Clinical Orthoptics

SECTION I

1

Extraocular Muscle Anatomy and Innervation

This chapter outlines the anatomy of the extraocular muscles and their innervation and associated cranial nerves (II, V, VII and VIII).

There are four rectus and two oblique muscles attached to each eye. The rectus muscles originate from the Annulus of Zinn, which encircles the optic foramen and medial portion of the superior orbital fissure (Fig. 1.1). These muscles pass forward in the orbit and gradually diverge to form the orbital muscle cone. By means of a tendon, the muscles insert into the sclera anterior to the rotation centre of the globe (Fig. 1.2).

The extraocular muscles are striated muscles. They contain slow fibres, which produce a graded contracture on the exterior surface, and fast fibres, which produce rapid movements on the interior surface adjacent to the globe. The slow fibres contain a high content of mitochondria and oxidative enzymes. The fast fibres contain high amounts of glycogen and glycolytic enzymes and less oxidative enzymes than the slow fibres. The global layer of the extraocular muscles contains palisade endings in the myotendonous junctions, which are believed to act as sensory receptors. Signals from the palisade endings passing to the central nervous system may serve to maintain muscle tension (Ruskell 1999, Donaldson 2000).

Muscle pulleys

There is stereotypic occurrence of connective tissue septa within the orbit and stereotypic organisation of connective tissue around the extraocular muscles (Koornneef 1977, 1979). There is also stability of rectus extraocular muscle belly paths throughout the range of eye movement, and there is evidence for extraocular muscle path constraint by pulley attachment within the orbit (Miller 1989, Miller et al. 1993, Clark et al. 1999). High-resolution MRI has confirmed the presence of these attachments via connections that constrain the muscle paths during rotations of the globe (Demer 1995, Clark et al. 1997). CT and MRI scans have shown that the paths of the rectus muscles remain fixed relative to the orbital wall during excursions of the globe and even after large surgical transpositions (Demer et al. 1996, Clark et al. 1999). It is only the anterior aspect of the muscle that moves with the globe relative to the orbit.

Figure 1.1 Orbital apex.

Figure 1.2 Extraocular muscles.

Histological studies have demonstrated that each rectus pulley consists of an encircling ring of collagen located near the globe equator in Tenon fascia attached to the orbital wall, adjacent extraocular muscles and equatorial Tenon fascia by sling-like bands, which consist of densely woven collagen, elastin and smooth muscle (Demer et al. 1995, Porter et al. 1996). The global layer of each rectus extraocular muscle, containing about half of all extraocular muscle fibres, passes through the pulley and becomes continuous with the tendon to insert on the globe. The orbital layer containing the remaining half of the extraocular muscle fibres inserts on the pulley and not on the globe (Demer et al. 2000, Oh et al. 2001, Hwan et al. 2007). The orbital layer translates pulleys while the global layer rotates the globe through its insertion on the sclera. The inferior oblique muscle also has a pulley that is mechanically attached to the inferior rectus pulley (Demer et al. 1999).

The general arrangement of orbital connective tissues is uniform throughout the range of human age from foetal life to the tenth decade. Such uniformity supports the concept that pulleys and orbital connective tissues are important for the mechanical generation and maintenance of ocular movements (Kono et al. 2002).

Ocular muscles

Medial rectus muscle

This muscle originates at the orbital apex from the medial portion of the Annulus of Zinn in close contact with the optic nerve. It courses forward for approximately 40 mm along the medial aspect of the globe and penetrates Tenon's capsule roughly 12 mm from the insertion. The last 5 mm of the muscle are in contact with the eye and the insertion is at 5.5 mm from the limbus with a width of 10.5 mm. The muscle is innervated by the inferior division of the III nerve, which enters the muscle on its bulbar side. Its function is adduction of the eye (Fig. 1.3).

Figure 1.3 Medial rectus action.

Lateral rectus muscle

This muscle arises by two heads from the upper and lower portions of the Annulus of Zinn where it bridges the superior orbital fissure. It courses forward for approximately 40 mm along the lateral aspect of the globe and crosses the inferior oblique insertion. It penetrates Tenon's capsule at roughly 15 mm from the insertion and the last 7–8 mm of the muscle is in contact with the eye. The insertion is at 7 mm from the limbus with a width of 9.5 mm. The muscle is innervated by the VI nerve, which enters the muscle on its bulbar side. Its function is abduction of the eye (Fig. 1.4).

Figure 1.4 Lateral rectus action.

Superior rectus muscle

This muscle arises from the superior portion of the Annulus of Zinn and courses forward for approximately 42 mm along the dorsal aspect of the globe forming an angle of 23° with the sagittal axis of the globe. Superiorly, it is in close contact with the levator muscle. It penetrates Tenon's capsule at roughly 15 mm from the insertion and the last few mms of the muscle are in contact with the eye. The insertion is at 7.7 mm from the limbus with a width of 11 mm. The muscle is innervated by the superior division of the III nerve, which enters the muscle on its bulbar side. Its functions are elevation, intorsion and adduction of the eye (Fig. 1.5).

