Post-Receptoral Mechanisms of Colour Vision in New World Primates

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Vision Research 38 (1998) 3329–3337

Post-receptoral mechanisms of colour vision in new world primates

Luiz Carlos L. Silveira a,*, Barry B. Lee b, Elizabeth S. Yamada a, Jan Kremers c, David M. Hunt d a Departamento de Fisiologia, Uni6ersidade Federal do Para´, Centro de Cieˆncias Biolo´gicas, 66075-900 Bele´m, Para´, Brazil b Department of Neurobiology, Max Planck Institute for Biophysical Chemistry, Am Fassberg, D-3400 Go¨ttingen, Germany c Department of Experimental Ophthalmology, Uni6ersity of Tu¨bingen Eye Hospital, Ro¨ntgenweg 11, D-72076 Tu¨bingen, Germany d Department of Molecular Genetics, Institute of Ophthalmology, Uni6ersity College London, London, England, UK Received 10 July 1997; received in revised form 29 September 1997

Abstract

Diurnal platyrrhines, both di- and trichromats, have magnocellular (M-) and parvocellular (P-) retinal ganglion cells which are morphologically very similar to those found in catarrhines. Catarrhine central P ganglion cells contact single midget bipolar cells, which contact single cones. Physiological recordings of retinal ganglion cells of dichromatic Cebus monkeys showed very similar cell properties to the catarrhine macaque, except that P ganglion cells lacked colour-opponency. We describe the presence of single-headed midget bipolar cells in the Cebus retina. These midget bipolar cells have axon terminal sizes in the same range as the dendritic tree sizes of P ganglion cells as far as 2 mm of retinal eccentricity. This result supports the view that, as in catarrhines, central P ganglion cells of platyrrhines receive input from single midget bipolar cells which in turn, receive input from single cones. This ﬁnding is consistent with the idea that a P pathway with one-to-one connectivity was present in the anthropoid ancestor before the divergence between catarrhines and platyrrhines. © 1998 Elsevier Science Ltd. All rights reserved.

Keywords: Bipolar cells; Ganglion cells; Color opponency; Trichromacy; Dichromacy

1. Introduction Others species have mixed populations of trichromatic and dichromatic individuals [5–13]. There are also spe- The only mammals enjoying trichromatic vision are cies in which all individuals are monochromats [14,15]. primates. This ability arises from receptoral and post- This diversity in colour vision phenotypes among receptoral retinal mechanisms, whose output is con- platyrrhines poses the question of whether such diver- veyed via the lateral geniculate nucleus (LGN) to the sity is reﬂected in the post-receptoral mechanisms. primary visual cortex. The retina of all Old World The morphology of retinal neurones has been investi- anthropoids, the catarrhines, have three different cone gated in some platyrrhines. Ganglion cells were studied classes. Cone photopigments are very similar in all in Saimiri [16], Cebus and Aotus [17–20] and Callithrix catarrhine species, including human trichromats, with [21–23]. There are also a few studies dedicated to the absorbance spectra peaking at 430, 535 and 565 nm, for physiology of the retinal ganglion cells and LGN relay the short-, middle- and long-wavelength sensitive cones neurones of some platyrrhines, such as the Ateles [24], (SWS-, MWS- and LWS-cones), respectively [1]. Saimiri [25,26], Aotus [27], Callithrix [28–31] and Cebus In contrast to the catarrhines, the New World an- [32]. thropoids, the platyrrhines, display a remarkable vari- The Cebus retina is a valuable model for comparative ety of phenotypes [2,3]. There are species exhibiting full studies. It differs from the retina of another frequently trichromacy similar to the one found in catarrhines [4]. studied platyrrhine, Callithrix jacchus. The Cebus retina is of larger size and has a smaller cone density than the * Corresponding author. Tel.: +55 91 2111616; fax: +55 91 Callithrix retina. On the other hand, the Cebus retina is 2111568; e-mail: [email protected]. similar in size [33] and has a similar photoreceptor [34]

