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ThomasH. Lewis 1505 Avenue D Billiogs, Mootana 59102 The Anatomy and Histology of the RudimentaryEye ol Neurotrichus Abstract Fossorial inse<tivores ate functionally adapted to relative darknes and show anatomical regression in eye morphology. Scalopt has retaioed the vitreous body, and the retina has rods and cooes. Talta has embryonal lens cells. Notoryrrer, a {ossorial marsupial, has a rudimentary retina without rods and cones, and has lo6t the vitreous, lens, ^nd, p.upll. Nearotr;ch r is a late shrew-like mole with mioute optic globes. These are unique in the pteseoce of a pigmented extension of the retina, covering rhe anterior surfa.e of the oFic lens. The globe is collapsed upon the retina and the embryonal lcns. Rod and cone cells are poorly defined. The vitreous is missing. Ihere is no pabebral fissure, and the extraocular musclei do not have a proximal bony attachment. The centtal pan of the iris is markedly proliferated. Behavioral studies indicated that Ne*rottichat is blind, which raises a qu€stiorl about the possible function of the pigmented lentic,ular covering and the proliferated iris. Loss of visual perceptiofl has occurred in several verteblate groups, notably in the cavedwelling fishes and salamanders.In the mammals, two families of the Insectivora (Talpidae, Chrysochloridae) aod ooe family of Marsupalia (Notoryctidae) are of fossorial habit, and have accompanying diminution in visual function. In Scalops, Slonaker (1!02) demonstrated that despite the rudimentary and presumably noofunctiooal eye, rhe virreous is retained in some individual specimensand rods aod cones are present. In TaQa, another genus of moles, Kohl (i895) and Quilliam (1964) found that the vitreous and aqueousare retained in much the sarneeye structure as io sighrcd mammals. Ritter (1899) describedin Tal.pa a nearly nomal lens srnrctllre. Fraoz (1934) (atter Sweet) described Notorycter ,lphlopr h which the vitreous, lens, and pupil are absent, the letina is rudimentary aod without fods aod coles, and the extraocularmusclesare oot striated.A compatisonof these studies with Neuronicbus, a talpid in which rhe eye structure has oot yet been examined,is noteworthy. Newotrichu is the smallestof the North American Talpidae, measuringabout 100 mm in total length. This talpid is also the leasr fossorialof the moles,and in its hundng habits on the surfaceof the foresr floor resemblesthe shrews.Neurotrichur is restricted to the humid coastal forests of British Columbia, I(ashington, Oregon, and Nothern California.There is one species(gibb:ii) and three subspecies(hycinthas, gibbtii, and ninor). The eye of Neurotricbut is subcutaneousand minute. Dalquest and Orcutt (1947 ) aod Reed (1944) have studied Neurotrichas in the labotatory and concluded that the animal is blind. This paper describesthe ocular anatomy of specimensof Neuotichus gibbtii minor collecred. at Seattle,Washington. Melhods Five adult specimenswere fixed eotire and decalcified.The head was then sectioned sagittally.Twenty adult specimenswere dissectedand the eyes removed with a block Northwesr Science.Vol. 57. No. 1. 