Figure 1.5 Superior rectus action. The course of the superior rectus is at an angle of 23° to the medial wall of the orbit. Actions in adduction are principally intorsion and adduction; in the primary position, actions are elevation, intorsion and adduction; action in abduction is principally elevation.

Figure 1.6 Inferior rectus action. The course of the inferior rectus is at an angle of 23° to the medial wall of the orbit. In adduction, the actions are principally extorsion and adduction; in the primary position, actions are depression, extorsion and adduction; action in abduction is principally depression.

Inferior rectus muscle

This muscle arises from the inferior portion of the Annulus of Zinn and courses forward for approximately 42 mm along the ventral aspect of the globe forming an angle of 23° with the sagittal axis. It penetrates Tenon's capsule roughly 15 mm from the insertion and the last few millimetres of the muscle are in contact with the eye as it arcs to insert at 6.5 mm from the limbus. The width of insertion is 10 mm. The muscle is innervated by the inferior division of the III nerve, which enters the muscle on its bulbar side. Its functions are depression, extorsion and adduction of the eye (Fig. 1.6).

Superior oblique muscle

This muscle originates from the orbital apex from the periosteum of the body of the sphenoid bone, medial and superior to the optic foramen. It courses forward for approximately 40 mm along the medial wall of the orbit to the trochlea (a V-shaped fibrocartilage that is attached to the frontal bone). The trochlear region is described by Helveston et al. (1982).

The muscle becomes tendonous roughly 10 mm posterior to the trochlea and is encased in a synovial sheath through the trochlea. From the trochlea, it courses posteriorly, laterally and downwards forming an angle of 51° with the visual axis of the eye in the primary position. It passes beneath the superior rectus and inserts on the upper temporal quadrant of the globe ventral to the superior rectus. Its insertion is fanned out in a curved line 10–12 mm in length. The muscle is innervated by the IV nerve that enters the muscle on its upper surface roughly 12 mm from its origin. Its functions are intorsion, depression and abduction of the eye (Fig. 1.7).

Figure 1.7 Superior oblique action. The course of the superior oblique tendon is at an angle of 51° to the medial wall of the orbit. Action in adduction is depression; in the primary position, actions are depression, intorsion and abduction; in abduction, action is intorsion.

Inferior oblique muscle

This muscle arises from the floor of the orbit from the periosteum covering the anteromedial portion of the maxilla bone. It courses laterally and posteriorly for approximately 37 mm, forming an angle of 51° with the visual axis. It penetrates Tenon's capsule near the posterior ventral surface of the inferior rectus, crosses the inferior rectus and curves upwards around the globe to insert under the lateral rectus just anterior to the macular area. The muscle is innervated by the inferior division of the III nerve that enters the muscle on its bulbar surface. Its functions are extorsion, elevation and abduction of the eye (Fig. 1.8).

Figure 1.9 illustrates the muscle insertions in relation to the anterior segment of the eye. Figure 1.10 illustrates the positions of main action of each extraocular muscle and Table 1.1 illustrates all primary, secondary and tertiary muscle actions.

Figure 1.8 Inferior oblique action. The course of the inferior oblique is at an angle of 51° to the medial wall of the orbit. Action in adduction is elevation; actions in the primary position are elevation, extorsion and abduction; in abduction, action is extorsion.

Figure 1.9 Extraocular muscle insertions. SR, superior rectus; MR, medial rectus; LR, lateral rectus; IR, inferior rectus.

Figure 1.10 Cardinal positions of gaze – position of main action of extraocular muscles.

Levator palpebral superioris

This muscle originates from the under surface of the lesser wing of sphenoid bone above and in front of the optic foramen by a short tendon that blends with the origin of the superior rectus. It runs forward and changes directly from horizontal to vertical at the level of the equator of the globe. At approximately 10 mm above the superior margin of the tarsus, it divides into anterior and posterior lamellae. The anterior lamellae form the levator aponeurosis that is inserted into the lower third of the entire length of the anterior surface of the tarsus. Its fibres extend to the pre-tarsal portion of the orbit and skin. The posterior lamellae form Muller's muscle that is attached inferiorly to the superior margin of the tarsus.

Table 1.1 Primary, secondary and tertiary extraocular muscle actions.

Innervation

The extraocular muscles are innervated by the III, IV and VI nerves.

III nerve

The III nerve (third/oculomotor) supplies the superior rectus, inferior rectus, medial rectus, inferior oblique and levator muscles. Its visceral fibres innervate the ciliary muscle and sphincter pupillary muscle that synapse in the ciliary ganglion.

