Some suggestions concerning vertebrate visual cells

mfm ReJ. vol. 8. pp. 483-. 488pcrpmon Prm1968.RbuadiaanuBriuin.

LETlXRTOTHEEDITORS

SOME

SUGGESTIONS

CONCERNING VISUAL CELLS

VERTEBRATE

(Rec&ed 30 November 1%7)

THE CONCBPTof two categories of vertebrate visual cells-rods and cones-has served well since it was originally propounded by MAYC S~HULT~~ (1866) a century ago. It has been particularly successful in interpreting most of the observed facts relating to placental mammals. However in most other vertebrate groups the visual cell structures and patterns are more complex; WALU (1942) surveyed the field and made a large personal contribution to our knowledge. Two widespread organelles not found in placental mammahan oil-droplet, often coloured, and a refringent body of glycogen, the paraboloid-although generally found in cones do occur in some rods (class&d by the shape of their outer segments). Walls more gravely compromised the traditional distinction by adducing evidence in support of the idea that visual cells may undergo evolutionary transmutation; his most persuasive cases relatul to transmutation of cones to rods in geckos and in the Lmnpropcltis-Arizosla-Cmrophorh~~ ties of snakes, they have been amply 1956, uND3RWODD 1951,1%7a). supported by further evidence (Cw Studies of the fine structure of visual cells by electron microscopy have revealed no new sharp differences between the inner segments of rods and cones (reviewed by PEDLW 1965a and b). Pedler’s studies of the foot pieces co&m the distinctness of the two types recognised by metallic impregnation techniques. There are small (rod) footpieces that receive only one, two or, at most, three dendrites from bipolar or horizontal cells and large (cone) footpieces that receive from two hundred to five hundred dendrites. However, in Alligator KALBERERand PED~ (1963) found a minority of cone-like outer segments amongst very numerous rod-like outer segments in combination with a majority of large complex pedicles and relatively few small simple pedicles. The conclusion was inescapable that there must be many cells with “rod” outer segments and “cone” footpieces. The authenticity of the rods by classical criteria is supported by Crescitelli’sfinding of rhodopsin in the dark adaptedretina (1956). The distinction between the rods and cones was further compromised by the observation that many cells with rod outer segments contain a paraboloid, a supposedly cone organelle. My own observations on the snake Vipera berw indicate that it has more than 50 per cent rod outer segments but very few, if any, simple pedicles. These observations suggest that the differentiation of visual cells in ontogeny involves the activation of several operationahy discrete groups of genes; that in the evolution of Alligator there has been a trend towards evocation of an increasing proportion of complex pedicles and that the evocation of complex pedicles and paraboloids is not or is not completely, linked to the evocation of cone outer segments, thus giving rise to a new type of visual cell: a rod with a complex pedicle. The other mode of origin of such a new cell 483

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bTTERTOTHB~l'l'ORS

type is by the evolutionary enlargement of the cone outer segments of a pure cone retina to become rod-like outer segments, as in geckos, in continuing association with complex pedicles (F%DLER and TILLY 1964). Thus we can recognise two kinds of evolutionary transformation of visual cells: “Walls transformation” by gradual evolutionary change of a cell organelle from one type to another and “Pedler transformation” by mosaic recombination, in cellular morphogenesis, of discrete types of organelles (Fig. 1). These two kinds of evolutionary change, clearly shown by visual cells, may well occur in other cells in other tissues.

Flo. 1. Diagram of WaUs transformation, based on inferred history of geckos. Ron bottom to top: cone of diurnal lizard; intermediate cell of partially modified noctumal lizard (as seen in ~anrrcsia); primitive gecko rod (as seen in Arisrclfiger); fully converted geckorod (as sum in Coleonyx). Diagram of Pedler tr~sfor~tion. From bottom to top: hy~t~~ retina moderately modified in association with nocturnal habits with cones containing paraboloids but iacking oil-droplets and with oligosynaptic rods; hypothetical retina with polysynaptic pedicles to some rods; extensively modified retina with numerous polysynaptic rods, some of them with paraboloids (as seen in Alligator). c=colourless oil-droplet, y= yellow oii-droplet.

