Vision - Extraocular Muscle Development

From Embryology

Introduction

Human extraocular muscles 01.jpg

These notes introduce the development of the eye muscles. The adult eye has contributions from several different embryonic layers eventually forming neuronal, supportive connective tissue, optical structures, and muscular tissues. Additional pages are being developed to cover specific issues of this anatomical structure.


A study by Gilbert (1957)[1] described the origin and development of the human extrinsic ocular muscles.


Vision Links: Introduction | Lens | Retina | Placodes | Extraocular Muscle | Cornea | Eyelid | Abnormalities | Student project 1 | Student project 2 | Category:Vision
Historic Vision Embryology  
1906 Eye Embryology | 1907 Development Atlas | 1912 Eye Development | 1912 Nasolacrimal Duct | 1918 Grays Anatomy | 1921 Eye Development | 1922 Optic Primordia | Historic Disclaimer
Senses Links: Introduction | Placodes | Hearing and Balance | Vision | Smell | Taste | Touch | Stage 22 | Category:Senses

Some Recent Findings

  • Palisade Endings Are a Constant Feature in the Extraocular Muscles of Frontal-Eyed, But Not Lateral-Eyed, Animals[2] "To test whether palisade endings are a general feature of mammalian extraocular muscles (EOMs). Palisade endings are not a universal feature of mammalian EOMs. So, if they are proprioceptors, not all species require them. Because in frontal-eyed species, the medial rectus muscle has the highest number of palisade endings, they likely play a special role in convergence."
  • Eyelid closure in embryogenesis is required for ocular adnexa development[3] "Mammalian eye development requires temporary fusion of the upper and lower eyelids in embryogenesis. Failure of lid closure in mice leads to an eye open at birth (EOB) phenotype. ...In addition to providing a protective barrier for the ocular surface, eyelid closure in embryogenesis is required for the development of ocular adnexa, including eyelid and extraocular muscles."
More recent papers
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Search term: Extraocular Muscle Embryology

Suzanne M Michalak, Mary C Whitman, Jong G Park, Max A Tischfield, Elaine H Nguyen, Elizabeth C Engle Ocular Motor Nerve Development in the Presence and Absence of Extraocular Muscle. Invest. Ophthalmol. Vis. Sci.: 2017, 58(4);2388-2396 PubMed 28437527

Ramesh Murthy Congenital dystrophic medial rectus muscles. Indian J Ophthalmol: 2017, 65(1);62-64 PubMed 28300745

Elif Demirkilinc Biler, Onder Uretmen Multiple Pathological Ocular Findings in a Patient With PHACE Syndrome. J Pediatr Ophthalmol Strabismus: 2016, 53;e72-e74 PubMed 27977032

Yasha Modi, Benjamin Erickson, Isha Ranadive, Joshua Pasol, Sara Wester, Kara Cavuoto Idiopathic Unilateral Enlargement of the Extraocular Muscles in an Infant. Ophthal Plast Reconstr Surg: 2016, 32(6);e143-e145 PubMed 27828922

Daniel R Richardson, Laura A Gadzala, Dean J Bonsall, Jeffery P Hogg, H James Williams, John Nguyen Congenital Paradoxical Lower Eyelid Retraction With Upgaze due to an Anomalous Extraocular Muscle. Ophthal Plast Reconstr Surg: 2016, 33(4);e101-e102 PubMed 27811631

Extraocular Muscles

Extraocular muscles are required to move the eye within the orbit. Their embryonic origin requires an interaction between the cranial mesoderm and the migrating neural crest cells.

The following is from a recent paper comparing human to zebrafish muscle development.[4]

About the Muscles Legend
  • Five of the six muscles (inferior rectus, superior rectus, lateral rectus, medial rectus, and superior oblique) originate at a common tendinous ring of fibrous tissue (the Annulus of Zinn).
    • The Annulus of Zinn surrounds the optic nerve, ophthalmic artery, and ophthalmic vein at their entrance through the apex of the orbit.
  • The sixth muscle (inferior oblique) has a separate origin point on the orbital side of the bony maxilla at the anterior inferomedial strut.
  • IR - inferior rectus
  • SR - superior rectus
  • LR - lateral rectus
  • MR - medial rectus
  • SO - superior oblique
  • IO - inferior oblique
Human extraocular muscles 01.jpg

Ciliary Muscles

Human Lens (stage 22)

The lens focusses by refracting light as it passes through the biconvex lens, which can be altered in shape (accommodation) by surrounding ciliary muscles. These ciliary muscles are activated (contracted) by parasympathetic innervation from the ciliary ganglion itself innervated by the oculomotor nerve (Cranial Nerve III) (More? Cranial Nerves).

surface ectoderm -> lens placode -> lens pit -> lens vesicle -> lens fibres -> lens capsule and embryonic/fetal nucleus.


Eyelids

Muscles of the eyelids are the Levator palpebræ superiors, Orbicularis oculi and Corrugator. The Orbicularis oculi and Corrugator are both supplied by the facial nerve.
  • The Orbicularis oculi (Orbicularis palpebrarum) arises from the nasal part of the frontal bone, from the frontal process of the maxilla in front of the lacrimal groove, and from the anterior surface and borders of a short fibrous band, the medial palpebral ligament
  • The Corrugator (Corrugator supercilii) is a small, narrow, pyramidal muscle, placed at the medial end of the eyebrow, beneath the Frontalis and Orbicularis oculi.

