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each eye. On observation, he had noticeable tremors with an unsteady gait. Distance alternating cover test showed exophoria with a right hyperphoria. Near alternating cover test revealed a significantly larger exophoria accompanied by a reduced near point of convergence. Additional testing with a 24- 2 Humphrey visual field and optical coherence tomography (OCT) of the nerve and macula were unremarkable. The patient underwent DBS implantation five weeks after initial examination, and the device was activated four weeks thereafter. At follow up, the patient still complained of intermittent diplopia. There was no significant change in the manifest refraction or prism correction. On observation, the patient had remarkably improved tremors with a steady gait. All parameters measured were unchanged. The patient was evaluated again seven months after device activation. Although vergence ranges at all distances were improved, the patient was still symptomatic for intermittent diplopia. OCT scans of the optic nerve showed borderline but symmetric thinning in each eye. All other parameters measured were unchanged.

Conclusion: The case found no significant changes on ophthalmic examination after DBS implantation and activation in a patient with PD. To the best of the authors’ knowledge, there are no other cases in the literature that investigated the effects of DBS on the visual system pathway in a patient with PD before and after DBS implantation and activation.

INTRODUCTIONParkinson’s disease (PD) is a progressive

neurodegenerative disorder caused by a dopamine deficiency in the substantia nigra presenting with clinical motor features such as bradykinesia, muscular rigidity, and resting tremors. Non- motor features including olfactory dysfunction, cognitive impairment, psychiatric symptoms, sleep disorder, autonomic dysfunc-tion, and sensory dysfunction can also present

Correspondence regarding this article should be emailed to Ashley Mitchell, OD, at mitche.ash@gmail.com. All state ments are the authors’ personal opinions and may not reflect the opinions of the College of Optometrists in Vision Development, Vision Development & Rehabilitation or any institu­tion or organization to which the authors may be affiliated. Permission to use reprints of this article must be obtained from the editor. Copyright 2019 College of Optometrists in Vision Development. VDR is indexed in the Directory of Open Access Journals. Online access is available at covd.org. https://doi.org/10.31707/VDR2019.5.3.p158.

Mitchell A, To C. Visual effects of deep brain stimulation in a patient with Parkinson’s Disease. Vision Dev & Rehab 2019;5(3)158-73.

Keywords: binocular vision, convergence insufficiency, deep brain stimulation,

diplopia, Parkinson’s disease

Visual Effects of Deep Brain Stimulation in a Patient with Parkinson’s DiseaseAshley Mitchell, OD

Chung To, OD, FAAO

ABSTRACTBackground: Parkinson’s disease (PD) is a progressive neurodegenerative disorder caused by a dopamine deficiency that presents with motor symptoms. Visual disorders can occur concomitantly but are frequently overlooked. Deep brain stimulation (DBS) has been an effective treatment to improve tremors, stiffness and overall mobility, but little is known about its effects on the visual system.

Case Report: A 75- year-old Caucasian male with PD presented with longstanding binocu-lar diplopia. On baseline examination, the best- corrected visual acuity was 20/25 in

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PD can be treated surgically with deep brain stimulation (DBS) for qualifying candidates.3,4 Patients can sometimes reduce the dosage or discontinue the use of levodopa/carbidopa altogether post- surgical treatment. DBS is an effective treatment where a neurostimulator device is implanted unilaterally or bilaterally to provide electrical stimulation to the brain, specifically to the subthalamic nucleus, globus pallidus internus, and/or thalamus, to improve motor functions.5