I suggest that some revision of visual cell terminology is required to accommodate this new knowledge. Clearly the recognition of two categories of outer segment remains valuable; COHEN (1963) has stressed that the distinction is so widespread that it must

Some Suggestions (hncem&

vertebrate visual cells

485

surely have some functional significance. I suggest that we return to the original use of the terms “rod” and “cone” based solely on the form of the outer segments. Where we have clear evidence of transmutation, as in geckos, we may speak of “secondary rods” and where the transmutation has taken place in the presence of “ordinary” rods, as in boigine snakes (UNDERWOOD 1966), we may distinguish in the one retina between “primary rods” and “secondary rods”. For the simple footpiece I suggest the term “oligosynaptic pedicle” and for the large complex footpiece “polysynaptic pedicle”. Pedler’s three categories of visual cells would thus become “polysynaptic cones” (group A “insensitive multi-channel differentiators”), “polysynaptic rods” (group B “sensitive multi-channel differentiators”) and “oligosynaptic rods” (group C “sensitive single channel integrators”). If we wish to abbreviate these terms we can use the Greek initial letters (to avoid confusion with the Roman letters already in use), viz x-cones (pi-cones), x-rods (pi-rods) and o-rods (omicron-rods). If we base the distinction between rods and cones solely on the shape of the outer segments then the term “duplex retina” would mean “retina possessing both rod and cone type outer segments”. A retina possessing both oligosynaptic and polysynaptic pedicles could conveniently be termed “heterosynaptic”. Most duplex retinas, as usually understood, would thus be “duplex heterosynaptic”. Roman letters can continue to be used to denote the several cell types in one retina, distinguished by the other organelles (oil-droplet, paraboloid) or by the cell interrelationships (doubles, twins). For lixards Walls used the letters “A” and 3” for the single and double cells respectively; these letters can be applied to cones (diurnal lixards) or rods (geckos). For snakes Walls used the letters “A” and ‘3” for the large single and double cells respectively @ones in most snakes) and “C” and “C”’ for smalI single cones and small single rods respectively. UNDERWOOD(1951) found a second type of double cell in geokos and called it type “C”. DUNN (1966) objected that the letter “C” had already been used for a visual cell type in snakes and called these double cells type “D;‘. By this time however UNDERWOOD(1966) had already used “D” for Walls’ type “c”’ cell of snakes on the grounds that “C” and “C”’ are confusing designations for discrete cell types. Surely the same letters applied to different groups of animals will not be. confusing if we indicate the group under consideration. Otherwise we can scarcely avoid relettering the type B double cells of snakes that are so different from the type B double cells of tetrapods that the two can scarcely be homologous. A further source of confusion lies in the naming of the parts of double cells. The double cells of marsupials, monotremes, birds, lizards, crocodilians, chelonians, amphibians and a few Ssh, but not of snakes, share a common plan (Wm 1942). There is a cell that usually contains a large paraboloid (not in mammals), this cell never contains an oil-droplet (except in Australian marsupials). Applied to this large cell is a slender member that partly embraces the paraboloid of the larger and never itself contains a paraboloid; this slender member contains an oil-droplet when this is present in the single cells, and occasionally when it is not (Fig. 2). For these two members of a double cone Walls translated the German terms “Hauptxapfen” and “Nebenxapfen” as “chief cone” and “accessory cone”. This interpretation of the status of the members is supported by the observation of N-N (1964) that the chief member of a frog double cone makes the same contacts with other visual cells as do the single cones; it is the accessory member that makes different contacts. It is nevertheless evident that a number of workers find it confusing to call the larger member “accessory” and the smaller “chief”, indeed in a number of studies the terms are

