Extraocular Muscles & Headaches & Migraines
Anatomy of the extraocular muscle
There are seven extraocular muscles.
Four rectus muscles:
Medial rectus muscle.
Attachments: common tendinous ring* & dural sheath of the optic nerve --> sclera. Action: adducts eye.
2. Lateral rectus muscle.
Attachments: common tendinous ring* > greater wing of sphenoid --> sclera. Action: abducts eye
3. Superior rectus muscle.
Attachments: common tendinous ring* & dural sheath of optic nerve --> upper part of the sclera. Action: elevates and adducts cornea. Also medially rotates.
4. Inferior rectus muscle.
Attachments: common tendinous ring* --> sclera. Action depression > adduction & lateral rotation cornea. Depresses lower eyelid.
*: The common tendinous ring is a fibrous ring that surrounds the optic canal and part of the superior orbital fissure at the apex of the orbit. It gives origin to the four recti muscles.
The optic nerve and opthalamic artery enter the orbit via the optic canal lying within the tendinous ring.
Two oblique muscles:
Superior oblique muscle.
Attachments: body of sphenoid & tendinous attachment of superior rectus --> trochlea --> sclera. Action: elevates posterior part of eyeball and depresses anterior part of eyeball < in adducted position. Abducts eye and intorts eyeball.
2. Inferior oblique muscle.
Attachments: orbital surface of the maxilla --> sclera. Action: depresses the posterior part of the eyeball and elevates the anterior part of the eyeball < in adducted position. Abducts and extorts the eye.
Wright (1999) describes the intervening connective tissue between the superior rectus and medial rectus muscles that envelopes the superior oblique tendon as the intermuscular septum.
Robertson (1983) identified an intermuscular fascial septum between the sheaths of the inferior oblique and the lateral and inferior recti. This fascia forms a sling for the inferior oblique sheath and helps to maintain its line of action.
Levator palpebrae superioris.
Attachments: lesser wing sphenoid --> anterior surface tarsus, (--> orbicularis oculi) skin of upper eyelid & conjunctiva (via the common sheath of fascia between levator palpebrae superioris and superior rectus).
Aponeurosis of the levator palpebrae superioris attaches medially to the medial palpebral ligament & laterally to the orbital tubercle of the zygomatic bone (Standring 2015).
Action: primarily responsible for eyelid elevation.
Ettl et al (1996) identified the connective tissue system of the levator palpebrae superioris muscle as consisting of:
i. Network of radial septa connecting the fascial sheath of the levator palpebrae superioris with the periorbit of the orbital roof.
ii. Septa surrounding the sheath of the levator palpebrae superioris.
iii. Superior transverse ligament (Whitnall's ligament).
iv. Common sheath of fascia between the levator palpebrae superioris superiorly and the superior rectus muscle inferiorly. The anterior band-like component of this common sheath of fascia is called transverse superior fascial expansion of the superior rectus muscle and levator palpebrae superioris. Extending between these two muscles the sheath attaches on to the conjunctiva.
The transverse superior fascial expansion of the superior rectus muscle and levator palpebrae superioris:
i. Mainly extends from the connective tissue of the trochlea --> fascia of the lacrimal gland.
ii. Sends connective tissue attachments to the medial and lateral rectus muscle.
iii. Blends with Tenon's capsule.
iv. Send expansions inferiorly to insert into the connective tissue of the medial and lateral rectus muscle.
v. Blends with the superolateral intermuscular septum (? the lateral rectus-superior rectus muscle band, Nam et al 2019).
The relationship of Tenon’s capsule to the common sheath of the levator palpebrae superioris/superior rectus, superior transverse ligament is discussed in the section ‘Tenon’s capsule’.
Myofascial continuity from the neck to the eye
There is a direct myofascial link whereby tension in the posterior superficial cervical fascia pulls on and stimulates mechanoreceptors in Muller’s (supratarsal) muscle via the occipitofontalis and levator palpebrae superioris (Bordoni & Zanier, 2014). Muller's (supratarsal) muscle is the smooth muscle fibers of the levator palpebrae superioris attached to the medial and lateral rectus muscle pulley (refer 'Tenon's capsule') (Kakizaki et al 2010).
