Purpose of review

INTRODUCTION

Cerebrovascular accidents (CVAs) occur from decreased cerebral perfusion that results in neuronal death. According to the American Stroke Association, there are three types of strokes: ischemic, hemorrhagic, and transient. Ischemic strokes constitute 85% of all CVAs and can be thrombotic, with blood clots forming locally in the artery, or embolic, where one or more blood clots formed elsewhere, either in the heart, aorta, carotid arteries, or in the venous system with arterial crossover (paradoxical strokes). Ischemic strokes can also happen without clot formations in cases of cerebral hypoperfusion because of systemic shock. Hemorrhagic stroke may be caused by intraparenchymal or subarachnoid hemorrhage, whereas transient ischemic attacks (TIAs) are transient episodes of neurologic dysfunction, regardless of duration, caused by focal brain ischemia without acute infarction [1,2].

Whatever the cause of the stroke, consequences can vary from minor transient focal neurological deficits to permanent damage or even death. Any part of the body can be affected by stroke, and the eyes are no exception. In fact, the majority of CVAs

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have ocular manifestations whether they involve the afferent pathways (vision), efferent pathway (eye movements), or both [3–7].

The present article aims at reviewing all the ocular manifestations that can happen after a CVA with a focus on new interventional methods thataim atrestoring visionand ocularfunction after CVAs (Table 1).

REDUCED VISUAL ACUITY

Clinically up to 70% of patients will develop acutely decreased visual acuity after a stroke [8–14], and this vision loss can be multifactorial. Siong [15] found

a b Department of Ophthalmology, Department of Neurology and c Department of Neurosurgery, University of Colorado School of Medicine, Aurora, Colorado, USA Correspondence to Prem S. Subramanian, MD, PhD, Professor of Ophthalmology, Neurology, and Neurosurgery, 1675 Aurora Ct, Mail Stop F731, Aurora, CO 80045, USA. Tel: +1 720 848 2500; fax: +1 720 848 5014; e-mail: Prem.subramanian@ucdenver.edu Curr Opin Ophthalmol 2017, 28:564–572 DOI:10.1097/ICU.0000000000000414

The majority of patients with cerebrovascular accident (stroke) have visual dysfunction. Injury to the visual system from stroke causes decreased quality of life. Recovery of function often occurs but is variable, and no standard therapeutic interventions exist. Restoring neurological function, rather than compensating for lost ability, may be possible but will likely require multimodal therapy and extended training for patients.

15% of 113 Hong Kong Chinese stroke patients had visual acuity less than 0.5log MAR and noted unilateral visual field defects in 26.5% of patients and bilateral defects in 11%. In a broad review of visual impairment after stroke, 75% of patients were noted to have normal vision, whereas 18.9% had difficulty watching television or reading, 1.2% were not able to read or watch television at all, and 0.6% were almost blind [7]. Although a large prospective UK study found reading problems in 177/915 (19.3%) of patients, only a minority had decreased acuity as the cause [16].

Factors that contribute to decreased vision include reduced contrast sensitivity (reported in up to 60% of patients after strokes affecting the parietal, temporal and occipital cortices [17,18]), perception defects, convergence insufficiency, visual field defects, reduced stereopsis, and dry eye from poor blinking or facial nerve palsies. Three studies have noted that the ‘drop’ in vision in many patients was related to dirty, lost, or broken glasses [9–11]. Decreased visual acuity because of cortical blindness from bilateral occipital lobe infarcts is rare [7].

Littleisreportedontherecoveryofcentralvision following stroke. Rowe [16] showed that 43% of stroke patients had partial improvement in reading abilities while 11% had complete recovery.

