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

Abstract

1. The ability of foreign sensory neurones 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.2. 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 neurones located in an adjacent ganglion (d.r.g. 3); these neurones normally never grow into the arm.3. These neurones were shown, by labelling with horseradish peroxidase, to project into the arm and into the region of the brachial spinal cord occupied by motoneurones innervating muscles in the arm. These projections do not occur at any time during normal development.4. Intracellular recordings from identified motoneurones 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 motoneurones were normal, although the latencies of the synaptic potentials were somewhat longer.5. 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 connexions onto motoneurones.6. 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 neurones.7. Many d.r.g. 3 neurones still innervated their normal sensory targets in the thorax. These neurones never formed monosynaptic connexions onto brachial motoneurones in either normal or experimental animals. In experimental animals, the polysynaptic projections of these third nerve sensory neurones to brachial motoneurones were stronger than in normal animals independent of when d.r.g. 2 was removed during development.8. Thus foreign sensory cells can form specific, functionally appropriate connexions between peripheral targets and motoneurones if the sensory cells that normally mediate this reflex pathway are removed sufficiently early during development.