Sensory - Vision Development

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Introduction

Historic retina drawing.jpg
Adult Human Retina histology[1]

These notes introduce vision development of the eye: induction and regional specification of the eye structures, maturation and formation of retina and optic tectum neuronal connections.

The adult eye has contributions from several different embryonic layers eventually forming neuronal, supportive connective tissue, optical structures, and muscular tissues. Historically determined that at birth, the human eyeball volume is about 3.25 cc and the estimated weight is about 3.40 grams.[2]

There are additional pages shown in the vision links, covering specific topics of vision development.

Vision Links: vision | lens | retina | placode | extraocular muscle | cornea | eyelid | lacrima gland | vision abnormalities | Student project 1 | Student project 2 | Category:Vision | sensory
Historic Embryology - Vision 
Historic Embryology: 1906 Eye Embryology | 1907 Development Atlas | 1912 Eye Development | 1912 Nasolacrimal Duct | 1917 Extraocular Muscle | 1918 Grays Anatomy | 1921 Eye Development | 1922 Optic Primordia | 1925 Eyeball and optic nerve | 1925 Iris | 1927 Oculomotor | 1928 Human Retina | 1928 Retina | 1928 Hyaloid Canal | Historic Disclaimer


Senses Links: Introduction | placode | Hearing and Balance hearing | balance | vision | smell | taste | touch | Stage 22 | Category:Sensory

Some Recent Findings

  • Vision-dependent specification of cell types and function in the developing cortex[3] "The role of postnatal experience in sculpting cortical circuitry, while long appreciated, is poorly understood at the level of cell types. We explore this in the mouse primary visual cortex (V1) using single-nucleus RNA sequencing, visual deprivation, genetics, and functional imaging. We find that vision selectively drives the specification of glutamatergic cell types in upper layers (L) (L2/3/4), while deeper-layer glutamatergic, GABAergic, and non-neuronal cell types are established prior to eye opening. L2/3 cell types form an experience-dependent spatial continuum defined by the graded expression of ∼200 genes, including regulators of cell adhesion and synapse formation. One of these genes, Igsf9b, a vision-dependent gene encoding an inhibitory synaptic cell adhesion molecule, is required for the normal development of binocular responses in L2/3. In summary, vision preferentially regulates the development of upper-layer glutamatergic cell types through the regulation of cell-type-specific gene expression programs."
  • Endocrine regulation of multichromatic color vision.[4] "Vertebrate color vision requires spectrally selective opsin-based pigments, expressed in distinct cone photoreceptor populations. In primates and in fish, spectrally divergent opsin genes may reside in head-to-tail tandem arrays. Mechanisms underlying differential expression from such arrays have not been fully elucidated. Regulation of human red (LWS) vs. green (MWS) opsins is considered a stochastic event, whereby upstream enhancers associate randomly with promoters of the proximal or distal gene, and one of these associations becomes permanent. We demonstrate that, distinct from this stochastic model, the endocrine signal thyroid hormone (TH) regulates differential expression of the orthologous zebrafish lws1/lws2 array, and of the tandemly quadruplicated rh2-1/rh2-2/rh2-3/rh2-4 array. TH treatment caused dramatic, dose-dependent increases in abundance of lws1, the proximal member of the lws array, and reduced lws2 Fluorescent lws reporters permitted direct visualization of individual cones switching expression from lws2 to lws1 Athyroidism increased lws2 and reduced lws1, except within a small ventral domain of lws1 that was likely sustained by retinoic acid signaling. Changes in lws abundance and distribution in athyroid zebrafish were rescued by TH, demonstrating plasticity of cone phenotype in response to this signal. TH manipulations also regulated the rh2 array, with athyroidism reducing abundance of distal members. Interestingly, the opsins encoded by the proximal lws gene and distal rh2 genes are sensitive to longer wavelengths than other members of their respective arrays; therefore, endogenous TH acts upon each opsin array to shift overall spectral sensitivity toward longer wavelengths, underlying coordinated changes in visual system function during development and growth."
  • Fetal ocular development in the second trimester of pregnancy documented by 7.0 T postmortem Magnetic Resonance Imaging[5] "Few investigators have analyzed fetal ocular growth with Magnetic Resonance Imaging (MRI) of high magnetic strength. Our purpose is to obtain normative biometrics for fetal ocular development in the second trimester of pregnancy. Sixty specimens with a gestational age (GA) of 12-23 weeks were scanned using a 7.0 T MRI scanner. The linear interocular and binocular distances (IOD and BOD, respectively), globe diameter (GD) and lens diameter (LD) were measured on the transverse section of the largest diameter of the eyeballs. The three dimensional (3D) visualization model of the eyeball was reconstructed with Amira software. Then, the globe and lens volumes (GV and LV, respectively) were obtained. All the measurements were plotted as a function of GA. The fetal ocular structures in the second trimester of pregnancy could be clearly delineated on 7.0 T postmortem MRI images. All the linear measurements logarithmically increased with GA, while, the volumetric measurements linearly increased with GA. Postmortem MRI of high magnetic strength can clearly document fetal ocular growth in the second trimester of pregnancy. These quantitative data may be a valuable reference for the assessment of normal fetal eyeball development in clinical settings and may be considered a supplement to anatomical investigations."
More recent papers  
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More? References | Discussion Page | Journal Searches | 2019 References | 2020 References

