Multiple optic fiber patterns in the catfish retina. No. 10 Reports 1431 Fig. 2. Characteristic...
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No. 10 Reports 1429 From the Department of Ophthalmology and Visual Science (Mi- chael Jacobson, Yog Raj Sharma, and Edward Cotlier) and the De- partment of Molecular Biophysics and Biochemistry (Jan Den Hol- lander), Yale University, New Haven, Connecticut. Supported by N1H Grants EY02490 and AM27121. Submitted for publication: July 29, 1982. Reprint requests: Dr. Edward Cotlier, Department of Ophthalmology, The New York Hospital, Cornell University Medical Center, 515 E. 71 Street, New York, NY 10021. References 1. Kinoshita JH, Kador P, and Catiles M: Aldose reductase in diabetic cataracts. JAMA 246:257, 1981. 2. Winegrad AI, Morrison AD, and Clements RS J r Polyol pathway activity in aorta. In Vascular and Neurological Changes in Early Diabetes, Camerini-Davalos RA and Cole HS, editors. New York, Academic Press, 1973, pp. 117-124. 3. Chylack LT Jr, Henriques HF, Cheng H-M, and Tung WH: Efficacy of alrestatin, an aldose reductase inhibitor, in human diabetic and nondiabetic lenses. Ophthalmology 86:1579,1979. 4. Varma SD, Mikuni I, and Kinoshita JH: Flavonoids as inhibitors of lens aldose reductase. Science 188:1215, 1975. 5. Handelsman DJ and Turtle JR: Clinical trial of an aldose re- ductase inhibitor in diabetic neuropathy. Diabetes 30:459, 1981. 6. Sharma YR and Cotlier E: Inhibition of lens and cataract aldose reductase by protein-bound anti-rheumatic drugs: salicylate, in- domethacin, oxyphenbutazone, sulindac. Exp Eye Res 35:21, 1982. 7. Peterson MJ, Sarges R, Aldinger CE, and MacDonald DP: CP- 45, 634: a novel aldose reductase inhibitor that inhibits polyol pathway activity in diabetic and galactosemic rats. Metabolism 28:456, 1979. 8. Clements RS, Morrison AD, and Winegrad AI: Polyol pathway in aorta: Regulation by hormones. Science 166:1007, 1969. 9. Stevens VJ, Rouzer CA, Monnier VM, and Cerami A: Diabetic cataract formation: Potential role of glycosylation of lens crys- tallins. Proc Natl Acad Sci USA 75:2918, 1978. 10. Judzewitsch RG, Jaspan JB, Polonsky KS, Weinberg CR, Halter JB, Haler E, Pfeifer MA, Vukadinovic C, Bernstein L, Schneider M, Liang K-Y, Gabbay KH, Rubenstein AH, Porte D Jr. Aldose reductase inhibition improves nerve conduction velocity in di- abetic patients. N Engl J Med 308:119, 1983. Multiple Optic Fiber Patterns in the Catfish Retina Beryn L. Frank and Stephen Goldberg The retinas of certain catfish contain multiple optic discs. This report describes the patterns of optic nerve fibers and optic discs as seen in silver-stained flat mounts, in 11 different families of catfish. As many as 50 optic discs may exist in a single retina, in paired and unpaired combinations, and in slit and ring-like arrays. Invest Ophthalmol Vis Sci 24:1429- 1432, 1983 Multiple optic discs have been found in the retinas of a variety of species offish,amphibians, and certain members of the deer family. 1 " 5 The retinalfiberpatterns of these animals do not appear to have been described. In our studies of the retinas of a variety of fishes, we found that the feature of multiple optic discs is a striking peculiarity of the catfish retina. The present study is an analysis of the variety of retinalfiberpatterns in a broad range of catfish families, as seen with silver- stained flat mounts. Materials and Methods. Forty-six species of catfish, representing 11 families, were examined for retinal fiber pattern. These includedfishnative to North, Cen- tral, and South America, Europe, Asia, India, Thailand, and Africa. Enucleated eyes were fixed in 50% pyridine:50% Carnoy's solution overnight, and then washed in tap water. Pigmented eyes then were bleached for 1-2 days in 3% hydrogen peroxide pribr to partial dehydration in 70% ethanol (overnight). After a 3- to 4-day incu- bation in 1.5% AgNO 3 (in distilled water) at 37°C, optic axons were stained by pyrogallic acid reduction. 