THE DISTRIBUTION OF CHOLINE ACETYLTRANSFERASE ACTIVITY IN VERTEBRATE RETINA1

Abstract— Choline acetyltransferase (ChAc) activity was determined in retinal layers from 10 vertebrates. In all animals, the highest activity was in the inner plexiform layer, intermediate activity in the inner nuclear and ganglion cell layers, and very low activity in the photoreceptor and outer plexiform layers and optic nerve. The pattern of distribution of enzyme activity within the inner nuclear layer corresponds quantitatively to the distribution of amacrine cells within that layer. A species difference of almost 90-fold was found between the lowest and highest values for ChAc activity in inner plexiform layer. The variation in enzyme activity found among homeotherms in inner nuclear and inner plexiform layers is related to the number of amacrine cell synapses in the inner plexiform layer. But the differences in enzyme activity are generally greater than those which have been found in numbers of amacrine cell synapses between species. The data suggest that cholinergic neurons in retina are to be found predominantly among the amacrine cell types and that not all amacrine cells will be found to be cholinergic.     

墨龙与红鲫的视网膜和视盖解剖结构比较

墨龙是一种由红鲫进化来的龙睛种金鱼(Carassius auratus)。随机取体长10—12 cm, 重约35 g的墨龙和红鲫各4尾, 解剖取出整个眼球及脑, 并常规石蜡切片, HE染色。在光学显微镜下观察墨龙和红鲫的视网膜、视盖系统的显微结构变化并比较各层厚度, 发现与红鲫相比, 墨龙视网膜的总厚度下降29.9%, 其中外网状层厚度增加2.5%、内网状层厚度增加11.8%; 而内核层厚度下降21.6%、外核层厚度降低35.6%, 神经节细胞层、杆锥层也变薄, 且后两者分层不规则; 墨龙视盖壁整体厚度增加28.9%, 其中除围脑室层厚度减少22.6%外, 中央纤维层厚度增加12.8%, 中央细胞层厚度增加30.6%, 表面纤维层厚度增加21.9%, 且纤维远较红鲫密集, 视神经层厚度增加91.7%, 边缘层厚度增加35.6%。结果表明长期的人工选择不但改变了墨龙的外形, 而且使其中枢神经组织结构也发生了较大变化, 并推测墨龙的眼球直径及视网膜面积较大, 从而导致自视网膜传入视盖的纤维增多, 是视网膜和视盖中的传递神经冲动的神经元、神经纤维所在层段增厚的主要原因; 同时墨龙视网膜中色素上皮层向杆锥层交错对插, 富含神经元的视网膜外核层、内核层以及视盖中的围脑室层厚度也降低, 可以减少因视网膜面积大而造成的强光伤害; 此外由于墨龙的围脑室层厚度降低, 导致其游动及平衡能力较红鲫差。     

Adenylate Cyclases in the Vertebrate Retina: Distribution and Characteristics in Rabbit and Ground Squirrel

Adenylate cyclase activity and the effects of EGTA, 5'-guanylylimidodiphosphate (GPP(NH)P), and dopamine were measured in microdissected layers of rod-dominant (rabbit) and cone-dominant (ground squirrel) retinas, The distribution of basal enzyme activity was similar in both species, with the highest levels found in the inner plexiform and photoreceptor cell inner segment layers, EGTA inhibited adenylate cyclase in the inner retina of both species and stimulated activity in rabbit outer and inner segment layers, but had no effect in these layers from ground squirrel. Enzyme activity was stimulated in all regions by GPP(NH)P, except in the outer segments of the photoreceptors. Dopamine stimulated the enzyme in the outer and inner plexiform and inner nuclear layers in rabbit, but only in the inner plexiform layer in ground squirrel. These data demonstrate that the enzymatic characteristics of adenylate cyclase vary extensively from region to region in vertebrate retina and suggest that cyclic AMP may have multiple roles in this tissue. A model for the distribution of the different forms of adenylate cyclase in retina is proposed.     

Histochemical and cytochemical localization of acetylcholinesterase in retina and optic tectum of teleost fish.