The nuclei are in the mesencephalon at the level of the superior colliculus. There is an elongated mass of cells that form the nuclei. Peripheral motor neurones innervate multiply innervated extraocular muscle fibres and central motor neurones innervate single innervated muscle fibres. Dorsal nucleus fibres pass to the ipsilateral inferior rectus, intermediate nucleus fibres pass to the ipsilateral inferior oblique, ventral nucleus fibres pass to the ipsilateral medial rectus, paramedian nucleus fibres pass to the contralateral superior rectus, central caudal nucleus fibres pass to both levator muscles, and the anterior median/Edinger-Westphal nucleus contains the parasympathetic fibres (Bienfang 1975). The nerve fibres emerge from the mesencephalon ventrally where they are closely associated with the posterior cerebellar and superior cerebral arteries. The nerve courses forward through the subarachnoid space to pierce the dura mater at the posterior clinoid process and enter the cavernous sinus.

The third cranial nerve pathway is supplied by branches of the basilar artery including the superior cerebellar arteries, posterior cerebral arteries, mesencephalic perforating arteries, collicular and accessory arteries in the midbrain; the thalamoperforating arteries supplemented by the superior cerebellar artery, posterior communicating artery and posterior cerebral artery in the proximal nerve pathway; and inferior cavernous sinus arteries, medial posterior choroidal artery and tentorial arteries in the distal nerve pathway (Marinkovic & Gibo 1994, Cahill et al. 1996).

IV nerve

The IV nerve (fourth/trochlear) supplies the superior oblique. The nucleus lies in the mesencephalon at the level of the inferior colliculus. The nerve fibres decussate (although about 3% do not decussate but retain ipsilateral projection) and emerge from the brainstem dorsally. The nerves curve around the brainstem and course forward through the subarachnoid space to pierce the dura mater and enter the cavernous sinus.

The fourth cranial nerve pathway is in close association or contact with branches of the basilar artery in the midbrain including the superior cerebellar artery, vernian artery and collicular artery. It is supplied by posterior cerebral artery and posterior communicating artery in its proximal pathway and by the internal carotid artery, medial posterior choroidal artery and tentorial arteries in the distal pathway (Marinkovic et al. 1996, Yousry et al. 2002).

VI nerve

The VI nerve (sixth/abducens) supplies the lateral rectus. The nucleus is situated in the pons in the floor of the IV ventricle near the midline, medial to VIII nucleus and proximal to the paramedian pontine reticular formation. The medial longitudinal fasciculus lies medial to the nucleus. The nerve fibres emerge from the brainstem ventrally and course forward and laterally over the petrous tip of the temporal bone and under the petrosphenoid ligament. The nerve pierces the dura mater to enter cavernous sinus. The nerve divides into two distinct trunks along its pathway between the brainstem and the lateral rectus muscle.

The sixth cranial nerve pathway is supplied with branches of the basilar artery including the anterior inferior cerebellar artery, posterior inferior cerebellar artery, pontomedullary artery and accessory arteries in the pons and clivus region. The distal pathway is supplied by the internal auditory artery, anterolateral artery and tentorial artery (Marinkovic et al. 1994, Yousry et al. 1999).

Common nerve pathways

The III, IV and VI nerves course forward together in the lateral aspect of the cavernous sinus entering the orbit through the superior orbital fissure. The III and VI nerves enter within the muscle cone.

The III nerve divides into the superior and inferior divisions. The superior division enters the superior rectus on its bulbar surface and passes through the muscle to terminate in the levator muscle. The inferior branch supplies the medial rectus, inferior rectus, and then passes beneath the optic nerve to the floor of the orbit and terminates in the inferior oblique. The terminal branch also sends a short branch to the ciliary ganglion. The VI nerve passes forward and laterally to enter the lateral rectus bulbar surface. The IV nerve enters through the superior orbital fissure laterally and superior to the Annulus of Zinn. It passes anteriorly and medially crossing the III nerve, levator muscle and superior rectus, and enters the superior oblique on its orbital surface.

Associated cranial nerves

Autonomic nerves

These nerves supply smooth muscles and source ganglia. Smooth muscles include the muscular blood vessels, Muller's muscle, pulley smooth muscle, sclera myofibroblasts and choroidal smooth muscle (Demer et al. 1997). Source ganglia include the pterygopalatine ganglion, ciliary ganglion and superior cervical ganglion.

Proprioceptive nerves

These nerves consist of palisade endings and spindles. Palisade endings innervate myotendonous cylinders at the termination of each multiply innervated global layer fibre in the rectus extraocular muscles (Lienbacher et al. 2011). Spindles are composed of several orbital layer myofibres and have nerve terminals within a very thin capsule.

II nerve

The II (optic) nerve serves the sensory function of vision. Its pathway commences in the eye at the receptor cells in the retina. There is a complex arrangement of nuclei and processes from three layers of photoreceptors, bipolar cells and ganglion cells. There are in the region of 1.2–1.5 million retinal ganglion cells and 105 million photoreceptors with an average ratio of 1 retinal ganglion cell to 100 photoreceptors. At the fovea, the ratio is 1:1 for retinal ganglion cells to photoreceptors.

