Postnatal refinement of proprioceptive afferents in the cat cervical spinal cord

Abstract

Proprioceptive afferent (PA) information is integrated with signals from descending pathways, including the corticospinal tract (CST), by spinal interneurons in the dorsal horn and intermediate zone for controlling movements. PA spinal projections, and the reflexes that they evoke, develop prenatally. The CST projects to the spinal cord postnatally, and its connections are subsequently refined. Consequently, the tract becomes effective in transmitting control signals from motor cortex to muscle. This suggests sequential development of PAs and the CST rather than co-development. In this study we determined if there was also late postnatal refinement of PA spinal connections, which would support PA-CST co-development. We examined changes in PA spinal connections at 4 weeks of age, when CST terminations are immature, at 8 weeks, after CST refinement, and at 11 weeks, when CST terminations are mature. We electrically stimulated PA afferents in the deep radial nerve. Evoked PA responses were small and not localized at 4 weeks. By 8 and 11 weeks, responses were substantially larger and maximal in laminae VI and dorsal VII. We used intramuscular injection of cholera toxin β subunit to determine the distribution of PAs from the extensor carpii radialis muscle in the cervical enlargement at the same ages as in the electrophysiological studies. We found a reduction of the distribution of PAs with age that paralleled the physiological changes. This age-related sharpening of PA spinal connections also paralleled CST development, suggesting coordinated PA-CST co-development rather than sequential development. This is likely to be important for the development of adaptive motor control.