Electrical stimulation has been used to modulate and regulate the central nervous system since ancient times using electric fish and electroshock therapy, such as applying an electric ray to the cranial surface for the treatment of headaches. The origins of DBS actually preceded medicinal intervention. In 1947, the first pallidotomy was performed on a patient with Huntington’s disease, a progressive brain disorder that causes uncontrolled movements, emotional disturbances, and loss of cognition. A pallidotomy is a surgical procedure that places electric probes in the globus pallidus (a subcortical component of the basal ganglia associated with voluntary movement) and heated to destroy small areas of the brain creating permanent lesions. This procedure was soon applied to similar conditions, such as the treatment for PD, but was gradually abandoned in the late 1950s and replaced by the thalamotomy. A thalamotomy is a similar surgical procedure that specifically targets the thalamus (adjacent to the globus pallidus associated with relaying sensory signals, including motor signals, to the cerebral cortex). By targeting the thalamus, a thalamotomy had a more predictable outcome on lessening tremor symptoms. DBS was first utilized in 1963 using high frequency thalamic stimulation for sustained tremor control. Meanwhile, medical intervention with levodopa had become available in 1969, which provided a less invasive and less damaging treatment option to effectively control PD symptoms. Later, the resurgence and popularity of DBS grew in

in PD but are often overshadowed and usually not considered prominent features.1,2

The management of mild motor symptoms in PD is primarily treated medically with the use of either a dopamine agonist or dopamine replacement agent like levodopa. Dopamine agonists are typically initiated in patients with mild to early disease that present at a younger age of onset. Levodopa is given to older patients with more moderate to advance disease. Dopamine agonists directly stimulate post- synaptic dopamine receptors whereas levodopa, a precursor to dopamine, is converted to dopamine with the help of the naturally occurring enzyme dopa decarboxylase. Levodopa readily crosses the blood- brain barrier before converting to dopamine but is first absorbed in the gastrointestinal tract and is quickly degraded by the gastric enzyme dopa decarboxylase before reaching the brain. To combat this, levodopa is frequently combined with carbidopa, a drug that blocks the gastric enzyme preventing peripheral conversion of levodopa to dopamine. This inhibition of peripheral metabolism of levodopa increases cerebral levodopa bioavailability and reduces peripheral adverse effects of dopamine such as nausea and vomiting.3,4 Levodopa and carbidopa collectively have been shown to be more effective with the relief of PD symptoms, but dopamine agonists have a lower incidence of motor complications and side effects. In late- stage PD treatment, about 40% of patients develop motor fluctuations and dyskinesia after five years of continuous levodopa and carbidopa use. Patients begin to experience a “wearing off” effect from these medications, described as a shorter duration of benefit, and the former motor symptoms resurface. A dopamine agonist, monoamine oxidase B inhibitor, or catechol O- mehtyltransferase inhibitor can usually be added to the treatment plan when this occurs. Alternatively, with improved imaging and neurosurgical techniques, advanced stages of

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acuity, refractive error, color vision, pupils, extraocular motility, binocularity, visual field, optical coherence tomography (OCT) of the macula and optic nerve in a patient with PD before and after DBS implantation and activation.

CASE REPORTA 75- year- old Caucasian male with PD

presented to our clinic on August 30, 2017, with longstanding binocular vertical diplopia at distance and near for the last 3- 5 years. He stated that the diplopia had worsened over the last 3- 4 months. He was previously seen by an outside neuro- -ophthalmologist on November 2016, for the same diplopic complaints. The extensive diplopic work up at that visit was negative for myasthenia gravis, thyroid related ophthalmopathy, and cranial nerve palsies. Magnetic resonance imaging of the brain with and without contrast was obtained on November 27, 2016, in which mild volume loss with moderate white matter disease was noted without evidence of acute infarct, hemorrhage, or enhancing mass. His previous ocular history was remarkable for convergence insufficiency, a right hyperphoria, dry eyes, and early cataracts in both eyes. Medical history was remarkable for PD, tremors, hypertension, hyperlipidemia, osteoarthritis, hearing loss, cardiovascular disease, and normocytic anemia. Current medications included carbidopa 50 mg/levo-dopa 200mg for PD, ondansetron 8 mg for nausea, atorvastatin 80 mg for cholesterol, gabapentin 400 mg and tramadol 50 mg for pain, and artificial tear drops four times a day in both eyes for dry eyes. No known drug allergies were noted. The patient denied prior history of smoking, alcohol, or illicit drug use.

