Changes in the electrical properties of olfactory epithelial cells in the tiger salamander after olfactory nerve transection

Transection of olfactory nerves causes degeneration of receptor neurons in the olfactory epithelium, followed by generation of new receptor neurons. We have carried out intracellular recordings to document changes in epithelial cell populations during receptor neuron degeneration and regrowth at 1, 2, and 4 weeks following olfactory nerve transection in the salamander. Receptor neurons were greatly reduced in numbers at 1 week, and gradually returned to the normal percentage of intracellular penetrations by 4 weeks. They had a resting membrane potential between -30 and -50 mV and high input resistance, 100 to 600 megohms, characteristically seen in normal epithelium. However, at 1 week, the receptor neurons were able to generate only a single spike in response to injected current, and did not re-acquire their ability to respond repetitively until 4 weeks. Cells with the properties of immature receptor neurons (resting membrane potential between -30 and -50 mV and high input resistance, 100 to 600 megohms, but unable to generate spikes) increased significantly in number in the post-transection period. This correlates with the burst of mitotic activity giving rise to new receptor neurons after nerve transection. Supporting cells changed their properties in the aftermath of transection. One type (A) showed a decrease in resting membrane potential and a small increase in input resistance. A second type (B) showed a very large increase in input resistance. These results imply that the degenerating receptor neurons transmit a signal that leads to changes in the functional properties of the glial-like supporting cells. These may involve changes in the membrane properties or in electrical coupling between cells.

[1]  G. Shepherd,et al.  Electrophysiological properties of identified cells in the in vitro olfactory epithelium of the tiger salamander , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  B W Connors,et al.  Carbon dioxide sensitivity of dye coupling among glia and neurons of the neocortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  M. Cohen,et al.  Regeneration of an identified central neuron in the cricket. I. Control of sprouting from soma, dendrites, and axon , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  J. Russell,et al.  Action potentials in macrophages derived from human monocytes. , 1983, Science.

[5]  M. Selzer,et al.  Effects of axotomy on lamprey spinal neurons , 1981, Experimental Neurology.

[6]  T. Getchell,et al.  Physiological activity of newly differentiated olfactory receptor neurons correlated with morphological recovery from olfactory nerve section in the salamander. , 1981, Journal of neurophysiology.

[7]  T. Getchell,et al.  Neurogenesis in olfactory epithelium: loss and recovery of transepithelial voltage transients following olfactory nerve section. , 1981, Journal of neurophysiology.

[8]  M. Cohen,et al.  Synaptic regeneration in identified neurons of the lamprey spinal cords. , 1979, Science.

[9]  B. Gustafsson Changes in motoneurone electrical properties following axotomy. , 1979, The Journal of physiology.

[10]  P. Graziadei,et al.  Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons , 1979, Journal of neurocytology.

[11]  M. Selzer Mechanisms of functional recovery and regeneration after spinal cord transection in larval sea lamprey. , 1978, The Journal of physiology.

[12]  J. Gallin,et al.  Interaction of chemotactic factors with human macrophages: induction of transmembrane potential changes , 1977, The Journal of cell biology.

[13]  R. Llinás,et al.  Control of rhythmic firing in normal and axotomized cat spinal motoneurons. , 1977, Journal of neurophysiology.

[14]  T. Getchell Analysis of intracellular recordings from salamander olfactory epithelium , 1977, Brain Research.

[15]  W. F. Windle,et al.  Factors in recovery from spinal cord injury Summarized Transactions of a Conference held May 24–25, 1976, in Granville, Ohio, under the Auspices of Denison University and Help Them Walk Again Foundation , 1976, Experimental Neurology.

[16]  D. Kerjaschki,et al.  The development of mouse olfactory vesicles and their cell contacts: a freeze-etching study. , 1976, Journal of ultrastructure research.

[17]  S. Takagi,et al.  Secretion and electrogenesis of the supporting cell in the olfactory epithelium , 1974, The Journal of physiology.

[18]  R Llinás,et al.  Enhancement of synaptic transmission by dendritic potentials in chromatolysed motoneurones of the cat , 1970, The Journal of physiology.

[19]  B LIBET,et al.  The behaviour of chromatolysed motoneurones studied by intracellular recording , 1958, The Journal of physiology.

[20]  P. Graziadei,et al.  Continuous Nerve Cell Renewal in the Olfactory System , 1978 .

[21]  G. Somjen Electrophysiology of neuroglia. , 1975, Annual review of physiology.

[22]  P. Graziadei,et al.  Cell dynamics in the olfactory mucosa. , 1973, Tissue & cell.