Control of the development of the ipsilateral retinothalamic projection in Xenopus laevis by thyroxine: Results and speculation

Abstract

The ipsilateral retinothalamic projection of the frog Xenopus laevis is formed by the axons of a subset of retinal ganglion cells which are found throughout peripheral and non-nasodorsal retina. Unlike the crossed retinotectal and retinothalamic projections, which begin to form during early embryonic stages, the ipsilateral projection does not begin to develop until late in tadpole life, at stages when thyroxine first becomes detectable in the circulation. Blocking the production of thyroid hormone in tadpoles prevents the development of the ipsilateral projection, in a reversible manner. Intraocular injection of thyroxine can "rescue" the development of the projection in tadpoles which otherwise remain premetamorphic. In addition, the projection from one eye of a metamorphically-blocked tadpole can be induced to form by an intraocular injection of thyroxine at a dose which has no detectable effect on retinal development in the other, untreated eye. These results indicate that the development of the ipsilateral retinothalamic projection is dependent upon thyroxine, and strongly suggest that the hormone acts at the level of the eye, rather than at the optic chiasm or thalamic target, to bring about the development of a new pathway. A number of ways in which thyroxine might act in the system are discussed.

Thyroid Hormone and Retinal Development: An Emerging Field

“…2B) (34). The Xenopus ipsilateral ganglion cells, and their connection to thyroid hormone, have been elegantly described in a series of reports by Hoskins (45)(46)(47); whether a similar "metamorphic" retina exists in other organisms remains to be seen.…”

Developmental and Regional Patterns of GAP-43 Immunoreactivity in a Metamorphosing Brain

“…In visual pathways of several anuran species, anatomical changes during larval development include the progressive expansion of terminations of retinal ganglion fibers from the rostral/lateral to the caudal/ medial contralateral OT, the progressive growth of the more superficial layers of the OT compared to the deep layers, and the development and elaboration of ipsilateral retinotectal and retinothalamic projection pathways during climax [Currie and Cowan, 1975;Hoskins, 1986;Kollros and Thiesse, 1988]. Specifically in the bullfrog, the cell layers of the OT become more pronounced as larval development proceeds, although the major change in thickness and differentiation of these layers seems to have occurred by the end of the hatchling period .…”

“…All sensory systems undergo considerable reorganization over metamorphic development. In the visual system, for example, ipsilateral projections from the retina to the optic tectum and to the thalamus fully develop later in larval life than do contralateral projections, which are present at the earliest postembryonic stages [Currie and Cowan, 1975;Hoskins, 1986]. In all but permanently aquatic species such as the African clawed frog, Xenopus laevis , the lateral line system degenerates during metamorphic climax [Fritzsch et al, 1984].…”

The Visual Pathways of Eutherian Mammals and Marsupials Develop According to a Common Timetable (Part 2 of 2)

“…In this context it is noteworthy that thyroid hor mones (particularly thyroxine) have been shown to influence the rates of neuronal proliferation, neu ronal death and synaptogenesis in vertebrate central nervous systems [for reviews, see Jacobson, 1978;Hoskins, 1986], In addition, glucocorticoid hormones [Puro, 1983] and insulin [Puro and Agardh, 1984] have been shown to regulate the timing of the developmen tal step in which cholinergic neurons of the retina in rats become capable of releasing acetylcholine in re sponse to excitatory stimulation in vitro. In view of these findings it seems likely that hormones may play a role in helping to synchronise the development of widely disparate parts of the central nervous system.…”