Spatiotemporal pattern of ontogenetic expression of calbindin-28/kD in the retinorecipient layers of rat superior colliculus

Abstract

Using an antibody against calbindin-28kD, we have studied the spatial pattern of expression of this protein in the superior colliculi (SC) of four strains of mature laboratory rats. In all four strains, calbindin-expressing cells (CECs) formed horizontally oriented tiers in the retinorecipient and intermediate gray layers but were diffusely distributed throughout the deep layers. Ontogenetically, calbindin-28kD was expressed for the first time in the retinorecipient layers at postconceptional day 20 (PCD 20), by cells located in the rostrolateral region where the first born retinal ganglion cells (RGCs) are represented. Although on the day of birth (PCD 22/23), the CECs were distributed more widely, they were still absent in the most medial part of the SC, that is, the region where the latest born RGCs are represented. The spatial distribution of CECs became adultlike only by PCD 29, that is, at the end of the period of the naturally occurring death of the RGCs. Monocular eye enucleations on PCD 23 prevented the expression of calbindin in the medial fifth of the retinorecipient layers of the contralateral SC, while the unilateral removal of the visual cortices had no discernable effect on the numbers and distribution of the CECs in either SC. Thus, the spatiotemporal pattern of ontogenetic expression of calbindin-28kD in the retinorecipient layers of SC reflects the spatiotemporal pattern of generation of the RGCs, and the retinal input appears to induce neuronal expression of calbindin-28kD in these layers.

Spatiotemporal patterns of ontogenetic expression of parvalbumin in the superior colliculi of rats and rabbits

“…Furthermore, somal sizes of PECs are not significantly different from the somal sizes of CB-expressing cells as long as they are located in the same collicular layers (cf. the present study with the study by Dreher et al, 1996).…”

“…Scale bar ϭ 1 mm for A,D. stained colliculi of juvenile and adults rats (Langer and Lund, 1974;Tokunaga and Otani, 1976;Labriola and Laemle, 1977) and rabbits (Mathers, 1977), whereas horizontal cells are present among collicular neurons expressing CB in both species ; (4) although PECs in the RRLs and the intermediate layers of SC of cat (Mize et al, 1992b) tend to be projection neurons, CB-expressing cells in cat SC tend to be interneurons (Mize et al, 1991); (5) PECs, unlike CB-expressing cells, form radially oriented patches in the SGI rather than a continuous distinct horizontally oriented tier; (6) PECs, unlike CB-expressing cells, are distributed fairly densely in the lateral parts of the deep layers rather than scattered at low density throughout the entire mediolateral extent of the deep layers; and (7) PECs, unlike CB-expressing cells, are absent from the PAG (for reviews, see Mize et al, 1992b;Dreher et al, 1996).…”

“…The distributions and the time courses of the ontogenetic expression of two cytosolic proteins, which belong to the EF-hand family of CaBPs, vitamin Ddependent calbindin-D-28-kDa (CB) and parvalbumin (PV; molecular weight ϭ 12 kDa), have been intensely studied in the visual system of several species of eutherian mammals (including humans). Thus, apart from the expression of CB and PV by distinct groups of cells in mammalian retinae (for reviews, see Pasteels et al, 1990;Yan, 1997), CB and PV have been reported to be expressed in morphologically heterogeneous groups of neurons in the dorsal lateral geniculate nuclei, the superficial (retinorecipient) layers of superior colliculi (SC), and striate and extrastri-ate visual cortices of both developing and mature eutherian mammals (Jones and Hendry, 1989;Demeulmeester et al, 1989Demeulmeester et al, , 1991Van Brederode et al, 1990;Hendrickson et al, 1991;Tigges and Tigges, 1991;Mize and Luo, 1992;Mize et al, 1992a,b;Alcantara et al, 1993;Diamond et al, 1993;Glezer et al, 1993;Hendry and Carder, 1993;Palestini et al, 1993;Arckens et al, 1994;Casagrande, 1994;Hogan and Berman, 1994;Spatz et al, 1994;Yan et al, 1995;Cao et al, 1996;Dreher et al, 1996;Leuba and Saini, 1996;Sanchez-Vives et al, 1996).…”

“…It has been established that the time courses of the ontogenetic onset of expression of CB in the RRLs of cat, rat, and rabbit SC overlap completely with the periods of naturally occurring death of retinal ganglion cells and the periods of elimination of the topographic errors in the retinal map in the SC (Mize and Banfro, 1994;Barker and Dreher, 1996;Dreher et al, 1996). In rats, at least, the expression of CB in the RRLs is induced by the activity of retinal input and is not affected by the presence or absence of the corticotectal projection from the visual cortex .…”

“…In rats, at least, the expression of CB in the RRLs is induced by the activity of retinal input and is not affected by the presence or absence of the corticotectal projection from the visual cortex . Furthermore, the spatiotemporal pattern of the ontogenetic onset of CB expression in the RRLs of both rats and rabbits reflects the spatiotemporal pattern of generation of the retinal ganglion cells (RGCs) and appears to indicate the spatiotemporal pattern of neuronal maturation in the RRLs of the SC Dreher et al, 1996). By contrast, PV is not expressed during the period of establishment and refinement of the retinotopic maps in the SC (cat: Mize and Banfro, 1994;rat: Barker et al, 1995).…”