To extend the myofascial chain from the superficial cervical fascia to the Levator Palpebrae Superioris further the Levator Palpebrae Superioris and superior rectus muscle is connected with Tenon’s capsule. As well as forming a fascial sleeve for the extraocular muscles Tenon’s capsule surrounds the optic nerve where it terminates in the eye, blending with the meningeal tissue.
Could it be that tension in the fascial area in the upper cervical spine affects the movement of the eyeball, altering the visual field and posture, or causing dysfunction related to the fascial traction on the optic nerve, with resultant alteration in the ocular reflexes? (Bordoni Zanier 2014).
Tenon’s capsule
Tenon’s capsule is a thin fascial sheath (fascia bulbi) that envelopes the eyeball from the optic nerve to the corneoscleral junction. The optic nerve and the extraocular muscles pass through Tenon's capsule. The fascia that makes up Tenon's capsule blends with the meningeal tissue of the optic nerve as well as the extraocular muscles.
The extraocular muscles pierce Tenon’s capsule (fascia bulbi). This fascia reflects back as a sleeve or tubular sheath around each muscle. The muscles pass straight through this sheath to insert on to the sclera of the eye.
This fascial tubular sheath encircling each rectus muscle creates a pulley (Nam et al 2019). These pulleys function to constrain each extraocular muscle and maintain its position in relation to its insertion. Kono et al (2005) found each rectus pulley coupled to:
Orbital wall: attaching to the orbital wall as check ligaments the fascia provides a firm attachment for the muscle.
Tenon’s capsule: Tenon's capsule, the fascia bulbi, reflects back from the eyeball as a tubular fascial sleeve that forms the pulley. The rectus muscles pass through this fascial sleeve to attach on to the sclera.
Adjacent extraocular muscles: the outer (orbital) muscle fibers of the rectus muscles are meant to attach on to this fascial pulley from Tenon's capsule. However McClung et al (2006) could find no muscle fibers leaving the rectus muscles to attach on to the pulley. These authors suggest the collagen expansions from the rectus muscles that are meant to attach on to the pulleys instead form the check ligaments.
The individual fascial tubular sheaths of the four recti merge to form a fascial ring (Standring 2015)
These pulleys posses smooth muscle fibers under parasympathetic innervation. This gives the pulleys dynamic neural control.
Nam et al (2019) found suspensory bands of connective tissue running between these pulleys extending from:
Medial rectus muscle pulley to the inferior rectus muscle pulley.
Medial rectus muscle pulley to the superior rectus muscle pulley.
Lateral rectus muscle pulley to superior rectus muscle pulley.
Fascial expansions from Tenon’s capsule that forms the muscular fascia:
Fascial expansions from the medial rectus: attaches to the lacrimal bone. Forms the medial check ligament. Limits the actions of the medial rectus muscle.
Fascial expansions from the lateral rectus: attaches to the zygomatic bone. Forms the lateral check ligament. Limits the action of the lateral rectus muscle.
Inferior rectus: blends with the sheath of the inferior oblique. This thickened fused sheath has an expansion into the lower eyelid. Here it is augmented by some of the fibers of the orbicularis oculi where it attaches to the inferior tarsus as the inferior tarsus muscle.
Not only are the check ligaments formed from the expansion of Tenon’s capsule that form the muscular fascia but McClung et al (2006) found the check ligaments attached on to the outer layer of the rectus muscles. These authors suggest the projections from the rectus muscles attaching onto the pulley on MRI images are in fact the collagen bundles of the check ligament.
The suspensory ligament of the eye (Lockwood’s ligament) extends from the medial to the lateral check ligaments stretching below the eyeball. It encloses the inferior oblique and inferior rectus muscles.
Other fascial extension of Tenon’s capsule are:
Superior transverse ligament (Whitnall's ligament): medial and lateral transverse expansions attach on to the orbit.
The relations of the transverse superior fascial expansion of the superior rectus muscle and levator palpebrae superioris to Tenon’s capsule is discussed in anatomy of the extraocular muscles.
Function of the muscle pulleys
Refer to 'Tenon's capsule' for the anatomy of the muscle pulleys.
The paths of the extraocular muscles through the orbit is constrained by connective tissue pulleys formed from Tenon's capusle. The normal pulley positions are necessary to maintain each extraocular muscle in its proper location with respect to its insertion, simplifying neural control of eye movement and balancing the forces of antagonist extraocular muscles.