486

Standard tetrapod

Ro. 2. TJxee rypesof double cells; the transversesections are at the level of the r&in~t body (rb). In tbe standard tetrapod double c4l tbe refringent body is a paraboloid of glm; in the advanond m the rcfringent body consists of several large mod&d mitochondria; in the snake the lafrialpln body consists of granules witbin the mitochomiria, the peripheral cell of the snake has an aggregation of paramzlear mitockmdria (p).

reversed (CARASO 1956, KALBERER and PEDLER 1963, PEDLERand TILLY 1964, YASUZUMI, TEZUICAand IKEDA 1958). The double cells of snakes were first properly described by Walls. The disparity in size of the two members is greater than in other double cells. In this case however the larger member (“chief” of Walls) closely resembles the large single (type A) cells of the same retina, the smaller member (“accessory” of Walls) is very slender and lies alongside the larger; it is unique in possessing a “paranuclear body” closely applied to the outer side of the nucleus. TANSLEY and JOJZINSON (1956) showed that the ellipsoids of the cones of Nat& nut& are refringent. My own observations indicate that there are refringent bodies within the ellipsoids of the large type A cells and the chief me s bets of the double cells, but not in the accessory members or the small (type C) cones (UNDERW~D 1967b and Fig. 2). Further, the paranuclear body turns out to be an aggregation of mitochondria (YAMADA,ISHIKAWAand HATAB, 1966, on Eluphe and personal observations on Vipera and Heterodon). Here again detailed study supports Walls’ use of the terms chief and accessory. No~ths~ding the differences there are resemblances to the double cells of tetrapods; the large central member contains a refringent body, the smaller member lies to one side of and is closely applied to the larger. I suggest therefore that we may conveniently call the larger member the “axial cell” (=accessory of tetrapods, chief of snakes) and the smaller member the “peripheral cell” (=chief of tetrapods, accessory of snakes); these topographic terms can hardly give rise to confusion. The functional significance of double cells has remained a mystery since their discovery. A former colleague,, Dr. Michael Locke, now of Western Reserve University, suggested, on seeing tangential sections of gecko retina, that they may serve as polarised light analysers. The structure certainly seems to be compatible with this idea, In tetrapods and, as is now clear, in snakes also the incident light passes through a refringent body in the axial cell before reaching the outer segment. The refringent body should scatter light preferentiahy in the plane of polarisation. The outer segment of the peripheral cell lies to one side of

that of the axial cell. So if the synaptic co~cctions allow comparison of the signals from the two members of a double cell we have a system that should be able to detect polarisation of light. Further support for this idea is provided by the observations of PBDLBnand TILLY(1964) on gecko visual cells. In the double cells of some geckos the paraboloid is greatly reduced, but there is dense refiingent material within the mitochondria of the axial ellipsoid; one refringent body has been supplanted by another within the group (Fig. 2). Double cones are numerous in the retinas of birds and we may wonder in passing whether an ability to detect the plane of polarisation of light coming from the sky might assist their navigation, as it does that of bees. The above discussion would not hold good for the type C double cells that are seemingly universal in and pecuhar to geckos (UNDERWOOD 1951, TANSEY 1959 and 1961, DUNN 1966). The Australian lizards of the family Pygopodidae, undoubtedly related to geckos, have a visual cell mosaic resembling that of geckos save that there arc no type C doubles (Fig. 3); d the horizontal rows of type B doubles there are two sires of single cells that clearly correspond with the two sines of single cones reported by VxLr5u (1951) for Lmerta and Sphenodon and observed personally in other lizards and in the turtle Ckslydra (Fig. 3). In Aiwlis the larger single cones have a yellow oildroplet, the more slender 8

lizard

PYWPOd

Gecko

colourless droplet. Gecko type C double ceils have clearly orig&&d by union of the two sizes of single cones common in other lizards. I suggest that these two sizes of single cones be known as “major” and “minor” cones (they may be lettered Ai and A2 mepectively) and that the terms major and minor be also applied to the mg members of gecko type C double cells. Where two identical cells are joined together we may foIlow Walls in calling them “twin cells” (found in fish and geckos).

