Ultrastructural changes in olfactory receptor neurons following olfactory nerve section

1981 ◽  
Vol 197 (2) ◽  
pp. 237-257 ◽  
Author(s):  
Peter A. Simmons ◽  
Jose A. Rafols ◽  
Thomas V. Getchell
1981 ◽  
Vol 45 (3) ◽  
pp. 529-549 ◽  
Author(s):  
P. A. Simmons ◽  
T. V. Getchell

1. Extracellular unitary recordings were made from the olfactory epithelium of the salamander, Ambystoma tigrinum, at numerous time points following olfactory nerve section. Unitary response properties were correlated with histological examination of the same tissues. 2. At 10 days following nerve section, unitary activity was rarely recorded in all regions of the epithelium. Histological examination indicated that virtually the entire mature olfactory receptor cell population had undergone retrograde degeneration. Transneuronal degeneration was not observed in the olfactory bulb, although the olfactory nerve and glomerular layers were substantially reduced in size. 3. At subsequent times, unitary impulse activity gradually returned, consisting of both spontaneous activity and odor-evoked discharges. Anatomical recovery of the olfactory epithelium preceded that of the olfactory bulb. A positive correlation was found between neuronal differentiation in the olfactory epithelium and the recovery of receptor cell function. 4. Patterns of spontaneous activity, odor specificities, intensity-response functions, and adaptive properties studied in newly differentiated olfactory receptor neurons were indistinguishable from those observed in control units. This indicated that these properties were intrinsic to the receptor neurons. 5. Spontaneously active and responsive units were encountered prior to olfactory nerve connection with the bulb. It is concluded that receptor neurons pass through two phases of functional maturity: the first independent of bulbar contact and the second dependent on presumed synaptic contact with bulbar neurons.


1986 ◽  
Vol 66 (3) ◽  
pp. 772-818 ◽  
Author(s):  
T. V. Getchell

The interaction of an odorant with the chemosensitive membrane of olfactory receptor neurons initiates a sequence of molecular and membrane events leading to sensory transduction, impulse initiation, and the transmission of sensory information to the brain. The main steps in this sequence are summarized in Figure 6. Several lines of evidence support the hypothesis that the initial molecular events and subsequent stages of transduction are mediated by odorant receptor sites and associated ion channels located in the membrane of the cilia and apical dendritic knob of the olfactory receptor neuron. Similarly, the membrane events associated with impulse initiation and propagation are mediated by voltage-gated channels located in the initial axonal segment and the axolemma. The ionic and electrical events associated with the proposed sequence have been characterized in general using a variety of experimental techniques. The identification, localization, and sequence of membrane events are consistent with the neurophysiological properties observed in specific regions of the bipolar receptor neuron. The influence of other cells in the primary olfactory pathway such as the sustentacular cells in the olfactory epithelium, the Schwann cells in the olfactory nerve, and the astrocytes in the olfactory nerve layer in the olfactory bulb on the physiological activity of the olfactory receptor neuron is an emerging area of research interests. The general principles derived from the experimental results described in this review provide only a framework that is both incomplete and of necessity somewhat speculative. As noted in the Introduction, the multidisciplinary study of the primary olfactory pathway is undergoing a renaissance of research interest. The application of modern biophysical, cell, and molecular biological techniques to the basic issues of odorant recognition and membrane excitability will clarify the speculations and lead to the establishment of new hypotheses. Three broad areas of research will benefit from such studies. First, the application of biophysical techniques will lead to a detailed characterization of the membrane properties and associated ion conductance mechanisms. Second, the isolation and biochemical characterization of intrinsic membrane and cytosolic proteins associated with odorant recognition, sensory transduction, and the subsequent electrical events will result from the utilization of cell and molecular biological techniques.(ABSTRACT TRUNCATED AT 400 WORDS)


1981 ◽  
Vol 45 (3) ◽  
pp. 516-528 ◽  
Author(s):  
P. A. Simmons ◽  
T. V. Getchell

1. Unilateral olfactory nerve section was performed on the salamander, Ambystoma tigrinum. Physiological recordings and macroscopic observations were made to investigate the physiological correlates of functional recovery in the olfactory epithelium. 2. Slow transepithelial voltage transients, Veog, evoked by several odorous stimuli systematically decreased in amplitude during the initial 7 days and were not recorded at 10 days following nerve section, suggesting retrograde degeneration of receptor neurons. This was true for negative Veog(-), and positive, Veog(+), response components. Responses obtained from the untreated contralateral side of each animal remained similar to nonaxotomized controls. 3. Progressive recovery of the voltage transients was studied at 24, 45, 80, and 100 days following nerve section. At all stages of recovery, the wave form and time course of the responses were characteristic for each stimulus. This suggested that the response properties of the newly differentiated neuronal population were similar to those of the mature population. 4. At 100 days, response amplitudes evoked by all stimuli were similar to control values at all recording sites on the epithelial surface. The simultaneous loss and recovery of positive and negative components of the Veog indicated that the sources of both are dependent on the presence of functionally mature olfactory receptor neurons. 5. Visual inspection indicated that the olfactory nerve was reconstituted and reconnected to the olfactory bulb between 30-60 days following transection. The fact that physiological activity was recorded in the epithelium prior to this event suggests that molecular recognition and sensory transduction are not dependent on connectivity with the olfactory bulb. 6. It is concluded that physiological recovery of the olfactory receptor cell population occurs following axotomy. The time course of recovery was consistent with morphological evidence (see Ref. 57), indicating that newly differentiated receptor neurons are derived from cells in the basal region of the epithelium and replace the population lost through retrograde degeneration.


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