0042-6989/98/$19.00 © 1998 Elsevier Science Ltd. All rights reserved. PII: S0042-6989(97)00335-0 3330 L.C.L. Sil6eira et al. / Vision Research 38 (1998) 3329–3337 and ganglion cell density [33] to the retina of Macaca deeply anaesthetised state by the intramuscular admin- fascicularis, one of the better studied catarrhines, mak- istration at 1–2 h intervals of 0.5–1.0 ml/kg of a 1:4 ing the direct comparisons between dichromatic anaesthetic mixture of 2% xylidine-tiazine chlorhydrate platyrrhines and trichromatic macaque monkeys easier. solution (Rompun, Bayer, Sao Paulo, SP, Brazil) and In catarrhines, central parvocellular (P) ganglion cells 5% ketamine chlorhydrate solution (Ketalar, Parke- contact single midget bipolar cells which, in turn, re- Davis, Guarulhos, SP, Brazil). The animals were moni- ceive input from single MWS- or LWS-cones [35–37]. tored by electrocardiography and body temperature This neural circuit constitutes the basis for red-green was continuously measured and kept near 37°C. Sur- colour opponency of trichromatic primates [38]. In this vival time ranged between 16 and 48 h. After this study, we addressed the question of whether dichro- period, animals received a lethal dose of Thionembutal matic platyrrhines also have such a circuit, despite (Abbott, Sao Paulo, SP, Brazil) and were then perfused lacking red-green colour-opponency. Of considerable transcardially with 0.9% NaCl buffered solution, fol- importance is whether dichromatic Cebus monkeys lowed by 4% paraformaldehyde in 0.1 phosphate buffer have midget bipolar cells with axons that establish the (pH=7.2–7.4). After perfusion and retinal dissection, same, one-to-one, connections with P ganglion cells as the Biocytin labelling was revealed using the method of those seen in catarrhines. Foveal P ganglion cells of Picanço-Diniz et al. [39]. The procedure involves im- dichromatic Cebus monkey have dendritic tree sizes mersion for 30–60 s in a 0.1% collagenase (Boehringer- similar to the P ganglion cells found in the fovea of Mannheim, Germany) solution, incubation for 12–48 h humans, macaques and other catarrhines [19]. This in ABC solution (Standard Kit, Vector Laboratories, makes Cebus a suitable species to investigate this Burlingame, CA), and peroxidase histochemistry using question. 3,3%-diaminobenzidine tetrahydrochloride (DAB; In the present paper we describe results on the mor- Sigma) as chromogen. phology and physiology of the retinal post-receptoral mechanisms of dichromatic Cebus monkeys and com- 2.3. Carbocyanine labelling of retinal neurones pare them with those obtained in catarrhines and other platyrrhines. Our results show that Cebus monkeys After perfusion with saline and fixative solutions (see share many similarities with catarrhines. The results above), the retina was dissected and small crystals of support the idea that, in contrast to the difference at 1,1%,dioctadecyl 1-3,3,3%,3%tetramethylindocarbocyanine the receptoral level, the post-receptoral mechanisms are perchlorate (DiI; Molecular Probes, Eugene, OR) were highly conserved among anthropoids. inserted in the retinal tissue. The retina was kept in fixative for a period of 4–21 days. The labelling was then photoconverted to a DAB product using a mer- 2. Material and methods cury lamp (HBO 200 W/4, Carl Zeiss).

2.1. Animals 2.4. Morphometric analysis

The retinas of 15 adult male capuchin monkeys, Outlines of cell bodies, dendritic trees and axonal Cebus apella, were studied using three different meth- terminals of selected cells were performed using a cam- ods. Retinal ganglion cells of seven animals were retro- era lucida attached to a microscope (Nikon Labophot grade labelled after the deposition of Biocytin in the 2, Garden City, NY) under a ×100 oil immersion optic nerve. Single unit recordings of retinal ganglion objective with a ﬁnal magniﬁcation of ×1500. The cells were performed in six animals. Retinal neurones of areas of the contours were measured using a bit pad three animals, one of them also used for retinal record- connected to an IBM-PC microcomputer. The contour ing, were post-mortem labelled with carbocyanine. The sizes were expressed as diameters of circles having animals were bred in the Centro Nacional de Primatas equivalent areas, and plotted as a function of distance (CENP, Ananindeua, State of Para´, Brazil). All the to the fovea. Retinal eccentricity was normalised to a experiments were performed observing the NIH Guide- fovea-optic disk distance of 3.190.1 mm, which corre- lines regarding the care and use of animals for experi- sponds to measurements performed in non-retracted mental procedures. Cebus retina [33].

