Retinal influences specify cortico‐cortical maps by postnatal day six in rats and mice

Abstract

Studies of callosal projections in striate cortex show that the retina is involved in the development of topographical connections. In normal animals callosal fibers connect retinotopically corresponding, nonmirror-symmetric cortical loci, whereas in animals bilaterally enucleated at birth, callosal fibers connect topographically mismatched, mirror-symmetric loci. Moreover, in rodents the overall pattern of visual callosal connections is adult-like by postnatal day 12 (P12). In this study we delayed the onset of retinal deafferentation in rats and mice in order to determine the period when retinal influences are critically needed for the development of retinotopically matched callosal linkages. Callosal maps were revealed by placing small injections of retrogradely and anterogradely transported tracers into different loci of lateral striate cortex. We found that the patterns of callosal linkages in rats enucleated at P12, P8, and P6 were nonmirror-symmetric, as in normally reared rats. In contrast, the patterns of linkages in rats enucleated at P4 closely resembled the mirror-symmetric pattern seen in rats enucleated at birth (P0). A similar reversal in topography (from symmetric to nonsymmetric) occurred in mice when enucleation was delayed from P4 to P6. These findings indicate that retinal input prior to P6, but not prior to P4, is sufficient for specifying normal callosal topography. Moreover, they suggest that development of retinotopically matched callosal linkages depends critically on retinal influences during a brief period between P4 and P6, when callosal connections are still very immature.

Topography and axon arbor architecture in the visual callosal pathway: effects of deafferentation and blockade of TV-methyl-D-aspartate receptors

“…2B), while the injection of RB produced a dense accumulation of retrogradely labeled cells centered on the 17/18a border (black dots in left panel). These results, schematically represented in the top inset in Figure 2B, provide evidence that callosal linkages are not arranged as a mirror image of the injections sites, as it occurs in neonatally enucleated rats (Olavarría and Hiroi, 2003). Similar results were observed in 5 additional rats treated with MK-801.…”

“…To analyze the effect of NMDAR blockade on axonal Neurons and axon terminals of the callosal pathway accumulate in a column-like zone that straddles the border between area 17 and area 18a (see Olavarría and Hiroi, 2003). Note however that in all diagrams, the areas indicated in gray represent only the portion of the 17/18a callosal zone falling within area 17.…”

“…1). Studies in rodents (Lewis and Olavarría, 1995;Olavarría and Hiroi, 2003) have shown that visual callosal fibers interlink opposite cortical loci that are in retinotopic, rather than anatomic, correspondence (i.e., interconnected loci are not mirrorsymmetric with respect to the brain midline, see Fig. 1A, B).…”

“…1C), whereas removal of retinal input at or after P6 resulted in the normal, non-mirror symmetric topography (Fig. 1B, Olavarría and Li, 1995;Olavarría and Hiroi, 2003). Olavarría and Li (1995) proposed that bilateral projections from temporal retina relay synchronous activity to retinotopically corresponding points in both hemispheres, leading to the stabilization of non mirrorsymmetric interhemispheric connections through Hebbian-like (Hebb, 1949) mechanisms (Fig.…”

“…1A, B). Moreover, development of this topography requires retinal input during a brief critical period extending from postnatal day 4 (P4) to P6 (Olavarría and Hiroi, 2003). These authors showed that removal of retinal input at, or prior to P4 produced abnormal, mirror-symmetric patterns of callosal linkages (Fig.…”