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 qustiorl 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 thickeqd 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

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't.
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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
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.

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

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Figure 6. The scleta (center) and the pigmcnted choroid are cxternal to thc pootly defined rcceptor
cells to the left.

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Figure 7. Amorphous receptor cell layer (right)

1.4

Lewis

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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 .
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sibbsii mhor. Amer Midl Nilt. 27:187-401.
Dctwilcr, S. R. 1941. Veftebrare Photorceltors. 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 vertebrats 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 .
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et al., Betlin 2 (2) : 989'1292.
Heapc, \7. 1886. The development o[ the mole ('faltta eztobea)- Quart. J. Micro Sc. 21: 121-164.
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Neurology 13: 302'316.
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and oriein oI the blind soecies. Memoirs Nat Acad Sci. 1r: 1-150.
Polyak, S. l. lt.i1. The Retina. Univ. Chicago Press.
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Quilliam, T. A. 1964. Special features of the eye of the mole
1.18: 396.
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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,

Recebed Ap.ril 24, 1981

AcceDtedfor fublicatio'n Ja e 9. 198]

The RudiorenraryEye of \eurotricht.t

L'