VISUAL FIELD LOSS

The reported percentage of patients with visual field loss after a stroke varies widely, ranging from 45 to 92% acutely and 8–25% chronically [9,19–28]. In localizing the visual field defects, Pambakian and Kennard reported 50% arose from occipital stroke, 30%fromparietal,25%fromtemporal,and5%from damage to the optic tract and/or lateral geniculate nucleus[29].Zhangetal.reportedsimilarfindingsin a cohort of over 850 patients [30]. Several smaller studies have demonstrated that up to 57% of stroke patients have persistent visual field defects, with contralateral homonymous hemianopsias and quadrantinopsias being most common [21–27].

In 2013, Rowe reported the results of a prospective study involving 915 patients throughout the United Kingdom to look at the visual outcome of patients with stroke (VIS study). Visual field loss was the sole visual symptom in 47.2% of the patients. The most common type of visual field loss was complete or partial homonymous hemianopia in 57 and 19.5%, respectively, followed by homonymous quadrantanopia, constricted visual fields scotomas, cortical blindness, and temporal crescent defect [9]. In an analysis of an acute stroke database of 11 900 patients, Ali et al. found 60.5% of patients had acute visual impairment. Complete recovery occurred in 42.6 and 45.0% patients by 30 and 90 days, respectively. Only 5.8% (693 patients) were judged to have had a preexisting visual problem [28]. A major limitation of this study is the precise nature of the visual deficit was not known and could include visual field loss and other problems.

Determining the prevalence of visual field loss can be difficult and is most likely underestimated becausemanypatientswhodevelopMCAstrokeswill havedecreasedlevelsofconsciousnessandareunable to report vision loss. In bilateral occipital lobe infarcts, patients can develop anosognosia (Anton Syndrome) and will deny vision loss [31,32]. Many visual field defects can be missed if confrontational visual field testing alone is used [33]. In a prospective study of 32 patients, 62% failed to recognize their right- or left-sided visual field defect [34], and in the VIS Study, only 45% of patients with visual field loss reported symptoms [9].

Recovery

Complete recovery of visual field loss after an ischemic attack has been reported in 44% of patients, whereas partial recovery can reach up to 72% [20,25,28,35–38]. All of these studies, however, are limited by the duration of follow up and the method of assessing visual fields.

Spontaneous recovery usually occurs within the first 3 months, and in a series of 254 patients, 55% showed improvement in the first month, whereas recovery was unlikely after 6 months [20]. However, after 6 months, fixation patterns in patients with homonymous hemianopia change; many develop compensatory mechanisms and produce a series of hypometric saccades into the blind field until they find the object of intent [39–41]. Pediatric patients with hemianopia may have a compensatory exotropia or head turn toward the side of the visual field defect which will cause anomalous correspondence

Table 1. Ocular manifestations of different cerebrovascular occlusions

Circulation
Anterior (70%)	Ophthalmic artery	Ocular ischemic syndrome
	Anterior cerebral artery		Case reports of ocular motor and eyelid closing apraxia due to involvement of branches to the supplementary motor area and corpus callosum

Anterior communicating Aneurysms can compress the supero-anterior portion of the optic artery              chiasm causing bilateral homonymous hemianopsia or the

poseterior portions of the optic nerves.

Middle cerebral artery

Homonymous hemianopia Quadrantopias, Hemineglect (nondominant hemisphere) Conjugate deviation to the side of the lesion, Decrease reflexive saccades Voluntary saccades and memory driven saccades opposite to the lesion (FEF, PEF, DLPFC, temporal lobe), Suppression of caloric induced nystagmus (temporal lobe) Suppression of antisaccades Ocular motor apraxia (bilateral FEF) Apraxia of eyelid openings Convergence insufficiency

Anterior choroidal Homonymous quadruple sectoranopia artery

Posterior communicating Artery Aneurysm Third nerve palsy, pupil involving

Posterior (30%)		Posterior cerebral artery		Congruous contralateral homonymous hemianopia, Macular sparing if anterior Macular homonymous hemianopia if posterior Cortical blindness if bilateral often with Anton syndrome or visual anosagnosia Unilateral temporal crescent visual field loss Balint’s syndrome (simultagnosia, optic ataxia, ocular motor apraxia)
		Lateral posterior choroidal artery		Horizontal, homonymous sectoranopia

