Abstract

Our understanding of the development of the retina and visual pathways has seen enormous advances during the past 25years. New imaging technologies, coupled with advances in molecular biology, have permitted a fuller appreciation of the histotypical events associated with proliferation, fate determination, migration, differentiation, pathway navigation, target innervation, synaptogenesis and cell death, and in many instances, in understanding the genetic, molecular, cellular and activity-dependent mechanisms underlying those developmental changes. The present review considers those advances associated with the lineal relationships between retinal nerve cells, the production of retinal nerve cell diversity, the migration, patterning and differentiation of different types of retinal nerve cells, the determinants of the decussation pattern at the optic chiasm, the formation of the retinotopic map, and the establishment of ocular domains within the thalamus.

In 1986, when Vision Research published its 25th Anniversary Issue, there was no chapter dedicated to developmental visual anatomy, being the summary descriptor provided by the editors for the present chapter. The closest coverage was provided within a chapter on visual development, focusing upon the acquisition of visual function, the consequences of early visual deprivation or restricted visual exposure, and on the associated plasticity within visual cortex ( Teller & Movshon, 1986). It is interesting to re-visit that historical overview now, 25years later, to appreciate the excitement within the field during those golden years of visual neurophysiology. Three pioneers in our understanding of the development of the visual system received the Nobel Prize in Physiology or Medicine during that era, in 1981, Roger Sperry, David Hubel and Torsten Wiesel, and the contributions of two of them feature prominently within that article. As acknowledged by the authors, In 1960, the neurobiology of visual development was dominated by the work of Roger Sperry. But rather than this being the prelude to a tribute, Sperry is taken to task for his preoccupation with the hard-wiring of the visual pathway, and his impact for the era under review was largely dismissed: Sperrys relentless emphasis on the independence of neural development from neural function in the developing animal was to have a short life after 1961 (p. 1486, original italics).

Since that anniversary issue in 1986, the past 25years have witnessed unprecedented experimental as well as conceptual advances in our understanding of the development of the retina and sub-cortical visual pathways, much of it occurring well before the onset of visual function. Many of these advances vindicate a hard-wiring perspective such as Sperrys, relying upon cell-signaling interactions independent of neural transmission, while others show that neural function long before the onset of photo-transduction plays a critical role in the formation of neural circuitry. The phenomenal scientific pace of the past 25years has been made possible largely by new technologies that continue to expand the front of developmental neurobiology in general. The experimental advances have been a consequence of the revolution in molecular biology and by the availability of new imaging technologies, permitting genetic dissection of the molecular factors and cellular interactions underlying retinal and optic pathway development, and the visualization of single neurons or populations of cells as they pass through the cell cycle, express transcription factors and the downstream genes they regulate, migrate to their specific layers, differentiate their characteristic morphologies, navigate an axonal trajectory to central visual structures, establish and refine their synaptic connections, and undergo programmed cell death. The present review will not consider in detail those technical advances themselves; the reader is directed to another recent colorful review providing ample coverage of this ever-expanding toolbox (Mason, 2009). The consequent experimental results have led to new conceptual insights, altering the ways in which we think about retinal development and target innervation, and the present focus will be upon these changes in our understanding.

One should not fault the myopia of the former review too much; without a doubt, we simply could not appreciate the full nature of the neurobiological issues at play 25years ago.1 Visual cortex was where the action was, and electrophysiology was the tool of choice for understanding the mechanics underlying visual function. We now know so much more about the pre-visual development of the retina and sub-cortical visual pathways, from a decidedly cellular and molecular biological perspective, that I will restrict the present coverage accordingly, and unashamedly, as vision will hardly be mentioned.