2.2. Optic ner6e deposit of Biocytin 2.5. Single unit recording

A detailed account of the whole method has been Retinal recordings were performed in six adult males. published previously [39]. Biocytin (Sigma, St. Louis, Standard recording techniques for Old World monkey MO) deposits in the optic nerve were performed under retina were employed [40]. Ganglion cell activity was aseptic conditions. Animals were maintained in a recorded with a tungsten-in-glass microelectrode low- L.C.L. Sil6eira et al. / Vision Research 38 (1998) 3329–3337 3331 ered into the retina. Cells were initially classified by descends to branch in the outer or inner third of the their response to flashed spots, using criteria developed IPL, forming a very small dendritic bouquet, with a for thalamic and retinal neurones of macaque monkeys diameter of 891.6 and 791.3 mm at 0.5 mm temporal [40–42]. Some aspects of responses, such as time and nasal to the fovea, respectively. Towards the retinal course, spectral sensitivity, and temporal contrast sensi- periphery, the dendritic trees of Cebus P ganglion cells tivity, were studied in more detail. Stimuli were pre- have a characteristically dense, bushy branching pat- sented through a Maxwellian view system [43] and were tern. Their size changes very little up to about 2 mm of composed of the light emitted by three LEDs, whose eccentricity and then steadily increases, reaching about dominant wavelengths were 638, 554 and 470 nm. By 100 mm at the far periphery. Cells located in the nasal appropriately adjusting the relative luminance of the quadrant are smaller than those located in the tempo- three LEDs, it was possible to stimulate cell receptive ral, dorsal and ventral quadrants of the retina [19]. fields with luminance or chromatic flicker, or to isolate Foveal P ganglion cells of the dichromatic Cebus mon- the MWS- or LWS-cone mechanism by silent substitu- key have very small dendritic tree sizes, similar to P tion. Photopigment genotypes were assessed by molecu- ganglion cells found in the fovea of trichromat primates lar genetic analysis, using the single-strand such as humans, macaques and other catarrhines. conformation polymorphism method [28]. The capability of the axon terminals of midget bipolar cells of dichromatic Cebus monkeys to establish one-to-one connections with P ganglion cells was inves- 3. Results tigated using anterograde and retrograde diffusion of DiI. Distinct classes of bipolar cells were labelled in the 3.1. The P pathway of the Cebus monkey Cebus monkey retina, including midget bipolar (MB), SWS-cone bipolar (BB), diffuse bipolar (DB) and rod We studied only male Cebus monkeys which have bipolar (RB) cells, as well as H1 and H2 horizontal been found to be exclusively dichromats [7]. In a group cells, several classes of amacrine cells, and ganglion of six animals, electrophysiological measurements confi- cells. Two subclasses of MB cells were stained (Fig. 2); rmed that all subjects were dichromats. In addition, we one class had cell bodies located in the outer half of the determined which MWS/LWS cone photopigment was inner nuclear layer (INL) and axon terminals branching present in each individual [32] using heterochromatic in the inner third of the IPL (Fig. 2A–D), and the flicker photometry and a phase paradigm [28,44]: four second class had cell bodies located in the central of them had the 562 and two the 535 nm photopigment. region of the INL and axon terminals branching in the Subsequent molecular analysis supported this outer third of the IPL (Fig. 2E–G). The first subclass conclusion. of MB cells in the Cebus match the morphological Retinal ganglion cells of several distinct classes were description of the invaginant MB (IMB) cells of labelled by retrograde transport of Biocytin. The qual- catarrhines, while the second subclass corresponds to ity of dendritic labelling allowed us to classify and the flat MB (FMB) cells of catarrhines [36,47–50]. measure cells at different distances from the fovea. The FMB and IMB cells with either single or double majority of the retinal ganglion cells of the Cebus dendritic bouquets were observed. ‘Single-headed’ cells monkey could be classified as magnocellular (M) or were found at all eccentricities whilst ‘double-headed’ parvocellular (P) ganglion cells (also called parasol and cells were present only at eccentricities larger than 5 midget ganglion cells), following criteria previously em- mm. Fig. 2(H and I) illustrates an example of a ‘dou- ployed for catarrhines [35,36,45]. Cebus M ganglion ble-headed’ FMB cell located in the nasal periphery. cells have large cell bodies, and large, radiate dendritic The cone mosaic was observable in the same prepara- trees, whilst P ganglion cells have small cell bodies, and tion. The spacing between the dendritic bouquets of small, bushy dendritic trees. Their morphology and size ‘double-headed’ FMB and IMB cells is similar to the are similar to their catarrhine counterparts at equiva- cone spacing. Thus, whilst ‘single-headed’ FMB and lent visual field eccentricities [19,20]. Both cell classes IMB cells contact a single cone, ‘double-headed’ cells occur in two varieties, one with dendrites branching in contact two neighbouring cones. the outer half of the inner plexiform layer (IPL), and In the Fig. 3, the diameters of FMB and IMB axon another with dendrites branching in the inner half of terminals are compared to the dendritic tree diameters the IPL. In catarrhines, the inner and outer subclasses of P ganglion cells at different distances from the fovea. of M and P ganglion cells correspond to the on and off A total of 441 P ganglion cells were measured, 419 from varieties of receptive fields [46], and it is likely to be the the temporal or nasal quadrants, and 22 from the same in platyrrhines. dorsal periphery. Since there is no significant difference Fig. 1 illustrates the change with eccentricity of the between the diameters of outer and inner P ganglion dendritic trees of Cebus P ganglion cells. In the central cells [19], they were plotted together. A total of 23 MB retina, these cells have a single primary dendrite which cells were measured; the IMB and FMB cells have been 3332 L.C.L. Sil6eira et al. / Vision Research 38 (1998) 3329–3337