(modified from Gray's Anatomy)

Gray0379.jpg

Timeline

Embryonic Development

  • Weeks 3 - 4 Eye Fields-Optic Vesicle
  • Weeks 5 - 6 Optic Cup, Lens Vesicle, Choroid Fissure, Hyaloid Artery
  • Weeks 7 - 8 Cornea, Anterior Chamber, Pupillary Membrane, Lens, Retina
  • Weeks 9 - 15 Iris, Ciliary Body
  • Weeks 8 - 10 Eyelids
Eye and retina cartoon.jpg

Carnegie Stages - Eye

The following data is from a study of human embryonic carnegie stages[5] and other sources.

  • Stage 10 - optic primordia appear.
  • Stage 11 - right and left optic primordia meet at the optic chiasma forming a U-shaped rim.
  • Stage 12 - optic neural crest reaches its maximum extent and the optic vesicle becomes covered by a complete sheath,
  • Stage 13 - By the end of the fourth week the optic vesicle lies close to the surface ectoderm. Optic evagination differentiation allows identification of optic part of retina, future pigmented layer of retina, and optic stalk. The surface ectoderm overlying the optic vesicle, in response to this contact, has thickened to form the lense placode.
  • Stage 14 - (about 32 days) the lens placode is indented by the lens pit, cup-shaped and still communicates with the surface by a narrowing pore.
  • Stage 15 - (about 33 days) the lens pit is closed. The lens vesicle and optic cup lie close to the surface ectoderm and appear to press against the surface.
  • Stage 16 - (37 days) Growth of the lens body results in a D-shaped lens cavity. Perilental blood vessels (tunica vasculosa lentis) are visible. Prior to the development of the eyelids, one small sulcus or groove forms above the eye (eyelid groove) and another below it.
  • Stages 17 - 19 - Retinal pigment is visible and the retinal fissure is largely closed. Eyelids grooves deepen, eyelid folds develop, first below, and then above, the eye.
  • Stages 18 - Mesenchyme invades the region between the lens epithelium and the surface ectoderm.
  • Stages 19 - 22 - the eyelid folds develop into the eyelids and cover more of the eye as the palpebral fissure takes shape. The upper and the lower eyelids meet at the outer canthus in Stage 19.
  • Stage 20 - The lens cavity is lost and a lens suture begins to form. The inner canthus is established.
  • Stage 23 - The retina comprises the pigmented layer, external limiting membrane, proliferative zone, external neuroblastic layer, transient fiber layer, internal neuroblastic layer, nerve fiber layer, and internal limiting membrane. Eyelids closure is complete (Note - shown as still open in the Kyoto embryo).

Neural Crest

Mouse eye neural crest.jpg

Mouse eye neural crest[6]

Mouse eye TGF-beta model.jpg

Mouse eye TGF-beta model[6]

Links: Image - Mouse eye neural crest | Image - Mouse eye TGF-beta model | Vision Development | Neural Crest Development | Head Development

Additional Images

Historic Images

References

  1. Gilbert PW. The origin and development of the human extrinsic ocular muscles. (1957) Carnegie Instn. Wash. Publ. 611, Contrib. Embryol., 36: 59-78.
  2. Roland Blumer, Barbara Maurer-Gesek, Bernhard Gesslbauer, Michael Blumer, Elisabeth Pechriggl, María A Davis-López de Carrizosa, Anja K Horn, Paul J May, Johannes Streicher, Rosa R de la Cruz, Ángel M Pastor Palisade Endings Are a Constant Feature in the Extraocular Muscles of Frontal-Eyed, But Not Lateral-Eyed, Animals. Invest. Ophthalmol. Vis. Sci.: 2016, 57(2);320-31 PubMed 26830369
  3. Qinghang Meng, Maureen Mongan, Vinicius Carreira, Hisaka Kurita, Chia-Yang Liu, Winston Kao, Ying Xia Eyelid closure in embryogenesis is required for ocular adnexa development. Invest. Ophthalmol. Vis. Sci.: 2014; PubMed 25377219
  4. Daniel S Kasprick, Phillip E Kish, Tyler L Junttila, Lindsay A Ward, Brenda L Bohnsack, Alon Kahana Microanatomy of adult zebrafish extraocular muscles. PLoS ONE: 2011, 6(11);e27095 PubMed 22132088 | PLoS One.
  5. A A Pearson The development of the eyelids. Part I. External features. J. Anat.: 1980, 130(Pt 1);33-42 PubMed 7364662
  6. 6.0 6.1 Lars M Ittner, Heiko Wurdak, Kerstin Schwerdtfeger, Thomas Kunz, Fabian Ille, Per Leveen, Tord A Hjalt, Ueli Suter, Stefan Karlsson, Farhad Hafezi, Walter Born, Lukas Sommer Compound developmental eye disorders following inactivation of TGFbeta signaling in neural-crest stem cells. J. Biol.: 2005, 4(3);11 PubMed 16403239 | J Biol.

Online Textbooks

Reviews

Ching-Hwa Sung, Jen-Zen Chuang The cell biology of vision. J. Cell Biol.: 2010, 190(6);953-63 PubMed 20855501

| JCB Gena Heidary, Elizabeth C Engle, David G Hunter Congenital fibrosis of the extraocular muscles. Semin Ophthalmol: 2008, 23(1);3-8 PubMed 18214786

Hung Ping Shih, Michael K Gross, Chrissa Kioussi Muscle development: forming the head and trunk muscles. Acta Histochem.: 2008, 110(2);97-108 PubMed 17945333

The International Journal of Developmental Biology Vol. 48 Nos. 8/9 (2004) Eye Development

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Cite this page: Hill, M.A. 2017 Embryology Vision - Extraocular Muscle Development. Retrieved September 24, 2017, from https://embryology.med.unsw.edu.au/embryology/index.php/Vision_-_Extraocular_Muscle_Development

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