Retinal ganglion cells include midget (parvocellular), parasol (magnocellular), koniocellular and other cells. Midget ganglion cells are responsible for slow conduction of impulses with low temporal resolution and require high contrast stimuli. Parasol ganglion cells are responsible for fast conduction of impulses with high temporal resolution and requiring low contrast stimuli. Midget cells have colour selectivity whereas parasol cells have little or no colour selectivity. Koniocellular cells have moderate conduction velocity and moderate sensitivity to light and spatial resolution. They have some colour selectivity and may have a role in motion detection and visual attention. Other cells include light reflex ganglions and photosensitive neurones.

Retinal ganglion cells pass in nerve fibre bundles to the optic discs and pass from each eye to the intracranial cavity along the optic nerves. The optic nerves merge in the optic chiasm where there is crossing of nasal retinal fibres. Ipsilateral temporal and contralateral nasal fibres pass along the optic tracts to the lateral geniculate nuclei where the first synapse of retinal nerve fibres occurs. The post-synaptic fibres then pass via the optic radiations to the visual cortex. The visual cortex (V1) occupies the calcarine sulcus in the occipital lobe and is the primary visual area.

V nerve

The V nerve (fifth/trigeminal) serves sensory and motor functions and the nuclei extend through the pons down into the medulla. The sensory nerve has three branches.

Sensory nerves

The ophthalmic division serves the sensory function to the lacrimal gland, conjunctiva, forehead, eyelids, anterior scalp and mucous membranes of the nose. The sensory fibres pass through the superior orbital fissure to the cavernous sinus and pass inferiorly to the trigeminal ganglion, which is located under the cavernous sinus in Meckel's cave (a groove in the skull). Fibres pass from the ganglion posteriorly to the pons to the trigeminal nuclei.

The maxillary division serves the sensory function to the cheeks, upper gums and teeth and lower eyelids. The sensory fibres pass through the foramen rotundum, underneath the cavernous sinus to the trigeminal ganglion and then onto the nuclei in the pons.

The mandibular division serves the sensory function to the teeth, gums of the lower jaw, pinna of ears, lower lip and tongue. The sensory fibres pass through the foramen ovale underneath the cavernous sinus to the trigeminal ganglion and then onto the nuclei in the pons.

Motor nerves

Motor fibres of the V nerve serve the muscles of mastication. The motor nuclei are located in the pons near the seventh nerve nuclei and aqueduct. Nerve fibres leave ventrally and medially and pass anteriorly to the trigeminal ganglion, through the foramen ovale to the muscles of mastication.

VII nerve

The VII nerve (seventh/facial) serves sensory and motor functions. The VII nerve has central connections to the motor face area of the cerebral cortex and the nuclei are divided into upper and lower halves. Corticobulbar fibres double decussate for the upper face but there is single decussation for lower face fibres.

Sensory fibres

Ganglion cells supply taste buds in the palate and tongue and sensory fibres are also present in the skin, in and around the external acoustic meatus. Fibres pass to the geniculate ganglion situated in the internal auditory meatus and pass back to the pons.

Motor fibres

The nuclei are located in the lateral part of the pons and fibres loop around the abducens nuclei, forming the facial colliculus, before leaving the pons ventrally. Fibres pass anteriorly and enter the internal auditory meatus. The nerve enters a narrow bony canal above the labyrinth and descends to the stylomastoid foramen where a branch supplies the stapedius muscle. It leaves the skull and supplies the facial muscles (frontal, zygomatic, buccal, mandibular marginal and cervical branches).

VIII nerve

The VIII nerve (eight/auditory) serves the sensory function of hearing and balance.

Cochlear nerve (hearing)

Receptor cells are hair cells in the organ of Corti. Fibres pass from the spiral ganglion along the Cochlear nerve through the internal auditory meatus to the cisterna pontis, to the inferior cerebellar peduncle and to the cochlear vestibular nuclei in the pons/medulla.

Vestibular nerve (balance)

Receptor cells are hair cells in the utricles, saccules and semicircular canals. Fibres pass from Scarpa's ganglion along the vestibular nerve through the internal auditory meatus to the cisterna pontis and to the vestibular nuclei in the pons/medulla. Within the internal auditory meatus, the vestibular and cochlear nerves are in close association with the facial nerve. Within the acoustic foramen and intracranial cavity, these nerves are closely associated with both the sixth and facial nerves.

References

Bienfang DC. Crossing axons in the third nerve nucleus. Investigative Ophthalmology and Visual Science. 1975; 14: 927–31.

Cahill M, Bannigan J, Eustace P. Anatomy of the infranuclear blood supply to the intracranial oculomotor nerve. British Journal of Ophthalmology. 1996; 80: 177–81.