Search term: Vision Development | Vision Embryology

Older papers  
These papers originally appeared in the Some Recent Findings table, but as that list grew in length have now been shuffled down to this collapsible table.

See also the Discussion Page for other references listed by year and References on this current page.

  • The relationship between eye movement and vision develops before birth [6] "While the visuomotor system is known to develop rapidly after birth, studies have observed spontaneous activity in vertebrates in visually excitable cortical areas already before extrinsic stimuli are present. Resting state networks and fetal eye movements were observed independently in utero, but no functional brain activity coupled with visual stimuli could be detected using fetal fMRI. This study closes this gap and links in utero eye movement with corresponding functional networks. BOLD resting-state fMRI data were acquired from seven singleton fetuses between gestational weeks 30-36 with normal brain development. During the scan time, fetal eye movements were detected and tracked in the functional MRI data. We show that already in utero spontaneous fetal eye movements are linked to simultaneous networks in visual- and frontal cerebral areas. In our small but in terms of gestational age homogenous sample, evidence across the population suggests that the preparation of the human visuomotor system links visual and motor areas already prior to birth."
  • Activation of c-Jun N-Terminal Kinase (JNK) during Mitosis in Retinal Progenitor Cells[6] "Most studies of c-Jun N-terminal Kinase (JNK) activation in retinal tissue were done in the context of neurodegeneration. In this study, we investigated the behavior of JNK during mitosis of progenitor cells in the retina of newborn rats. ... The data show, for the first time, that JNK is activated in mitotic progenitor cells of developing retinal tissue, suggesting a new role of JNK in the control of progenitor cell proliferation in the retina."
  • Rearrangement of retinogeniculate projection patterns after eye-specific segregation in mice[7] "When monocular enucleation was performed after eye-specific segregation, rearrangement of retinogeniculate axons in the dorsal lateral geniculate nucleus (dLGN) was observed within 5 days. ...We also examined the critical period for this rearrangement and found that the rearrangement became almost absent by the beginning of the critical period for ocular dominance plasticity in the primary visual cortex."
  • The long noncoding RNA RNCR2 directs mouse retinal cell specification[8] "We find that the RNCR2 is selectively expressed in a subset of both mitotic progenitors and postmitotic retinal precursor cells. ShRNA-mediated knockdown of RNCR2 results in an increase of both amacrine cells and Müller glia, indicating a role for this lncRNA in regulating retinal cell fate specification."