Thalamoperforating Vertical gaze palsy arteries/percheron artery

Esotropia

Top of the basilar

Dorsal midbrain syndrome Vertical gaze palsy (upgaze and downgaze) Convergence insufficiency Convergence spasm Convergence retraction nystagmus on upgaze Pseudosixth due to failure of ocular abduction Collier sign or lid retraction ’Plus minus sign’ Ocular tilt reactions in which there is a head tilt to the ipsilateral shoulder with incyclotorsion of the higher eye that is the contralateral eye Skew deviation, ocular torsion, and abnormal estimation of the visual vertical. Small, fixed, and slightly reactive to light Light near dissociation Correctopia Iridae

Table 1 (Continued)

Circulation
	Caudal Lesions: third nerve palsy

Basilar artery Nuclear third nerve palsy:

ipsilateral third nerve palsy þ contralateral ptosis and superior rectus dysfunction

If the nuclear lesion is rostral, it will involve the Edingar Westphal nucleus leading to pupillary involvement with muscle sparing.

Fascicular Third nerve:

Superior cerebellar peduncle (Nothnagel’s Syndrome): ipsilateral 3rd nerve palsy þ cerebellar ataxia.

Lesions at the Red Nucleus (Benedikt’s Syndrome): ipsilateral 3rd nerve palsy and contralateral involuntary movement.

Lesion at the cerebral peduncle (Weber’s syndrome): ipsilateral

3rd nerve palsy and contralateral hemiplegia

Claude syndrome: distal territory of the mesencephalon, leading to contralateral hemiparesis, contralateral ataxia, and contralateral hemiplegia of the lower face, tongue, and shoulder in addition to ipsilateral oculomotor nerve palsy

Horizontal gaze palsy,

Internuclear ophthalmoplegia

One and a half syndrome

Vertical gaze palsy

Contralateral fourth nerve palsy

Anterior cerebellar artery

Lateral pontine Syndrome Gaze holding and pursuit deficit

Horner’s syndrome

Skew deviation

Sixth nerve nucleus: Ipsilateral gaze palsy þ ipsilateral facial nerve palsy

sixth nerve fasciculus: ipsilateral abduction deficit

Eight and a half syndrome: one and a half syndrome þ facial palsy

Foville syndrome: ipsilateral gaze palsy, facial palsy, facial hypoesthesia, peripheral deafness, Horner’s syndrome and contralateral hemiparesis, ataxia, pain, and thermal hypoesthesia

Millard–Gubler or ventral pontine syndrome: sixth nerve palsy, ipsilateral facial palsy, probably involving the root fibers and with contralateral hemiplegia or hemiparesia resulting from involvement of the corticospinal tract

Vertebral Arteries:

Wallenberg syndrome (lateral medullary syndrome) Ipsilateral impairment of pain and temperature on the face and contralateral impairment in the body Ipsilateral horner Skew deviation/ocular tilt reaction Ipsilateral lateropulsion Ipsipulsion of saccade tilt of the vertical normal towards side of the lesion Horizontal nystagmus beating away from lesion Upbeat nystagmus Ocuopalatine myoclonus

Superior cerebellar Saccadic contrapulsion artery

Tilt of the vertical normal away from the side of the lesion

Table 1 (Continued)
Circulation
Posterior inferior cerebellar artery	Vestibular nystagmus
	Lateral medullary syndrome Saccadic dysmetria (hyper o hypometria) Gaze evoked, rebound, downbeat nystagmus Periodic alternating nystagmus Impaired VOR suppression Square wave jerk Esophoria Exophoria

to develop and thus overcome the complete visual field defect without diplopia [42,43].

More than 50% of patients with homonymous hemianopia will not achieve adequate recovery of visual function. Rehabilitative methods have centered on both compensatory use of the remaining visualfield and attempting to restorefunction inthe hemianopic field. This latter goal remains elusive and controversial.