6 Retinal whole mounts were prepared and examined for optic discs and organization of optic axons (Fig. 1). Phase contrast microscopy confirmed the staining of all or most optic axons and the essential correctness of the patterns seen in silver stains. Results. We found the following 11 distinct patterns of retinalfibersand optic nerve forms among the catfish examined (see Table 1 and Figs. 2A-K): (A) central optic nerve head and a radial pattern of relatively evenly spaced fascicles of fibers, as in most mammals; (B) ventral fissure with fibers entering in a smooth layer along the entire fissure as is common in birds; (C) radial pattern with six evenly spaced, well-isolated bundles; (D) radial pattern with 10 to 14 well-separated, but smaller, radial fascicles; (E)fibersenter the fissure in discreet fascicles, rather than in a smooth layer; (F) at least 25 separate and distinct optic discs on each side of the fissure, through which fibers exited; (G) a straight ventral line of four to six optic discs that dif- fered in size; (H) a single large optic disc on each end of a straight row of paired exit holes, located ventrally at the site of thefissure;(I) a single large exit centrally, a row of paired exits, and then a single row of one to five discs toward the retinal periphery. Slight variations were seen (in different species) that lacked the more peripheral singles; (J) forms that lacked the central large disc, but did include a row of paired exit points of varying size, and then one to five discs in a row 0146-0404/83/1000/1429/$1.00 © Association for Research in Vision and Ophthalmology Downloaded from iovs.arvojournals.org on 12/28/2019
Transcript of Multiple optic fiber patterns in the catfish retina. No. 10 Reports 1431 Fig. 2. Characteristic...
No. 10 Reports 1429
From the Department of Ophthalmology and Visual Science (Mi-chael Jacobson, Yog Raj Sharma, and Edward Cotlier) and the De-partment of Molecular Biophysics and Biochemistry (Jan Den Hol-lander), Yale University, New Haven, Connecticut. Supported byN1H Grants EY02490 and AM27121. Submitted for publication:July 29, 1982. Reprint requests: Dr. Edward Cotlier, Departmentof Ophthalmology, The New York Hospital, Cornell UniversityMedical Center, 515 E. 71 Street, New York, NY 10021.
References
1. Kinoshita JH, Kador P, and Catiles M: Aldose reductase indiabetic cataracts. JAMA 246:257, 1981.
2. Winegrad AI, Morrison AD, and Clements RS Jr Polyol pathwayactivity in aorta. In Vascular and Neurological Changes in EarlyDiabetes, Camerini-Davalos RA and Cole HS, editors. New York,Academic Press, 1973, pp. 117-124.
3. Chylack LT Jr, Henriques HF, Cheng H-M, and Tung WH:Efficacy of alrestatin, an aldose reductase inhibitor, in humandiabetic and nondiabetic lenses. Ophthalmology 86:1579,1979.
4. Varma SD, Mikuni I, and Kinoshita JH: Flavonoids as inhibitorsof lens aldose reductase. Science 188:1215, 1975.
5. Handelsman DJ and Turtle JR: Clinical trial of an aldose re-ductase inhibitor in diabetic neuropathy. Diabetes 30:459, 1981.
6. Sharma YR and Cotlier E: Inhibition of lens and cataract aldosereductase by protein-bound anti-rheumatic drugs: salicylate, in-domethacin, oxyphenbutazone, sulindac. Exp Eye Res 35:21,1982.
7. Peterson MJ, Sarges R, Aldinger CE, and MacDonald DP: CP-45, 634: a novel aldose reductase inhibitor that inhibits polyolpathway activity in diabetic and galactosemic rats. Metabolism28:456, 1979.
