Early postnatal muscle contractile activity regulates the carbonic anhydrase phenotype of proprioceptive neurons in young and mature mice: Evidence for a critical period in development

• Published in: Neuroscience 1996-04, Vol.71 (3), p.787-795
• Main Authors: Mayeux, V., Pons, F., Baldy-Moulinier, M., Valmier, J.
• Format: Article
• Language: English
• Subjects: Age Factors; Animals; Animals, Newborn - physiology; Biological and medical sciences; Carbonic Anhydrases - physiology; Cell Count; Development. Senescence. Regeneration. Transplantation; dorsal root ganglion; dystrophin; Female; Fundamental and applied biological sciences. Psychology; Ganglia, Spinal - growth & development; mdx mice; Mice; Mice, Inbred Strains; Muscle Contraction - physiology; Neurons - physiology; Phenotype; Sciatic Nerve - ultrastructure; sciatic nerve transection; sensory neuron; tenotomy; Time Factors; Vertebrates: nervous system and sense organs
• ISSN: 0306-4522; 1873-7544
• DOI: 10.1016/0306-4522(95)00504-8

Carbonic anhydrase activity, a marker of mouse proprioceptive neurons in adult dorsal root ganglia, is first detectable in the perinatal period, increases until postnatal day 60 and remains stable in adulthood. The onset of carbonic anhydrase staining begins after the neurons have made connections with their targets suggesting that neuron-target interactions regulate carbonic anhydrase phenotype development. To examine this possibility, we first analysed carbonic anhydrase expression in mdx mice which are characterized by a massive but reversible degeneration of skeletal muscle concomitant with the carbonic anhydrase ontogenesis. Neuronal carbonic anhydrase expression in mdx mice stopped developing when the period of muscular degeneration-regeneration began. Furthermore this alteration persisted during adulthood. We then analysed carbonic anhydrase expression in fifth lumbar dorsal root ganglion of developing control mice before and after surgical procedures that might interfere with central and peripheral target influences on dorsal root ganglion neurons. Central disconnection (dorsal rhizotomy) did not affect the development of carbonic anhydrase activity. Disrupting neuron-peripheral target interactions by sciatic nerve transection or blocking muscle contraction by tenotomy stopped the development of neuronal carbonic anhydrase content. Finally, recovery was monitored following sciatic nerve crush. In adults, recovery of carbonic anhydrase activity was obtained after functional recuperation; similar manipulations during the first month of life induced irreversible alteration of the carbonic anhydrase phenotype. These results show that the development of carbonic anhydrase activity in proprioceptive neurons is regulated by neuron-muscle interactions (i.e. muscle contraction). They also provide evidence for a critical period in the development of the carbonic anhydrase phenotype. We suggest that these two mechanisms are responsible for the altered carbonic anhydrase phenotype of the dorsal root ganglion neurons in mdx mice, a model of human muscular dystrophy.