On baseline optometric examination, five weeks prior to the DBS procedure, the best- corrected visual acuity through the manifest refraction of +0.75- 0.75X085 right eye and +1.00- 1.75X110 left eye was 20/25 right eye and left eye, respectively. The patient’s habitual distance spectacles also had a 4 base

the early 1990s as an alternative treatment to symptomatic regression of tremors after using levodopa. Today, DBS is used to target either the subthalamic nucleus or globus pallidus when symptomatic regression occurs after medical treatment or when severe tremors are not effectively controlled with medications alone.6,7,8

Motor features of PD have been widely studied. Ocular and visual disorders can occur concomitantly with the motor disorders but are frequently overshadowed. Convergence insufficiency (CI) and extraocular motility dysfunctions (i.e. saccadic and smooth pursuits) have been more recently reviewed in PD patients.9 In a large study by Irving et al, 43.8% of PD patients were found to have CI, comparable to roughly one- third of PD patients reported by Lepore and Shibaski.9,10,11 Saccadic dysfunction and abnormal pursuits were found in approximately 75% of PD patients, according to Armstrong et al. In saccadic dysfunction, PD patients exhibit hypometria or undershooting of conjugate eye movements when directed towards a target while pursuits showed interruptions of smooth conjugate eye movements following a target.2 DBS has been shown to improve saccadic dysfunction, but there are conflicting studies on its effects of smooth pursuits.5 The effects of DBS on the visual system pathway have not been extensively studied, and long- term studies are limited.

Dry eyes and primary open angle glaucoma have also been found to be prevalent in PD patients. Studies have shown a reduced blink rate in PD patients that often leads to a staring appearance contributing to an abnormal tear film and symptomatic dry eyes. Glaucomatous visual field defects were found in 24% of patients suggesting that there may be an association or increased rate of glaucoma in patients with PD.2

The following case study investigates the effects of DBS on the visual system pathway by the following criteria: best- corrected visual

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4 prism diopters of base down vertical prism in the right eye were needed to alleviate diplopia at near through a +2.50 diopter add with the manifest. Worth 4- dot with the full prism correction showed flat fusion with no suppression of either eye. Motilities were full in all nine positions of gaze in both eyes. Distance supra- vergence showed a break at 3 prism diopters with recovery at 2 prism diopters in the right eye and a break at 2 prism diopters with recovery at 1 prism diopter in the left eye. Distance base- out horizontal ranges were 4 prism diopters break with recovery at 1 prism diopter. Near base- out horizontal ranges were 1 prism diopter break with recovery at 0 prism diopters. Base- in horizontal vergences were 6 prism diopters break with recovery at 4 prism diopters at distance and 14 prism diopters break with recovery at 12 prism diopters at near (see Table 1).

A 24- 2 Humphrey visual field was com-pleted at the initial exam in both eyes with good reliability. The right eye showed some scattered central points but was otherwise full. The left eye was full without any defects

down ground in prism in the right lens. On observation, the patient had significant tremors with an unsteady gait. Pupils were equal and reactive with no afferent pupillary defect in either eye. Confrontation visual fields were full to finger counting in both eyes. Unilateral cover test revealed no evidence of apparent strabismus at distance and near. Distance alternating cover test through the manifest refraction without prism correction showed a 3 prism diopters exophoria with 4 prism diopters right hyperphoria. The magnitude and direction of the alternating cover test remained the same in all nine positions of gaze. A stable 4 prism diopters base down in the right eye was measured as previously prescribed to alleviate diplopia. Near alternating cover test through a +2.50 diopter add without prism revealed 15 prism diopters of exophoria and 4 prism diopters of right hyperphoria. Near point of convergence showed a break at 9 inches with recovery at 11 inches with subjective diplopia at the break and the right eye was observed to be turned out. It was determined that 4 prism diopters of horizontal base in prism along with

Table 1. Summary of exam findings before and after DBS (1 and 7 months) activation.

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Figure 1A. 24-2 Humphrey visual field before DBS activation.