Trainingprotocolshavebeendevised toincrease awareness of the blind area; patients are instructed to make organized saccades into the blind hemifield [19,44]. Exploratory saccade training (EST), using a software program that generated a random array of digits where the patient was asked to move the cursor toward a specific digit without over or undershooting, was shown to improve saccadic behavior, natural search, and scene exploration on the blind side and was associated with subjective improvement in activities of daily living [45]. In a separate randomized trial employing a systematic, anticipatory scanning strategy [46^&], patients demonstrated subjective improvement in mobility-related activities but not in reading, visual counting, and visual search [47^&&]. Other interventions have integrated auditory stimuli into the visual scanning training procedure [48,49,50^&].

Another approach is to make use of optical aids, by applying binocular prisms directed with base out away from the blind field. A prerequisite for these prism to work is to have gaze directed into the prism [51], and improved visual task performance but not in activities of daily living has been shown [52]. High power monocular sector prisms are an alternative, as the function in all directions of gaze and are commercially available; improved function including return to driving has been shown [53,54]. Nonetheless, a recent study of 87 patients showed the use of prisms and visual search training was not superior to standard care in increasing the visual field area afterstroke, and prisms were associated ahigh (69%) incidence of headaches [55^&&]. A case report using computerized technology (Google Glass) has demonstrated the potential of such methods to expand the visual field [56^&].

The above interventions compensate for but do not restore lost visual field. Restorative therapies purport to stimulate cortical neuroplasticity, a method supported by adult animal models of vision deprivation [57–59]. Sabel et al. devised a computerbased method (NovaVision) to stimulate the border zone of visual field defects, where improvement through retraining was most likely to occur. In their initial report, 30% of treated patients with retrochiasmal lesions showed improvement in visual field, and there was a shift in the transition zone of 5 to 68 among VRT-trained patients [60]. Similar improvements were demonstrated in subsequent studies [61,62]. Using a different visual discrimination training strategy, Cavanaugh and Huxlin found that 17 patients who underwent training recovered 108 deg² of vision on average, whereas 5 untrained patients improved over an area of 16 deg² [63^&&].

Subsequent critiques of these methods postulated that patients had developed adaptive saccadic compensationratherthanatrueincreaseinthevisual field.HortonclaimedthatSabelandhisgroupdidnot report fixation losses, false positives, and false negatives,andthattheiruseofblindspotmonitoringwas inadequate to detect small saccades [64]. Indeed, small case series of patients treated with various flickering stimulus regimens seemed to show that responses in the blind field were not improved when fixation was monitored by methods different from those used in NovaVision restoration therapy [40].

Nonetheless, more accurate and reproducible target detection has been shown in patients treated with dual static and kinetic stimulation [65,66]. Also, vision restoration therapy combined with transcranial direct current stimulation (tDCS) was found to be superior to vision restoration therapy alone [67,68]. A recent pilot study by Sabel’s group showed that a combination of tDCS and VRT is well tolerated and seems to be more effective than standard vision training procedures [69^&]. A confirmatory, larger-sample, controlled, randomized, and double-blind trial is now underway to compare real-tDCS-augmented versus sham-tDCS-augmented visual field training in the early vision rehabilitation phase [69^&]. Finally, some critics have advocated delaying any therapy to avoid the mistaken conclusion that an intervention has been useful, because improvement may have been spontaneous. However, early intervention in hemiparetic patients improves outcomes, and to take advantage of neuroplasticity, early treatment with the goal of visual field restoration also may be justified [68,70,71^&,72].

In conclusion, the efficacy of VRT and other interventions in expanding visual fields post strokes remains inconclusive despite animal data and human experience that support neuroplasticity in human visual systems.

