TRAINEES

Unravelling ocular motility

cular motility can often be exists an intricate interweaving body suppression of the image coming from a slightly abstract concept of connections that make him function one eye, the brain has lost the ability to during the earlier years of so well (textbooks have been written coordinate both eyes at the same time. Oophthalmology training. on his complexity). All eye movement, Hence, the (usually poorer seeing) eye A large variance on what embodies whether calibrated by the navigator in drifts to a ‘resting position’, the good normality; mythical concepts like fusion the back seat (cerebellum) or voluntarily eye fixates on the target, and you see a and , examination directed by the little lobes of brain at manifest squint or a tropia. techniques that can be fiddly, and the top (frontal eye field) will have to Often the science makes sense, complex neuroanatomy all conspire to be performed by our chauffeur, the an accommodative occurs make it an awkward topic to learn. brainstem. because the accommodation effort The concepts that are more The eyes work best as a pair. If to overcome the hypermetropic pertinent to general training relate humans had only one eye by design, blur causes an overconvergence. to the diagnosis and management of parts of our brainstem would probably Occasionally though, through pathologies that will lead to be more rudimentary (and doing a cover mechanisms that are not completely and / or diplopia. test will look very silly) but having two understood, the dynamics of the opens up a whole world of motor and characters in our story are strained and Basic control of eye sensory function. the final message sent to the eyes is movements To stabilise the eyes, a constant signal mixed, resulting in non-alignment. In our oversimplified analogy, the brain is sent in order to keep them relatively In a child, when a motility problem stem is a complex guy as you can tell in the correct position. If both eyes leads to diplopia / confusion, the brain from his expression in Figure 1. He can individually see well the brain can really dislikes it as you can imagine, grew up in a complex environment coordinate both foveas to fixate on the and is forced to suppress one image in with complex relationships and apart required target. When we disassociate order to be of any use to society. It can from driving the movement of the eyes the eyes, i.e. an alternate cover test, we also be the other way around where the is also responsible for a multitude of halt that process and the eyes return to vision is affected first and the brain no vital basal functions. He is a skilled that ‘resting position’, hence we are able longer has a pair of good images that driver of the eyes and has honed these to see the latent squint or a phoria. it can use in order to develop precise skills through years of inherited and Think about a manifest squint in coordination. It then could partially acquired learning. Inside his body there an amblyopic exotropic eye. Due to switch off depending on its mood and may just leave things be to the ‘resting tone’ or tweak a little here and there occasionally. Therefore, this resting tone, although there are default settings that come with a new brainstem, is subject to change during development, can vary slightly over time and within individuals, and can be occasionally swayed by pathology. As human beings when we get older or more tired, we decompensate in many areas unfortunately. The fusional vergence system is subject to this as well. When it breaks down, the eyes will drift to its resting position but because we are not covering either eye, the foveas are not in sync and we see double. A decompensating is the most common cause for an intermittent diplopia. Being very visual beings, we depend a lot on our vision to orientate us on this plane as well as to track objects of Figure 1: A caricature of ocular motility (Illustration by Shindy Je). interest, either when making a bifoveal

eye news | APRIL/MAY 2016 | VOL 22 NO 6 | www.eyenews.uk.com TRAINEES

note that as we go further backwards, it gets a little less familiar and the words become fancier. The eyes need to travel as a pair so a mechanical defect affecting one eye or both will impair the movement of the eyes (orbital / pathology). Examining the eyes is what we are good at so this is our comfort zone. The reins of the brainstem (cranial nerve pathology) can be affected partially or fully, isolated or in combination and this will result in the eye or eyes not being able to make specific movements. This is the infranuclear pathway and we can usually relate better to pathologies in this area. The brainstem. Here we can have pathology affecting the nucleus of the reins, the connections between the cranial nerves (the medial longitudinal fasciculus), or the supranuclear gaze

