The formation of appropriate central and peripheral connexions by foreign sensory neurones of the bullfrog

Abstract

The ability of foreign sensory neuron to form novel reflex pathways was studied in bullfrogs by removing, during early larval stages of development, the dorsal root ganglion (d.r.g. 2) that normally provides the entire sensory innervation of the front limb. After the operation these tadpoles metamorphosed into frogs that responded to sensory stimuli and had nearly normal use of the limb. Sensation in the limb was mediated by sensory neuron located in an adjacent ganglion (d.r.g. 3); these neurons normally never grow into the arm. These neurons were shown, by labeling with horseradish peroxidase, to project into the arm and into the region of the brachial spinal cord occupied by motoneuron innervating muscles in the arm. These projections do not occur at any time during normal development. Intracellular recordings from identified motoneurons demonstrated that when the operations were done before developmental stage 9 appropriate monosynaptic sensory-motor pathways were established. The relative strengths of synergistic and antagonistic sensory projections onto motoneurons were normal, although the latencies of the synaptic potentials were somewhat longer. When the operation was performed after stage 9 but before metamorphosis, d.r.g. 3 sensory afferents grew into the arm and into the brachial spinal cord but did not make monosynaptic connections onto motoneurons. Removal of d.r.g. 2 from adult bullfrogs failed to produce either central or peripheral changes in the projections of d.r.g. 3 sensory neurons. Many d.r.g. 3 neurons still innervated their normal sensory targets in the thorax. These neurons never formed monosynaptic connections onto brachial motoneurons in either normal or experimental animals. In experimental animals, the polysynaptic projections of these 3rd nerve sensory neurons to brachial motoneurons were stronger than in normal animals independent of when d.r.g. 2 was removed during development. Thus, foreign sensory cells can form specific, functionally appropriate connections between peripheral targets and motoneurons if the sensory cells that normally mediate this reflex pathway are removed sufficiently early during development.