The activity of cholinesterase and its cellular and subcellular localization were investigated in the retina and optic tectum of Eugerres plumieri and in the retina of Carassius carassius by means of radiometric, histochemical, and cytochemical procedures. In both fishes only the presence of acetylcholinesterase could be demonstrated. This study, besides confirming previous findings that acetylcholinesterase is located in the ganglion and amacrine cells of the retina as well as in the inner plexiform layer, in addition provides evidence that the enzyme is also present at the region of photoreceptor synapses between the cell bodies and apposing extensions of the horizontal cells of the same layer. The latter localization may indicate the involvement of a cholinergic mechanism at the functional contacts (transferapses) between the horizontal cells. In the optic tectum of Eugerres plumieri, histochemistry reveals fine distinguishable bands of acetylcholinesterase activity; two of the bands are quite sharply defined, whereas three others have rather a more diffuse appearance. The presence of these bands and their distribution may suggest a widespread distribution of cholinergic elements in the optic tectum.     

Changes of lysosomal enzymes during hereditary degeneration and histogenesis of retina in mice

Summary During the post-natal development of the retina in mice, macrophages which are selectively stained for N-Acetyl--glucosaminidase enter the retina through the vascular route. Most of these cells finally occupy the outer and the inner levels of the inner nuclear layer adjoining the plexiform layers and are transformed into very small cells which persist in the adult retina without further change.In mice with hereditary retinal degeneration (rd rd) these -glucosaminidase positive macrophages enter the outer nuclear layer of the retina, soon after the onset of degeneration undergo extensive hypertrophy and rapidly phagocytize the degenerating photoreceptor cells. After the digestion of the ingested materials the enzyme activity is very much reduced and the cells become smaller in size. They eventually acquire the morphological features seen in the normal retina.     

Taurine trophic modulation of goldfish retinal outgrowth and its interaction with the optic tectum

Summary. Goldfish retinal explant outgrowth in the presence of fetal calf serum is stimulated by taurine. In the absence of it, but with glucose in the medium, length of neurites is still elevated by the amino acid. Using the medium in the presence of glucose, but in the absence of fetal calf serum, we explored the effect of optic tectum medium from cultures of them coming from goldfish without crush of the optic nerve or 3, 5, 10, 14 and 20 days after crush. Retinal explants, intact or from goldfish with crush of the optic nerve 10 days prior to starting the culture, were employed in order to measure the possible effect of optic tectum media and the inter action with taurine. In other type of experiments the optic nerve was crushed 1, 2, 4, 7 and 10 days before dissection of the optic tectum, and then co-cultured with intact or 10 days post-crush retinal explants. Optic tectum media produced a time-dependent effect on outgrowth in lesioned retinas with a maximum effect around 5 days after the lesion for the corresponding optic tectum. Taurine, 4 mM, did not further affect the outgrowth in the presence of optic tectum media, but did significantly increase length of neurites either in intact or in post-lesion retinas. Co-culture of optic tectum at different days post-lesion and retinas at 10 days post-lesion increased the outgrowth around 4 days post-lesion, in a preparation resulting in mutual effects of both types of tissues. The addition of taurine in these conditions did not further increase outgrowth, rather inhibited it according to the time after lesion of optic nerve corresponding to the co-cultured optic tectum. The effect of taurine was concentration-dependent, since 0.2 mM was more effective than 2 or 4 mM in the presence of optic tectum with lesion of 2 days. These results demonstrate the time-course of the regeneration processes in the visual system of goldfish, indicating the crucial periods after crush in which the tectum could produce stimulation and later decrease or no effect on outgrowth from the retina. In addition, they are evidences of the interaction between taurine and optic tectum production of time-produced specific agents. The mechanisms underlying these effects are closely related to calcium, as it was demonstrated by the addition of extracellular or intracellular chelators to the medium, which inhibited the effects of the optic tectum and the trophic properties of taurine in this system. The inhibitor of taurine transport, guanidoethylsulfonate, also decreased the stimulatory effects of the optic tectum and of taurine, indicating an interaction of substances produced by the tectum with taurine, and an effect of taurine mediated through its entrance to the cells. Overall, retinal explants outgrowth in the absence of fetal calf serum, the interaction of agents of the optic tectum and taurine modulates outgrowth from the retina, and these effects are mediated by calcium levels and by the levels of intracellular taurine.     

On the distributive patterns of ATPase activity and its functional significance in retinae of certain birds.