8. Clements RS, Morrison AD, and Winegrad AI: Polyol pathwayin aorta: Regulation by hormones. Science 166:1007, 1969.
9. Stevens VJ, Rouzer CA, Monnier VM, and Cerami A: Diabeticcataract formation: Potential role of glycosylation of lens crys-tallins. Proc Natl Acad Sci USA 75:2918, 1978.
10. Judzewitsch RG, Jaspan JB, Polonsky KS, Weinberg CR, HalterJB, Haler E, Pfeifer MA, Vukadinovic C, Bernstein L, SchneiderM, Liang K-Y, Gabbay KH, Rubenstein AH, Porte D Jr. Aldosereductase inhibition improves nerve conduction velocity in di-abetic patients. N Engl J Med 308:119, 1983.
Multiple Optic Fiber Patterns in the Catfish Retina
Beryn L. Frank and Stephen Goldberg
The retinas of certain catfish contain multiple optic discs.This report describes the patterns of optic nerve fibers andoptic discs as seen in silver-stained flat mounts, in 11 differentfamilies of catfish. As many as 50 optic discs may exist ina single retina, in paired and unpaired combinations, and inslit and ring-like arrays. Invest Ophthalmol Vis Sci 24:1429-1432, 1983
Multiple optic discs have been found in the retinasof a variety of species of fish, amphibians, and certainmembers of the deer family.1"5 The retinal fiber patternsof these animals do not appear to have been described.
In our studies of the retinas of a variety of fishes,we found that the feature of multiple optic discs is astriking peculiarity of the catfish retina. The presentstudy is an analysis of the variety of retinal fiber patternsin a broad range of catfish families, as seen with silver-stained flat mounts.
Materials and Methods. Forty-six species of catfish,representing 11 families, were examined for retinalfiber pattern. These included fish native to North, Cen-tral, and South America, Europe, Asia, India, Thailand,and Africa.
Enucleated eyes were fixed in 50% pyridine:50%Carnoy's solution overnight, and then washed in tapwater. Pigmented eyes then were bleached for 1-2 daysin 3% hydrogen peroxide pribr to partial dehydrationin 70% ethanol (overnight). After a 3- to 4-day incu-bation in 1.5% AgNO3 (in distilled water) at 37°C,
optic axons were stained by pyrogallic acid reduction.6
Retinal whole mounts were prepared and examinedfor optic discs and organization of optic axons (Fig.1). Phase contrast microscopy confirmed the stainingof all or most optic axons and the essential correctnessof the patterns seen in silver stains.
Results. We found the following 11 distinct patternsof retinal fibers and optic nerve forms among the catfishexamined (see Table 1 and Figs. 2A-K): (A) centraloptic nerve head and a radial pattern of relatively evenlyspaced fascicles of fibers, as in most mammals; (B)ventral fissure with fibers entering in a smooth layeralong the entire fissure as is common in birds; (C)radial pattern with six evenly spaced, well-isolatedbundles; (D) radial pattern with 10 to 14 well-separated,but smaller, radial fascicles; (E) fibers enter the fissurein discreet fascicles, rather than in a smooth layer; (F)at least 25 separate and distinct optic discs on eachside of the fissure, through which fibers exited; (G) astraight ventral line of four to six optic discs that dif-fered in size; (H) a single large optic disc on each endof a straight row of paired exit holes, located ventrallyat the site of the fissure; (I) a single large exit centrally,a row of paired exits, and then a single row of one tofive discs toward the retinal periphery. Slight variationswere seen (in different species) that lacked the moreperipheral singles; (J) forms that lacked the centrallarge disc, but did include a row of paired exit pointsof varying size, and then one to five discs in a row
0146-0404/83/1000/1429/$1.00 © Association for Research in Vision and Ophthalmology
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1430 INVE5TIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / October 1983 Vol. 24
Fig. 1. Typical silver-im-pregnated retinal flat mount,showing optic axon bundlesand multiple optic papillae inSorubim lima.
more peripherally; and (K) an oval ring containingvarying numbers of optic discs.
It is apparent from studying Table 1 that some fishconsidered closely related by present classifications mayhave radically different patterns. In all cases, the in-dividual optic discs connected with individual nerverootlets that fused into one optic nerve once outsidethe eye. Within the eye, individual axons were un-branched and, essentially, the nerve fibers associatedwith a given optic disc originated in the correspondingsector of retina.
