ELECTROTONIC STRUCTURE OF OLFACTORY SENSORY NEURONS ANALYZED BY INTRACELLULAR AND WHOLE CELL PATCH TECHNIQUES

Experimental studies employing whole cell patch recordings from freshly isolated olfactory sensory neurons of the salamander (Ambystoma tigrinum) yield much higher estimates of specific membrane resistance (R(m)) than studies using conventional intracellular recordings from in situ neurons. Because R(m) is critical for understanding information transfer in these cells, we have used computational methods to analyze the possible reasons for this difference. Compartmental models were constructed for both the in situ and isolated neurons, using SABER, a general-purpose simulation program. For R(m) in the in situ cell, we used a high value of 100,000 Ω·cm2, as estimated in the whole cell recordings from isolated cells. A shunt across the cell membrane caused by the penetrating microelectrode was simulated by several types of shunt mechanisms, and its effects on lowering the apparent value of resting membrane potential (MP), input resistance (R(N)), and membrane time constant (τ(m)) and increasing the electrotonic length (L) were analyzed. A good approximation of the electrotonic properties recorded intracellularly was obtained in the in situ model with high R(m) combined with an electrode shunt consisting of Na and K conductances. A raised K conductance (1-5 nS) helps to maintain the resting MP while contributing to the increased conductance, which lowers R(N) and shortens the apparent τ(m) toward the experimental values. Combined shunt resistances of 0.1-0.2 GΩ (5-10 nS) gave the best fits with the experimental data. These shunts were two to three orders of magnitude smaller than the values reported from intracellular penetrations in muscle cells and motoneurons. This may be correlated with the smaller electrode tips used in the recordings from these small neurons. We thus confirm the prediction that even small values of electrode shunt have relatively large effects on the recorded electrotonic properties of small neurons, because of their high R(N) (2-5 GΩ). We have further explored the effects on electrotonic structure of a nonuniform R(m) by giving higher R(m) values to the distally located cilia compared with the proximal soma-dendritic region, as indicated by recent experiments. For the same R(N), large increases in ciliary R(m) above 100,000 Ω·cm2 can be balanced by relatively small decreases below that value in soma-dendritic R(m). A high ciliary R(m) appears to be a specialization for transduction of the sensory input, as reported also in photoreceptors and hair cells.