Conversely, abnormal pulley positions destabilize control of eye movements by both changing the direction of the extraocular muscle force applied to the globe and unbalancing the forces of the abnormally placed extraocular muscle with its antagonist (Clark 2015).
These pulleys shift position during contraction and relaxation of the extraocular muscles. This dynamically changes the biomechanics of force transfer from the tendon onto the globe.
Clark (2015) found normal pulley positions are important in facilitating neural control of eye movements. Abnormal pulley positions introduce unbalanced muscle forces within the orbit that destabilize neural control of eye position and help create incomitant strabismus (Clark 2015).
Trochlea
The trochlea of the superior oblique is a pulley-like structure in the eye. Anatomically this is different from the pulleys from the other extraocular muscles. The tendon of the superior oblique muscle passes through it.
The trochlea is a cartilaginous "U" shaped structure attached to the periosteum that overlies the trochlear fossa of the frontal bone in the superior nasal quadrant of the orbit.
Within the trochlea, a connective tissue wraps around the superior oblique tendon in an onion-skin configuration (Wright 1999).
Kikuta et al (2019) found the relationship of the supratrochlear nerve and the trochlea was classified into three types:
Type I: the supratrochlear nerve passes lateral to the trochlea. 52.6% of cases.
Type II: the supratrochlear nerve passes through the trochlea. 42.1% of cases.
Type III: the supratrochlear nerve passed medial to the trochlea. 3.4% of cases.
Hypertrophy of the superior oblique muscle where it passes through the trochlea has the potential to entrap the supratrochlear nerve (type II).
Sandford-Smith (1975) found a stenosing tenosynovitis of the superior oblique is characterised by hypertrophy of the tendon where it changes direction in the trochlea.
This author found these changes were demonstrable by tenderness on gentle palpation using the ball of the thumb over the trochlea and just posterior to it while the patient was actively elevating and depressing the eye in adduction.
A swelling, if present, could be felt just posterior to the trochlea in a depression, which moved forwards to abut against the trochlea in attempted elevation.
Cachinero-Torre et al (2017) attributed disorders in the trochlear region as causing orbital pain.
Anatomy of the supratrochlear (V1) and supraorbital (V1) nerves
Trigeminal nerve --> opthalamic nerve --> enters the posterior orbit at the superior orbital fissure --> opthalamic nerve divides into three branches. One of the branches the frontal nerve runs between the levator palpebrae superioris and the periosteum (Hagan et al 2016). Terminal branches of the frontal nerve are: (lateral branch) supraorbital nerve & (medial branch) supratrochlear nerves.
Supraorbital nerve
Passes through the supraorbital notch (or foramen). Sensory innervation to the skin of the forehead (reaching as far as the temporal and parietal areas) and the extraocular muscles (Cachinero-Torre 2017). Probably provides the postganglionic sympathetic fibers which innervate the sweet glands of the supraorbital area (Haladaj et al 2019).
Just after exiting the supraorbital notch, the supraorbital nerve: superficial branch passes over the frontalis muscle. Innervates skin over the forehead. Deep branch: runs deep to the corrugator supercilii and frontalis muscles and across the lateral forehead between the galea aponeurotica and the pericranium. Innervates the frontoparietal scalp.
For causes of disorders of the supraorbital nerve refer to 'Extraocular muscles and headaches and migraines'.
Supratrochlear nerve
Kikuta et al (2019) found the relationship of the supratrochlear nerve and the trochlea was classified into three types:
Type I: the supratrochlear nerve passes lateral to the trochlea. 52.6% of cases.
Type II: the supratrochlear nerve passes through the trochlea. 42.1% of cases.
Type III: the supratrochlear nerve passed medial to the trochlea. 3.4% of cases.
The supratrochlear nerve passes through the frontal notch (or, very rarely, foramen). Sensory innervation to the bridge of the nose, medial part of the upper eyelid, and medial forehead.
For causes of disorders of the supratrochlear nerve refer to 'Extraocular muscles and headaches and migraines'
Extraocular muscles and headaches and migraines
The relationship between the extraocular muscles and headaches and migraines has been well established (Fernández-de-Las-Peñas 2006). The pathology associated with these extraocular muscles includes:
Trapped nerves.