By comparison with the other chapters in this special issue of Vision Research, the purview of the present chapter is vast, encompassing advances not only in our understanding of the various components establishing the complex architecture and connectivity of the neural retina, but also of the visual pathways and their innervation of target visual structures. Any such review of strides taken over a defined period of time must to some extent be idiosyncratic (as in that former paper), but I believe these issues largely summarize the major conceptual and experimental advances during the past 25years. I have chosen to highlight eight issues, briefly recapitulating these advances and sacrificing much detail due to space limitations. Each of these topics has been reviewed in far greater detail elsewhere, and doubtless researchers working on development of the visual system will find reason enough to feel frustrated by the brevity of the present effort. Rather, my intended audience has been that collection of vision researchers that digest the literature on retinal and pathway development with only modest fervor, to give them a synopsis of the major advances during this era, as well as current students and post-docs working within this field of developmental neurobiology that may not appreciate the degree to which this field has advanced. The latter group need only compare the coverage of the developing retina and visual pathway provided by textbooks then in use (e.g. Jacobson, 1978andPurves and Lichtman, 1985) with that provided more recently ( Sanes, Reh, & Harris, 2006) to appreciate the remarkable evolution in our understanding of these developmental processes. The former textbooks reflect the strong foundations of the field drawn from experimental embryology and neurophysiology but now seem sadly deficient in providing much account of the histotypical interactions between cells or of the genes expressed and molecular signals they set in motion that participate in these events.

Twenty-five years ago, while we had some appreciation that an early eye field was derived from the neural plate and was critical for the development of the retina, we had no knowledge of the transcriptional control of this process by a handful of early eye-field genes that are now understood to command a downstream cascade of genes critical for assembling the mature retina (Zuber & Harris, 2006). As the eye cup emerges and expands in size, the factors modulating cell cycle kinetics have been dissected with increasing detail, including the molecular mechanisms driving interkinetic nuclear translocation, the intracellular and extracellular determinants of cell-cycle exit, and the factors that coordinate the wave of neurogenesis progressing from its site of initiation (Agathocleous and Harris, 2009, Baye and Link, 2007, Del Bene et al., 2008, Dyer and Cepko, 2001, Levine and Green, 2004, Martins and Pearson, 2008andNorden et al., 2009). The present coverage will begin with the emerging neural retina at the outset of neurogenesis, considering advances in our understanding of the lineage relationships between retinal neurons, the determination of neuronal cell-types and the production of species-specific retinal architecture, the control of neuronal positioning, and the determinants of morphological differentiation.

Retinal progenitors were understood to expand the pool of post-mitotic precursor cells that would ultimately adopt various cellular fates, but there was no firm understanding of whether dedicated progenitors yielded particular types of cell, or if progenitors were multi-potent. While birth-dating studies had already shown that each type of retinal nerve cell was born in a distinct window during retinal neurogenesis (Carter-Dawson and LaVail, 1979, Drger, 1985, Hinds and Hinds, 1979, Sidman, 1961andYoung, 1985), these provided no insight into the clonal relationships between the cells of the retina. In the late 1980s, two different approaches were employed to label single retinal progenitor cells in order to identify their progeny at subsequent stages of maturity. One was to inject single cells with cytoplasmic tracers that would remain detectable within progeny despite progressive dilution following repeated cell divisions (Holt et al., 1988andWetts and Fraser, 1988). The other was to use replication-deficient retroviruses encoding reporter genes to infect single cells, therein bypassing the problem of progressive dilution with repeated mitoses (Turner and Cepko, 1987andTurner et al., 1990). Both approaches yielded comparable findings that retinal progenitor cells were in fact multi-potent, producing clones of cells that included a variety of retinal neuronal types as well as Mller glia. They lacked, however, any retinal astrocytes, handily accounted for, at roughly the same time, by the demonstration that astrocytes are immigrants to the neural retina, being derived from a distinct progenitor cell in the optic stalk and migrating into the inner retina during the period of retinal neurogenesis (Ling and Stone, 1988, Stone and Dreher, 1987andWatanabe and Raff, 1988).

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Development of the retina and optic pathway - ScienceDirect

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