Fig. 1. Dendritic tree of P ganglion cells at increasing distances from the fovea. Cells were retrogradely labelled with Biocytin deposited in the optic nerve. All cells are from the retina of a dichromatic Cebus monkey. (A) Inner P cell, 0.57 mm temporal. (B) Inner P cell, 0.92 mm temporal. (C) Two inner P cells, 1.4 mm temporal. (D) Outer P cells, 2.2 mm temporal. (E) Outer P cell, 3.2 mm temporal. (F) Outer P cell, 4.5 mm temporal. (G) Outer P cell, 11 mm dorsal to the fovea. Scale bar=25 mm. plotted with different symbols in Fig. 3. In the central as M or P. We have therefore relied on the achromatic region, up to 2 mm from the fovea, MB axon terminals temporal characteristics of their responses to make the and P dendritic trees are similar in size. At more distinctions. Using this method, we have identified two peripheral regions, they increase at different rates, and cell classes with distinct properties, which we regard as P dendritic trees become much larger than the MB putative M and P ganglion cells. Both have concentri- axon terminals (Fig. 2E). We conclude that the midget cally organised receptive fields. In Fig. 4, we have bipolar system in Cebus is similar to that of catarrhines. compared the responses of M and P ganglion cells to We have also studied the physiological aspects of the luminance pulses of different contrasts. The stimuli P pathway of dichromatic Cebus monkeys. In the ab- were presented in Maxwellian view and both the centre sence of red-green colour-opponency in the retina of and surround regions of the receptive field were stimu- these animals, it is difficult to classify the ganglion cells lated. P cells are relatively insensitive to contrast and L.C.L. Sil6eira et al. / Vision Research 38 (1998) 3329–3337 3333

Fig. 2. Midget (MB) bipolar cells of dichromatic Cebus monkey. Cells were labelled by retinal deposits of DiI. (A–C) Axon terminals, cell bodies and dendritic bouquets of two ‘single-headed’ IMB cells, 2 mm temporal to the fovea. Arrow heads and arrows indicate the two cells. (E–G) Axon terminal, cell body, and dendritic bouquet of a ‘single-headed’ FMB cell, 4.6 mm temporal to the fovea. In (E) the FMB axon terminal and the dendritic tree of a neighbour outer P cell are illustrated in the same plane of focus. (H–J) Axon terminal, cell body and dendritic bouquets of a ‘double-headed’ FMB cell, 7.3 mm nasal to the fovea. Scale bar=25 mm.

