Dendritic impulse initiation in an epithelial sensory neuron

Abstract

The effect of transepithelial voltage on the generation of nervous impulses in an epithelial mechanoreceptor cell has been studied in the tibial hair sensilla of the cricketAcheta. Other studies have demonstrated sensilla to be a part of a ‘tight’ epithelium. A natural transepithelial voltage (TEV) of about 20 mV exists across the epithelium studied (outside positive). 1. In the mechanically unstimulated state, both increase and decrease of TEV elicits repetitive nerve impulses. Their time course is diphasic in transepithelial recordings. During positive polarization the temporal order of impulse phases is the same as for mechanically induced impulses, whereas it is inverted during negative polarization. Following application of Tretrodotoxin (TTX) at the apical side, the regularly subsequent (negative) impulse phase is abolished and negative polarization becomes ineffective in generating impulses. 2. Adequate mechanical stimulation decreases increment sensitivity of impulse generation for most transepithelial voltages (impulse frequency incrementΔF/ΔTEV). Following application of TTX, mechanically induced impulse frequency is lowered by decreased or negative TEV; the increment sensitivity-ΔF/-ΔTEV of this influence of TEV is increased by increasing the mechanical stimulus strength. In contrast, little change ofΔF/ΔTEV is caused by TTX in the domain of increased positive TEV with respect to the effect of mechanical stimuli. 3. Mechanical sensitivity of afferent spike frequency in this receptor is increased by an increase of TEV only for small mechanical stimuli; negative TEV diminishes mechanical sensitivity in general. This dependence of sensitivity on TEV cannot be generalized for comparable sensilla. 4. We conclude: A transepithelial current traverses the sensory cell via its apical dendritic membrane (the membrane of the ciliary outer segment mainly) and it leaves the cell at the basal side of the epithelium via the membrane of the basal dendritic region (ciliary inner segment). The current enters the cell via a conductance which is increased by adequate mechanical stimuli and via a conductance which is considerably high in the mechanically unstimulated state. In order to explain the complex effects of combined mechanical and electrical stimulation, we suggest that some apical conductance is controlled by the membrane voltage as a rectifying K+-conductance is. Both apical and basal membrane areas of the dendrite are able to initiate impulses repetitively; the regular site of impulse initiation is in the basal area.