Figure 2: Cartoon of a confused caveman. control centres. A host of other cranial nerves and other important structures (like the bundles of nerve between smooth pursuit of a rabbit scurrying opposite partner will take over and the brain and spinal cord) travel within the across the forest floor, or a patient’s eyes will move to the affected side. brainstem so other neurology can easily quick saccades around the operating The cerebropontocerebellar pathway, coexist (and should not be missed). room as he is lying on the operating AKA pursuit pathway (wheels of the As we enter supra-brainstem territory, table trying to determine if you or the carriage), maintains smooth pursuit it gets more complex but generally consultant will do his cataract. of an object while optical feedback we have the saccadic pathway and Horizontal strabismus is more is constantly being regulated by the pursuit pathway which is initiated common, because we have complex the cerebellum (wise old man with and regulated separately but recent vergence mechanisms that function to binoculars) so that the movement is evidence suggests they work a lot closer converge and diverge the eyes allowing at the right velocity (if the speed and together than once thought. us to focus on objects along the same direction of where the eyes should go plane so there are more things that next are not determined, we will be Our role as ophthalmologists can ‘go wrong’ during the development useless at fixating on a moving object). With our understanding of the visual of binocular vision. Why horizontal? Cerebellar disease is a common cause of system, we should be equipped to do the Because our eyes are placed side by side . following: and not on top of one another (Figure 2). All these signals communicate with What about vertically? The basic role one another via interconnecting neurons Diagnosis: Localising the disease of the vertical centres is to make sure in order to generate a message that tells By working through what governs that our set of horizontally placed eyes the brainstem where to go, how fast to motility, we can work our way from an stay level in relation to each other, as get there, and when to stop. inferior orbital floor fracture leading to well as adapting to the earth’s vertical The brainstem with this information failure in unilateral upgaze and vertical line. Without these mechanisms, we will then directs the eye movements via diplopia. Or a cerebellarpontine angle be fuddled with the slightest of head impulses sent through the third, fourth tumour leading to a mixed craniopathy movements. and sixth nerve on both sides. As he is a and nystagmus. There is merit in clever little chap himself (even receiving localising well as we could potentially The players sensory input directly from retinal diagnose life-threatening disease. The frontal cortex on each side initiates ganglion cells), he makes little decisions It is not uncommon for this a conjugate saccadic process to the in his supranuclear centres before caseload of patients to present to the contralateral side. This starts the deciding how to direct his reins to do team first. saccadic pathway which travels down horizontal or vertical manoeuvres and to the superior colliculus. To aid in when to converge or diverge depending Management remembering, if you refer to our lovely on the type of movement he has been Once we know the aetiology, we can: drawing, you can see that the characters told to make. • Treat the underlying cause. This stood on top of the carriage are pointing could range from fixing the refractive to the other side. An agitated lobe (i.e. Things that can go wrong error to treating orbital inflammatory an irritative lesion like epilepsy) will be We have already discussed disease medically to repairing a more demanding, make a bit more noise, developmental features but what about muscle avulsion. and this will cause the driver to move acquired disease? • Treat if it exists. Patching is in that direction. If the lobe is quiet (i.e. Let’s take our analogy and work our a wonderfully rudimental treatment destructive lesions like a stroke), his way from front to back. It is natural to that has survived the test of time.

eye news | APRIL/MAY 2016 | VOL 22 NO 6 | www.eyenews.uk.com TRAINEES

• Maintain alignment. Generally, once STEP ONE: Primary position things are stable, we are able to (diplopia / / cover test) improve vision or improve cosmesis “In an exam situation 1. Ask patient: “Do you have any double by manually strengthening or vision?” weakening individual muscles. we are expected The presence or absence of diplopia (and its features: horizontal, vertical, tilted) Quick examination of patients to come up with a in either the primary position or other for exam purposes diagnosis based on our positions will help narrow down the In an exam setting, it makes sense condition. to have a methodology which is three minute motility 2. Hirschberg Test to recheck primary comprehensive and includes all aspects deviation. of motility. However, one should be examination.” 3. Cover Test (if you do it properly first careful not to do too many unnecessary time you only need to cover each eye steps. This system is designed to pick ONCE) distance then near. up the likely diagnosis as soon as 4. Alternate Cover Test (again, do it possible in order for you to decide on properly the first time if possible). which subsequent examination to use nerve palsy, head tilt – fourth nerve Testing with spectacles may not next. Keep in mind that as soon as you palsy, chin depression – bilateral be necessary if they have a high recognise the diagnosis, you have to fourth nerve palsy, chin elevation prescription and can’t fixate well modify the rest of your examination – chronic progressive external without the aid of their glasses. accordingly. For example, if you spot a ophthalmoplegia (CPEO). prosthetic eye from the moment you see • Eyelids: unilateral ptosis – Horner’s STEP TWO: Horizontal gaze the patient, you don’t want to waste any / third nerve / trauma / myasthenia, (dextroversion / laevoversion) time getting them to fish their elusive bilateral ptosis – CPEO, myasthenia, 1. Tell patient: “Let me know if you see spectacles out of the coat pocket so lid retraction – thyroid disease, double.” you can do a near and distance cover contralateral ptosis, enophthalmos 2. Move the eyes across the horizontal test with and without their spectacles. – enucleation socket syndrome, gazes. Once to the left and once to Conversely, those steps might be the proptosis – orbital / cavernous sinus the right. This one move volunteers a most important ones for conditions disease. lot of information like an overaction / like a distance esotropia or a fully • Aperture: Anisocoria – Horner’s underaction, upshots / downshoots, accommodative esotropia so make sure / third nerve, mid-dilated pupils impaired / increased velocity, you consider them in those scenarios. – parinauds, constricted pupils – impaired pursuit, i.e. showing small An impression of being ‘slick’ comes convergence spasm. saccades instead, or even a gaze- not from doing things very quickly but • Deviation: nystagmus, internuclear evoked nystagmus. This step is rather from doing the required steps ophthalmoplegia, wall-eyed bilateral crucial. As a lot of pathologies affect correctly the first time around. internuclear ophthalmoplegia horizontal movement, they will reveal Unlike real life, where we have the (WEBINO), , , themselves here! benefit of doing something devious skew deviation, , 3. If the patient sees double, stop there called taking a history, in an exam cranial nerve palsies, mechanical and ask them to describe the nature of situation we are expected to come up entrapment, axial and nonaxial the diplopia and then cover each eye with a diagnosis based on our three proptosis. asking them which image disappears. minute motility examination with If you make a spot diagnosis after the The more outwardly placed image is usually only a little background of the H.E.A.D phase, you can do a little wry being seen by the paretic eye. If the underlying problem. smile because the game is over (but cover is already there, do an alternate don’t make that smile too awkward). If cover test to have an idea of the size Start off looking for the you see a down and out eye with a blown of the deviation in that position. obvious – and a ptosis, you can mention it 4. If there is underaction at any stage, Head Posture, Eyelids, Aperture immediately and then cater the rest of try to see if duction = version or (pupils), Deviation (H.E.A.D) your examination accordingly. So in the otherwise. This is the inspection phase. It is not example of a third nerve palsy, do the exhaustive but each feature in the necessary eye movements then find • Orbital acronym is crucial because if present out if it is complete or partial, isolated – isolated horizontal muscle failure / it may very well lend itself to a spot or mixed, nuclear or peripheral (Oxford weakness / entrapment. diagnosis! Handbook Third Edition page 700) and • Cranial nerves If they are normal, it only takes 5.3 so on. – sixth nerve palsy showing seconds to say: “This patient has no NB: When you see a third, fourth or ipsilateral underaction in abnormal Head tilt, normal Eyelids with sixth cranial nerve palsy at any stage, abduction no obvious asymmetry, no abnormalities make sure you test (or at least mention – fourth nerve palsy showing with the pupil Apertures, and no it) for all the other cranial nerves ipsilateral hypertropia in Deviation on primary gaze.” (especially from second to eighth). adduction Even before you actually start, you The Ophthalmology Examinations – third nerve palsy showing would have considered a myriad of Review by Wong et al. has excellent ipsilateral underaction in conditions. Example: clinical approaches to different motility adduction (potentially in other • Head Posture: face turn – sixth conditions. directions as well).

