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Traumatic brain injury (TBI) is a major cause of morbidity and mortality. Concussion, a form of mild TBI, might be
associated with long-term neurological symptoms. The eects of TBI and concussion are not restricted to cognition
and balance. TBI can also aect multiple aspects of vision; mild TBI frequently leads to disruptions in visual
functioning, while moderate or severe TBI often causes structural lesions. In patients with mild TBI, there might be
abnormalities in saccades, pursuit, convergence, accommodation, and vestibulo-ocular reex. Moderate and severe
TBI might additionally lead to ocular motor palsies, optic neuropathies, and orbital pathologies. Vision-based testing
is vital in the management of all forms of TBI and provides a sensitive approach for sideline or post-injury concussion
screening. One sideline test, the King-Devick test, uses rapid number naming and has been tested in multiple athlete
cohorts.
Introduction
Traumatic brain injury (TBI) is increasingly recognised as
a major cause of morbidity and mortality worldwide, with
estimates of its incidence ranging from 106 to 790 per
100 000 people per year.1,2 Because around half of the
circuits in the brain are involved in vision, many aspects of
the visual system are vulnerable to moderate, severe, or
mild TBI.3 Not surprisingly, a wide range of visual
complaints might follow head trauma, including
photophobia, double vision, blurred vision, loss of vision,
and visual processing problems. The topic of sports
concussion, a mild form of TBI, has received a lot of media
attention as a result of increased recognition of potential
long-term deleterious eects of repeated concussive
events, such as depression, altered cognition, and
neurodegenerative diseases (eg, chronic traumatic
encephalopathy and Alzheimers disease).4,5 Improvement
of the ways in which we screen for concussion is
imperative, particularly since objective ndings can be
subtle and athletes often under-report their symptoms.6
Examination of the integrity of the visual system helps to
both screen and monitor the recovery of patients with TBI.
Review
Smooth pursuit
Predictive visual tracking can be used to assess higher
cognitive functioning, because it requires attention,
anticipation, working memory, as well as smooth, and at
times saccadic eye movements to maintain gaze on a
xed target (gure 3).25 Smooth pursuit of a predictive
target is programmed by the cerebellum and is based on
retinal and higher cortical input, including input from
the prefrontal cortex.17,26 Suh and colleagues27,28 had
controls and patients with mild TBI track a target
moving in a circle at a xed rate, with or without
temporarily extinguishing the target. The patients with
TBI had decreased target prediction with increased eye
position error and variability of eye position, with more
robust ndings when the target was temporarily
extinguished, which requires an increased degree of
predictive tracking.27,28 These smooth pursuit decits
correlated with scores of attention and executive function
on the California Verbal Learning Test.28 Maruta and
colleagues29 correlated variability of eye position in the
www.thelancet.com/neurology Vol 13 October 2014
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Purpose
Anatomical pathway
Saccades
Pursuit
Vestibulo-ocular reex
Vergence
Vergence
Excitatory
Inhibitory
SEF
FEF
PEF
DLPC
!
!
! CN
SNPR
SC
BGC
Visual
cortex
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Attention
Gap saccade test
The participant xates on one central target on a computer
screen, which then disappears and a peripheral target, either
to the left or right, appears after a variable period of time. The
deviation of the participants eyes when the second object
appears is measured using infrared tracking devices.
Visually cued saccades
The participant xates on a central target while a cue
indicates the possible location of an upcoming target; then a
congruent or incongruent target to the cue appears,
generating saccades. The deviation of the eyes is measured.
Smooth pursuit of a predictive target
The participant tracks an object on a known trajectory (eg, a
circle); the object might at times be transiently obscured at
any point in its trajectory. Eye velocity and gaze positional
errors are recorded using visual tracking devices.
Executive function
Antisaccades
The participant is asked to look away from a presented object.
Memory
Memory-guided saccades
The participant focuses on a central target while a peripheral
target appears briey; after a variable delay, usually between
500 and 1500 ms, the participant is asked to xate by
memory on where the peripheral target was located.
Memory-guided sequences
The participant is presented with targets on a screen and then
asked to memorise the sequence in which they appear. The
participant generates saccades in the memorised order.
Figure 2: Saccades
Saccades can be tested by having the patient (A) look at a target in the periphery
and then (B) look at a target directly in front of their face. Saccades can be
assessed for speed and accuracy. This test is shown in an accompanying video.
Accommodation
Accommodative dysfunction is also frequently
described in patients with mild TBI. Accommodative
insuciency manifests as decreased accommodative
amplitude (panel 1). Accommodative amplitude is age
dependent and the minimal amount expected can be
estimated by the formula 15 ( 025 age in years). So, a
20-year-old patient might be expected to have about
10 dioptres of accomodative amplitude. Capo-Aponte
and colleagues24 prospectively studied a population with
blast-related mild TBI and showed that 13 (65%) of
20 patients versus 3 (15%) of 20 controls had
abnormalities in accommodative amplitude. Other less
frequent abnormalities of accommodation described in
patients with mild TBI include accommodative
insuciency and slowness in changing from one level
of accommodation to another, which manifests as
transient blurring.
www.thelancet.com/neurology Vol 13 October 2014
Figure 3: Pursuit
Pursuit can be tested by having the patient x and follow a slowly moving
object, such as the end of a reex hammer. Please see accompanying video.
Review
Figure 4: Convergence
Covergence can be assessed by moving the patients thumb towards their nose
and measuring the distance at which fusion is broken or the distance at which an
exotropia is developed. Note the constricted pupils with the near response. This
test is shown in an accompanying video.
Review
Intracanalicular portion
Oculomotor nerve At the exit from the midbrain; superior orbital ssure
Trochlear nerve
Abducens nerve
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*
C
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was greatest at the site of the dural entry point and the
petrous apex, and identied injury at the site of
anastomosis with the sympathetic plexus along the
internal carotid artery.87 Delayed abducens injury can
occur in the setting of elevated intracranial pressureeg,
due to traumatic haemorrhage or oedema, and has also
been described with normal imaging, suggesting
additional mechanisms such as ischaemia or local
oedema.86,88 Investigators of a prospective natural history
study noted that seven of 25 patients with unilateral
cranial nerve VI palsies and three of eight patients with
bilateral palsy spontaneously recovered at 6 months.89
Predictors of non-recovery include inability to abduct past
midline and bilateral palsy.90
Brainstem injury
In addition to the cranial nerve palsies, brainstem injury
in TBI can cause several neuro-ophthalmic ndings,
including pupillary and motility disturbances.
Brainstem injury often occurs in association with severe
blows to the back of the head.91 Traumatic internuclear
ophthalmoplegia due to medial longitudinal fasciculus
injury has been described as occurring bilaterally in 3
(16%) and unilaterally in 1 (05%) of 181 patients with
TBI who were referred for neuro-ophthalmological
assessment.92 When 410 inpatients with internuclear
ophthalmoplegia were reviewed, 20 (5%) had brain
trauma as the cause. 84 Dorsal midbrain syndrome is also
rare in patients with TBI, occurring in 2 (03%) of 326 of
patients in one retrospective series.49 Dorsal midbrain
syndrome is characterised by paralysis of upgaze,
pseudo-Argyll Robertson pupils, convergence retraction
nystagmus, and eyelid retraction.
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Declaration of interests
LJB has received consulting fees for the development of visual outcome
measures for multiple sclerosis clinical trials from Vaccinex, Biogen-Idec,
Questcor, and Novartis. SLG has received honoraria for consulting from
Biogen-Idec, Genzyme, and Vaccinex. REV declares no competing
interests.
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