Segregation of callosal and association pathways during development in the visual cortex of the primate

Abstract

The segregation of callosal and association pathways in the developing visual cortex of the monkey was studied using the retrograde tracers fast blue and diamidino yellow. Quantitative analysis of the laminar distribution of labeled callosal and association neurons made it possible to reveal the shifting pattern of connections that characterizes the development of these two pathways. In the adult, callosal neurons are restricted to supragranular layers, where they are concentrated at the bottom of layer 3. Association neurons are located both in infra- and supragranular layers. Supragranular layer association neurons are concentrated in layer 2, with limited spread into layer 3 so that there is little overlap with callosal neurons. In the immature brain, callosal neurons are characterized by a tangential distribution that is more widespread than in the adult, while their laminar distribution undergoes little developmental change. Association neurons show two types of changes in their laminar distribution: (1) in the early fetus, there is a large excess of association neurons in supragranular layers, the adult distribution being achieved some time after birth; and (2) during maturation there is a selective elimination of at least 50% of the projections originating from the lower part of layers 2/3. Hence, the adult radial segregation of association and callosal pathways is achieved in part by regressive phenomena. The developmental reduction of bihemispheric projections is largely independent of changes in the organization of association neurons. Quantitative analysis of the morphology and spatial location of neurons sending axon collaterals to both hemispheres suggests that they constitute a subset of callosal neurons and that their frequency is determined by factors that regulate directly this population. These results are discussed with respect to the specification of visual cortical pathways during ontogenesis.

Development of connections within and between areas V1 and V2 of macaque monkeys

“…In contrast, two recent studies (Meisserel et al, 1991;Barone et al, 1995) have reported that the projection from V2 to V1 in the macaque initially involves a transient, excessive projection from the superficial layers. Their results were obtained using multiple large injections of fluorescent retrograde tracers into V1.…”

Callosally projecting neurons in the macaque monkey V1/V2 border are enriched in nonphosphorylated neurofilament protein

“…Interestingly, the neurons projecting from area VI to area MT, that are characterized by high levels of neurofilament protein, are all very large and have large axons, up to 3 /xm in diameter (Rockland, 1989(Rockland, , 1995, whereas short corticocortical connections are characterized by relatively lower levels of neurofilament protein immunoreactivity and originate from smaller neurons (Campbell et al, 1991;Hofetal., \995a,b, 1996). It should be kept in mind that the distribution of callosal connections in the primate visual system is not limited to the V1/V2 border, but that extensive sets of complex commissural projections exist in the prestriate cortex as well, that subserve additional roles such as completion of large receptive fields and interactions between field center and suppressive surrounds, and color constancy (Zeki, 1970;Van Essen et al, 1982;Antonini et al, 1983;Land et al, 1983;Maunsell & Van Essen, 1987;Spatz et al, 1987;Meissirel et al, 1991;Desimone et al, 1993). It should be kept in mind that the distribution of callosal connections in the primate visual system is not limited to the V1/V2 border, but that extensive sets of complex commissural projections exist in the prestriate cortex as well, that subserve additional roles such as completion of large receptive fields and interactions between field center and suppressive surrounds, and color constancy (Zeki, 1970;Van Essen et al, 1982;Antonini et al, 1983;Land et al, 1983;Maunsell & Van Essen, 1987;Spatz et al, 1987;Meissirel et al, 1991;Desimone et al, 1993).…”

Large‐scale maintenance of dual projections by callosal and frontal cortical projection neurons in adult mice

“…Despite having a common topology and common morphologies and occupying similar laminar distributions in layers II/III and V, callosal and association projection neurons in the monkey neocortex have been reported to differ on the basis of terminal projections and are two separate populations of neurons that rarely have dual projections Goldman-Rakic, 1982, 1984;Andersen et al, 1985;Johnson et al, 1989;Meissirel et al, 1991). Similar studies performed in rats have previously shown that callosal projections in the developing cortex are initially widespread but that these callosal projections are later lost or "pruned" as ipsilateral projections are made to the motor cortex in areas corresponding to the barrel fields (Ivy et al, 1979(Ivy et al, , 1984Killackey, 1981, 1982;O'Leary et al, 1981).…”