Comparative neurology of the optic tectum in ray-finned fishes: patterns of lamination formed by retinotectal projections

Retinal and visual function returns following retinal destruction by ouabain in adult goldfish (Carassius auratus). Although the precise cellular mechanisms are unclear, the ability to regenerate CNS neurons and connections that subsequently sustain visual behavior is remarkable, especially for an adult vertebrate. In this paper, we ask whether visual stimulation via new retinal cells can activate existing cells in the optic tectum, which normally receives the largest retinal projection in this species. The right eyes of adult goldfish were injected with ouabain. After 1–18 weeks the conscious, freely moving fish were exposed to spatially and temporally varying visual stimuli and the resulting tectal metabolic activity was determined with the autoradiographic deoxyglucose method. In normal controls without lesions, visual stimulation produced equally strong metabolic activity in both tectal hemispheres, peaking in the layer where most retinotectal projections terminate (N = 6). One week after ouabain injection, metabolic activity in the contralateral, deprived tectum was dramatically reduced (N = 5), closely resembling the effect of unilateral ocular enucleation (N = 5). However, 9–18 weeks after ouabain injection, metabolic activity in the deprived tectum recovered to a level that was statistically indistinguishable from normal controls (N = 6). These findings suggest that, after a comprehensive cytotoxic lesion of the retina, regenerated ganglion cells not only establish new connections with the preexisting optic tectum, but also effectively transmit visual information they receive from newly generated photoreceptors to the “old” tectum.

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The discontinuous visual projections on the Xenopus optic tectum following regeneration after unilateral nerve section

Development ◽

10.1242/dev.94.1.121 ◽

1986 ◽

Vol 94 (1) ◽

pp. 121-137

Author(s):

D. J. Willshaw ◽

R. M. Gaze

Keyword(s):

Optic Nerve ◽

Horseradish Peroxidase ◽

Optic Tectum ◽

Small Proportion ◽

The Other ◽

Nerve Transection ◽

Nerve Section ◽

Retinotectal Projections ◽

Uniform Background ◽

Whole Mounts

The establishment of retinotectal projections following transection of one optic nerve in developing Xenopus has been investigated. Between 3 weeks and 11 months after the operation, the nerve fibre tracer horseradish peroxidase (HRP) was applied to either the operated or the unoperated nerve, and the brains were prepared for examination as whole mounts. In most cases fibres from the operated nerve innervated both tecta, with the result that one tectum was doubly innervated and one tectum singly innervated. Two months after transection of the optic nerve in tadpole life, between stages 50 and 54, this nerve usually made a uniform projection on the contralateral tectum and a striped projection on the ipsilateral, doubly innervated, tectum. The projection made by the unoperated nerve on this tectum was a similar pattern of stripes, which ran generally rostrocaudally. Two months after transection of the optic nerve of newly metamorphosed animals, the projection formed by the operated nerve on the doubly innervated tectum was usually a pattern of spots or spots mixed together with stripes in no particular orientation superimposed on a roughly uniform background. In a small number of cases the projections made by the same nerve on the two tecta were approximately complementary; that is, the presence of label on one tectum corresponded with its absence on the other tectum. The results are examined in the context of the development of the retina and of the tectum. It is suggested that the consistently oriented stripes which result from nerve transection at a stage at which only a small proportion of the retinal fibres had reached the tectum are formed by the interaction of two equally matched sets of developing fibres, stripe orientation being determined by the mode of growth of the optic tectum. The formation of patterns of spots or spots mixed together with stripes following nerve transection after the end of the main phase of tectal histogenesis, and when 50 % of the optic fibres had already reached the tectum, is attributed to an unequal competition between the two sets of fibres.

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