Figure 2A. Macular OCT before DBS activation.

Right Eye Left Eye

(see Figure 1A). A baseline optical coherence tomography (OCT) (Heidelberg Spectralis) scan of the macula and optic nerve was completed. The scans of the macula were flat with normal foveal contours and normal central macular thickness in both eyes (see Figure 2A). The peripapillary retinal nerve fiber layer (pRNFL) of the optic nerve head was found to be within normal limits without abnormalities in both eyes (see Figure 3A). A more in depth analysis of the average macular thickness of the full retinal layers, which include the retinal

nerve fiber layer (RNFL), ganglion cell layer (GCL), inner plexiform layer (IPL), inner nuclear layer, outer plexiform layer, outer nuclear layer, retinal pigment epithelium, and the inner and outer retinal layers, was also performed. Segmentation of the inner retinal layers of the macula, specifically the RNFL, GCL, and IPL, was also measured and analyzed with the Heidelberg Spectralis OCT and compared to mean normative values of patients aged 69- 87 composed by Nieves- Moreno et al.12 The diameter of the macular scans was set

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Figure 3A. Optic nerve OCT before DBS activation.

based on the Early Treatment of Diabetic Study macular map of 1, 3, and 6 mm rings for analysis. However, only the inner 1 and 3 mm rings were evaluated for comparison due to poor image acquisition of the outer 6mm ring. The retinal macular thickness in all quadrants was slightly thinner than normative values but remained greater than the 5th percentile. The RNFL had slightly thinner values nasally and superiorly. The GCL was normal in all quadrants. The IPL was slightly thinner in the inner nasal quadrant. Each inner retinal layer value was greater than the 5th percentile. The GCL+IPL complex appeared within normal limits in all quadrants (See Table 2, Figures 4 and 5).

Anterior segment evaluation showed mod-er ate erosions on the corneal surface contrib-uting to dry eyes and mild to moderate nuclear cataracts bilaterally. Both upper and lower eyelids were in normal position with normal eyelid closure. Intraocular pressure (measured by Goldmann applanation with 0.25% fluorescein sodium and 0.4% benoxin-

Table 2. Average thickness values for macular retina and inner layers (RNFL, GCL, and IPL), 1 and 3 mm rings, com­pared to mean normative data by Nieves­Moreno et al.12

ate hydrochloride) was found to be 11 mmHg in each eye. The patient was dilated with one drop of 1% tropicamide and 2.5% phenylephrine in each eye. Posterior segment showed healthy, perfuse and distinct optic nerves with a cup- to- disc ratios of 0.3/0.3 in each eye. The macula and vitreous were clear bilaterally. The vessels were normal, and the periphery showed no retinal breaks, tears, or defects in either eye.

The patient was diagnosed with converg-ence insufficiency with a decompensated right hyperphoria likely exacerbated by his PD. He also had dry eyes, cataracts, and hyperopic regular astigmatism with presbyopia in both eyes. No changes to the current habitual glasses and prisms were made since the patient had a scheduled DBS procedure with neuro- surgery within five weeks after the initial optometric examination. The patient was to follow up in four months to be evaluated again after his DBS procedure, implantation, and activation.

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Figure 4. Macular OCT segmentation and average thickness of the right eye before DBS implantation, 4A) Macular OCT scan and segmentation layers, 4B) Retinal layer thickness, 4C) RNFL thickness, 4D) GCL thickness, and 4E) IPL thickness.

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Figure 5. Macular OCT segmentation and average thickness of the left eye before DBS implantation, 5A) Macular OCT scan and segmentation layers, 5B) Retinal layer thickness, 5C) RNFL thickness, 5D) GCL thickness, and 5E) IPL thickness.

