Early divergence of magnocellular and parvocellular functional subsystems in the embryonic primate visual system

Abstract

In both human and Old World primates visual information is conveyed by two parallel pathways: the magnocellular (M) and parvocellular (P) streams that project to separate layers of the lateral geniculate nucleus and are involved primarily in motion and color͞form discrimination. The present study provides evidence that retinal ganglion cells in the macaque monkey embryo diverge into M and P subtypes soon after their last mitotic division and that optic axons project directly and selectively to either the M or P moieties of the developing lateral geniculate nucleus. Thus, initial M projections from the eyes overlap only in prospective layers 1 and 2, whereas initial P projections overlap within prospective layers 3-6. We suggest that the divergence of the M and P pathways requires developmental mechanisms different from those underlying competition-driven segregation of initially intermixed eye-specific domains in the primate visual system.The segregation of motion and feature vision is a pervasive attribute of primate brain organization at all levels of the neuraxis, from the retina to the frontal lobe (1, 2). In Old World primates motion and color͞form discrimination is carried out by separate, magnocellular (M) and parvocellular (P) neuronal pathways that originate in the retina and project to separate M-and P-dedicated layers of the lateral geniculate nucleus (LGN) situated in the thalamus (refs. 3 and 4; Fig. 1). This segregated information then is transmitted from the LGN to M-and P-related sublayers and modules in the visual cortex (5-8). Although the details of the physiology have not been agreed on, it is generally accepted that neurons belonging to these separate streams can be distinguished on the basis of their time of origin (9), morphology (10, 11), connectivity (12, 13), biochemistry (14, 15), and different signaling molecules (16,17).In spite of the significance of the separation of M and P systems for understanding the functional anatomy of the human brain, surprisingly little is known about their development. In contrast, the development of ocular dominance pathways, which transmit information from the eyes via separate synaptic chains to the cerebral cortex, has been extensively studied and used as a premier model system for understanding principles governing the segregation of neuronal connections in the mammalian brain (18-21). A major step in understanding the development of this system was made in the 1970s when the injection of radioactive axonal tracers into the eyes of macaque embryos revealed that visual connections from the eyes initially overlap in the LGN (22, 23). The subsequent discovery that optic axons are more numerous during this early period of overlap than in adults (24), and that prenatal enucleation results in the maintenance of a widespread projection from the remaining eye (25), demonstrated that competitive interactions play an important role in the segregation of initially overlapping retinal projections. These findings, as well as the seminal studies of Hubel, ...

Early and Rapid Targeting of Eye-Specific Axonal Projections to the Dorsal Lateral Geniculate Nucleus in the Fetal Macaque

“…To determine when eye-specific retinogeniculate projections emerge during development, we injected a macaque fetus on E68, the earliest age when the full cohort of axons from the two eyes has arrived in the dLGN (Meissirel et al, 1997), and then killed the fetus on E69. Axons from the two eyes extensively overlap through most of the E69 dLGN ( Fig.…”

“…During development, the macaque dLGN undergoes substantial rotation between E50 and E90 (Rakic, 1977a;Meissirel et al, 1997), making it difficult to precisely delineate the M and P divisions at the ages we studied here. Indeed at E69, M and P divisions are not reliably discernable at all rostrocaudal locations (Fig.…”

“…Furthermore, much is known about the major developmental events in the embryonic macaque visual system, including the timing of retinal ganglion cell and dLGN cell birth and matura-tion (Rakic, 1977a;Shatz and Rakic, 1981;La Vail et al, 1991), the attrition of optic nerve axons (Rakic and Riley, 1983), the ingrowth and elaboration of retinogeniculate axons (Meissirel et al, 1997;Snider et al, 1999), and synapse formation in the dLGN (Hendrickson and Rakic, 1977). Because Rakic's study relied on tracers now known to be prone to "spillover" (LeVay et al, 1978;Ruthazer et al, 1999;Crair et al, 2001) and long postinjection survival periods, a precise delineation of when eye segregation occurs in this important model species is lacking.…”

Molecular Organization of the Ferret Visual Thalamus

“…Prenatal monocular enucleation does not prevent the formation of magnocellular and parvocellular zones (Rakic, 1981), and layer-specific cytoarchitecture emerges despite early binocular enucleation (Brunso-Bechtold et al, 1983;Guillery et al, 1985). Moreover, optic axons project selectively and directly to either the magnocellular or parvocellular zone of the developing LGN (Meissirel et al, 1997). To identify the molecular correlates of these functionally distinct streams, we used cDNA microarrays to analyze patterns of gene expression in the visual thalamus of a highly visual mammal, the ferret, whose altricial development allows ready access to tissues at the appropriate stage of development.…”

Perception of Biological Motion in Central and Peripheral Visual Fields

“…It might seem that in the case of motion analysis, the peripheral visual field should be more sensitive and specialised in analysing different motion stimuli, since the M ganglion cells forming the magnocellular pathway are more distributed in the peripheral retina than in fovea (Meissirel et al, 1997). However, all of the previously mentioned factors (cortical magnification, retinal cell density, etc.)…”