OCULAR MOTILITY DYSFUNCTION

The reported prevalence of ocular motility dysfunctionafterstrokerangesfrom22to70%[19,21,73–76]. Ocularmotilitydysfunctionincludesstrabismus,gaze palsy, nystagmus, and vergence deficits.

Strabismus

Strabismus after strokes is related to cranial nerve palsies, supranuclear palsies, internuclear ophthalmoplegia, skew deviations, ocular tilt reactions, and other abnormalities of ocular motor control. Prospective studies of patients with strokes have noted that strabismus can occur in 16.5 to 50% of patients [21,73,75–77]. Rowe reported that strabismus was mainly present with cortical strokes (69%), and 56.5% of patients with strabismus had only one ocularmotilityabnormality.Themostcommonstrabismus type was exotropia, seen in 74% of strabismic patients [73]. In a mixed population of stroke (129) andheadinjury(84)patients,Fowlerreportedthat89 (37%)ofpatientshadocularalignmentproblemsbut that only 32 (36% of those with strabismus) had symptoms, either because of the small deviation or because of decrease in vision or perception [75]. Interestingly,anidenticalrateofsymptomaticdiplopia with strabismus was found in the VIS UK Study [73]. Sixth and third nerve palsies are more common in stroke than fourth nerve palsy [10,73]. Within the spectrum of oculomotor nerve palsy, the medial rectus subnucleus may be affected in isolation [78–80].

Gaze palsy

Gaze palsy is the most common ocular motility disturbance after stroke and has been reported in 18–44% of patients with CVA [21,74,81–83]. It can be isolated or associated with other motility problems. Horizontal gazepalsies aremoreprevalentthan vertical, and complete palsies are more common than partial [73,74]. The presence of conjugate eye deviation on CT scan is associated with worse outcome [84] and higher NIH stroke severity scale score [85] in patients with acute ischemic stroke, and this predictive status remains despite interventions such as thrombolysis [86^&].

Nystagmus

Prevalence of nystagmus after stroke is likely underestimated, as many studies do not report nystagmus when assessingstrokeoutcomes [87];inone study, it was present in 24% of 407 patients with posterior circulation stroke [13]. Unsurprisingly, cerebellar stroke has the strongest association with acute findings of nystagmus [76,88]. Although the onset of nystagmus with focal neurological deficits is highly diagnostic for stroke [89^&], 11% of patients with isolated vertigo or dizziness (in which nystagmus often is present) were noted to have stroke in a recent study of 221 patients [90].

Vergence

Convergence insufficiency (CI) is quitecommon after stroke; Cilsby [21] reported its presence in 55% of stroke cases, whereas Rowe noted that in 109 CVA patients with reading difficulties, 54% had impaired nearpointofconvergence(NPC)morethan6cm,and 28% had NPC more than 10cm [16]. Siong reported reduced convergence (>15cm) in 21% of cases [15].

Recovery

Full recovery from CVA-associated cranial nerve palsies may occur in 7–28.5% of patients, and nearly all (92%)havesomeimprovement,withsixthnervepalsy being most likely to resolve completely [16,28,73,74]. Indeed, database analysis suggests some recovery occurs in all patients with horizontal gaze paresis [28]. More broadly, prospective data showed partial recovery of cranial nerve palsies in 43% and complete recovery in 22.5% of affected stroke patients; nystagmus improved partially in 42% whereas gaze palsy improved completely in 6% and partially in66%[73].

VISUAL PERCEPTION

Higher order cognitive deficits may lead to visual disturbancesafterstroke, asmay lack of awareness of visual information. Visual hemifield neglect, or visual anosognosia, is seen commonly middle cerebral artery (MCA) stroke of the nondominant hemisphere. Studies usually do not separate visual, spatial, and auditory neglect. Although visual neglect is more often seen in right MCA strokes, even in left MCA stroke there is contralesional attentional impairment that can be recorded [91].

The reported prevalence of visual neglect after strokes ranges from 14 to 82% [92–96], with this broad range attributable to the use of different methods of assessment, different inclusion criteria, and different areas of the brain being affected.