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The patient completed DBS implant ation approximately five weeks after his initial eye examination. A review of his hospital medical records indicated that the Medtronic’s Activa Deep Brain Stimulation Therapy System was successfully implanted by neurosurgery. The device was then activated four weeks after surgery, likely to ensure resolution of any swelling surrounding the leads.13 The patient was re- evaluated at the eye clinic four weeks after device activation. He continued to have complaints of intermittent diplopia which was stable to the last visit. Best- corrected visual acuity was 20/30 in the right eye and stable at

20/25 in the left eye. There was no significant change in the manifest refraction and vertical or horizontal prism. Motilities remained full in both eyes with the magnitude and direction of the alternating cover remaining stable in all nine positions of gaze. On observation, the patient had significantly improved tremors with steady movement and gait. Near point of convergence and horizontal base- out ranges at distance and near were stable. All other parameters measured were unchanged and stable from previous examination (see Table 1). Humphrey 24- 2 visual field and OCT scans of the macula and optic nerve were repeated

Figure 1B. 24-2 Humphrey visual field 1 month after DBS activation.

Figure 2B. Macular OCT 1 month after DBS activation.

Right Eye Left Eye

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and found to be stable (see Figures 1B, 2B and 3B). Macular thickness was not measured with OCT due to poor image acquisition. The most updated manifest distance prism glasses were dispensed for full- time wear, per the patient’s request. The patient reported no issues with the current near habitual prism glasses.

The patient was evaluated again seven months after activation of the DBS device. Best- corrected visual acuity was stable at 20/30 in the right eye and 20/25 in the left eye. There was no significant change in the manifest refraction nor vertical or horizontal prism. Motilities again remained full in both eyes with the magnitude and direction of the alternating cover remaining stable in all nine positions of gaze. The patient continued to have no tremors with steady movement and gait. Near point of convergence had not changed. Although vertical and horizontal ranges at distance and near improved clinically, the patient was still symptomatic for intermittent diplopia. There was a mild

lag with frequent undershoots in his horizonal and vertical saccades but no intrusions were observed. All other parameters measured were unchanged and stable to prior examinations (see Table 1). Humphrey 24- 2 visual field and OCT scans of the macula were found to be stable. Macular thickness measurements of the retina and segmented inner layers were consistent with those before DBS implantation (See Figures 6 and 7). OCT scans of the pRNFL of the optic nerve showed borderline but symmetric thinning inferior-temporally in each eye (see Figures 1C, 2C and 3C). Ocular health was stable anteriorly and posteriorly. Intraocular pressures were also stable at 11 mmHg in each eye. The patient was to follow up annually thereafter for routine eye exams.

DISCUSSIONThe case presented showed no significant

difference in subjective and objective visual findings in a PD patient before and after DBS implantation and activation. Best-corrected visual acuity was 20/30 in the right eye and 20/25 in the left eye, which remained stable in subsequent exams. The slight visual acuity reduction in the right eye may have been due to progression of PD or cataracts, but it is difficult to discern subtle changes. Poor visual acuity is a common visual symptom in PD patients and may be caused by lack of dopamine in the retina, abnormal eye movements or poor blink rates.2 There was no change in any entrance testing. Horizontal and vertical heterophorias were stable on unilateral and alternating cover test in all nine positions of gaze. The near point of convergence did not improve or worsen after the DBS procedure. Color vision and binocular fusion were stable. Supravergence ranges were balanced between the eyes post- DBS with full prism correction. Horizontal vergences at distance and near were improved at seven months but did not change the subjective and objective diplopia from the CI. 24- 2 Humphrey visual field remained full and stable to the initial exam in both eyes. Macular

Figure 3B. Optic nerve OCT 1 month after DBS activation.

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Figure 6. Macular OCT segmentation and average thickness of the righty eye after DBS activation, 6A) Macular OCT scan and segmentation layers, 6B) Retinal layer thickness, 6C) RNFL thickness, 6D) GCL thickness, and 6E) IPL thickness.

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Figure 7. Macular OCT segmentation and average thickness of the left eye after DBS activation, 7A) Macular OCT scan and segmentation layers, 7B) Retinal layer thickness, 7C) RNFL thickness,7D) GCL thickness, and 7E) IPL thickness.