Myofascial trigger points.
Trapped nerves
Supratrochlear nerve.
Kikuta et al (2019) found the supratrochlear nerve can pass through the trochlea in 42.1% of cases.
Sandford-Smith (1975) found a stenosing tenosynovitis of the superior oblique muscle is characterised by hypertrophy of the tendon where it changes direction in the trochlea. This could potentially cause an entrapment of the supratrochlear nerve at this location.
Diagnosis of this condition was through palpation using the ball of the thumb over the trochlea and just posterior to it while the patient was actively elevating and depressing the eye in adduction.
A positive finding was (i) tenderness and (ii) a swelling, if present, just posterior to the trochlea in the depression which moved forwards to abut against the trochlea in attempted elevation.
Cachinero-Torre et al (2017) attributed disorders in the trochlear region as causing orbital pain.
Extraocular sites of supratrochlear compression are the corrugator muscle (Janis et al 2013) and a periosteal or fascial band along the supraorbital rim (Hagan et al 2016).
Myofascial trigger points
Cachinero-Torre et al (2017) found trigger points produced from:
Overuse i.e. gazing for a long time in inappropriate conditions e.g. computer screens.
Disorders in the trochlear region.
Mechanosensitivity in the supraorbital nerve: (i) supraorbital notch/foramen (including the fascial band of the notch). (ii) Glabellar myofascial complex (including the corrugator muscle) (Janis et al 2013 & Fallucco et al 2012):
Lateral rectus
Symptoms: deep ache located at the supraorbital region or the homolateral forehead (Fernandez-de-Las Penas et al 2009).
Examination: pressure is applied to the anatomical projection of the lateral rectus, in the lateral corner of the orbit, for 20 seconds. Maintaining the pressure, the subject sustains a medial gaze to stretch the muscle (Cachinero-Torre et al 2017).
Superior oblique muscle
Symptoms: a deep ache is located at the retro-orbital region, sometimes extending to the supraorbital region or the ipsilateral forehead (Fernandez de la Penas et al 2005 & 2006).
Inferior oblique muscle
In some instances, the nerve to the inferior oblique muscle (inferior branch of the oculomotor nerve) may pierce the inferior rectus muscle (Haladal 2019). Could tightness in the inferior rectus muscle sensitise this nerve and cause trigger points in the inferior oblique muscle?
Levator palpebrae superioris
The levator palpebrae superior is innervated by the superior division of the oculomotor nerve. Some of those nerve fibers continue their course either around the medial border of the superior rectus or pierce it to innervate the overlying levator palpebrae superioris muscle (Haladal 2019). Could tightness in the superior rectus cause trigger points in the levator palpebrae superioris?
References
BROWN'S SYNDROME: DIAGNOSIS AND MANAGEMENT BY Kenneth W Wright (1999)
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Referred pain from the trochlear region in tension-type headache: a myofascial trigger point from the superior oblique muscle (2005). Fernandez de las Peñas C, Cuadrado ML, Gerwin RD, Pareja JA.
Referred pain elicited by manual exploration of the lateral rectus muscle in chronic tension-type headache (2009). Fernández-de-Las-Peñas C, Cuadrado ML, Gerwin RD, Pareja JA.
The intermuscular septum of the inferior oblique muscle: revised concepts (1983). Robertson I.
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Supraorbital Rim Syndrome: Definition, Surgical Treatment, and Outcomes for Frontal Headache (2016). Robert R. Hagan, Michael A. Fallucco, Jeffrey E. Janis
Relationship of the Lateral Rectus Muscle, the Supraorbital Nerve, and Binocular Coordination with Episodic Tension-Type Headaches Frequently Associated with Visual Effort (2017) Anxo Cachinero-Torre, Bele´n Dıaz-Pulido, and Angel As unsolo-del-Barco.
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Extraocular Connective Tissues: A Role in Human Eye Movements? (2006). J. Ross McClung; Brian L. Allman; Diana M. Dimitrova; Stephen J. Goldberg
The Role of Extraocular Muscle Pulleys in Incomitant Non-Paralytic Strabismus (2015). Robert A. Clark
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