Rat optic nerve: electrophysiological, pharmacological and anatomical studies during development.

Changes in conduction properties and in morphology were studied during rat optic nerve growth from birth (when no myelin is present and the glia have not differentiated) to adulthood (when the optic nerve is essentially 100% myelinated). Myelination begins around the sixth postnatal day and proceeds rapidly so that 85% of the fibers are myelinated at 28 days of age. Mean diameter of optic nerve axons remains about 0.2 micron for the first week and then increases rapidly if the fiber is being myelinated. Those axons not being myelinated remain about 0.2-0.3 micron in diameter. At birth the compound action potential has a single negative peak and a conduction velocity of about 0.2 m/s. The increase in conduction velocity prior to myelination is considerably greater than can be accounted for on the basis of increase in axonal diameter. There is no clear step increase in the velocity of the shortest latency peak correlated with the onset of myelination. During myelination the compound action potential develops multiple short latency components, which evolve into the adult-like 3 component compound action potential by 3-4 weeks of age. Durations of the relative refractory period and supernormal period decrease as age increases, but are not related to myelination in a simple manner. Sodium appears to be the only significant carrier of inward current at all ages. A measureable calcium conductance is not present at any age. Voltage-dependent potassium conductance contributes to the compound action potential at all ages, but the response to 4-aminopyridine in rapidly conducting fibers is apparently smaller than that in slowly conducting fibers. These results show that conduction can occur before myelination or the differentiation of glial cells. Moreover, changes in conduction velocity do not depend entirely on myelination or increases in axonal size. Finally, these results suggest a reorganization of axonal membrane properties during the development of rat optic nerve.

[1]  Stephen G. Waxman,et al.  The conduction properties of axons in central white matter , 1977, Progress in Neurobiology.

[2]  J. Fraher A quantitative study of anterior root fibres during early myelination. , 1972, Journal of anatomy.

[3]  R. Lund,et al.  Prenatal development of central optic pathways in albino rats , 1976, The Journal of comparative neurology.

[4]  L J Dorfman,et al.  Nerve fiber conduction-velocity distributions. I. Estimation based on the single-fiber and compound action potentials. , 1979, Electroencephalography and clinical neurophysiology.

[5]  H. Bostock,et al.  Effects of 4-aminopyridine on normal and demyelinated mammalian nerve fibres , 1980, Nature.

[6]  D. Price,et al.  Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. II. Time of origin , 1976, The Journal of comparative neurology.

[7]  T Brismar,et al.  Potential clamp analysis of membrane currents in rat myelinated nerve fibres. , 1980, The Journal of physiology.

[8]  S. Cullheim,et al.  Relations between cell body size, axon diameter and axon conduction velocity of triceps surae alpha motoneurons during the postnatal development in the cat , 1979, The Journal of comparative neurology.

[9]  T. Bullock Facilitation of conduction rate in nerve fibres , 1951, The Journal of physiology.

[10]  R. Foster,et al.  Development of the axon membrane during differentiation of myelinated fibres in spinal nerve roots , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[11]  D. Duncan A relation between axone diameter and myelination determined by measurement of myelinated spinal root fibers , 1934 .

[12]  S. Waxman,et al.  Ionic channel distribution and heterogeneity of the axon membrane in myelinated fibers , 1980, Brain Research Reviews.

[13]  A. Aguayo,et al.  AXON‐SCHWANN CELL RELATIONSHIPS IN NEUROPATHIES OF MUTANT MICE * , 1979, Annals of the New York Academy of Sciences.

[14]  J. M. Ritchie,et al.  A quantitative description of membrane currents in rabbit myelinated nerve. , 1979, The Journal of physiology.

[15]  R. Skoff,et al.  Pattern of myelination and distribution of neuroglial cells along the developing optic system of the rat and rabbit , 1980, The Journal of comparative neurology.

[16]  J W Moore,et al.  Simulations of conduction in uniform myelinated fibers. Relative sensitivity to changes in nodal and internodal parameters. , 1978, Biophysical journal.

[17]  A. Willard Electrical excitability of outgrowing neurites of embryonic neurones in cultures of dissociated neural plate of Xenopus laevis. , 1980, The Journal of physiology.

[18]  R. Skoff The pattern of myelination along the developing rat optic nerve , 1978, Neuroscience Letters.

[19]  A. Paintal A comparison of the nerve impulses of mammalian non‐medullated nerve fibres with those of the smallest diameter medullated fibres , 1967, The Journal of physiology.

[20]  H. Swadlow Properties of antidromically activated callosal neurons and neurons responsive to callosal input in rabbit binocular cortex. , 1974, Experimental neurology.

[21]  M H Ellisman,et al.  Molecular specializations of the axon membrane at nodes of Ranvier are not dependent upon myelination , 1979, Journal of neurocytology.

[22]  R. Dow,et al.  The inception of conductivity in the corpus callosum and the cortico‐ponto‐cerebellar path‐ way of young rabbits with reference to myelinization , 1944 .

[23]  M. Bennett,et al.  Relative conduction velocities of small myelinated and non-myelinated fibres in the central nervous system. , 1972, Nature: New biology.

[24]  B. Freeman,et al.  The optic nerve of the brush‐tailed possum, Trichosurus vulpecula: Fibre diameter spectrum and conduction latency groups , 1978, The Journal of comparative neurology.

[25]  P. Greengard,et al.  Restoration by barium of action potentials in sodium‐deprived mammalian B and C fibres , 1959, The Journal of physiology.

[26]  P. Huttenlocher,et al.  Myelination and the development of function in immature pyramidal tract. , 1970, Experimental neurology.

[27]  I. Parnas,et al.  Membrane conductance and action potential of a regenerating axonal tip. , 1981, Science.

[28]  H. Swadlow,et al.  Variations in conduction velocity and excitability following single and multiple impulses of visual callosal axons in the rabbit , 1976, Experimental Neurology.

[29]  J. M. Ritchie,et al.  Potassium channels in nodal and internodal axonal membrane of mammalian myelinated fibres , 1980, Nature.

[30]  Y. Palti,et al.  Potassium channels in the nodal membrane of rat myelinated fibres , 1981, Nature.

[31]  R. Skoff,et al.  Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve I. Cell proliferation , 1976, The Journal of comparative neurology.

[32]  N. Spitzer Ion channels in development. , 1979, Annual review of neuroscience.

[33]  JOHN W. Moore,et al.  Tetrodotoxin Blockage of Sodium Conductance Increase in Lobster Giant Axons , 1964, The Journal of general physiology.

[34]  Carpenter Fg,et al.  Excitation and conduction in immature nerve fibers of the developing chick. , 1957 .

[35]  J. Tao-Cheng,et al.  Nodal and paranodal membrane structure in complementary freeze-fracture replicas of amphibian peripheral nerves , 1980, Brain Research.

[36]  S. Waxman,et al.  Absence of potassium conductance in central myelinated axons , 1980, Nature.

[37]  B. Freeman Myelin sheath thickness and conduction latency groups in the cat optic nerve , 1978, The Journal of comparative neurology.

[38]  S. Waxman,et al.  Cytochemical differentiation of the axon membrane in A- and C-fibres. , 1977, Journal of neurology, neurosurgery, and psychiatry.

[39]  A. Peters,et al.  Nerve Fibres in Optic Nerve of Rat , 1967, Nature.

[40]  A J Sefton,et al.  Electrical activity of lateral geniculate nucleus and optic tract of the rat. , 1964, Vision research.