Disorders of eyeball position and movement

By | July 20, 2013

As discussed previously, there is an intimate functional association between the innervation to the extraocular muscles and the vestibular system. The extraocular muscles are innervated by cranial nerve III (oculomotor), cranial nerve IV (trochlear) and cranial nerve VI (abducent) (). Any strabismus due to a lesion in one or more of these cranial nerves must be differentiated from lesions affecting the extraocular muscles (including traumatic rupture and extraocular myositis).

  • • Lesions simultaneously affecting CNs III, IV and VI result in external ophthalmoplegia, and internal ophthalmoplegia if the pupillary constrictor (CN III) is affected.
  • • Lesions with only cranial nerve III involvement may present with a ventrolateral strabismus; more rarely lesions may only affect single muscle groups, resulting in a strabismus opposite to the normal function of the denervated muscle.
  • • Lesions affecting the trochlear nerve in isolation are extremely rare but, where they do occur, will result in loss of function of the ipsilateral dorsal oblique muscle (brainstem lesions may result in loss of function, ipsilateral or contralateral). The dorsal oblique muscle functions to rotate the dorsal portion of the globe nasally (intortion); lesions of the dorsal oblique muscle are therefore evidenced by rotation of the eyeball, with the dorsal portion of the eyeball deviated temporally (laterally). In cats this is evident as rotation of the normally vertical pupils, but in dogs, with a round pupil, this is only apparent on demonstrating lateral deviation of the dorsal retinal arteriole and vein on ophthalmoscopic examination ().
  • • Abducent lesions are extremely rare in isolation but, where they do occur, will result in medial strabismus of the affected eye (the abducent nerve innervates the lateral rectus and retractor bulbi muscles of the eyeball). Lesions of the abducent nerve can be distinguished from congenital medial strabismus by the absence of eyeball retraction in the affected eye on performing the corneal reflex ().

Eyeball movement is further controlled by the vestibular and saccadic systems. The function of the vestibular system with regard to vision is to maintain the visual image in a steady position on the retina in response to movements of the head. This is achieved by inducing eye movements, via the vestibulo-ocular reflex, that are equal to but in the opposite direction to the head movements. In contrast to the vestibular system, the saccadic system functions to change the

line of sight to focus a new visual stimulus on the retinal region with the highest visual acuity (usually the area centralis). Saccadic eye movements occur in response to startle reflexes (sudden visual and auditory stimuli) and during the fast-phase eye movements of the vestibulo-ocular reflex.

Congenital nystagmus

Congenital nystagmus may be recognized in association with ocular abnormalities and congenital visual deficits but occasionally nystagmus may be present in the absence of other ocular abnormalities (). The nystagmus associated with congenital visual deficits is characterized as a continuous fine oscillation of both globes, often rotatory, or may be characterized as random eye movements (amaurotic nystagmus or ‘searching nystagmus’). Rotary nystagmus has been described in association with microphthalmos and congenital cataracts in puppies, even though vision is not totally lost. Animals that lose their vision at a young age may develop nystagmus ().

Pendular nystagmus may occur secondary to congenital abnormalities of the visual pathway in Belgian Sheepdogs. In these dogs decussation is lost at the optic chiasm and all the retinal ganglion projections are into the ipsilateral optic tract (). Congenital nystagmus in Siamese and related cat breeds is discussed below.

Congenital strabismus

Congenital strabismus is seen occasionally in the absence of identifiable underlying causes () or may be associated with albinism (see Congenitally abnormal visual pathways in Siamese and related breeds), congenital vestibular syndrome or brachycephalic breeds.

Congenitally abnormal visual pathways in Siamese, Birman and Himalayan cats

Albino and imperfect albino animals (including Siamese, Birman and Himalayan coat cats) demonstrate congenital abnormalities of the visual pathways (). The consequent clinical anomalies demonstrated in the Siamese and related breeds include convergent strabismus (esotropia) () and occasionally spontaneous pendular nystagmus. The majority of the axonal projections from the temporal retina usually do not cross at the level of the optic chiasm, but in melanin-deficient animals there is increased cross-over of these normally uncrossed pathways at the optic chiasm. It is likely that melanin or a closely linked gene is important in determining the correct axonal path of retinal ganglion cells during development. The consequence of this abnormal cross-over is that conflicting visual information from both visual fields is mapped at each lateral geniculate nucleus, with the abnormally crossed information in reverse. Affected animals are able to make some sense of the conflicting visual inputs by blocking the projections of the inappropriately crossed afferents into the visual cortex and thus restore some vision. The consequence, however, is that the consciously perceived visual field and binocularity is reduced ().

