Journal of Neuroscience, Vol 7, 1537-1549, Copyright © 1987 by Society for Neuroscience
Peripheral specification of sensory neurons transplanted to novel locations along the neuraxis
CL Smith and E Frank
Thoracic dorsal root ganglia in bullfrogs contain sensory neurons that
innervate the skin of the trunk and have synaptic connections in the dorsal
horn of the spinal cord. The ganglion that innervates the forelimb
contains, in addition to cutaneous afferents, many muscle afferents that
project more ventrally in the spinal cord and make monosynaptic connections
with motoneurons. In the present study, we have transplanted thoracic
sensory neurons to the brachial level in tadpoles to discover whether they
can innervate forelimb muscles and, if so, whether they form central
connections characteristic of forelimb muscle afferents. The ganglion that
normally supplies the forelimb was removed from tadpoles and replaced with
2 thoracic ganglia. After the tadpoles completed metamorphosis, the
peripheral and central connections of the transplanted thoracic sensory
neurons were examined with anatomical and electrophysiological techniques.
When the ganglia were transplanted at stage XIV or earlier, transplanted
sensory neurons innervated the forelimb and projected into the brachial
spinal cord. Electrical stimulation of forelimb muscle nerves evoked
impulses in the dorsal root, indicating that some centrally projecting
sensory neurons were muscle afferents. Furthermore, muscle afferents were
also activated by stretching muscles which suggest that they terminated on
spindles. HRP labeling of the central projections revealed that
transplanted sensory neurons terminated at sites characteristic of both
cutaneous and muscle afferents. The pattern of synaptic connections was
assessed by recording intracellularly from motoneurons. Stimulation of
muscle afferents produced monosynaptic EPSPs in motoneurons. As in normal
frogs, triceps muscle afferents projected more strongly to triceps
motoneurons than to subscapularis and pectoralis motoneurons, while
subscapularis afferents projected to all 3 types of motoneurons. Thus, the
transplanted sensory neurons formed central connections appropriate to
their novel peripheral targets. These observations suggest that
interactions between sensory neurons and their targets may be important in
determining their central connections.
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