19[t3 of epidermis and surrounding tissue.Sioce the eyesare mioute, no intrinsic optic axis could be discovered in specimens fixed in Bouin or Gibson solution- The blocks were sectioned, therefore, at sevetal angles relative to the head. Slides were prepared by paraffin and celloidin block. Sections wete stained with haemotoxylneosin,Verhoff, 'Weigert myelin, Mallory Triple, and Van Gieson. Neurotrichut is a rare animal' Few field naturalistshave observedit, and no embryologicatmaterial for sectiooiogwas collected.No EM material has beenobtained to date. GrossAnatomy There is no palpebral opening. The eye is completely covered by a densely furred integument and is not visible externally except by parting the Suard hairs and undercoat The pigmented globe is then visible through the skin Directly extetnal to the globe, rhe skin is hairless and thinner, and thrown into shallow peri-ocular fqlds. The skin is freely moveable over the eye. When the skin is removed, the eye remains imbedded in the subcuteaneoustissue and is connected, as is the cornea, to the corium by delicate strandsof conoectivetissue. The eye is a deeply pigmented sPhele0.7 to 1.0 mm in diameter. A thin oPaque covering of coonective tissue forms a delicate equatorial ring attached to the dermis. No pupil or iris is visible in gross fixed specimens.The extraocular muscles are large at the equatorial ring but rapidly attenuate as they PassPosteriody, close to the course 'fhe of the optic nerve, to disappear in the sukutaneous tissue over the M matsetet eye is oot contained in a bony orbit but is positioned on the lateral side of the rather conical head at the level of the fourth maxillary tooth- The eye of an embryo specimen (33 mm in total leogth, head 17 mm) photographedby Dalquest (1947) was deeply pigmented and easilyvisible through the almost haitlessskin Histology Tenon's capsule is thio and caooot be traced anterior to the conjunctival aogle. The sclera is composedof severallayers oI fibroblasts varying from seven to rwelve The cornea is poody differentiated from the sclera. The cornea is slightly thinner, and the Iibroblastsof the substantiapropria have more widely separatednuclei. No Bowmans membrane is distinguishable.A few scatered epithelial cells may representthe corneal mesenchymalepithelium. The choroid is a denselypigmented layer enveloping the globe of the eye excePt for rhe small pupillary aperture.At the ciliary body the choroid is much thickened,and here the pars ciliaris retinae separatesfrom it to pass as an adherent pigmented layer acrossthe entire anterio! surface of the lens except at the pupil. The non-pigmented cells oI this part of the ciliary epithelium, continuous with the nzural retinal layer, are cuboidal with eosinophilic cytoplasm.Some of these cells are deflected onto the surfaceof the lens posterior to the equator, but most form a cotrtinuouslayer in contact with the aoterior capsularcells. The pigmented layer is visible to the puPillary margin. From the ciliary body rhe choroid extends anteriody, closely applied to the innet surfaceol the scleraand cornea.The choloid is much thickened at the PuPil, with lightcolored vascularand muscle cells telieving its usually dense pigmentation. There is a well developed pupillary margin. Nearby, in some sections! the pigmented cells of the lhe Kudrmenrary Lye ol 1\errolrt(t)r\ antetior surfaceof the lens are tenuously adherent ro the posterior surfaceof the iris. Orherwise, there is much difficulty rryiog ro distinguish any elements of the pars iridica retinae. The outer surface of the iris has a one- to nvo-cell layer of epithelium reflected from the inner surfaceof the cornea.The entire iris is rhick and heavily pigmented. The ciliary body, composedin rhe main by the markedly thickened choroid, contains no recollnizablemuscle cells or fibers of a supensoryligament. The retina and lens fill the eye.There is no vitre<xrs.The inner limiting membrane is lrot seenin the sectioo,but mosr of the remaining retinal layersare clearly dematcated. The optic nerve fibers and ganglion cells are promioent, aod nerve fibers loop vertically through rhis layer. Cells with large ouclei containing a nucleolus and iregular da.tk_ staining bodies in the