Migratory paths of neurons and glia in the embryonic chick spinal cord

Abstract

To study the migration of chick spinal cord neurons, we labeled individual cells in the ventricular zone with recombinant retroviruses, then identified their progeny histochemically. First, we analyzed cell mixing in the ventricular zone. Some clones labeled at early neural tube stages spread widely along both the dorsoventral and rostrocaudal axes. However, clones labeled later were confined to narrow domains along both axes. These results imply that displacement of cells within the ventricular zone becomes progressively restricted. Second, we studied the migration of cells out of the ventricular zone by infecting embryos at a fixed stage and varying the time of analysis. At first, most clones consisted of radial arrays of cells, suggesting that the initial migration is predominantly radial. In many clones, however, neurons turned orthogonally from parental radial arrays and migrated along the path of circumferentially oriented axons. By hatching, clonally related cells in the gray matter were usually distributed in narrow transverse slabs, but some white matter glial cells had migrated longitudinally for up to several segments. We conclude that the dispersal of clonally related cells results from (1) early mixing of progenitors within the neural tube; (2) radial stacking of progeny in the ventricular zone; (3) migration of progeny from the ventricular zone in spoke-like routes; (4) circumferential migration of some neurons along axons; (5) short-distance dispersal of differentiating neurons; and (6) a late, longitudinal migration of glia through white matter tracts. Finally, we show that floor plate cells differ from other spinal cord cells in both their

Tangential migration of neuronal precursors of glutamatergic neurons in the adult mammalian brain

“…A very small number of glutamatergic modulatory interneurons are also generated in the adult SVZ and migrate tangentially to the olfactory bulb (24). Motor neurons in the spinal cord possess both radial and tangential migration (25). Additionally, neurons originating from the diencephalon can migrate tangentially to populate the amygdala, a telencephalic nucleus (26).…”

Commissural axonal corridors instruct neuronal migration in the mouse spinal cord

“…There is good evidence to support the idea that in some contexts pioneer axons provide a growth substrate for newly migrating axons and cell bodies [10][11][12] . In addition, there are a number of reports of neuronal cell bodies that have the morphological appearance of migrating along axonal tracts 13,14,29,43,44 . For example, in the rat spinal cord, preganglionic cholinergic neurons have been shown to be in close apposition to commissural axonal tracts 14,43,44 .…”

“…Conversely, there is also evidence to support the idea that pioneer axons provide a growth substrate for newly migrating axons and cell bodies [10][11][12] . In addition, during a form of tangential migration, photographic evidence suggests that the migrating neuronal cell bodies appear as if they are using axons as migration scaffolds 5,6,[13][14][15] . However, direct experimental evidence supporting the possibility of such neurophilic migration as a general mechanism remains sparse 5,[16][17][18][19][20] .…”

Onset of Electrical Excitability during a Period of Circus Plasma Membrane Movements in DifferentiatingXenopusNeurons

“…In the period between final mitosis and morphological differentiation, neurons in both the cortex (Rakic, 1972;McConnell, 1991) and the spinal cord (Chu-Wang et al, 1981;Leber and Sanes, 1995) migrate radially to achieve their appropriate positions. Significantly, these movements can be influenced by Ca 2ϩ influx (Komuro and Rakic, 1992, 1993, 1995; however, biophysical recordings from neurons in this developmental period are lacking, in part because of the scarcity of in vitro models in which postmitotic but morphologically undifferentiated neurons can be distinguished from other cell types found in primary cultures of embryonic neural tissue.…”

“…These cellular translocations appear similar to those described previously for the motile deep cells of Fundulus blastula and gastrula (Trinkaus, 1973), in which lobopodial extension and adhesion are followed by contraction and net cellular movement. Although various factors (e.g., contact inhibition of movement) could regulate the motility of circus cells in vivo, Xenopus primary spinal neurons may have a developmental profile similar to differentiating neurons in both cerebral cortex (Rakic, 1972;McConnell, 1991) and spinal cord (Chu-Wang et al, 1981;Leber and Sanes, 1995), wherein a period of postmitotic migration occurs before morphological differentiation. This comparison is supported further by the shared cytochalasin B-dependence of circus movements and neuronal migration (Rivas and Hatten, 1995).…”