Other perceptual deficits reported in the literature include cerebral achromatopsia [97], optic ataxia [98], simultagnosia [99], extinction [92], and visual hallucinations [17,94,95,96,100] In a series of 189 stroke patients age at least 65 years, 93 (49.2%) had one or more visual perceptual problems [101]. A lower prevalence of 20% was described in a population of 323 stroke patients of all ages [100]; in thisstudy,visualhallucinationswereseenin4%and visual agnosia in 2.5% of patients. Visual and tactile attentional testing of 454 patients in the United Kingdom with subacute stroke was performed and demonstrated contralateral (left) visual extinction in 28% of participants with right hemisphere stroke versus only 6.8% of participants with right visual extinction from left hemisphere stroke [102].

Recovery

Recovery of visual neglect across several studies ranges from 29% to 78% [25,28,103]. Visual neglect has been correlated with a longer stay in hospital and poorer prognosis for functional recovery [103]. Recovery is mostly seen within 3 months post onset with approximately 10% full recovery within the first 2 weeks [25,28]. When CVA patients undergoing visual restoration therapy were asked (19 prospectively, 121 retrospectively) about visual hallucinations, they reported a median duration of 28 days and recovery within 90 days [36].

As with visual field defects, interventions to improvehemifieldneglecthavebeenstudiedbuthave inconclusive results. Right half field patching studies showeda positive butinconsistent trend toward effectiveness [104–106]. Smooth pursuit eye movement therapytowardtheneglectedfieldwasfoundeffective inachievingsomefunctionalimprovementinpatients with neglect in the setting of subacute stroke [107,108].However,arandomizedtrialwasconducted among 21 patients with acute (<14 days) stroke and left-sidedneglectandshowednobenefitforcombined hemifield eye patching and optokinetic stimulation [109]. Other suggested therapies include videogame [110]andvirtualrealitytraining[111].Visualscanning training similar to that discussed with visual field defects has also been studied and found to be effective in overcoming visual neglect, although functional improvement was not assessed [112,113]. Prism adaptation was found effective in some case reports [114], but randomized controlled studies did not show any functional benefits of prisms in patients with neglect [115–117]. Results of cognitive therapy are similarly inconclusive [118]. Recent assessments of tDCS suggestitmay behelpful[119,120],especially whencombinedwithothertreatmentmodalities[121^&,122,123].

CONCLUSION

The majority of patients with stroke will experience either transient or permanent visual deficits. This review serves as an overview of the most recent and important data that outlines the prevalence of defects in the visual, perceptual, and oculomotor systems following CVAs. We paid special attention to the interventions that are thought to help restore or compensate for visual field loss and visuospatial neglect. This isacontroversialtopic,anddata aswell as expert opinions are still not conclusive on whether these interventions are useful, but clinical evidence supports the potential use of noninvasive brain stimulation in combination with other optical, cognitive, or plasticity-training therapies to improve the visual outcomes.

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56. Trese MGJ, Khan NW, Branham K, et al. Expansion of severely constricted

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Novel technology employment in a stroke patient- possible future uses exist.

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This article showed improved performance on standard, clinically relevant tests of visual field after visual restoration training that controls for fixation. The clinical significance remains to be seen, but this study addresses many of the prior concerns about saccadic movements giving a false sense of improvement.

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Open label (unmasked) study that shows potential efficacy of combined therapies.

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Overview of current attempts to restore visual field.

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Demonstration of outcome prediction being possible from a simple data point regarding eye position on CT.

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The authors showed that bedside testing and even MRI may miss clinically relevant posterior fossa strokes.

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Further proof of concept.

122. La`davas E, Giulietti S, Avenanti A, et al. a-tDCS on the ipsilesional parietal cortex boosts the effects of prism adaptation treatment in neglect. Restor Neurol Neurosci 2015; 33:647–662.
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