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


Human Eye Development
Carnegie Stage Event
10 optic primordia appear.
11 Right and left optic primordia meet at the optic chiasma forming a U-shaped rim.
12 optic neural crest reaches its maximum extent and the optic vesicle becomes covered by a complete sheath,
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.
14 (about 32 days) Lens placode is indented by the lens pit, cup-shaped and still communicates with the surface by a narrowing pore.
15 (about 33 days) Lens pit is closed. The lens vesicle and optic cup lie close to the surface ectoderm and appear to press against the surface.
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.
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.
18 Mesenchyme invades the region between the lens epithelium and the surface ectoderm.
19 - 22 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.
20 Lens cavity is lost and a lens suture begins to form. The inner canthus is established.
23 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).
Data from a study of human embryonic carnegie stages[9] and other sources.
Week: 1 2 3 4 5 6 7 8
Carnegie stage: 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23


See below the drawings of sections of the whole eye from week 8 of development.[10]

Optic Nerve

  • Carnegie stage 19 - Optic nerve small, slender. Lumen practically whole length of stalk. Few or no fibers.
  • Carnegie stage 20 - Ependymal arrangement partially retained along stalk. Remnant of ependyma along whole length of stalk. Hyaloid groove at bulbar end. A few fibers arriving at brain.
  • Carnegie stage 21 - Remnant of ependyma present.
  • Carnegie stage 22 - Sheath layer beginning to form. Vascular canal present.
  • Carnegie stage 23 - Early nerve sheath. Reticular spongioblastic framework, striate arrangement of nuclei, bundles of fibers. Definite nerve sheath.

Lens

Human Lens (Carnegie stage 22)

The lens or crystalline lens or aquula (Latin, aquula = a little stream) has a key role in focussing light (with the cornea) upon the neural retina. The lens embryonic origin is from surface ectoderm of the sensory placodes that form in the head region (More? Week 4 - Placodes). 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.


Links: Vision - Lens Development

Stage 22 Eye

The images below link to virtual slides of the human developing eye at Carnegie stage 22. Click on the image to open or select specific regions from the regions of interest links.

Stage 22 - Eye and Nose

Stage 22 image 008.jpg

 ‎‎Mobile | Desktop | Original

Stage 22 | Embryo Slides
Stage 22 - Eye

Stage 22 image 008-eye.jpg

 ‎‎Mobile | Desktop | Original

Stage 22 | Embryo Slides

Virtual Slide - Regions of Interest

Links: Embryo Virtual Slides

Retinotopic Map

This neuroscience term describes how the developing retina is precisely "mapped" onto the visual cortex through a series of signaling and activity dependent mechanisms. This follows from Hubel and Wiesel (1981 Nobel Prize in Physiology or Medicine) key discoveries (1959-70) of how in development system matching occurs in the visual system. The topographic map establishes an ordered neuronal connection between sensory structures and the central nervous system.

The retinotectal map (eye to brain) of birds (lower vertebrates):

  • temporal (posterior) retina is connected to the rostral (anterior) part of the contralateral optic tectum
  • nasal (anterior) retina to the caudal (posterior) tectum
  • ventral retina to the dorsal (medial) tectum
  • dorsal ventral (lateral) tectum

Retinal waves a form of coordinated spontaneous activity that occurs in the developing retina. These waves of electrical activity (action potentials) are thought to have a role in establishing the initial retinotopic map by correlating/coordinating the activity of neighbouring retinal ganglion cells.

EphA/ephrin-A molecular signaling also thought to have a role in establishing the initial retinotopic map.

Neural Crest

Mouse eye neural crest.jpg

Mouse eye neural crest[11]

Mouse eye TGF-beta model.jpg

Mouse eye TGF-beta model[11]

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

Schlemm's canal

Mouse Schlemm's canal development 01.jpg

Schematic showing the stages of Schlemm's canal development in the postnatal mouse by the novel process of canalogenesis.[12] (Cartoons have been drawn for clarity and are not intended to suggest that most early sprouts arise from the LVP.)