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OCT showed no significant changes and was in normal range. Segmentation analysis of the RNFL, GCL, and IPL remained stable with only a slight reduction when compared to age based normative data values.12 On pRNFL optic nerve OCT scans, there were symmetric, borderline thinning changes in the inferior- temporal quadrant at the seven- month follow up in both eyes, but more data is needed to determine progression.

There are limited studies of DBS effects on the visual system. There have been cases reported of improved saccadic function, smooth pursuits, and forced eyelid closure after DBS.5,14,15 In our particular case, there was no change in the saccadic eye movements or smooth pursuits, and eyelid closure appeared normal before and after DBS. Ortiz- Pérez et al reported a delayed complication status post DBS which caused vertical diplopia from

Right Eye Left Eye

Figure 1C. 24-2 Humphrey visual field 7 months after DBS activation.

Figure 2C. Macular OCT 7 months after DBS activation.

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a skew and an ocular tilt reaction.16 No short term complications were noted in the case presented.

In the absence of DBS treatment, several studies reported a thinner GCL+IPL complex in patients with PD.17,18,19,20 This is likely due to the retinal dopaminergic neuro- degeneration that occurs in patients with PD resulting in atrophy and thinning of the inner retinal layers.17,18,19,20

Contrary to this case study, macular retinal thickness was found to be slightly reduced with normal GCL+IPL thickness when analyzed before DBS activation, and parameters remained stable after DBS activation. According to Sari et al, the GCL+IPL complex thinning may be correlated with PD severity and duration, but larger cohort studies are needed as inconsistent results have been reported by authors such as Zivokic et al.17,20 Macular GCL+IPL thickness may be a useful tool to follow PD progression.17,20 A recently published meta- analysis performed by Chrysou

et al found significant thinning of the pRNFL, which supports current literature.18,19,21

However, there are a few studies that have found no difference between healthy controls and PD patients.17,21 Disease stage severity, incomplete assessment of controls, and variable sensitivities between different OCT equipment have been speculated to account for the discrepancy in literature.21 The pRNFL in this case report showed some early borderline thinning in the inferior- temporal quadrant of both eyes at seven months after DBS activation, but more data is needed to show progression since early thinning may be attributed to progression of PD rather than an effect of DBS treatment.

While the mechanism of DBS is not com-pletely understood, it is theorized that DBS works by functionally stimulating adjacent neural structures without destroying brain cells like that of pallidotomy. Another theory hypothesizes that DBS is mediated by activation of axonal fibers via the excitatory/inhibitory mechanism in which certain neural cells require a higher activation threshold to function properly. The excitation of efferent fibers combined with the inhibition of afferent fibers may control or mediate the action of the cells using DBS.7

Patients who undergo DBS have been shown to improve rigidity, bradykineasia and tremors.22,23 The following patient in this case study presented at the one month and seven month follow up visit with noticeably less tremors and significantly improved mobility and function, which proved a successful DBS treatment. Candidates who qualify for the DBS procedure may have, but are not limited to, the following criteria: typical PD (not secondary or atypical), presence of motor fluctuations, possess tremors not satisfactorily treated by medication, younger than 70 years of age, without dementia or any psychiatric disorders, and/or any other contraindications for neurosurgery. DBS is generally well-tolerated but risk of surgical complications

Figure 3C. Optic nerve OCT 7 months after DBS activation.

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include intracranial hemorrhage (1-10%), stroke (0- 2%), infection (0–15%), lead erosion without infection (1–2.5%), lead fracture (0–15%), lead migration (0–19%), and death (0–4.4%). The most common adverse effect is impairment of axial motor performance (i.e. speech, gait, and postural stability). Less common side effects include eyelid apraxia, dysphagia, ipsilateral sweating/mydriasis/hypersalivation, and diplopia.7 Although the patient presented in this case study is over the age of 70, there are exceptions to qualifications above given his level of severity of the disease and time of diagnosis.

