Elsevier

Brain Research Reviews

Volume 52, Issue 1, 30 August 2006, Pages 1-57
Brain Research Reviews

Review
The centrifugal visual system of vertebrates: A comparative analysis of its functional anatomical organization

https://doi.org/10.1016/j.brainresrev.2005.11.008Get rights and content

Abstract

The present review is a detailed survey of our present knowledge of the centrifugal visual system (CVS) of vertebrates. Over the last 20 years, the use of experimental hodological and immunocytochemical techniques has led to a considerable augmentation of this knowledge. Contrary to long-held belief, the CVS is not a unique property of birds but a constant component of the central nervous system which appears to exist in all vertebrate groups. However, it does not form a single homogeneous entity but shows a high degree of variation from one group to the next. Thus, depending on the group in question, the somata of retinopetal neurons can be located in the septo-preoptic terminal nerve complex, the ventral or dorsal thalamus, the pretectum, the optic tectum, the mesencephalic tegmentum, the dorsal isthmus, the raphé, or other rhombencephalic areas. The centrifugal visual fibers are unmyelinated or myelinated, and their number varies by a factor of 1000 (10 or fewer in man, 10,000 or more in the chicken). They generally form divergent terminals in the retina and rarely convergent ones. Their retinal targets also vary, being primarily amacrine cells with various morphological and neurochemical properties, occasionally interplexiform cells and displaced retinal ganglion cells, and more rarely orthotopic ganglion cells and bipolar cells. The neurochemical signature of the centrifugal visual neurons also varies both between and within groups: thus, several neuroactive substances used by these neurons have been identified; GABA, glutamate, aspartate, acetylcholine, serotonin, dopamine, histamine, nitric oxide, GnRH, FMRF-amide-like peptides, Substance P, NPY and met-enkephalin. In some cases, the retinopetal neurons form part of a feedback loop, relaying information from a primary visual center back to the retina, while in other, cases they do not. The evolutionary significance of this variation remains to be elucidated, and, while many attempts have been made to explain the functional role of the CVS, opinions vary as to the manner in which retinal activity is modified by this system.

Introduction

The question of the existence of a centrifugal visual pathway in vertebrates, that is to say cerebral projections to the retina, has been the subject of extensive discussion and controversy since the end of the 19th century. Centrifugal visual fibers terminating in the avian retina were described by Cajal, 1888, Cajal, 1889 and Dogiel (1895) using both the silver impregnation method of Golgi and the intravital methylene blue method introduced by Ehrlich. Subsequent demonstrations of centrifugal visual fibers in other species, based on similar techniques (lampreys (Tretjakoff, 1916); teleosts (Cajal, 1892, Cajal, 1893); amphibians (Rozemeyer and Stolte, 1931); mammals (Cajal, 1911, Polyak, 1957)), have been widely contested [see Repérant et al., 1989b for review]. The electrophysiological evidence in favor of an efferent innervation of the retina, reviewed by Repérant et al. (1989b), is also less than compelling. However, the introduction of experimental tract-tracing methods in the 79s (Cowan et al., 1972, Kristensson and Olsson, 1971a, Kristensson and Olsson, 1971b, LaVail and LaVail, 1972, LaVail and LaVail, 1974, Streit and Reubi, 1977), together with the development of fluorescence microscopy and immunohistochemical techniques (Björklund and Nobin, 1973, Fuxe et al., 1970, Sternberger et al., 1970), have led, particularly over the last 15 years, to the accumulation of a considerable amount of evidence obtained in different groups of vertebrates, not only related to the existence of such projections but also to the location and neurochemical properties of their cells of origin and the nature of the afferent supply of the latter. We also note, without discussing them further, that centrifugal visual fibers have been described in a variety of invertebrate species (see Suzuki and Yamamoto, 2002 for review).

It should be pointed out that access to much of the data regarding the CVS of vertebrates is, as a whole, rather difficult to obtain since, with the exception of some groups (birds, teleosts and lampreys), these findings are often reported accessorily and succinctly, sometimes in studies of subjects that are quite unrelated to that of the CVS. Consequently, the information is widely dispersed and must be extracted and reassembled after carefully screening through a very abundant literature. It is also worth noting that much of the early literature is relatively inaccessible because of its age, the obscurity and unavailability of some of the publications, and the difficulty of the language in which it was published Three attempts were made over 15 years ago to review the accumulated knowledge on the CVS of vertebrates (Repérant et al., 1989b, Uchiyama, 1989, Ward et al., 1991). However, given the limited and fragmentary data available, it was not possible, in these reviews, to formulate any credible hypotheses regarding the evolution of this system. Even to this day, the CVS remains a subject of study that is marginal, and this component of the visual system is still relatively misunderstood, if not neglected. Indeed, among the huge recent and extensive body of outstanding literature available on the comparative neurology of the CNS (Butler and Hodos, 1996, Nieuwenhuys et al., 1998), data related to the CVS do not provide an adequate overview of its organization and possible evolution in vertebrates.

The present review constitutes a detailed survey of our present knowledge of the functional anatomical organization of the CVS of vertebrates. For each taxonomic group (see cladogram in Fig. 1), we shall consider, when data are available, the location of the centrifugal visual neurons, their mode of innervation of the retina, their neurochemical properties, as well as their afferent supplies, and we discuss the possible function of the CVS. On the basis of these various data, and by means of a cladistic analysis, we propose, in a subsequent paper (Repérant et al., in preparation), some evolutionary hypotheses concerning this component of the vertebrate visual system.

Section snippets

Agnatha

The Agnatha, or jawless vertebrates, belong to the most ancient extant vertebrate group (Forey and Janvier, 1993, Forey and Janvier, 1994, Janvier, 1981, Janvier, 1996). The living representatives of these ancestral vertebrates constitute two groups, the Myxinidae (hagfish), of which six genera containing some 32 species have been recognized, and the Petromyzontidae (lampreys), whose six genera contain about 41 species. In spite of their superficial resemblance, hagfish and lampreys diverged

Conclusions

On the basis of the present comparative analysis, it appears that the CVS constitutes a permanent component of the vertebrate CNS. However, from one group to the next, this component undergoes a high degree of variation and, in a second paper devoted to this question (Repérant et al., in preparation), we shall attempt to address the evolutionary significance of this phylogenetic diversity. The variations of the CVS are multiple and above all concern the topographical localization of the

Acknowledgments

The authors thank B. Jay for his help with computer drawings. This work was supported by CNRS (UMR 5166), MNHN (USM 501), INSERM (U616), France, FQRNT (Grant no. 88454), and NSERC (Grant no. 0G0053), Canada, and the Academy of Sciences of Russia (Russian President's Grant no. 2165.3003.4, Grants no. 02-04.49576 and 03-04-49637 from the Russian Foundation for Basic Research).

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