The Extraocular Muscles

(1)
University of Sydney, Sydney, Australia
 

Overview

  • Four rectus (superior, inferior, medial, and lateral) and two oblique (superior and inferior) extraocular muscles (EOMs) insert onto the eye and contribute to all ocular movements [1, 2].
  • The EOMs produce eye movements over a range of amplitudes and velocities, including:
    (a)
    Slow changes in eye position to track or stabilize visual targets
     
    (b)
    Fine-tuned micromovements
     
    (c)
    Large, rapid saccades [3]
     
  • They are the most highly specialized and structurally diverse skeletal muscles in the body [4].

Anatomy (Fig. 16.1)

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Fig. 16.1
(a). The extraocular muscles. (b). Insertions of the extraocular muscles (spiral of Tillaux) [5, 9] (Based on Kanski, 2007) [12]
1.
Four rectus muscles
  • These arise from a common tendinous ring (annulus of Zinn) at the orbital apex [2, 5–7].
  • From here they travel anteriorly through the orbit forming a muscle cone.
  • They follow the globe curvature to insert onto the anterior sclera [7, 8].
  • The mean positions of the tendinous insertions are described by the spiral of Tillaux (Fig. 16.1b) [9]; however, interindividual variation of up to 4 mm has been observed [10].
  • Motor nerves penetrate the muscles posteriorly from within the cone [11].
 
2.
The superior oblique
  • The superior oblique (SO) arises from the posterior orbital wall superomedial to the apex [5].
  • It travels superiorly along the medial orbital wall to reach the trochlea, where it is redirected posteriorly, inferiorly, and toward the globe [13].
  • It passes beneath the superior rectus, crosses the equator, and inserts onto the posterolateral globe [14].
 
3.
The inferior oblique
  • The inferior oblique (IO) arises in the nasal bony orbit and passes inferior to the inferior rectus [5].
  • Its path mirrors the superior oblique tendon and inserts onto the posterolateral inferior globe.
 
4.
The levator palpebrae superioris (see Chap. 1. Protective Mechanisms of the Eye and Eyelids)
  • The levator palpebrae superioris arises at the orbital apex superior to the annulus of Zinn.
  • It continues anteriorly through the superior orbit and becomes an aponeurosis, inserting onto the upper lid skin crease and superior tarsal plate.
  • The levator controls upper eyelid opening and has many similarities to the extraocular muscles in development, ultrastructure, and function [15, 16].
 
5.
Pulley systems (Fig. 16.2)
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Fig. 16.2
The extraocular muscle pulleys
  • Each rectus muscle is connected to the orbital wall by a fibroelastic pulley consisting of smooth muscle, collagen, and elastin bands [17, 18].
  • The pulleys provide adjustment of the EOM force vectors in different gaze positions, acting as functional origins of the rectus muscles [19].
 
6.
Geometric anatomy of the orbit, eye, and extraocular muscles [1, 5]
  • The orbit forms a pyramid; the lateral and medial walls are 45° to one another.
  • The central axis of the orbit is at a 23° lateral deviation to midline (Fig. 16.3a).
    A347009_1_En_16_Fig3_HTML.gif
    Fig. 16.3
    (a) The geometric anatomy of the orbit. (b) The angles of insertion of the recti and oblique muscles in primary gaze
  • In the primary gaze position (both eyes facing forward):
    (a)
    The superior rectus (SR) and inferior rectus (IR) form an angle of 23° with the visual axis.
     
    (b)
    The IO and SO form an angle of 51° with the visual axis (Fig. 16.3b).
     
 
7.
Orbital connective tissue septae
  • A complex framework of orbital connective tissue septae exists.
  • This consists of a smooth muscle and connective tissue network containing nerves and vessels [20].
  • These constrain and stabilize the EOMs, controlling the direction of force during muscle contraction and allowing predictable globe movements [21].
 

General Characteristics of the Extraocular Muscles

EOMs are skeletal muscles; their fibers resemble other skeletal muscle fibers in the following ways:
1.
Muscle fiber structure (Fig. 16.4)
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Fig. 16.4
(a) Extraocular muscle fiber structure. (b) The sarcomere
  • EOM fibers are long and cylindrical multinuclear cells.
  • Within the cell membrane (sarcolemma) are peripheral nuclei and longitudinal myofibrils [5, 22].
 
2.
Myofibril structure
  • Myofibrils are composed of longitudinally linked contractile units (sarcomeres).
  • These are formed by partially overlapping thick (myosin) and thin (actin) filaments together with titin and nebulin filaments (Fig. 16.4b) [23].
  • The actin filaments insert onto a central actin backbone (Z-band) [24].
 