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.[13]

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


Links: Extraocular Muscles

Additional Images

Historic Images

Historic Disclaimer - information about historic embryology pages 
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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

References

  1. Swaroop A & Zack DJ. (2002). Transcriptome analysis of the retina. Genome Biol. , 3, REVIEWS1022. PMID: 12186651
  2. Scammon RE. and Armstrong EL. On the growth of the human eyeball and optic nerve. (1925) J. Comp. Neurol. 33(2):165-219.
  3. Cheng S, Butrus S, Tan L, Xu R, Sagireddy S, Trachtenberg JT, Shekhar K & Zipursky SL. (2022). Vision-dependent specification of cell types and function in the developing cortex. Cell , 185, 311-327.e24. PMID: 35063073 DOI.
  4. Mackin RD, Frey RA, Gutierrez C, Farre AA, Kawamura S, Mitchell DM & Stenkamp DL. (2019). Endocrine regulation of multichromatic color vision. Proc. Natl. Acad. Sci. U.S.A. , 116, 16882-16891. PMID: 31383755 DOI.
  5. Zhang Z, Lin X, Yu Q, Teng G, Zang F, Wang X, Liu S & Hou Z. (2019). Fetal ocular development in the second trimester of pregnancy documented by 7.0 T postmortem Magnetic Resonance Imaging. PLoS ONE , 14, e0214939. PMID: 30947240 DOI.
  6. 6.0 6.1 Ribas VT, Gonçalves BS, Linden R & Chiarini LB. (2012). Activation of c-Jun N-terminal kinase (JNK) during mitosis in retinal progenitor cells. PLoS ONE , 7, e34483. PMID: 22496813 DOI.
  7. Hayakawa I & Kawasaki H. (2010). Rearrangement of retinogeniculate projection patterns after eye-specific segregation in mice. PLoS ONE , 5, e11001. PMID: 20544023 DOI.
  8. Rapicavoli NA, Poth EM & Blackshaw S. (2010). The long noncoding RNA RNCR2 directs mouse retinal cell specification. BMC Dev. Biol. , 10, 49. PMID: 20459797 DOI.
  9. Pearson AA. (1980). The development of the eyelids. Part I. External features. J. Anat. , 130, 33-42. PMID: 7364662
  10. Streeter GL. Developmental Horizons In Human Embryos Description Or Age Groups XIX, XX, XXI, XXII, And XXIII, Being The Fifth Issue Of A Survey Of The Carnegie Collection. (1957) Carnegie Instn. Wash. Publ. 611, Contrib. Embryol., 36: 167-196.
  11. 11.0 11.1 Ittner LM, Wurdak H, Schwerdtfeger K, Kunz T, Ille F, Leveen P, Hjalt TA, Suter U, Karlsson S, Hafezi F, Born W & Sommer L. (2005). Compound developmental eye disorders following inactivation of TGFbeta signaling in neural-crest stem cells. J. Biol. , 4, 11. PMID: 16403239 DOI.
  12. Kizhatil K, Ryan M, Marchant JK, Henrich S & John SW. (2014). Schlemm's canal is a unique vessel with a combination of blood vascular and lymphatic phenotypes that forms by a novel developmental process. PLoS Biol. , 12, e1001912. PMID: 25051267 DOI.
  13. Kasprick DS, Kish PE, Junttila TL, Ward LA, Bohnsack BL & Kahana A. (2011). Microanatomy of adult zebrafish extraocular muscles. PLoS ONE , 6, e27095. PMID: 22132088 DOI.

Online Textbooks

  • Kolb H, Fernandez E, Nelson R, editors. Webvision: The Organization of the Retina and Visual System [Internet]. Salt Lake City (UT): University of Utah Health Sciences Center; 1995-. Available from: http://www.ncbi.nlm.nih.gov/books/NBK11530/

Reviews

Beby F & Lamonerie T. (2013). The homeobox gene Otx2 in development and disease. Exp. Eye Res. , 111, 9-16. PMID: 23523800 DOI.

Sung CH & Chuang JZ. (2010). The cell biology of vision. J. Cell Biol. , 190, 953-63. PMID: 20855501 DOI.

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

Articles

Paquette LB, Jackson HA, Tavaré CJ, Miller DA & Panigrahy A. (2009). In utero eye development documented by fetal MR imaging. AJNR Am J Neuroradiol , 30, 1787-91. PMID: 19541779 DOI.


