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

Abstract

We have investigated the development of intrinsic and interareal connections in areas V1 and V2 of the macaque monkey using postmortem transport of the lipophilic fluorescent tracer diI, applied to brains fixed at different pre- and postnatal ages. Intrinsic connections in the deep layers of V1 are evident on embryonic day 108 (E108), but are not robust in the superficial layers until around E118, when migration is largely complete. Both intrinsic horizontal projections and extrinsic projections to V2 initially have a continuous distribution. Patchy projections are first evident in V1 around E145, the same age at which cytochrome oxidase blobs appear, presumably signaling the differentiation of the blob-dominated and interblob-dominated streams in the primary visual cortex. The magnocellular-dominated stream becomes distinct at earlier stages (by E122), as judged by connectional and histochemical criteria. In area V2, intrinsic connections initially (at E108) involve only deep layer cells and do not have a clustered organization. By E130, superficial layer cells are involved and the V2 intrinsic connections have a patchy distribution; by E145, an adult-like pattern is present. The projection from V2 to V1 passes through an early stage (up to E133) of originating principally from deep layer cells, and thereafter originating from superficial as well as deep layers. We found evidence for changes in dendritic morphology during development. Most notably, at E118, many neurons in layer 6 which are involved in intrinsic or interareal connections have dendrites that extend well into the superficial layers, even into layer 1, a characteristic not reported in the adult.

Microstructural Changes of the Baboon Cerebral Cortex during Gestational Development Reflected in Magnetic Resonance Imaging Diffusion Anisotropy

“…Although the rudiments of a six-layered adult laminar structure can be seen in E125 brains (Dieni et al, 2004), the immature isocortex of E90 and E125 brains do not yet possess a mature, differentiated morphology (Fig. 2b) (Sidman and Rakic, 1982;Coogan and Van Essen, 1996;Dieni et al, 2004). Nevertheless, immature neurons of superficial layers excluding layer I are elongated (Dieni et al, 2004), have a relatively undifferentiated neuropil [Sidman and Rakic (1982) their Figs.…”

Delayed maturation of receptive field center/surround mechanisms in V2

“…The present results provide support for the growing body of evidence indicating that, although the basic anatomical connections in higher-order visual areas are present at or before birth (3,4,28,29), the maturation of the functional connections in the visual brain proceeds in a hierarchical order (4,7,23,24). Also, our results support the hypothesis that the anatomical feedback connections from extrastriate visual areas to V1 or V2 mature much slower than the feedforward connections in these cortical areas (4).…”

“…This result is consistent with previous anatomical studies (4,28,29). Functionally, however, these surround connections were extremely immature in 2-week-old monkeys, and many subnormal responses persisted even at 8 weeks of age (Fig.…”

Development of Temporal Response Properties and Contrast Sensitivity of V1 and V2 Neurons in Macaque Monkeys

“…The basic connections and structural organization of the LGN, V1, and extrastriate visual areas are qualitatively adultlike by birth (Burkalter et al 1993;Coogan et al 1996;Horton and Hocking 1996;Rakic 1976Rakic , 1977. According to an emerging view of visual system development, however, the functional maturation of the primate visual system appears to proceed at a slower rate in higher-order visual areas (Barone et al 1996;Batardiere et al 2002;Kiorpes and Movshon 2004b;Rodman and Consuelos 1994;Rodman et al 1993;Zhang et al 2005).…”