their response is sustained, whilst M cells are very cells of macaque and human retina, as revealed by sensitive to contrast and their response is transient. in 6itro intracellular injection of neurotracers. The These cells also differ in their response to sinusoidal inner dendritic tree is larger and denser than the luminance flicker [32]. The response amplitude of P outer dendritic tree, and of comparable overall diame- ganglion cells increases with contrast with little or no ter to neighbouring M cells. Electrophysiological sin- saturation, whilst the response amplitude of M gan- gle-unit recordings showed that blue-on ganglion cells glion cells saturates at relatively low levels of con- in Cebus retina have similar features to those trast. The contrast-phase relationship shows a phase recorded in catarrhines. Chromatically opponent cone advancement for M ganglion cells, which is absent inputs appeared balanced, so that there was little re- for P ganglion cells. These findings are consistent sponse to luminance modulation but vigorous re- with the presence of a contrast gain control mecha- sponses to SWS-cone modulation. Responses were nism in M ganglion cells which is absent in P gan- sustained, with a low-pass temporal response and no glion cells, as in Old World primates. evidence of contrast gain control. We encountered cells with excitatory SWS-cone input in the Cebus 3.2. The S-cone pathway of the Cebus monkey retina with about the same frequency (ca 10% of cells encountered) as in the macaque retina. We have not In the macaque monkey, the blue-on, +SWS- yet found cells with inhibitory SWS-cone input. These (MWS+LWS)-cone ganglion cells correspond to the occur in the macaque retina and LGN [51,52], and in small-field bistratified ganglion cells. The morphology the LGN of Saimiri [25,26] and Callithrix [31]. There- of Cebus small-field bistratified cells revealed by Bio- fore, they are probably also present in the Cebus cytin retrograde filling is similar to that described for retina. 3334 L.C.L. Sil6eira et al. / Vision Research 38 (1998) 3329–3337

4. Discussion the common marmoset Callithrix jacchus [21,22,28–30]. In another study, we have found that the nocturnal Retinal ganglion cells that are red-green colour-op- Aotus, a monochromatic platyrrhine which have far ponents subtract the outputs of LWS- and MWS-cones fewer cones than diurnal species [14], has M and P cells [40,42,44,52–54], whilst those that are blue-yellow morphologically similar to those of diurnal primates colour-opponent subtract the outputs of SWS-cones although of larger size [20]. from those of MWS- and LWS-cones We have found that the central retina of dichromatic [40,42,46,52,53,55]. Studies made in catarrhines have Cebus monkeys preferentially has ‘single-headed’ MB shown that the P ganglion cells and the small-field bipolar cells, and that these cells have axon terminals bistratified ganglion cells are the substrates for the whose sizes are in the range of the dendritic tree sizes of red-green and blue-yellow pathways, respectively [46]. foveal P ganglion cells of these primates. These findings We have found that the P pathway of dichromatic suggest that one-to-one connections between MWS/ Cebus monkeys is, in many aspects, morphologically LWS cones, MB bipolar cells, and P ganglion cells are a feature of the P pathway shared by diurnal catarrhi- similar to that of trichromatic primates. We have also nes and platyrrhines, independently of the presence of found cells with similar electrophysiological properties one or two MWS/LWS-cone photopigments in their as catarrhine P ganglion cells. The major difference retina. Our results for the Cebus monkey, a diurnal between P ganglion cells of dichromatic Cebus monkeys platyrrhine, contrast with those of Ogden [56] who and trichromatic catarrhines is that they do not exhibit found that in the nocturnal Aotus with a single MWS/ red-green colour opponency, owing to the presence of a LWS-cone photopigment [14,15], ‘double-headed’ MB single MWS/LWS cone photopigment in each individ- cells are a frequent occurrence in the central retinal ual. These results are consistent with morphological region. and physiological findings reported for dichromatic and There are three possibilities for the evolution of trichromatic individuals of another diurnal platyrrhine, trichromatic vision in primates [57]. First, platyrrhines and catarrhines may have evolved trichromacy independently. Secondly, the simian ancestor had a polymorphic platyrrhine-like colour vision system and that the catarrhine trichromacy was a later development. Lastly, platyrrhines may have possessed full trichromacy at one point, and then lost it. There is at least one platyrrhine genus, Alouatta, which possesses full trichromatic vision similar to that found in catarrhines [4]. In this scenario therefore, Alouatta would have regained full trichromatic vision. How might the P pathway have evolved in these scenarios to allow trichromatic vision? We have shown that diurnal platyrrhines have all the necessary elements for a one-to-one type of connectivity to be present in the central retina. Therefore, platyrrhines have a P pathway very similar to that of the catarrhines. These results support the idea that the P pathway with one-to- one connectivity was present in the anthropoid ancestor before the divergence between catarrhines and platyrrhines. One possibility is that the P pathway evolved solely to subserve colour vision. This is consistent with the hypothesis that the anthropoid ancestor had full trichromatic colour vision, which was maintained in catarrhines and degenerated in platyrrhines. This would also be consistent with the hypothesis that the anthropoid ancestor had platyrrhine-like colour vision and that the P pathway evolved only for the benefit of trichromatic females. Alternatively, the P pathway with one-to-one connectivity might have Fig. 3. Comparison between the sizes of the dendritic trees of P ganglion cells (small squares) and the sizes of axon terminals of MB evolved as a high spatial resolution system, with the P cells at increasing distance from the fovea. All cells are from dichro- ganglion cells becoming red-green colour-opponent af- matic Cebus monkeys. IMB cells: open squares. FMB cells: triangles. ter the appearance of separate MWS and LWS-cone L.C.L. Sil6eira et al. / Vision Research 38 (1998) 3329–3337 3335

