to the eyes and then pulled manifested by slowed self-paced saccades.21 Patients who away until the patient sees it clearly. Typically, the 20/30 line on a near card is used. For have recovered well from their TBI and do not have instance, a patient who has blurry vision at 10 centimetres has 1/(0.10 metres) or ongoing symptoms do not seem to have continued 10 dioptres of accommodative amplitude. 21 saccadic dysfunction, although further studies are Convergence fusional amplitude necessary to characterise the exact evolution of these eye The amount of prism glass that can be placed in front of the eyes at a particular distance movement abnormalities. Tests of saccades recorded before double vision is seen. It can be measured with a base out prism (eg, with the with video oculography enable examiners to provide an thicker edge facing outwards so the light is bent towards the nose) over one eye when the objective correlate to concussive and post-concussive patient focuses on a target. symptoms. Defi cits in saccades can also be identifi ed with a Phoria cursory clinical examination, though detecting Misalignment of the eyes that occurs only some of the time, such as when one eye is abnormalities of individual eye movements at the covered and the synchronisation between eyes is broken. The presence of phoria can be bedside or on the sideline can be challenging and tested for with the cross-cover test, in which the subject focuses on an object while each requires clinical experience (fi gure 2). In one prospective eye is alternatively covered while the uncovered eye is observed for movement. study of patients with blast-induced mild TBI, six (30%) Convergence insuffi ciency often leads to near phorias because the eyes cannot move in of 20 patients had saccadic dysfunction versus none of 20 tandem to align on a target. 24 in the control group. Exotropia A type of eye misalignment in which one eye is manifestly deviated outward. It can be Smooth pursuit congenital or acquired, constant, or intermittent. Predictive visual tracking can be used to assess higher cognitive functioning, because it requires attention, Exophoria anticipation, working memory, as well as smooth, and at Eye misalignment in which the eyes are deviated outward from each other in the absence times saccadic eye movements to maintain gaze on a of binocular fusion.