The present study incorporates the details of distribution of adenosine triphosphatase amongst the various constituents of retinae of Passer, Psittacula, Streptopelia and Athene. The outer segments in all the cases are intensely positive for the enzyme. This is the part where the light strikes first and initiates the visual processes. The nuclear layers are also positive for the enzyme activity. It is interesting to note that inner plexiform layers show clear-out demarcations of various sub-synaptic layers in all the birds except Psittacula. The ganglion cells and optic nerve fibres are also positive for the enzyme.     

胭脂鱼眼早期形态发生研究

采用组织学方法观察了胭脂鱼(Myxocyprinus asiaticus) 眼的发生过程, 结果显示: 胭脂鱼眼的发育经历了眼原基形成期、眼囊形成期、视杯形成期、晶体板形成期、晶体囊形成期、角膜原基形成期、角膜上皮形成期、视网膜细胞增殖期、晶状体成熟期、眼色素形成期以及眼成型期等11个时期。视网膜发育最早, 起始于眼原基的形成, 直至眼成型期分化完成, 形成了厚度不一的8层细胞, 由内向外依次为神经纤维层、神经细胞层、内网层、内核层、外网层、外核层、视杆视锥层和色素上皮层, 且发育历时最长, 约264h。晶状体的发育在视网膜之后, 始于晶体板的形成, 于出膜前期成熟, 发育历时最短, 约74h。角膜发育最晚, 始于角膜原基的形成, 出膜1 d分化为透明的成熟角膜, 发育历时约96h。出膜4 d仔鱼眼色素沉积明显, 视网膜各层分化明显, 晶状体内部完全纤维化, 眼的形态结构基本发育完全。     

Studies of the developing chick retina using monoclonal antibody 8A2 that recognizes a novel set of gangliosides

A monoclonal antibody, Mab 8A2, that recognizes a novel set of gangliosides was produced by immunizing a mouse with Embryonic Day 14 chick optic nerve. Immunohistochemical studies of the developing chick retina revealed a complex pattern of Mab 8A2 immunoreactivity. Initially, staining is concentrated in the optic fiber layer in the central retina. Later in development, the most intense staining is seen at the periphery of the retina and 8A2 immunoreactivity appears in other retina layers. In the adult retina, 8A2 immunoreactivity is lost from the optic fiber layer but persists in the inner plexiform layer, inner nuclear layer, and outer plexiform layer. Cell culture experiments showed intense staining of neurites from retinal ganglion cells but no staining of Muller cells. Biochemical characterization of the epitope recognized by Mab 8A2 suggests that it includes a 9-O-acetyl group that is present on five different gangliosides. The 8A2 immunoreactive gangliosides are distinct from and have slower mobilities on thin-layer chromatographs than those recognized by Mab D1.1 which recognizes 9-O-acetyl GD3.     

Distribution of FMRFamide-like immunoreactivity in the brain,retina and nervus terminalis of the sockeye salmon parr,Oncorhynchus nerka

Summary Neurons displaying FMRFamide(Phe-Met-Arg-Phe-NH₂)-like immunoreactivity have recently been implicated in neural plasticity in salmon. We now extend these findings by describing the extent of the FMRF-like immunoreactive (FMRF-IR) system in the brain, retina and olfactory system of sockeye salmon parr using the indirect peroxidase anti-peroxidase technique. FMRF-IR perikarya were found in the periventricular hypothalamus, mesencephalic laminar nucleus, nucleus nervi terminalis and retina (presumed amacrine cells), and along the olfactory nerves. FMRF-IR fibers were distributed throughout the brain with highest densities in the ventral area of the telencephalon, in the medial forebrain bundle, and at the borders between layers III/IV and IV/V in the optic tectum. High densities of immunoreactive fibers were also observed in the area around the torus semicircularis, in the medial hypothalamus, median raphe, ventromedial tegmentum, and central gray. In the retina, immunopositive fibers were localized to the inner plexiform layer, but several fiber elements were also found in the outer plexiform layer. The olfactory system displayed FMRF-IR fibers in the epithelium and along the olfactory nerves. These findings differ from those reported in other species as follows: (i) FMRF-IR cells in the retina have not previously been reported in teleosts; (ii) the presence of FMRF-IR fibers in the outer plexiform layer of the retina is a new finding for any species; (iii) the occurrence of immunopositive cells in the mesencephalic laminar nucleus has to our knowledge not been demonstrated previously.     