Discussion. A number of closely related specieswithin one family (eg, Callichthyidae) demonstratedslightly different but very similar patterns. However,in some instances (eg, in the Loricariidae family) dif-ferent species showed radically different patterns (Figs.
2:B, D-I). One would expect fish closely related phy-logenetically to show similar, rather than divergent,patterns. Our study suggests that the present methodsand criteria used to place catfish species within ap-propriate families may be fallible and that there havebeen some erroneous classifications.
The variety of fiber patterns raises certain questionsabout the evolutionary and embryologic significanceof such nerve arrays. What, for instance, is the sig-nificance of an oval ring of optic discs? Does each exitrepresent a clustering of those neurons that adhereselectively to one another? Can the neurons associatedwith one disc trace common ancestry to one (or onegroup) of neuronal stem cells?
The topic of optic nerve organization is one of sig-nificant interest, and the species with multiple optic
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No. 10 Reports 1431
Fig. 2. Characteristic ret-inal fiber patterns in the var-ious species of catfish. Com-pare with Table 1.
nerve heads may be useful in analyzing such organi-zation. In all cases in this study, multiple optic nerverootlets combined to form a single optic nerve behindthe eye. Tracers such as horseradish peroxidase (HRP)can be injected into isolated optic discs to identifyoptic nerve and optic tract projections from isolatedsectors of the retina.
Recent studies8 suggest that certain catfish have ananterior (ipsilateral) projection to the brain. The presentstudy did not reveal any asymmetry in the fiber patternthat might relate to the question of an ipsilateral pro-jection, but tracer studies may help to clarify this.
We found no evidence for the presence of centrifugalfibers in the catfish retina. Ganglion cell bodies didnot stain clearly and the origins of fibers from ganglioncells could not be observed. In the mouse retina, wedetected probable centrifugal fibers by noting branchingof some axons as they were traced back from the opticdisc.9 We have not detected such branching in catfishretinas. In the chick, numerous centrifugal fibers weredetected by observing sprouting on the disc side ofretinal lesions.10 Although we have not performed sim-ilar lesions in the catfish retina, we have done so inthe goldfish (unpublished observations) and found no
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1432 INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / October 1983 Vol. 24
Table 1. Optic fiber patterns in the various species of catfish
Genus/species
Pattern AKryptopterus bicirrhus (2)
Pattern BAncistrus trivadiatus (2)Corydora julii (4)Corydora punctatus (1)Dianema longibarbis (4)Hypostomus bolivianus (2)Hypostomus plecostomus (2)
Pattern CAcanthadoras spinosissimus (2)
Pattern DAgamyxis peclinifrons (2)Amblydoras hancockii (1)Pseudodoras niger (2)Platydoras costatus (1)Rineloricaria parva (1)Bunocephalus coracoideus (2)
Pattern EPanaque Nigroulieatus (2)Ancistrus dolichopterus (2)Brochis coerlelus (2)Corydora agassizi (4)Corydora arcautus (1)
Pattern FAncistrus temmincki (2)Corydora agneus (10)Plecostomus Sp. (2)
Common name
glass cat
branched bristle noseleopard catspotted corydoraporthole catBolivian Hypostomusspotted plecostomus
Spiney Talking cat
spotted rafielcroaking catBlack Doradidstriped rafielwhip tail2-colored banjo
Royal Plecostomusbushy mouthedshort bodiedAgassi's corydoraskunk corydora
bristle nosedbronze/green corydorablue-eyed plecostomus
Family
Siluridae
LoricariidaeCallichthyidaeCallichthyidaePimelodidaeLoricariidaeLoricariidae