DBS has also been successfully used for the treatment of Tourette syndrome, epilepsy, depression, obsessive- compulsive disorder, and a variety of other psychiatric disorders.8

Previously, Medtronic was the only FDA approved device for DBS. However, Boston Scientific and Abbott/St. Jude’s have also entered the DBS market creating competition and driving development for improved products.24

LimitationsSaccadic function, saccades and anti- sac-

cades, were only measured at the seven-month endpoint and were not explicitly measured prior in this patient due to normal ocular motility findings at the initial exam. The patient had a subtle undershoot, but the degree was negligible and did not translate to significant clinical findings. Further long-term endpoints at one and two years are needed to determine progression in pRNFL. Inner retinal layers were measured on OCT imaging at baseline before DBS implantation and after DBS activation at 7 months only, but analysis was incomplete due to the absence of the outer 6mm of the macula.

CONCLUSIONLittle is known about the overall effects

of DBS on the visual system. The case report investigates the short-term effects of DBS on

the visual system in a patient with PD. There were no significant changes found subjectively and objectively on ophthalmic examination. This is contrary to some case studies which reported improvements in saccadic function, smooth pursuits, and forced eyelid closure. Further investigation with a larger sample size is required to understand the full effects of DBS on the visual system.

REFERENCES1. De Virgilio A, Greco A, Fabbrini G, et al. Parkinson’s disease:

Autoimmunity and neuroinflammation. Autoimmunity Reviews 2016;15(10):1005-1011.

2. Armstrong RA. Visual Symptoms in Parkinson’s Disease. Parkinson’s Disease 2011. https://doi.org/10.4061/2011/ 908306.

3. Koller WC, Rueda MG. Mechanism of action of dopaminergic agents in Parkinson’s disease. Neurology 1998;Jun;50(6 Suppl 6):S11-4; discussion S44-8.

4. Rao SS, Hoffman LA, Shakil A. Parkinson’s disease: diagnosis and treatment.Am Fam Physician 2006;74:2046-54.

5. Shaikh AG, Antoniades C, Fitzgerald J. Ghasia FF. Effects of Deep Brain Stimulation on Eye Movements and Vestibular Function. Front Neurol 2018;Jun 12;9:444. https://doi.org/10.3389/fneur.2018.00444. eCollection 2018.

6. Cif L, Hariz M. Seventy years of pallidotomy for movement disorders. Movement Disorders 2017;32:972-982. https://doi.org/10.1002/mds.27054.

7. Hartmann CJ, Filegen S. Groiss SJ et al. An update on best practice of deep brain stimulation in Parkinson’s disease. ThereAdv Neurol Disord 2019;Mar 28;12:1756286419838096. https://doi.org/10.1177/1756286419838096. eCollection 2019.

8. Sironi VA. Origin and Evolution of Deep Brain Stimulation. Frontiers inIntegrative Neuroscience 2011;5:42. DOI: 10.3389/fnint.2011.00042

9. Lepore FE. Parkinson’s Disease and Diplopia. Neuro- Ophthalmology 2006;30:37-40. https://doi.org/10.1080/ 01658100600742838

10. Shibasaki H, Tsuji S, Kuroiwa Y. Oculomotor Abnormalities in Parkinson’s Disease. Arch Neurol1979;36(6):360–364. https://doi.org/10.1001/archneur.1979.00500420070009

11. Irving EL, Chriqui E, Law C, et al. Prevalence of Convergence Insufficiency in Parkinson’s Disease. Mov Disord Clin Pract2017 May-Jun; 4(3): 424–429. https://doi/org/10.1002/mdc3.12453

12. Nieves-Moreno M, Martinez-de-la-Casa M, Cifuentes-Canorea P et al. Normative database for separate inner retinal layers thickness using spectral domain optical coherence tomography in Caucasian population. PLoS One. 2017; 12(7): e0180450. https://doi.org/10.1371/journal.pone.0180450

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13. Parkinson’s Disease, Deep Brain Stimulation: Practical Guide for Patients and Families. Okun MS and Zeilman PR. Parkinson’s Foundation 2019;Chapter 8, pp. 38-42.