Clark RA, Miller JM, Demer JL. Location and stability of rectus muscle pulleys. Muscle paths as function of gaze. Investigative Ophthalmology and Visual Science. 1997; 38: 227–40.

Clark RA, Rosenbaum AL, Demer JL. Magnetic resonance imaging after surgical transposition defines the anteroposterior location of the rectus muscle paths. Journal of American Association for Paediatric Ophthalmology and Strabismus. 1999; 3: 9–14.

Demer JL, Clark RA, Miller JL. Magnetic resonance imaging (MRI) of the functional anatomy of the inferior oblique (IO) muscle. (ARVO abstract). Investigative Ophthalmology and Visual Science. 1999; 40(4): S772.

Demer JL, Miller JM, Poukens V. Surgical implications of the rectus extra ocular muscle pulleys. Pediatric Ophthalmology and Strabismus. 1996; 33: 208–18.

Demer JL, Miller JM, Poukens V, Vinters HV, Glasgow BJ. Evidence for fibromuscular pulleys of the recti extra ocular muscles. Investigative Ophthalmology and Visual Science. 1995; 36: 1125–36.

Demer JL, Oh SY, Poukens V. Evidence for active control of rectus extra ocular muscle pulleys. Investigative Ophthalmology and Visual Science. 2000; 41: 1280–90.

Demer JL, Poukens V, Miller JM, Micevych P. Innervation of extraocular pulley smooth muscle in monkey and human. Investigative Ophthalmology and Visual Science. 1997; 38: 1774–85.

Donaldson IM. The functions of the proprioceptors of the eye muscles. Philosophical Transactions of the Royal Society of London Series B Biological Sciences. 2000; 355: 1685–754.

Helveston EM, Merriam WW, Ellis FD, Shellhamer RH, Gosling CG. The trochlea: a study of the anatomy and physiology. Ophthalmology. 1982; 89: 124–33.

Hwan Lim K, Poukens V, Demer J. Fascicular specialisation in human and monkey rectus muscles: evidence for anatomic independence of global and orbital layers. Investigative Ophthalmology and Visual Science. 2007; 48: 3089–97.

Kono R, Poukens V, Demer JL. Quantitative analysis of the structure of the human extra ocular muscle pulley system. Investigative Ophthalmology and Visual Science. 2002; 43: 2923–32.

Koornneef L. New insights in the human orbital connective tissue; result of a new anatomical approach. Archives of Ophthalmology. 1977; 95: 1269–73.

Koornneef L. Orbital septa: anatomy and function. Ophthalmology. 1979; 86: 876–80.

Lienbacher K, Mustari M, Ying HS, Buttner-Ennever JA, Horn AK. Do palisade endings in extraocular muscles arise from neurons in the motor nuclei? Investigative Ophthalmology and Visual Science. 2011; 52: 2510–19.

Marinkovic S, Gibo H. The neurovascular relationships and the blood supply of the oculomotor nerve: the microsurgical anatomy of its cisternal segment. Surgical Neurology. 1994; 42: 505–16.

Marinkovic SV, Gibo H, Stimec B. The neurovascular relationships and the blood supply of the abducent nerve: surgical anatomy of its cisternal segment. Neurosurgery. 1994; 34: 1017–26.

Marinkovic S, Gibo H, Zelic O, Nikodijevic I. The neurovascular relationships and the blood supply of the trochlear nerve: surgical anatomy of its cisternal segment. Neurosurgery. 1996; 38: 161–69.

Miller JM. Functional anatomy of normal human rectus muscles. Vision Research. 1989; 29: 223–40.

Miller JM, Demer JL, Rosenbaum AL. Effect of transposition surgery on rectus muscle paths by magnetic resonance imaging. Ophthalmology. 1993; 100: 475–87.

Oh SY, Poukens V, Demer JL. Quantitative analysis of extra ocular muscle global and orbital layers in monkey and human. Investigative Ophthalmology and Visual Science. 2001; 42: 10–6.

Porter JD, Poukens V, Baker RS, Demer JL. Structure function correlations in the human medial rectus extra ocular muscle pulleys. Investigative Ophthalmology and Visual Science. 1996; 37: 468–72.

Ruskell GL. Extraocular muscle proprioceptors and proprioception. Progress in Retinal and Eye Research. 1999; 18: 269–91.

Yousry I, Camelio S, Wiesmann M, Schmid UD, Moriggl B, Brückmann H, Yousry TA. Detailed magnetic resonance imaging anatomy of the cisternal segment of the abducent nerve: Dorello's canal and neurovascular relationships and landmarks. Journal of Neurosurgery. 1999; 91: 276–83.

Yousry I, Moriggl B, Dieterich M, Naidich TP, Schmid UD, Yousry T. MR anatomy of the proximal cisternal segment of the trochlear nerve: neurovascular relationships and landmarks. Radiology. 2002; 223: 31–38.