The developing avian retina expresses agrin isoforms during synaptogenesis

The localization, isoform pattern, and mRNA distribution of the synapse-organizing molecule agrin was investigated in the developing avian retina. Injection of anti-agrin Fab fragments into the vitreous humor of chick eyes of embryonic days 3 to 20, a procedure that labels only extracellular agrin, reveals staining in the inner and outer plexiform layers before, during, and after the period of synapse formation. The labeling in these layers changes from a diffuse to a punctate pattern at the time when synapses form. At all stages investigated, the inner limiting membrane (a basal lamina that separates vitreous from neural retina) is intensely labeled, as are the axonal processes of retinal ganglion cells in the optic fiber layer and in the optic nerve, although the staining intensity declines after embryonic day 10 in both retina and optic nerve. In culture, axons of retinal ganglion cells also express agrin-like immunoreactivity on their surfaces. Polymerase chain reaction analysis reveals that several different agrin isoforms are expressed in the developing neural retina. In situ hybridization studies show that agrin isoforms are expressed in the ganglion cell and inner nuclear layers, correlating well with the staining for agrin protein in the optic fiber and plexiform layers. The expression of mRNA coding for several agrin isoforms and the presence of extracellular agrin in the synapse-containing layers during the period of synapse formation is consistent with the idea that agrin isoforms might play a role during synapse formation in the central nervous system. © 1996 John Wiley & Sons, Inc.     

GABA concentration and GAD activity levels in normal and degenerated retinas from mice

Freeze-dried sections (14 m thick) were prepared from mice with normal (C57BL strain) and degenerated (C3H strain) retinas. GABA concentration and GAD activity were determined in the microsamples (1.8–20 ng dry weight) of retinal layers and sublayers, using an enzymatic amplication reaction, NADP cycling. 1) GABA was distributed over all layers of normal retina with a broad concentration peak covering both inner nuclear and plexiform layers. In contrast, GAD activity was mostly localized in the inner plexiform layer. 2) GABA concentration was similar in one-fourth of the sublayers of each inner nuclear or plexiform layer. GAD activity was highest in the innermost sublayer of the inner nuclear layer. An increasing gradient of GAD activity was present in the inward direction in the inner plexiform layer. 3) In the degenerated retina, lacking in photoreceptors, the inner nuclear and plexiform layers remained, and GABA and GAD levels in these layers were similar to those in normal retina.Special Issue dedicated to Dr. O. H. Lowry.     

Structure of the eye of Haideotriton wallacei, a North American troglobitic salamander

The eye of Haideotriton wallacei is more reduced histologically than those of othe troglobitic salamanders. The tiny eye is imbedded in a mass of adipose tissue. No extrinsic eye muscles are present. A rudimentary lens is present in about half of the eyes examined. In two instances the lens is surrounded by a small chamber; most eyes lack a chamber. The retina and iris are relatively undifferentiated. The relatively massive retina lacks rods and cones, an outer plexiform layer and subdivided nuclear layers. A tiny optic nerve runs to the brain.     

Target cells of vitamin D in the vertebrate retina

Using PAP technique, cellular localization of vitamin D-dependent calcium-binding protein (D-CaBP) was investigated in vertebrate retina with monospecific antisera against chick duodenal D-CaBP. In the chick retina, the receptor cells were positive. In the inner nuclear layer, horizontal cells and some bipolar cells were also positive. Some amacrine cells as well as different levels of the inner plexiform layer were also positive for D-CaBP. A few interspersed ganglion cells were positive but their axons forming the optic tract were negative. Müller's cells were negative. In 1-day-old chicks and 4-week-old rachitic chicks there was paucity and absence, respectively, of D-CaBP staining in horizontal cells. In the mouse, rat, and rabbit the receptors had only trace amounts of reaction product in their outer segment and pedicle. Horizontal cells were densely positive throughout their cellular body and processes. Some amacrine cells in the inner nuclear layer were positive. In the mouse and rat three horizontal levels of the outer plexiform layer were very prominent because of their dense staining for D-CaBP. Many ganglion cells were also positive along with their axons forming the optic nerve. In the rabbit, no positive layers were seen in the inner plexiform layer, and ganglion cells with their fibers were negative. In the frog retina there were smaller amounts of D-CaBP in the receptor cells and horizontal cells than that of the chick retina. Also, the fibers of the ganglionic cells were positive for D-CaBP. In all species studied, some amacrine cells were stained for D-CaBP. Because of its possible roles in membrane calcium transport and intracellular Ca++ regulation, it has perhaps similar functions in these positive cells. The synthesis of D-CaBP is dependent upon vitamin D. These positive cells are thus target cells of vitamin D.     