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LElWRTO-iTIEEDITORS

~~D~w~D 1%7a) have Both placental mammals and lower snakes (~enop~~a, lost doubie cells and have a simple pattern of single rods and cones. A few higher snakes retain this simple pattern (Pareas, Pseudoboa, Calemelaps, Atractmpr;P) but the great majority of those examined have double cells of peculiarly ophidian type. The double cells of snakes are so different from those of tetrapods that Walls is surely correct that they were redeveloped within the group as the eye was re-elaborated and vision reinstated as an important sense. It is noteworthy that in contrast with snakes no placental mammal with good eyes is knowk to have double cells. If ever we achieve control of human evolution it may be worth bearing this in mind. GARTHUNDBBWOOD*

Ac~~unindslJttdtoDr.RBUsrARDfora~OfthCA~~~ brtrton&,to Mr. D. N. SIWETfor an adder, V@eruherw, and to Dr. D. A. RCWJWAN for a rpecimen of the Hath&l&ananakei?Jii#r&wM=r. REFZRBNCRS cytopksmiques inframicmscopiques au niveau CAMMO, N. (1956). Mkc en 6vidssu-xde pr-ts du seament intwne das celhdes visuetks du gauko (Reptile). Cr. hebd. skurc. bad. Sci., Paris 242. 2988-&m CulmN, A,#(1963). v&&sate mtinal ealk and the& orgaokation. Bid. Rrv. ss, 427-459.

w F. (1956). Tbs natusu oftha gaeko viatml pigmtmt. I: gen. P&rfoi. 40.217-231. Dtmrs, R F. (1966). Studks on tba satina of Coleonyx mrt$far~. J. Ultrmtrnct. Res. 16, 651-692. w M. and ~IXSR, C. (1963). The visual cells of the a&&or: an eketron microscopic study. v&us RUE.3.323-329. NW, S. B. G. (1964). Interraxptor contacts in the retina of the frog (Rrrrtapipiens). J. U&rastruct. Res. 11,147-X65.

~EDLER, C. (1965a). Rods and wnes-a fiperimentul

fresh approach. Ciba Fownabtion Symposium on Physiology and Psychabgy of Caloar Vtsion, edited by G. E. W. Wolstenholme and J. Knight, Churchill,

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ppasctrjArch. ges. Physiol. 268, 213-220. Tm,

K. (1961). The mtina of a diurnal gecko Phebna madqtascariensis baghmdaee. Pfl*ers Arch. g&l. Physibl. m, 262-269. TNWLBY,K. and J~~~QK#N, B. K. (1956). The cones of the grass snake’s eye. Natare, Load. i78,1285-1286. UNDQ~WOOD, G. (1951). Kept&m retinas. Nuture, Land 167. 183-185, U~~anwooo, G. (1966). Gn the visual-cell pattern of a homalopsine snake. J. Anat. 160, 571-575. UNDO? G. (1967a). A anttrt~ to the classification of snakes. British Museum (Natural History), . UNDEEVWOD, G. (lW7b). A comprehensive approach to the ckssiition of higher snakea. Harpsobgica 23.161-168.

Vnsau, V. (1951). Vakur morphologique des photor&epteun retiniens chez la Hatterie (Sphcnodon punctatnt). Cr. he& semc. Acad. Sci., Paris 145.20-23. WAI,U, G. L. (1942). The v&&rate eye and its adaptive radiation. B& Cranbraok Inst. Sci, 19, l-785.

Y-A, H, Issng~w~, T. and HATA&T. (1966). Some obsc?rvationson the retinal tine structum of the S&h Znt. Gong. E?ectron Micrasasc., Kyoto, H, 495-496. snake. J?@hec~. YMIJZUW, G., ‘bzuK~, 0. and VA, T. (1958). The submicroscopiCstmcture of the iMCI mt8 of tlgsg

and cones in the retma of Vrolarodia strtata var. abmestica Flomr.

IPresent address: Sir John Cass College, Jewry St., London, E.C.3.

J. Uitrastrnct. Res. 1,