Expansion of the half retinal projection to the tectum in goldfish: An electrophysiological and Anatomical study

Abstract

The topographical retino-tectal projection of goldfish was electrophysiologically mapped a t various intervals after surgical removal of the nasal half of the retina and pigment epithelium. The remaining projection was initially restricted to the appropriate rostral half of the tectum, even if the nerve was crushed and allowed to regenerate. But later, after 137 days or more, it showed a progressive expansion onto the foreign caudal half of the tectum. The magnification factor, the number of micrometers of tectum per degree in the visual field, doubled in the rostro-caudal but not in the medio-lateral direction. Analysis of the sequence of the expansion showed that a few fibers originally projecting nearest the denervated area were the first to spread over it. Then, progressively more fibers moved caudally until a nearly uniform representation of the half retina was established on the tectum. Radioautography also demonstrated that retinal fiber terminals had invaded the caudal tectum. The retinae of these fish were also examined histologically. The density of ganglion cells had not increased, but they consistently showed the axonal reaction. This was not found to be associated with any initial surgical trauma, but rather with the movement of their fiber terminals within the tectum. Frozen sections, through half retinal and normal eyes, were cut and photographed for comparison of ocular geometry. Operated eyes were normal except for a slight but consistent loss of ocular volume. Analysis of the optical geometry showed that recording with fish in air produced two effects: Myopia (10" blur circle, or less) and enlargement of the visual field by 15% to 20%.The topographical retino-tectal projection of goldfish, which was once thought to be unmodifiable (Attardi and Sperry, '63; Jacobson and Gaze, '65; Sperry, '631, has more recently been found to be a very dynamic system (Gaze and Sharma, '70; Yoon, '71, '72a,b,c; Schmidt et al., '74). This shift in thinking began with the work of Gaze and Sharma ('70) who first demonstrated that, following removal of the caudal half tectum, the entire retinal projection could compress onto the remaining rostral half tectum.Although the results on half tectal compression have been verified by many others (Yoon, '72a, '71; Schmidt et al., '74; Meyer, '77), there is still disagreement about reorganizations following retinal ablations. Anatomical studies have shown little or no evidence for expansion of the half retinal projection. Attardi and J. COMP. NEUR., 177: Z~I -Z I~ Sperry ('63) waited only 30 days after optic nerve crush and partial retinal removal, and found that the regenerating fibers reestablished the original projection of the remaining retina but did not invade new areas of the tectum. More recently, Meyer ('75) using radioautography, found little evidence for expansion of the half retinal projection even after many months. Two short electrophysiological reports have also dealt with the projection of the half retina a t long postoperative intervals, but include ...

Competition is a driving force in topographic mapping

“…Thus, map expansions and contractions observed after retinal and tectal/collicular ablations (45)(46)(47)(48)(49), when competition between axons is modified, are consistent with the dual gradient, servomechanism, and competition models, because each includes competition as a mechanism to ensure uniform target coverage (4,21). Perhaps for this reason, recent reviews of mapping in the literature present the prevailing model for the topographic map formation as a dual gradient model along the A-P axis and a form of servomechanism along the M-L axis (50,51).…”

Competition regulates the efficacy of an identified synapse in crickets

“…One mechanism that is believed to regulate the number and efficacy of synaptic contacts is competition. The original idea, and much of the evidence for competitive interactions, come from studies of afferent projections in the visual system of vertebrates (Hubel et al, 1977;Schmidt et al, 1978;Tieman, 1984;Wiesel and Hubel, 1965). A direct demonstration, however, of the effects of competition on individual central synapses is difficult to obtain.…”

Growth dynamics and morphology of regenerating optic fibers in tectum are altered by injury conditions: An in vivo imaging study in goldfish

“…When half of tectum is removed and the optic nerve crushed, fibers from the entire retina become squeezed into the remaining half tectum to form a compressed retinotopic projection from the entire retina (13,44). Similarly, when half of retina is removed and the nerve crushed, regenerating fibers from the remaining half of retina can expanded across the entire tectum (36). Since the general result is that all fibers become accommodated and all tectum becomes innervated, it has been suggested that fibers compete for tectal space (18,26,39,42).…”

“…There are reasons to believe that the regulation of axonal growth is more complicated than a simple response to local cues. One reason for thinking this is the plasticity of the mapping (13,26,36,39,42,44). When half of tectum is removed, fibers will form a compressed retinotopic projection onto the remaining half of tectum.…”