Collagen-tailed and globular forms of acetylcholinesterase in the developing chick visual system

We have carried out a comparative study of the developmental profiles of the enzyme acetylcholinesterase, and of its collagen-tailed and globular structural forms, solubilized in the presence of 1 M NaCl, 1% (w/v) sodium cholate and 2 mM EDTA, in the chick retina and optic lobes. The overall acetylcholinesterase activities, both per mg protein and per embryo or chick, are substantially higher in tectum than in retina, from embryonic day 16. The A₁₂ collagen-tailed form of the enzyme is present in similar amounts in the embryonic retina and optic tectum; however, while the A₁₂ activity increases significantly in retina after birth, both by percentage and in absolute terms, the tectal tailed enzyme follows a declining developmental profile, reaching a minimum after 6 months of life. On the other hand, the globular G₄ species shows developmental profiles, both in retina and tectum, rather similar to those obtained for the overall enzyme activity, while the G₂ and G₁ forms are present in comparable concentrations in both tissues. Besides, G₄ is the predominant globular form in the chick optic lobe after hatching, G₂ and G₁ being enriched in the embryonic tectum. In the case of retina, however, all the globular forms contribute more evenly to the total acetylcholinesterase activity, along the developmental period considered.The potential significance of some of the postnatal developmental profiles is discussed in terms of the progressive adjustment of retina and tectum to the requirements of visual function.     

Specific cell surface labels in the visual centers of Xenopus laevis tadpole identified using monoclonal antibodies

Monoclonal antibodies (MAbs) against the optic tectum of Xenopus tadpoles were generated and screened by the immunofluorescent staining of frozen sections of tadpole brains. MAb-A5 stains the 8th and 9th plexiform layers of the optic tectum, whereas MAb-B2 stains all but the eighth and ninth plexiform layers of the optic tectum. MAb-A5 antigen is also detectable in the nucleus of Belonci, the corpus geniculatum thalamicum, the pretectal area, and the basal optic nucleus, all targets of the optic nerve, but is not detectable in the optic nerve or the optic tract. On the other hand, MAb-B2 does not stain any of these visual centers, though many fibers surrounding them are stained. Eye-enucleation experiments showed that MAb-A5 antigen is expressed in the optic tectum even when it is not innervated by optic nerves. Staining of viable brains with these MAbs indicates that these antigens are cell surface molecules. Immunoadsorption followed by SDS-PAGE suggests that proteins are constituents of these antigens. The MAb-A5 antigen in the diencephalon and the mesencephalon is not detectable at stage 35/36, but is detectable at stage 39 when the optic nerves begin to innervate the optic tectum. The spatial as well as the temporal patterns of the expression of the MAb-A5 antigen suggest that this molecule may be involved in the target recognition of optic nerve fibers.     

Modulation of taurine uptake in the goldfish retina and axonal transport to the tectum¶Effect of crushing the optic nerve or axotomy

Summary. Although there are a great number of studies concerning the uptake of taurine in several tissues, the regulation of taurine transport has not been studied in the retina after lesioning the optic nerve. In the present study, isolated retinal cells of the goldfish retina were used either immediatly after cell suspension or in culture. The high-affinity transport system of [³H]taurine in these cells was sodium-, temperature- and energy-dependent, and was inhibited by hypotaurine and β-alanine, but not by γ-aminobutyric acid. There was a decrease in the maximal velocity (V_max) without modifications in the substrate affinity (K_m) after optic axotomy. These changes were mantained for up to 15 days after the lesion. The results might be the summation of mechanisms for providing extracellular taurine to be taken up by other retinal cells or eye structures, or regulation by the substrate taurine, which increases after lesioning the optic nerve. The in vivo accumulation of [³H]taurine in the retina after intraocular injection of [³H]taurine was affected by crushing the optic nerve or by axotomy. A progressive retinal decrease in taurine transport was observed after crushing the optic nerve, starting at 7 hours after surgery on the nerve. The uptake of [³H]taurine by the tectum was compensated in the animals that were subjected to crushing of the optic nerve, since the concentration of [³H]taurine was only different from the control value 24 hours after the lesion, indicating an efficient transport by the remaining axons. On the contrary, the low levels of [³H]taurine in the tectum after axotomy might be an index of the non-axonal origin of taurine in the tectum. Axonal transport was illustrated by the differential presence of [³H]taurine in the intact or crushed optic nerve. The uptake of [³H]taurine into retinal cells in culture in the absence or in the presence of taurine might indicate the existence of an adaptive regulation of taurine transport in this tissue, however taurine transport probably differentially occurs in specific populations of retinal cells. The use of a purified preparation of cells might be useful for future studies on the modulation of taurine transport by taurine in the retina and its role during regeneration. Received June 11, 1999/Accepted August 31, 1999     