nucleoplasmand with eosinophilic cytoplasmare present,along with axonic fibers. The inner plexiform layer is present,and a prominent inner nuclear layer is composedof cells n'ith dark ouclei. The nuclear layer is about six cells io depth. There is a prominent outer plexiform layer. The outer nuclear layer is also about six cell layersin deprh,rhe nuclei dark in color. The receptorlayer is columnar in srrucrure, but cell derail is faint and definire rods and conescannot be distinsuished.There is a thin outer layer of cells wich deeply staining nuclei and pigmented cytoplasm. The optic oelve can be traced from rhe optic papilla as it coulsesposteriorly from the globe to the optic foramen,accompaniedby other nerve trunks. Somesectons show the optic nerve in close proximity to the ciliary ganglion. The optic oerve penerates the layersof rhe globe tangentially.Some fibers can be traced rhrouqh the entire thick_ nessot rhe rerinaas a paLhof cellsenreringrhe ganglioncell layer. The lefls is an ellipsoid sructure with a smoorhly curved posterior surface and a lesssmcnthly q:rved anreriot surface_The outline of the anterio! curvature is modified by the enlarged pupillary rim of the iris. The lens is composed of polyhedral, elongate or columoar cells, each with a dark-staining nucleus. The capsular cells u.a r-"11", and flattened. Thete are oumefous vacuolesin the lens substaoce,especiallynear the anterior surface. The posterior chamberof the eye is almost as extensiveas the widrh of the globe, extending from the ciliary bodies acrossthe aoterior surfaceof the lens to rhe minute pupil. The anterior chamber is all but eliminared by the adherenceof rhe choroid and iris to the inner surfaceof the sclereand cornea.There is a broad conluoctrval sac lined with epithelial cells.Theseare cuboidal aod one- to three-cellsthick on the interior surfaceof the integument, flattened over rhe coroea, and in thickeq€d layers in the fornices. The conjuctival sac contains desquamaredcells aod amorphous material. The cells have dark cyroplasrn and large oval or rounded, <leeply stainiog nuclei. Some small massesof tr-rbuloalveolar tissue are found adjacent to the conjunctiva, but they opeo ono the skin surface. Oiscussion The eye oI Neurotrichu presentscomlmrative anatomistswith a unique anatomical feature-i.e., rhe pigmented covering of the anterior surfaceof the lens.This pigmented tissue is ao exterior layer of the pars ciliaris recinae.No other knovro vertebrate has taken this wolutionary route. Ifalls (1943) ad \folff (1949), in their reviEws of the compalative anatomy of rhe vertebrate eye, describe no lenticular pigment layer 10 Lewis comparable to that found in Nearctricbus. Of further rrote it Neurorrich .! are the markedly proliferated tissueof the cenual part of the iris, the lossof the vitreous body with collapseof the globe upon the lens and retina, the embryonal structure of the leos, the lossof rods and cones,the lossof any proximal bony attachmentof the extra, ocular muscles,and the absenceof a palpebral aperture. The circadian rhythms of rest and activity in Neturotrich r are nor known. Presumably it maintains a high level of searchingand ingestion like the shrews (Sorex aod others), with even less dependenceon iocident light. Its efficient non-visual seosolyapparatusallows it to inhabit the dimly lit flcnr of heavy forests,in and bencath abundant surfacevegetation and detritus, where visual acuity is relatively superfluous. Shrews,in similar habitats,have functional eyes.Compamtiveanatomicaland behavioral studies of the microhabitat, which might allow evolutiooary discussions,are so fat sparse,and a correlationof Neurotricbut' pecr-rliarvisual anatomywith