Although the visual cortex projections of the misrouted visual afferents are blocked, this information is still available for the reflex control of eyeball position and this may explain both the convergent strabismus and occasional spontaneous nystagmus present in these cases. An alternative explanation for the convergent strabismus may be the result of a compensatory attempt to obtain increased overlap of the left and right visual fields. The spontaneous nystagmus is the consequence of the misrouted information being mapped in reverse at the level of the lateral geniculate nucleus. If an animal uses this misrouted and reversed information during attempts to fix the gaze on a visual target, the consequent eyeball pursuit movements are inverted and the eye moves in the opposite direction to the target movement. Repeated eyeball pursuit movements in the wrong direction are then made, resulting in nystagmus.

Divergent strabismus (exotropia) in brachycephalic breeds

Congenital divergent strabismus (exotropia), which may be unilateral or bilateral, occurs in brachycephalic breeds, including the Boston Terrier, English Bulldog and Pekingese. Vision and eye movements are normal and the condition appears non-progressive. Although no cause has been identified, paresis or abnormal caudal insertion of the medial rectus muscle have been suggested as possible explanations.

Vestibular disease

Disorders affecting the vestibular system (discussed in more detail in Chapter 10) may result in alterations in eyeball position and movement, typically the presence of nystagmus and/or strabismus. Nystagmus is categorized as vertical, horizontal or rotatory ().

In vestibular disease the strabismus is characteristically ventrolateral in direction and can be induced or exacerbated by holding the animal’s head with the nose elevated (). Bilateral vestibular disease may cause bilateral ventrolateral strabismus on elevating the head ().

Congenital hydrocephalus

In addition to the visual deficits associated with hydrocephalus under decreased vision with intact PLRs, congenital hydrocephalus is further characterized by the presence of bilateral ventrolateral strabismus ― the ‘setting sun sign’). This ventrolateral strabismus may be the result of conformation changes of the skull and orbit secondary to the hydrocephalus, with affected puppies usually developing a domed skull with open calvarial sutures, but is more likely to be secondary to compression of cranial nerve III, as the strabismus frequently resolves some time following the placement of a corrective ventricular shunt ().

Ocular tremor secondary to cerebellar disease

Afineoculartremor, usually only evident on ophthalmoscopic assessment, may be a feature of diffuse cerebellar disease. This is thought to be a form of cerebellar intention tremor affecting the extraocular muscles.

Cavernous sinus syndrome

Cavernous sinus syndrome is the most common cause of either external ophthalmoplegia (paralysis of the extraocular muscles) or total ophthalmoplegia (paralysis of the extraocular muscles, iris and ciliary muscles). Cavernous sinus syndrome is discussed under Disorders of pupil size and function, above.

Extraocular myositis

Inflammation of the extraocular muscles, with a presumed underlying immune-mediated aetiology similar to that of masticatory myositis, occurs occasionally in dogs (). During the acute inflammatory phase, affected dogs present with exophthalmos, strabismus and decreased range of eyeball movement due to the swelling of the extraocular muscles (). During the chronic stage of the inflammatory disease, muscle tissue is largely replaced by fibrosis and then (although the exophthalmos resolves) marked strabismus often develops. Diagnosis is by demonstrating enlargement and sometimes oedema of the extraocular muscles on MRI () and ultrasound examination, demonstrating elevated muscle enzyme levels and confirming inflammatory changes on muscle biopsy (). Although biopsy of the extraocular muscles is difficult, extraocular myositis may occur as part of a wider polymyositis and therefore biopsy of the readily accessible masticatory muscles is useful in some cases. Because of the presumed underlying immune-mediated aetiology, the disorder often responds to corticosteroid therapy ().

Fibrosing esotropia (Shar Pei strabismus)

Myositis and subsequent fibrosis of the extraocular muscles (with the medial rectus muscle most commonly affected) occur in young Shar Pei dogs and have also been described in the Irish Wolfhound, Dalmatian, Golden Retriever and Akita. The disease may occur unilaterally or bilaterally and has a presumed immune-mediated basis. Because of the preferential involvement of the medial rectus muscle, affected dogs present with convergent strabismus (esotropia) and enophthalmos. The esotropia is often so severe that the cornea is obscured by the conjunctiva and vision is consequently impaired ().

Cases may respond to immunosuppressive levels of corticosteroids but surgical resection may be required in the presence of severe fibrosis of the medial rectus muscle ( ).

Retrobulbar swelling or trauma

Retrobulbar swelling or mass effect may interfere with normal eyeball movement, with affected cases usually presenting with exophthalmos, protrusion of the third eyelid () and occasionally mechanical strabismus ().


Although the clinical signs of tetanus () are usually characteristic, strabismus () and brief, intermittent protrusion of the third eyelid may occur ().

Intracranial lesions causing strabismus

Intracranial lesions may selectively affect the innervation to certain extraocular muscles, resulting in a strabismus. Forebrain lesions causing circling and a head turn may be associated with a lateral strabismus in the direction of the head turn (). The mechanism for this is uncertain; either it may reflect loss of the innervation to the extraocular musculature (in particular cranial nerve III) as a result of raised intracranial pressure, or the neurological deficits responsible for the head turn may in turn induce a lateral strabismus.

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