Doradidae
DoradidaeDoradidaeDoradidaeDoradidaeLoricariidaeAspredinidae
LoricariidaeLoricariidaeCallichthyidaeCallichthyidaeCallichthyidae
LoricariidaeCallichthyidaeLoricariidae
Genus/species
Pattern GFarlowella acus (2)Kryptopterus macrocephalus (4)
Pattern HOtocinclus arnoldi (5)
Pattern ILoricaria filamen tosa (4)Pangasius sutchi (6)Synodontis alberti (4)Synodontis decorus (2)Synodontis nigriventris (4)Synodontis notatus (4)Synodontis pleurops (2)
Pattern JParauchenoglanis guttatus (4)Sorubim lima (4)Synodontis sp. (2)Synodontis nyassae (2)
Pattern KHelogenes Mormoratus (2)Ictalurus lacustris (2)Ictalurus punctatus (4)Leiocassis siamensis (1)Mystus tengera (2)Pimelodus blochii (2)Pimelodus picta (angelicus) (1)Pimelodella gracilis (6)Synodontis acanthomias (2)Synodontis melanostictus (2)
Common name
Poor Man's Glass
Arnold's sucker
whip tailirridescent sharkspotted AfricanClown Africanupside downspotted synodontis
African flatheadshovel noseLace synodontis
Marblealbino channelblue channelbarred Siamesefour linespotted pimelodusangelicastinging
Family
LoricariidaeSiluridae
Loricariidae
LoricariidaePangasiidaeMochokidaeMochokidaeMochokidaeMochokidaeMochokidae
BagridaePimelodidaeMochokidaeMochokidae
HelogeneidaeIctaluridaeIctaluridaeBagridaeBagridaePimelodidaePimelodidaePimelodidaeMochokidaeMochokidae
Compare with figure 2. Numbers in parentheses indicate the number of eyes examined (eg, "2" means left and right eyes from the same fish; "4" means left and right eyes from two fish,etc.).
sprouting on the disc side of lesions. Such negativedata, however, are not conclusive. Fiber tracing, usingHRP, will likely prove more useful in resolving thematter of centrifugal fibers, as well as other issues ofoptic pathway organization.
Key words: retina, optic disc, optic axons, catfish
From the University of Miami School of Medicine, Department
of Anatomy and Cell Biology, Miami, Florida. Supported in part
by National Institutes of Health grants EY02579-02 and 5-R01-
EY1981-04. Submitted for publication: December 28, 1982. Reprint
requests: S. Goldberg, University of Miami School of Medicine,
Department of Anatomy and Cell Biology (R124), P.O. Box 016960,
Miami, FL 33101
References1. AH MA and Anctil M: Retinas of Fishes: An Atlas. Berlin,
Springer- Verlag, 1976.
2. Arnott HJ, Best ACG, Ito S, and Nicol JAC: Studies on the eyes
of catfishes with special reference to the tapetum lucidum. Proc
R Soc Lond (Biol) 186:13, 1974.
3. Wagner HJ: Der Bau der Retina and der Multiple Optischen
Papillae bei Swei Synodontis-Arten (Teleosti, Siluroidea). Z
Morph Tiere 68:69, 1970.
4. Wagner HJ, Menenzes NA, and AH MA: Retinal adaptations
in some Biazilian tide pool fishes (Teleosti). Zoomorphologie
83:209, 1976.
5. Walls GL: The Vertebrate Eye and Its Adaptive Radiation. New
York, London, Hafner Publishing, 1963.
6. Goldberg S and Frank B: Pyridine-silver methods for the study
of optic axons in retinal whole mounts. Stain Technol 54:21,
1979.
7. Goldberg S, Frank B, and Krayanek S: End bulb swellings and
rapid retrograde degeneration following retinal lesions in young
animals. Exp Neurol, in press, 1983.
8. Rao PDP and Sharma SC: Retinofugal pathways in juvenile
and adult channel catfish Ictalurus (Ameiurus) punctatus: an
HRP and autoradiographic study. J Comp Neurol 210:37, 1982.
9. Goldberg S and Galin MA: Response of retinal ganglion cell
axons to lesions in the adult mouse retina. Invest Ophthalmol
12:382, 1973.
10. Goldberg S and Frank B: Will central nervous systems in the
adult mammal regenerate after bypassing a lesion? A study in
the mouse and chick visual systems. Exp Neurol 70:675, 1980.
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