A critical period for the influence of peripheral targets on the central projections of developing sensory neurons

During development, the projections that sensory neurons make within the spinal cord are influenced by the specific targets they contact in the periphery. If sensory ganglia normally supplying principally cutaneous targets are forced to grow into limb muscles, in early stage tadpoles, many sensory neurons within these ganglia innervate limb muscles and subsequently develop spinal projections appropriate for muscle spindle afferents. If the same procedure is performed with adult frogs, however, these novel projections do not form. In this study, we have determined the developmental stages at which this sensitivity to peripheral targets exists. Axons from sensory neurons in thoracic (largely cutaneous) dorsal root ganglia were re-routed into the front leg at various stages through metamorphosis, and the central spinal projections of these re-routed fibers were assessed with HRP labeling. We found that thoracic sensory axons could be made to project to limb muscles throughout development, but that the central projections of these neurons were only appropriate for spindle afferents if the fibers were re-routed before stage XVIII, shortly before metamorphic climax. Because sensory neurons can regenerate specifically into the appropriate spinal laminae even in adult frogs, these results suggest that changes in either the DRG or the arm musculature occur by stage XVII so that DRG neurons cannot respond to novel peripheral targets.