Development of the longitudinal projection patterns of lumbar primary sensory afferents in the chicken embryo

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Abstract
The literature on the anatomical organization of primary sensory afferents, though extensive, contains relatively little information about the longitudinal extent of the central collateral projections. Our understanding of intersegmental sensorimotor integration in the spinal cord and of the developmental mechanisms that establish its underlying circuitry could be significantly enhanced by a more complete description of these projections. To address this issue from a developmental perspective, we labeled the central projections of lumbar primary afferents in fixed preparations of the chicken embryo with the lipophilic tracer DiI. At late embryonic stages, the afferent projections had the following characteristics: Primary afferents originating from a single lumbar dorsal root ganglion bifurcated to project longitudinally in the dorsal funiculus or Lissauer's tract. Dorsal funiculus axons extended up to seven segments caudally and to at least ten segments rostrally, whereas axons in Lissauer's tract extended up to seven segments in each direction. Collaterals branched off the longitudinal axons over a range of about seven segments in each direction. Within this range, collaterals to specific terminal fields exhibited more restricted ranges. The development of these longitudinal patterns during earlier embryonic stages was followed from the time the afferents first reached the neural tube on day 4 of embryogenesis. The longitudinal axons lengthened as a single bundle up to day 10, with medial axons consistently longer than lateral axons. After day 10, the longitudinal axons were segregated into the dorsal funiculus and Lissauer's tract. Collaterals sprouted after about 2 days of longitudinal axon growth, by which time the axons had extended several segments in each direction. The segmental range over which collaterals were present reached a maximum of 20 segments at day 10. Collaterals to the different terminal areas differed in their segmental ranges already by this time. After day 10, the total segmental range of collaterals decreased to the stable level of about seven segments in each direction, which is characteristic of late-stage embryos.