Further reading

Apt L. An anatomical evaluation of rectus muscle insertions. Transactions of the American Ophthalmological Society. 1980; 78: 365–75.

Bach-y-Rita P. Neurophysiology of extraocular muscle. Investigative Ophthalmology. 1967; 6: 229–34.

Bjork A. Electrical activity of human extrinsic eye muscles. Experientia. 1952; 8: 226–7.

Brandt DE, Leeson CR. Structural differences of fast and slow fibers in human extraocular muscle. American Journal of Ophthalmology. 1966; 62: 478–87.

Duke-Elder S, Wybar KC. The anatomy of the visual system. System of Ophthalmology, Volume 2. St. Louis, MO, Mosby-Year Book, Inc. 1961.

Howe L. Insertion of the ocular muscles. Transactions of the American Ophthalmological Society. 1902; 9: 668–78.

Scobee RC. Anatomic factors in the etiology of strabismus. American Journal of Ophthalmology. 1948; 31: 781–95.

Sevel P. The origins and insertions of the extraocular muscles : development, histologic features and clinical significance. Transactions of the American Ophthalmological Society. 1986; 84: 488–526.

Souza-Dias C, Prieto-Diaz J, Uesegui CF. Topographical aspects of the insertions of the extraocular muscles. Journal of Pediatric Ophthalmology and Strabismus. 1986; 23: 183–9.

2

Binocular Single Vision

Binocular single vision is the ability to use both eyes simultaneously so that each eye contributes to a common single perception.

Normal binocular single vision occurs with bifoveal fixation and normal retinal correspondence in everyday sight. Abnormal binocular single vision occurs in the absence of bifoveal fixation usually with abnormal retinal correspondence in everyday sight.

Worth's classification

Binocular single vision can be classified into three stages:

1. Simultaneous perception and superimposition

2. Fusion

3. Stereoscopic vision

Simultaneous perception is the ability to perceive simultaneously two images, one formed on each retina. Superimposition is the simultaneous perception of the two images formed on corresponding areas, with the projection of these images to the same position in space. This may occur whether the correspondence is normal or abnormal. If fusion is absent, two similar images are seen as separate but superimposed and no fusion range is demonstrable.

Fusion may be sensory or motor. Sensory fusion is the ability to perceive two similar images, one formed on each retina, and interpret them as one. Motor fusion is the ability to maintain sensory fusion through a range of vergence, which may be horizontal, vertical or cyclovergence. Stereoscopic vision is the perception of the relative depth of objects on the basis of binocular disparity.

Development

The initial ocular position in the human neonate (Rethy 1969) is often one of divergence. In the early postnatal period, divergence decreases towards a binocular coincidental position resulting in similar visual stimulation of each eye, which in turn facilitates firing of binocular driven cells/neurones in the striate cortex (Hubel & Wiesel 1968), and once the straight position is attained, this is maintained preferentially. The globes are approximately 73% of adult size in infancy and the lens is relatively less convex. The size of eye (lens and cornea) renders the eye hypermetropic, which is overcome by amplitude of accommodation. Other developments include accommodation, ocular muscles and nerve supply, visual pathway and foveal development. Binocular single vision is dependent on retinal correspondence and disparity. Eighty percent of the striate cortex neurones are driven from either eye (binocular driven cells) whilst 10% are driven by the right eye only and 10% by the left eye only (Hubel & Wiesel 1968).

Some sensory and motor binocular associations exist in the visual system of the newborn. The binocular reflexes relate to the development of binocular single vision on the basis of continued use of the visual system. Postural reflexes are inborn and must be present if binocular single vision is to develop:

a. Static reflexes compensate for changes in position of the head relative to the body.

b. Statokinetic reflexes compensate for changes in head position relative to space.

Fixation reflexes form the mechanism from which binocular vision develops:

a. The primary fixation reflex achieves foveal fixation in either eye and is present at birth.

b. The refixation reflex allows foveal refixation from target to target and maintenance of foveal fixation on a moving target. This develops from 6 to 8 weeks of age. Most neonates are capable of locating and briefly fixing a moving target, and the eyes can move in a coarsely conjugate fashion. Thus, the refixation reflex, although unstable, appears to be present at birth, despite the fact that in the first months of life the fovea is still poorly differentiated.

c. The conjugate fixation reflex, where the eyes learn to move together during versions, is the first reflex by which the eyes move binocularly and develops from 2 to 3 weeks of age.

d. The disjugate fixation reflex allows binocular vision to be maintained through the range of vergence movements that follow changes of fixation distance and develops from 2 to 3 months of age.

e. The corrective fusion reflex allows binocular vision to be maintained under conditions of stress, such as overcoming prisms in clinical testing situations, and develops from 3 to 6 months of age.

f. Kinetic reflexes maintain binocular single vision through controlled accommodation and convergence.

