Skin sensory innervation patterns in embryonic chick hindlimb following dorsal root ganglion reversals

Abstract

During embryonic development skin sensory neurons in lumbosacral dorsal root ganglia (DRGs) establish their dermatomes and axonal projections in a precise, orderly fashion in the chick. To investigate mechanisms responsible for this specific outgrowth, the rostrocaudal order of DRGs T7-LS3 was reversed by rotating the corresponding segments of neural crest, either alone or together with the underlying neural tube in St.15-16 embryos. The resulting skin sensory innervation patterns, mapped physiologically or anatomically at St.29-40, differed between the two experimental groups. Following neural tube rotations DRGs tended to establish innervation patterns that were consonant with their original position in the embryo. Axons from these rotated DRGs generally projected into the appropriate pathways and innervated the appropriate region of skin. Neural crest rotations left the ventral neural tube (including the motor neuron precursors) largely intact. In this case rotated DRGs tended to establish innervation patterns in accordance with their new position in the embryo, almost as if no rotation had been made. These results cannot be explained solely by the inherent specificity of sensory neurons. Instead, the results are largely consistent with the suggestion (Honig et al., 1986; Landmesser and Honig, 1986) that motor axons can direct the outgrowth of sensory axons and thereby influence the establishment of sensory innervation patterns. Other mechanisms that may also affect the development of sensory innervation patterns are discussed.

Receptor Tyrosine Phosphatases Guide Vertebrate Motor Axons during Development

“…Our phenotypic analysis suggests that the whole nerve is affected by RPTP dsRNA electroporation, including the sensory component. This finding is consistent with a body of evidence linking sensory axon pathfinding to decisions made by earlier-extending motor axons Landmesser and Honig, 1986;Scott, 1986;Wang and Scott, 1997;Honig et al, 1998).…”

Prenatal development of rat primary afferent fibers: I. Peripheral projection

“…Although our results are in agreement with such a model, it should be noted that other studies involving small neural tube and neural crest reversals Scott, 1986) have produced results which are not always consistent with this hypothesis. For example, in some cases displaced sensory neurons are capable of innervating peripheral targets appropriate for their original locations Scott, 1986).…”

“…For example, in some cases displaced sensory neurons are capable of innervating peripheral targets appropriate for their original locations Scott, 1986). Thus, although general guidance cues are sufficient to describe the patterns observed in normal development, we cannot rule out the possibility that additional specific cues may also have a significant role.…”

Normal and abnormal pathfinding of facial nerve fibers in the chick embryo

“…for example, after transplanting projection neurons to an ectopic site or into a host of a different age (Ghysen, 1978;Constantine-Paton, 1983;Murphey, Johnson, and Sakaguchi, 1983;Harris, 1984Harris, , 1986Honig et al, 1986), by inserting a barrier in the normal pathway (Moody and Heaton, 1983c), and by eliminating pioneer fibers or intermediate targets (Edwards, Chen, and Berns, 198 1;Bentley and Caudy, 1983;Kuwada, 1986;Chitnis and Kuwada, 199 1 ;Bernhardt, Nguyen, and Kuwada, 1992;Pike et al, 1992). In vertebrates, studies of navigating nerve fibers have focused on pathfinding of motor axons ( Lance-Jones and Landmesser, 1980, I98 1 ;Landmesser, 1980;Purves and Lichtman, 1985) and peripheral pathfinding of neural crest-derived sensory ganglia (Lewis, Chevallier, Kieny, and Wolpert, 198 1 ;Landmesser and Honig, 1986;Scott, 1986), but little is known about central pathfinding abilities of sensory cells of pla-coda1 origin (SzCkely, 1959;Hamburger, 196 1;Constantine-Paton, 1983).…”