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Retinal Projections in a Nocturnal Lizard, Gekko Gecko (Linnaeus)

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Retinal Projections in a Nocturnal Lizard, Gekko Gecko (Linnaeus) Evolution of Reptilian Visual Systems: Retinal Projections in a Nocturnal Lizard, Gekko gecko (Linnaeus) R. GLENN NORTHCUTT AND ANN B. BUTLER 1 Depnrtment of Zoology, University of Michigun, Ann Arbor, Michigtrn 481 04 nnd Department of Neurologictrl Surgery, University of Viyginin School of Medicine, Chnrlottesville, Virgixiti 22901 ABSTRACT On the basis of the development of the dorsal ventricular ridge of the telencephalon, lizards can be divided into a type I group, to which Gehho and the majority of lizard families belong, and a type I1 group with more derived features, of which Iguana is representative. Most studies of retinal projections have utilized lizards of the type I1 group, which are adapted to a diurnal niche. Gehho gecho is differently adapted in that it is nocturnal. Study of the retinal projections was undertaken in Gehho gecho in order to insure that conclusions regarding the pattern of retinal pathways in saurians would be based on a sample which was more representative of the total range of variation. Unilateral removal of the retina by suction cannula was carried out on 12 adult specimens of Gehho gecho. After survival times of 10 to 74 days, brains were processed with various silver methods. The retina projects contralaterally to the pars dorsalis and pars ventralis of the lateral geniculate nucleus and the pars ventralis of the ventrolateral nucleus in the thalamus, nuclei geniculatus pretectalis, lentiformis mesencephali, and posterodorsalis in the pretectum, layers 8-14 of the optic tectum, and nucleus opticus tegmenti. Additionally, the retina projects ipsilaterally to the dorsal and ventral lateral geniculate nuclei and to the pretectal nuclei, as well as to the optic tectum, particularly layers 8 and 9. The finding of ipsilateral retinothalamic projections in Gehho supports the idea that this pathway is generalized among saurians. However, presence of ipsilateral retinothalamic projections and the degree of binocular overlap cannot be correlated when lizards, snakes, crocodiles, and turtles are compared. The functional significance of this pathway therefore remains obscure. Ipsilateral retinotectal projections have not been previously described in land vertebrates other than mammals. Whether their presence is correlated with nocturnal visual habits or is generalized among type I lizards remains to be determined. The pattern of retinal projections has been studied in too few representatives of non-mammalian land vertebrates to presently permit conclusions regarding the origin of non-decussating pathways. Among lizards there is a broad range of The second group, type I1 lizards, repre- morphological variation for a number of sented here by Iguana, includes the teiids, brain characters. Cross-sections at cor- varanids, agamids, iguanids, and chamael- responding mid-telencephalic levels of the eonids. brains of two lizards, Gehko gecho and Of particular relevance to a considera- Iguana iguana, are compared in figure 1. tion of the visual system are the striking They are representative of two different differences in the morphology of the dor- major groups of lizards, which can be sep- sal ventricular ridge (DVR) between these arated on the basis of the development of two types of lizards. Visual projections to the dorsal ventricular ridge (Northcutt, the DVR, from the optic tectum via the '72). The first group, type I lizards, repre- dorsal thalamic nucleus rotundus, have sented here by Gekho, includes such di- verse families as feyliniids, scincids, la- 1 Present address: Department of Anatomy, The George Washington University, School of Medicine, certids, xantusids, anguids, and others. 2300 I St., N.W., Washington, D.C. 20037. J. COMP. NEUR.,157: 453466. 453 454 R. GLENN NORTHCUTT AND ANN B. BUTLER been demonstrated in several reptiles (Hall lizards are not representative of the an- and Ebner, '70a,b; Braford, '72; Pritz, '73). cestral lacertilian stock (Camp, '23). More- Aspiration of the dorsal thalamus in over, type I1 lizards are restricted to a Iguana (Butler and Ebner, '72) and Gehho single adaptive zone, which is a diurnal (unpublished data) result in terminal de- one. generation in several discrete regions of The retinal projections described in the DVR; the most lateral region corre- type I1 lizards do not differ greatly from sponds topographically to the locus of the those described by Armstrong ('50) in rotunda1 input in the other reptiles studied. Lacerta. However, study of visual path- As seen in figure 1, the dorsal ventricu- ways in additional species of the more lar ridge of Gehho is formed by a core generalized type I lizards is important for nucleus surrounded by a corticoid band two reasons. First, the Nonidez silver of cells. This type I DVR pattern is also method used by Armstrong is less sensitive found in Sphenodon (Cairney, '26; Dur- than the recent modifications of the Nauta ward, '30) and in turtles (Northcutt, '70), silver impregnation met hod. Secondly , and probably represents the ancestral pat- Lacerta is a terrestrial, diurnal predator, tern of the reptilian DVR. This condition occupying a niche similar to that of the sharply contrasts to that seen in the type type I1 lizards; thus, the sample to date is I1 lizards, represented in figure 1 by not representative of the wide range of Iguana. In Iguana the DVR is composed diversity in saurian niches. of a number of nuclear groups and occu- The type I lizard, Gehho gecho, is ar- pies a relatively larger portion of the telen- boreal, as are many of the type I1 iguanas cephalon. and chameleons. However, in contrast to With the exception of Lacerta (Arm- the latter, geckos are nocturnal predators. strong, '50), the studies to date on visual The work of Citron and Pinto ('73) indi- projections in lizards are restricted to cates that the structure of the gecko eye members of the type I1 group (Ebbesson, produces a larger and more illuminous '70a; Butler and Northcutt, '71). These retinal image than that of the iguanid - Abbreviations used in figures 1-5 AT, area triangularis MOT, medial optic tract CP, cell plate of nucleus geniculatus pretectalis NOT, nucleus opticus tegmenti D, dorsal cortex NPD, nucleus posterodorsalis DLH, nucleus dorsolateralis hypothalami NS, nucleus sphericus Dm, dorsal cortex, pars medialis OT, optic tract DM, nucleus dorsomedialis P, nucleus periventricularis hypothalami DVR, dorsal ventricular ridge PD, nucleus geniculatus lateralis pars dorsalis DVRc, dorsal ventricular ridge, core nucleus PE, nucleus lentiformis thalami pars extensa DVRs, dorsal ventricular ridge, surrounding PP, nucleus lentiformis thalami pars plicata corticoid band R, nucleus rotundus GP, nucleus geniculatus pretectalis S, septum GLV, nucleus geniculatus lateralis pars ventralis SC, suprachiasmatic nucleus HC, habenular commissure SM, stria medullaris Hd, nucleus habenularis pars dorsalis SO, subcommissural organ Hv, nucleus habenularis pars ventralis SON, supraoptic nucleus L, lateral cortex ST, striatum LA, nucleus dorsolateralis anterior V, lateral ventricle LFB, lateral forebrain bundle Vd, nucleus ventrolateralis pars dorsalis LFBd, dorsal peduncle of lateral forebrain bundle VH, nucleus ventralis hypothalami LFBv, ventral peduncle of lateral forebrain bundle VM, nucleus ventromedialis of the thalamus LH, nucleus lateralis hypothalami VMt, nucleus ventromedialis of the LM, nucleus lentiformis mesencephali telencephalon LN, lateral neuropil of nucleus geniculatus Vv, nucleus ventrolateralis pars ventralis lateralis pars ventralis 1, layer 1 of Ramon of the optic tectum LOT, lateral optic tract 1-5, layers 1-5 of Ramon of the optic tectum M, nucleus medialis 3-7, layers 3-7 of Ramon of the optic tectum MC, medial cell plate of nucleus geniculatus 5, layer 5 of Ramon of the optic tectum lateralis pars ventralis 6, layer 6 of Ramon of the optic tectum MFB, medial forebrain bundle 7, layer 7 of Ramon of the optic tectum M1, medial cortex, pars lateralis 8-14, layers 8-14 of Ramon of the optic tectum Mm, medial cortex, pars medialis 111, third ventricle RETINAL PROJECTIONS IN GEKKO GECKO 455 Dm I MI -Mm L S ST -S I mm , Irnm Fig. 1 Representative cross sections of the telencephalons of G&ko gecho (A) and Igzrmzu igtrtrntr (B), representing lizard types I and 11, respectively. Note the greater degree of corticoid band development in the dorsal ventricular ridge of G&ko, as compared to Zgii(m(r. eye. Thus, comparison of the visual pro- perfusion with normal saline followed by jections in geckos with those of other rep- 10 % non-buffered formalin. The brains tiles should allow a more accurate as- were removed and fixed in 10% formalin sessment of those characters which are for a minimum of one week prior to being generalized among reptiles as opposed to embedded in either albumin-gelatin or those characters which are specialized as egg yolk, frozen, and sectioned on a slid- a result of particular adaptive pressures. ing microtome at 25 micra. Sections were stored in 2% formalin at 4" C, and were processed with various modifications of MATERIALS AND METHODS the Nauta silver impregnation method. Unilateral enucleations of either the These modifications included procedure I right or the left eye were carried out un- of the Fink-Heimer method ('67), the pro- der sodium pentobarbital anesthesia (20 cedure of Ebbesson and Heimer (Ebbesson, mglkg) on 12 adult specimens of the lizard '70b), and the Eager method ('70). Adja- Gehho gecko. The retina was removed by cent sections were stained with cresyl vio- suction cannula in order to preclude the let. The normal anatomy of diencephalic possibility of damage to vessels in the and pretectal nuclei was studied with sec- vicinity of the optic chiasm. The number tions stained with cresyl violet and the of animals examined and the survival Bodian method. The terminology of these times, indicated in parentheses, following nuclei follows that used in the green surgery were as follows: 2(10), 3(14), iguana (Butler and Northcutt, '73). 2(20), 1(31), 1(43), 1(54), l(64) and l(74).
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