Fig. 4. Response of P and M ganglion cells of a dichromatic Cebus monkey to luminance pulses at several levels of contrast. The animal had the M/L-cone photopigment peaking at 535 nm. photopigment loci by gene duplication [58,59]. Finally, c521640/96-2, CNPq/MPG c91.0234/94-9, and a P-like pathway with small-field, densely distributed CNPq/DAAD c91.0248-96.6. L.C.L. Silveira is a cells might have evolved initially for spatial vision, and CNPq Research Fellow. E.S. Yamada receives support then undergone further modification, acquiring one-to- from CNPq and Pew. J. Kremers is supported by one connectivity for trichromacy. DFG-grant ZR g/3-1. The authors thank Dr J.A.P. We have found that the dichromatic Cebus monkey Muniz, Head of the Centro Nacional de Primatas for has SWS-cone ganglion cells with similar morphologi- providing monkeys used in this work. The authors are cal and physiological properties to those described in grateful to Francinaldo L. Gomes, Walther A. de Car- humans and macaque monkeys [46,60,61]. The mor- valho and Ce´zar Akiyoshi Saito for their valuable phology of small-field bistratified cells of Callithrix contribution to this work. have been described and, in addition, it has been demonstrated that they make connections with SWS- References cone bipolar cells in this platyrrhine [21,23]. These findings support the view that the SWS-cone pathway is [1] Bowmaker JK, Dartnall HJA, Mollon JD. Microspectrophoto- similarly organised in diurnal dichromatic and trichro- metric demonstration of four classes of photoreceptors in an old matic primates, and may constitute the substrate for the world primate, Macaca fascicularis. J Physiol (Lond) 1980;298:131–43. primordial form of colour vision that evolved in these [2] Toveé MJ. The molecular genetics and evolution of primate animals [57,58]. colour vision. Trends Neurosci 1994;17:30–7. [3] Jacobs GH. Primate photopigments and primate color vision. Proc Natl Acad Sci USA 1996;93:577–81. Acknowledgements [4] Jacobs GH, Neitz M, Deegan II JF, Neitz J. Trichromatic colour vision in New World monkeys. Nature 1996;382:156–8. [5] Jacobs GH. Within-species variations in visual capacity among This work was supported by FINEP/FADESP squirrel monkeys (Saimiri sciureus): color vision. Vis Res c4.3.90.0082.00, CNPq c52.1749/94-8, CNPq 1984;24:1267–77. 3336 L.C.L. Sil6eira et al. / Vision Research 38 (1998) 3329–3337

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