Molecular mechanisms separating two axonal pathways during embryonic development of the avian optic tectum

During embryonic development of the avian optic tectum, retinal and tectobulbar axons form an orthogonal array of nerve processes. Growing axons of both tracts are transiently very closely apposed to each other. Despite this spatial proximity, axons from the two pathways do not intermix, but instead restrict their growth to defined areas, thus forming two separate plexiform layers, the stratum opticum and the stratum album centrale. In this study we present experimental evidence indicating that the following three mechanisms might play a role in segregating both axonal populations: Retinal and tectobulbar axons differ in their ability to use the extracellular matrix protein laminin as a substrate for axonal elongation; the environment in the optic tectum is generally permissive for retinal axons, but is specifically nonpermissive for tectobulbar axons, resulting in a strong fasciculation of the latter; and growth cones of temporal retinal axons are reversibly inhibited in their motility by direct contact with the tectobulbar axon's membrane.     

Human retinal development: ultrastructure of the inner retinal layers

Studies of the developing human retina from 6.5 to 18 weeks' gestational age (16–156 mm) by light and electron microscopy are concerned with the morphogenesis of neuroblast cells, plexiform layers, and inner limiting membrane. The transient layer of Chievitz is formed posteriorly by 20 mm (7 weeks), inner plexiform by 48 mm (9 weeks), outer plexiform layer by 83 mm (12 weeks), identifiable cones by 83 mm, and rods by 120 mm (15 weeks). Mitotic activity continues posteriorly until 120 mm and was seen in inner layers of the retina until 103 mm (13 weeks). Outer neuroblastic differentiation is marked by diversification from a uniform cell population to one containing at least three cell types differing in their nuclear shape, chromatin pattern, and cytoplasmic characteristics. Differentiating ganglion cells accumulate polysomes, rough endoplasmic reticulum, Golgi complexes, microtubules, and dense bodies. Müller cell bodies in ganglion and inner nuclear layers extend processes between ganglion cells, and radial fibers, containing extensive smooth endoplasmic reticulum, to the vitreal surface. Synapses appear in the inner and outer plexiform layers by 83 mm (12 weeks), and by 120 mm (15 weeks) demonstrate a variety of conventional and ribbon forms similar to those found in the adult. Synaptogenesis therefore begins considerably before the development of photoreceptor outer segments.     

Neuronal and synaptic organization in the gravity receptor system of the statocyst of Octopus vulgaris

Summary The optic tectum of Calamoichthys calabaricus (Polypteriformes) shows a relatively complex vertical stratification, with six main layers and a varied neuronal typology. In particular, pyriform neurons in the well developed stratum griseum periventriculare and some multipolar neurons in the stratum griseum profundum represent the efferent elements of the tectum, while the optic and lemniscal inputs to the tectum converge in the plexiform sublayers of the stratum fibrosum et griseum superficiale. In the circuitry of the tectum some modulation is achieved by some of the polymorphic cells of the stratum griseum internum and by the horizontal cells of the outer layers. Notwithstanding some differences with respect to the teleost optic lobe (i.e., the absence of a torus longitudinalis; the lack of a stratum fibrosum marginale; the modest size of the stratum fibrosum profundum; the paucity of neurons in the stratum fibrosum et griseum superficiale; and the ill-defined separation of the layers of the afferent and efferent fibers), the optic tectum of Calamoichthys resembles the mesotectal type characteristic of teleosts, anurans and reptiles. It exhibits higher degree of organization than the optic tectum of the Chondrostei.