eye news | APRIL/MAY 2016 | VOL 22 NO 6 | www.eyenews.uk.com TRAINEES

• Myogenic – fourth nerve palsy showing your casualty clinic but pretty much – Ocular Myasthenia Gravis ipsilateral hypertropia in impossible in your exam) or you’ve – CPEO. adduction and inferior oblique missed something subtle but at least • Supranuclear / internuclear overaction or superior oblique have demonstrated a wonderful – skew deviation (hypertropia underaction in the direction of technique. on abduction) that muscle’s action – INO and WEBINO – third nerve palsy showing Conclusion – one and a half syndrome ipsilateral underaction on Ocular motility is confusing. Most – horizontal gaze palsy elevation and adduction ophthalmologists don’t understand – brainstem pathology (potentially in order directions it and a portion of those have never – nystagmus. as well). understood it. This is a great shame • Myogenic / neurogenic as it opens the door to a beautiful STEP THREE: Vertical gaze – CPEO interaction between eye and brain 1. Tell patient: “Let me know if you see – Ocular Myasthenia Gravis. in both patient and ophthalmologist double.” Same principles apply: • Supranuclear and we hope this guide above makes a if they see double, ask them to – progressive supranuclear palsy difficult subject more accessible. describe it and do a cover test to – Parkinson’s find the paretic eye. – upbeat and downbeat nystagmus 2. Straight upgaze. – gaze palsy 3. Straight downgaze (lift the lids up +- – brainstem pathology. elevate the chin). SECTION EDITOR 4. Concentrate on the four oblique Other tests (three step test, movements. This will allow you to saccades, convergence, doll’s Gwyn Samuel test the elevators and depressors at head, optokinetic drum) Williams, Medical Fellow, its position of optimal function. It is These tests are used to supplement Moorfields Eye Hospital, easier at this stage to think in terms what you are already suspecting. There London, UK. of individual muscle action. will not be a condition where you have E: gwynwilliams@ to use all of them on the same patient! doctors.org.uk • Orbital If we look at our differentials, you – thyroid eye disease will see that at some point during your – isolated muscle failure / examination, something should show AUTHOR weakness / entrapment up, and 50% of them will potentially Damien Yeo, – age-related upgaze weakness have an obvious sign (hence why these Author, – monocular elevation deficit. patients were recruited for the exam). ST6, Singleton Hospital, Swansea, UK. • Cranial nerves If you’ve done the steps correctly and E: [email protected] – sixth nerve palsy showing everything still looks normal or the ipsilateral underaction in patient does not volunteer diplopia in upgaze and downgaze in any position of gaze, then the patient abduction is either normal (which will be ideal in

eye news | APRIL/MAY 2016 | VOL 22 NO 6 | www.eyenews.uk.com