its adaptive skills cao only be conjectural.The moles,more fossorialin habit, shoq' even more aoatomical regression in eye structures. L'.',.4 {,.::;} 't. ::', Figure 1. Subcutanarus eye of Ne ntichb. Layers of che re|in,r. choroid and scLcra,rnd the tens, iris, pupil, and conjunctival space are visiblc'. The Rudinrentrrl F,reL>l\eurotriclnr Il t t Figure 2. The sclem and pigmented choroid lie ro the rigit of the poorly defined tods and cones. Figure J. From.rhe right. eprdermis, dermis, conjunctival spa.ce,cornea-sclera, pupillary posterior chambrr, and pigmented parr rridica retinalis t2 margins, *-*:-u t Figure 4. The lens contair$cuhridal aod.elongare(ells._The crliary body ((enrer) lies at the equaro( of the lens. Anterior to the ciliary fody the tens is covired by the pifmented pars ;iidi,:a retinalis. I t.,I Figure ). The layers of the rctina are to rhe lefr Ar rhe tilrary body (ccnrl,r) rhe continuation of rhc retiM separatesfrom the choroiJ and passesin front of'rtre lens 1rop7. The ltuclirrentary Eve t>f iteatotrichu.r l) "''t#.';''l*, i,'^-':H!;i.?r. ffi.-?e -.tF-:rY.'.#.. D'' . ' - - r $ f r * r ' i . ' '. r "-Ef,i!.1-.1.{e . ..; i'? '2iAhI 'r: . 'tic'r+. .4. -'?5$'. r . i''}. .-: .r'Sf.r. . * ..r,ti*4' i . illlt :{ f, Figure 6. The scleta (center) and the pigmcnted choroid are cxternal to thc pootly defined rcceptor cells to the left. r itl' 1. , ll{:, r\f !ir - a t t 1\i i )... Figure 7. Amorphous receptor cell layer (right) 1.4 Lewis a t:l Literature Cited C u n n i n g h a m , J . T . f 9 8 1 . B l i n d a n i m a l s i n c a v e s .N a t u r e 4 7 : 1 2 1 9 . Dalquest, W- W., and D. R. Orcutt. 1947. The biology of the ieait shrew-rnole Ne/rtutrichat sibbsii mhor. Amer Midl Nilt. 27:187-401. Dctwilcr, S. R. 1941. Veftebrare Photor€celtors. MacMillan Cr., New York. Duke,Ilder, !7. S- 1939. Textbook of Ophthalmology. Vol. 1. The Development, Form, and Func' tion of the Visual Apparatus. C. v. Mosby Cr., Sr. louis. Eigenmann, C. H. 1899. The eyes of the blind vertebrat€s of Notth America. Arch. F. Eotwichclungs m c c h a n i k d e r o r g a n i s m e n .8 ( 4 ) : 5 4 t 6 1 7 . Forbes. S. A. 1882. Thc biiod cave fishcs and their ailies. Amer Nat 16: 1-t. Frar,z, \t. 1,914. Vergleichende Anatomie des Virbelthicraugon, lz Handb. vergl. Anat, Bulk, L. et al., Betlin 2 (2) : 989'1292. Heapc, \7. 1886. The development o[ the mole ('faltta eztobea)- Quart. J. Micro Sc. 21: 121-164. Kohl, C. 189t. Rudimcntare \flirbeltieraugen BibliDreca Z@logi(i V. Heft 14: l-278. I-und, R. D., nnd l. S. Lund. 1965. Thc v'sual sysrrm of rhe nole'L'alla e*nqaea. Experi.mental Neurology 13: 302'316. Packard, A. S. 1887. The cave fauna of North Amcrica with remarks on the aoatomy of the brain and oriein oI the blind soecies. Memoirs Nat Acad Sci. 1r: 1-150. Polyak, S. l. lt.i1. The Retina. Univ. Chicago Press. (,Tal,a e raPddr). Anatomical Record. Quilliam, T. A. 1964. Special features of the eye of the mole 1.18: 396. Rabl, C- 1900. Ubcr dcn Bau urld Entwickelung der Linsc. Pan III Saugetheite. Zeitschr. F. rtFissensch. Zool. Bd. 67. R e e d , C . A . 1 9 4 4 . B e h a r i o r o f r s h r c w m o l c i n c a p r i v i r y .J . M a m m . 2 i : l q 6 - l o Ritter, C. 1899. Die Linse des Maulwurfs. Arch. F. Mikr. Anat. u. Entwickelungsgcschichtc. Bd. 51, Heft 3: 385'396. Slonaker,"J. R. 1902. The eye of the common mole, Scal'ot aqxaticu machrin*. J. Crmp. Motph l 1941. The Venebrate F,yc and Its Adaprive Rrdiation. Cranbrook Press, B,loomficld Hills, Michigan. IJColff, E. 1949. The Anatomy of the Eye and Otbit. Blakiston Crl., Philadelphia 3d ed. \Vaft, d Recebed Ap.ril 24, 1981 AcceDtedfor fublicatio'n Ja e 9. 198] The RudiorenraryEye of \eurotricht.t L'