The newborn does not converge the eyes, but the attempt to converge may be seen as early as 1 month after birth. The macula is poorly developed at birth with incomplete migration of retinal ganglion cells from the foveal area. Saccadic eye movements are poorly controlled, and several movements are required to achieve foveation. By 5–6 weeks of age, the conjugate fixation reflex is developed, and the two eyes conjugately fix an object and follow it over a considerable range for at least a few seconds. Density of cones in the fovea increases with myelination of nerve fibres in the visual pathway. Smooth pursuit eye movement and colour vision develop from 2 months. Accommodation develops rapidly from 2–3 months and approaches the same levels of accuracy as adults (Horwood & Riddell 2004). Optokinetic nystagmus is asymmetrical up to 3 months with absent nasal to temporal movement, after which there is progression to symmetrical motion processing by the age of 6 months (Bosworth & Birch 2007). By 6 months, the conjugate movements of binocular vision become accurate and convergence is well developed. By 6–8 months, a fusional movement can be detected by placing a small prism over either eye.

A critical period occurs in the development of the visual system during which the visual system is susceptible to abnormal visual input (Daw 1998). The period of normal visual development is up to 5 years of age.

Retinal correspondence

This concerns the retinal areas of each eye that have the same visual direction during binocular vision.

Normal retinal correspondence

This is a binocular condition in which the fovea and areas on the nasal and temporal side of one retina correspond to and have, respectively, common visual directional sensitivity with the fovea and temporal and nasal areas of the retina of the other eye. Normal retinal correspondence is the normal state in which the visual direction of each fovea is the same (Flom & Weymouth 1961, Flom & Kerr 1967) (Fig. 2.1).

Figure 2.1 Projection in normal retinal correspondence with normal binocular single vision. Stimulation of corresponding points in both eyes results in localisation of the stimulus in the same direction in space. Both fovea, FL and FR, are corresponding points as are points on temporal and nasal retinas, TL and NR, NL and TR.

Abnormal retinal correspondence

This is a binocular condition in which there is a change in visual directional sensitivity such that the fovea of the fixing eye has a common visual directional sensitivity with an area other than the fovea of the deviating eye (Burian 1951). The pairing of all retinal areas is similarly changed. The condition may occur whichever eye is used for fixation (Fig. 2.2).

Figure 2.2 Projection in abnormal retinal correspondence with right esotropia. O is the fixation target. FL and FR are the fovea of both eyes and P is the pseudofovea of the right eye. FL and P are corresponding points as the right eye undergoes sensory adaptation with abnormal retinal correspondence. Stimulation of these corresponding points results in a single perception of the fixation target.

Harmonious abnormal retinal correspondence is present where the angle of anomaly is equal to the objective angle, and the subjective angle is zero. Unharmonious abnormal retinal correspondence is present where the angle of anomaly is different from the objective angle. The angle of anomaly is the difference between the objective and subjective angles of deviation. Abnormal retinal correspondence is present in constant manifest strabismus usually of a small angle less than 20 prism dioptres.

Physiology of stereopsis

The locations of all points in space that are imaged on corresponding retinal points are termed the horopter. Panum's space is a narrow band around the horopter within which object points give rise to binocular single vision. Objects are seen as single even though the object stimulates slightly disparate retinal elements.

Panum's area is the retinal area surrounding one corresponding retinal point within which disparity of correspondence may occur, whilst maintaining binocular single vision. Binocular single vision is the result not of a rigid point-to-point correspondence but of a point-to-area relationship. The amount of foveal image disparity that permits fusion is small, and disparity increases gradually from the fovea to the periphery. Panum's area is narrow at the fixation point and widens towards the periphery. The horizontal area at the fovea is approximately 6–10 minutes, and this increases towards the periphery measuring approximately 30–40 minutes at 12° from the fovea. It may be larger than this as moving random-dot stereograms have shown fusion of disparities of 2°–3° (Hyson et al. 1983, Erkelens & Collewjin 1985, Piantanida 1986). Increases can be related to anatomical and physiological differences known to exist between the foveal cone system and the rod and cone system of the peripheral retina. The increase in Panum's area parallels the increase in size of the retinal receptive fields. Performance with motor skills is related to the level of stereoacuity in that performance is considerably worse in the absence of stereopsis (O’Connor et al. 2010).

Physiological diplopia

This is a type of diplopia that exists in the presence of binocular vision. It consists of the appreciation that a near object appears double when a distant object is fixated (heteronymous or crossed diplopia), and a distant object appears double when a near object is fixated (homonymous or uncrossed diplopia) (Figs. 2.3 and 2.4).

Figure 2.3 Projection in heteronymous diplopia. X is the fixation target, which is seen as a single image by the corresponding fovea FL and FR. O is an object between the fixation target and the eyes that stimulates non-corresponding temporal retinal points, TL and TR, resulting in crossed physiological diplopia.

Figure 2.4 Projection in homonymous diplopia. X is the fixation target seen as a single image by the corresponding foveal points, FL and FR. O is an object further away than the fixation target that stimulates non-corresponding nasal retinal points, NL and NR, resulting in uncrossed physiological diplopia.

