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Responses to prolonged odour stimulation in frog olfactory receptor cells

Johannes Reisert and Hugh R. Matthews

1. The suction pipette technique was used to record receptor current and spiking responses from isolated frog olfactory receptor cells during prolonged odour stimuli.
2. The majority (70 %) of cells displayed 'oscillatory' responses, consisting of repeated bursts of spikes accompanied by regular increases in receptor current. The period of this oscillation varied from 3.5 to 12 s in different cells. The remaining cells responded either with a 'transient' burst of spikes at the onset of stimulation (10 %), or by 'sustained' firing throughout the odour stimulus (20 %).
3. In cells with oscillatory responses, the Ca²⁺-activated Cl^- channel blocker niflumic acid prolonged the period of oscillation only slightly, despite a 3.8-fold decrease in the receptor current. A 3-fold reduction in the external Cl^- concentration nearly doubled the receptor current, but had little effect on the oscillation period. These results imply that the majority of the receptor current underlying these oscillatory responses is carried by the Ca²⁺-activated Cl^- conductance, suggesting that the intracellular Ca²⁺ concentration oscillates also.
4. In cells with oscillatory responses, the period of oscillation was prolonged 1.5-fold when stimulated in a low-Na⁺ solution designed to incapacitate Na⁺-Ca²⁺ exchange, irrespective of whether Na⁺ was replaced by permeant Li⁺ or impermeant choline. The dependence of the oscillation period upon external Na⁺ suggests that it may be governed by the dynamics of Ca²⁺ extrusion via Na⁺-Ca²⁺ exchange.
5. Exposure to the membrane-permeable cyclic nucleotide analogue CPT-cAMP evoked a sustained rather than an oscillatory response even in cells with oscillatory responses to odour. The inability of CPT-cAMP to evoke an oscillatory response suggests that the cAMP concentration is likely to oscillate also.
6. Perforated-patch recordings revealed that oscillatory responses could only be evoked when the membrane potential was free to change, but not when it was clamped near the resting potential. Since substantial changes in Ca²⁺-activated Cl^- current, and hence odour-induced depolarisation, had little effect upon the period of oscillation, changes in membrane potential are suggested to play only a permissive role in these oscillatory responses.
7. These results are interpreted in terms of the coupled oscillation of Ca²⁺ and cyclic nucleotide concentrations within the olfactory cilia during prolonged odour stimulation.

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