3.
Electrical control of contraction
  • On neural stimulation, a depolarizing membrane potential travels along the sarcolemma.
  • The depolarizing potential enters the muscle fiber via an invaginating T-tubule system [25].
  • The T-tubules terminate near the sarcoplasmic reticulum (SR), an intracellular calcium (Ca2+) storage system.
  • Depolarizing signal from the T-tubules results in release of intracellular Ca 2+ from the SR.
 
4.
Molecular basis of contraction
  • Contraction occurs by ATP-dependent binding of actin to myosin.
  • Myosin slides over actin filaments via sequentially formed and broken covalent bonds [26].
  • Troponin and tropomyosin are regulatory proteins that prevent actin-myosin interaction at rest.
  • On stimulation, intracellular Ca2+ release prevents the troponin/tropomyosin complex from binding to actin, allowing interaction between actin and myosin to occur [27, 28].
 

Special Characteristics of the Extraocular Muscles

The EOMs have unique characteristics distinctive from other skeletal muscles:
1.
Layered organization
  • The EOMs consist of an outer orbital layer and an inner global layer (Fig. 16.2) [29]:
(i)
The global layer
  • The global layer extends the full muscle length and continues anteriorly as the muscle tendon.
  • It inserts onto the sclera to directly control globe movements [30]
 
(ii)
The orbital layer
  • The orbital layer inserts onto the EOM pulleys, positioning them along the muscle for optimal force vector translation [19, 30].
 
 
2.
Fiber types:
(i)
Typical skeletal muscle fiber classification
  • Most skeletal muscle fibers are broadly categorized into red, white, or intermediate determined by:
    (a)
    Blood supply
     
    (b)
    Concentration of myoglobin, an oxygen-binding red pigment
     
  • Red fibers predominantly use aerobic metabolism for slow, tonic, fatigue-resistant contractions.
  • White fibers use anaerobic glycolysis for rapid twitches and fatigue quickly.
 
(ii)
EOM fiber classification (Table 16.1) [31–37]
Table 16.1
Extraocular muscle fiber types [31–40]
 
Orbital layer
Global layer
Fiber type
Singly innervated
Multiply innervated
Red singly innervated
White singly innervated
Intermediate singly innervated
Multiply innervated
% Fibers within the layer
80
20
33
32
25
10
Contraction mode
Twitch
Mixed
Twitch
Twitch
Twitch
Non-twitch
Contraction speed
Fast
Fast and slow
Fast
Fast
Fast
Slow
Fatigue resistance
High
Variable
High
Low
Intermediate
High
  • EOM fibers are subclassified into 6 distinct fiber types characterized by:
    (a)
    Layer
     
    (b)
    Innervation type (singly or multiply)
     
    (c)
    Color (myoglobin content)
     
  • All fiber types participate in all classes of eye movements [1].
 
 
3.
Myosin isoforms:
(i)
Typical skeletal muscle myosin isoforms
  • Various myosin isoforms are present in skeletal muscles throughout the body; most skeletal muscles express only one heavy-chain isoform type [41].
  • Each isoform is suited to a particular contraction speed; broadly divided into slow (fatigue-resistant) and fast (rapidly fatiguing) twitch types [42].
 
(ii)
EOM-specific myosin isoform
  • EOMs contain multiple heavy-chain myosin isoforms.
  • These can coexist within individual myofibers and their distribution can vary along the myofiber [43].
  • They provide the muscle fibers with variable contractile speeds as well as fatigue resistance [44–46].
 
 
4.
Innervation pattern:
(i)
Typical skeletal muscle innervation
  • Most skeletal muscle fibers are innervated by one motor axon synapsing at a motor end plate [47].
  • The stimulated axon terminal releases acetylcholine, resulting in motor end plate depolarization [48].
  • An action potential (AP) propagates along the sarcolemma causing all-or-nothing contraction [25].
 
(ii)
Extraocular muscle fiber innervation
  • EOM fibers can be broadly divided into singly- and multiply-innervated fibers.
 
(iii)
Singly-innervated extraocular muscle fibers
  • Like other skeletal muscle fibers, singly-innervated EOM fibers are innervated by one motor axon.
  • However, they have unique motor end plates that are smaller and more simple than those found in typical skeletal muscle [49].
 
(iv)
Multiply-innervated fibers
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Oct 28, 2016 | Posted by in OPHTHALMOLOGY | Comments Off on The Extraocular Muscles

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