All objects outside Panum's space give rise to physiological diplopia. Physiological diplopia indicates that the patient is capable of using both eyes and is not suppressing one eye.

Fixation disparity

Fixation disparity is a phenomenon that occurs in binocular single vision in which the image is seen singly despite a slight underconvergence or overconvergence of the visual axes; the fixation target is imaged on slightly disparate retinal points within Panum's area. There is an apparent displacement of uniocularly observed details of targets whose other details are fused binocularly.

The phenomenon can be demonstrated clinically when targets, which have mainly identical features but also contain some dissimilar features, are presented to the eyes. Fusion occurs for the identical features, but a displacement occurs for the dissimilar features in the direction of the projection of the existing heterophoria.

Fixation disparity may be involved in the maintenance of binocular single vision. Disparity of retinal images causes fusional movements. At the end of a fusional movement, not all the disparity is annulled; a small disparity remains, which acts as an error signal. The residual fixation disparity may control the direction and strength of the innervation that maintains the new binocular position.

When visual objects are fused by being imaged on horizontally disparate points, within Panum's space, stereopsis results. The greater the horizontal disparity, the greater the depth effect. A vertical disparity produces no stereoscopic effect (Fig. 2.5).

Figure 2.5 Projection in stereopsis. O is the fixation target, which projects directly to the fovea of the left eye. This should also project directly to the right eye. However, due to slight under- or overconvergence of the right eye, direct stimulation may not occur, resulting in fixation disparity. In this figure, there is slight overconvergence of the right eye with stimulation of a point just nasal to the fovea. As this point falls within Panum's area, the stimuli to either eye are fused, resulting in a single image of the fixation target.

Local stereopsis occurs where localised features of objects are extracted from a visual scene and assigned relative depth values, indicating that one feature is further away from another. Global stereopsis occurs where the perception of whole objects in stereoscopic depth is achieved.

Monocular clues are important in the estimation of the relative distance of visual objects and are active in monocular as well as binocular vision. These clues are the result of experience:

Motion parallax: Targets further away move more in the horizontal plane than nearer targets.

Linear perspective: Objects of the same size decrease in size the further away they are.

Overlapping contours: Overlap in images determines which is in front or behind the other.

Distribution of highlights and shadows.

Size of known objects: When size is known, the relative distance can be determined.

Aerial perspective: Knowledge of colours and hues.

Fusion

Central fusion occurs when the images of an object are perceived by each fovea, and the area surrounding them, and are unified. This produces bifoveal binocular single vision with fusion. The highest levels of stereoacuity are associated with central fusion. Peripheral fusion results from unification of images outside the central region. Gross stereopsis is associated with peripheral fusion. Central and peripheral fusion usually function simultaneously. A patient's sensory status is considered crucial to the long-term stability of a successful surgical outcome. Fusion serves as the glue to maintain alignment (Burian 1941, Kushner & Morton 1992, Morris et al. 1993). It indicates the patient's ability to control their latent tendency for the eyes to drift. In order for fusion to occur, the images presented to each eye must be similar in size, brightness and sharpness. Peripheral fusion contributes significantly to the maintenance of binocular single vision (Bielchowsky 1935). If this is destroyed, even while maintaining good central vision, disruption of binocularity occurs.

When measured with large field stimuli, 8° of motor cyclovergence has been demonstrated in normals (Guyton 1988). Therefore, individuals can use this ability to fuse torted images without diplopia. This ability derives from the receptive fields in the peripheral retina being large compared to those in the central retina. This amount of motor cyclovergence combined with the 8° of sensory cyclofusion allows norms to fuse up to 16° of cyclodisparity.

Retinal rivalry

When dissimilar images are presented to corresponding retinal areas, fusion becomes impossible and retinal rivalry occurs. When dissimilar targets are presented to each eye, the patient will see one target, then the other, or a mosaic of contours, but not both simultaneously. Retinal rivalry is a physiological finding in binocular single vision and is distinct from suppression as it indicates a state of fluctuation between competing components. Retinal rivalry may also be produced by differences in colour and unequal illumination.

Suppression

Suppression is the mental inhibition of visual sensations of one eye in favour of those of the other eye when both eyes are open. This may occur in binocular single vision and commonly in manifest strabismus.

Physiological suppression is present in binocular single vision. Blurred images are suppressed when concentrating on one particular object. Pathological suppression is present in manifest strabismus and may alternate with alternating deviations (Fig. 2.6).

Figure 2.6 Projection in right esotropia with suppression. O is the fixation target, which stimulates the fovea of the left eye and a nasal retinal point of the right eye. The nasal retinal point is suppressed, which ensures a single perception of the fixation target.

Suppression may occur with interocular blur, suspension, binocular retinal rivalry or permanent suppression. Interocular blur