14. Fawcett AP, González EG, Moro E, Steinbach MJ, et al. Subthalamic nucleus deep brain stimulation improves saccades in Parkinson’s disease. Neuromodu lation. 2010 Jan;13(1):17-25. https://doi.org/10.1111/j.1525-1403.2009.00246.x. Epub 2009 Nov 13.

15. Nilsson MH, Patel M, Rehncrona S. Subthalamic deep brain stimulation improves smooth pursuit and saccade performance in patients with Parkinson’s disease, 2013, J Neuroengineeringand Rehab 2013;10:33-33. https://doi.org/10.1186/1743-0003-10-33

16. Ortiz-Pérez S, Sánchez-Dalmau B, Molina Jet al. Ocular tilt reaction as a delayed complication of deep brain stimulation for Parkinson disease. J Neuroophthalmol.2009 Dec;29(4): 286-8. https://doi.org/10.1097/WNO.0b013e3181b2822d.

17. Sari ES, Koc R, Yazici A, Sahin G, Ermis SS. Ganglion cell-inner plexiform layer thickness inpatients with Parkinson’s disease and association with disease severity and duration. J Neuroophthalmol.2015 Jun;35(2):117-21. doi: 10.1097/WNO.0000000000000203.

18. Ucak T, Alagoz A, Cakir Bet al. Analysis of retinal nerve fiber layer and ganglioncell – inner plexiform layer by OCT in Parkinon’s disease patients.Parkinsonism Relat Disord.2016 Oct;31:59-64. https://doi.org/10.1016/j.parkreldis.2016.07.004. Epub 2016 Jul 9.

19. Chrysou A, Jansonius NM, van Laar T. Retinal Layers in Parkinon’s Disease: A Meta-Analysis of spectral-domain opical cohehrence tomography studies.Parkinsonism Relat Disord.2019 Jul;64:40-49. https://doi.org/10.1016/j.parkreldis.2019.04.023. Epub 2019 Apr 30.

20. Živkovic M, Dayanir V, Stamenovic J, et al. Retinal ganglion cell/inner plexiform layer thickness in patients with Parkinson’s disease. Folia Neuropathol.2017;55(2):168-173. https://doi.org/10.5114/fn.2017.68584.

21. Guo L, Normando EM, Shah PA, et al. Oculo-visual abnormalities in Parkinson’s disease: Possible value as biomarkers:Mov Disord.2018 Sep;33(9):1390-1406. https://doi.org/10.1002/mds.27454.

22. Antoniades CA, Rebelo P, Kennard C et al. Pallidal deep brain stimulation improves higher control of the oculomotor system in Parkinson’s disease.JNeurosci 2015;35:13043-13052. DOI: https://doi.org/10.1523/JNEUROSCI.2317-15.2015

23. Krack P, Batir A, Van Blercom N. Five-Year Follow-up of bilateral stimulation of subthalamic nucleus in advanced Parkinson’s disease.N Engl J Med 2003; 349:1925-1934 DOI: https://doi.org/10.1056/NEJMoa035275

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CORRESPONDING AUTHOR BIOGRAPHY:Ashley Mitchell, ODTampa, Florida

Dr. Ashley Mitchell is originally from Lafayette, Louisiana. She completed her Bachelor of Science in Biological Engineering at Louisiana State University in 2007 and a Master of Science in

Biomedical Engineering at New Jersey Institute of Technology in 2009. For over four years, she conducted research by applying therapeutics to enhance bone healing at Rutgers University in Newark, New Jersey. She left her job to pursue a career in optometry where she found her passion.

She later received her Doctor of Optometry at Salus University in 2018 and completed a residency at the James A. Haley Veterans’ Hospital in Tampa, Florida, in ocular disease and traumatic brain injury. She currently works at a private optometric practice in the Tampa Bay Area and will start a position at the New Port Richey Veterans’ Eye Clinic serving the veteran population.