Bookshelf vision development

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Terms

Vision Terms  
  • annular tendon - (common tendinous ring, annulus of Zinn) fibrous tissue surrounding the optic nerve forming the origin for five of the six extra ocular muscles.
  • AXIN2 - a scaffold protein that is an antagonist and universal target of the Wnt/β-catenin pathway required for visual development. OMIM - AXIN2
  • canthus - (palpebral commissure) the corner of the eye where the upper and lower eyelids meet.
  • Cloquet's canal - historic term for the hyaloid canal. Named after Jules G. Cloquet (1790-1883) a French anatomist.
  • cranial nerve 2 - (CN II, optic nerve) the cranial nerve consisting of retinal ganglion cell axons and glia forming the connection with the brain (pathway: retina, optic disc, optic chiasma, optic tract, lateral geniculate nucleus, pretectal nuclei, and superior colliculus).
  • extraocular muscles - six muscles that control movement of the eye (superior, Inferior, lateral and medial rectus; superior and inferior oblique).
  • fovea - (fovea centralis; Latin, fovea = pit) retina region located in the center of the macula, required for sharp central vision.
  • ganglion cell layer - (retinal ganglion layer) the layer of the retina where retinal ganglion cell bodies lie.
  • hyaloid canal - a developmental feature in the embryo contains the hyaloid artery that supplies blood to the developing lens.
  • macula - (Latin, macula = spot; lutea = yellow) region near the center of the retina containing two or more layers of ganglion cells.
  • meibomian glands - eyelid gland that secrete meibum, generates the lipid layer of the tear film that prevents excessive evaporation of tear fluid.
  • nasolacrimal groove - (lacrimal groove) an embryonic surface feature between the maxillary and the lateral nasal process that will later fuse to form the lacrimal duct running between the eye and the nasal inferior meatus.
  • optic chiasm (optic chiasma) CN II region where some of the axons (partial) cross to the opposite side.
  • optic cup - the in-folded extension of the optic stalk from the diencephalon that forms the retina.
  • optic disc - (optic nerve head) region on the retina where the retinal ganglion cells exit to form CN II.
  • optic placode - (lens placode) surface ectoderm that folds inward to form the developing lens.
  • retina - The stratified sensory structure of the eye, formed from the neural ectoderm that extends from the forebrain (diencephalon) to form initially the folded optic cup. Vertebrates have ten identifiable layers formed from nerve fibers, neurons, membranes, photoreceptors and pigmented cells. Light must pass through nearly all these layers to the photoreceptors. (1. Inner limiting membrane - Müller cell footplates; 2. Nerve fiber layer; 3. Ganglion cell layer - layer of retinal ganglion cells their axons form the nerve fiber layer and eventually the optic nerve; 4. Inner plexiform layer - another layer of neuronal processes; 5. Inner nuclear layer; 6. Outer plexiform layer; 7. Outer nuclear layer; 8. External limiting membrane - layer separating inner segment portions of photoreceptors from their cell nuclei; 9. Photoreceptor layer - rods and cones that convert light into signals; 10. Retinal pigment epithelium).
  • retinal pigment epithelium - (RPE, pigmented layer) An epethial pigmented cell layer lying outside the sensory retina, formed from the outer layer of the folded optic cup. The RPE is firmly attached to the underlying choroid and overlying retinal visual cells, for which it has a nutritional role.
  • retinal waves - A form of coordinated spontaneous activity that occurs in the developing retina. These waves of electrical activity (action potentials) along with EphA/ephrin-A signaling are thought to have a role in establishing the initial retinotopic map by correlating/coordinating the activity of neighbouring retinal ganglion cells.
  • Stilling's canal - historic term for the hyaloid canal. Named after Benedict Stilling (1810-1879) a German anatomist.
  • YAP - (Yes-Associated Protein) transcriptional regulator required for retinal progenitor cell cycle progression and RPE cell fate acquisition. PMID 27616714 OMIM - YAP1
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Cite this page: Hill, M.A. (2024, March 19) Embryology Sensory - Vision Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Sensory_-_Vision_Development

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