Inhibition of lobster olfactory receptor cells by an odor-activated potassium conductance

W. C. Michel, T. S. McClintock, B. W. Ache

Research output: Contribution to journalArticlepeer-review

86 Scopus citations

Abstract

Whole cell current-clamp recordings show that odors not only depolarize but may also hyperpolarize lobster olfactory receptor cells. Odor-evoked hyperpolarizations occurred in 36% of 178 receptor cells examined. Cell-attached recordings of action potentials followed by current-clamp recordings in the same cell indicate that depolarizing and hyperpolarizing responses were associated with increases (excitation) and decreases (inhibition) in action potential frequency, respectively. Since odorants that hyperpolarized one receptor cell depolarized other cells and since individual cells may be both excited and inhibited, the inhibitory and excitatory nature of the response must be conferred by the odorant-receptor and transduction processes expressed by the receptor cell. The input resistance dropped from 1.73 GΩ at rest to 1.45 GΩ during odor-evoked hyperpolarization, and the membrane time constant correspondingly decreased from 114 to 61 ms. The increased conductance persisted throughout the stimulation period (5 s). Shifting the K+ reversal to a more negative potential by lowering the [K+](o) from 14 to 2.8 mM increased the magnitude of hyperpolarization. The hyperpolarization could be reversibly blocked by dendritic treatment with 5-10 mM 4-aminopyridine (4-AP) or 10 mM cesium ion, but not by 10 mM tetraethylammonium (TEA). Substituting 80% of the [Cl-](o) with NO-/3 increased the amplitude of the hyperpolarization. Based on a calculated equilibrium potential of -32 mV for chloride, an increase in chloride conductance in a low [Cl-](o) environment should have decreased the magnitude of the response. Presumably the change in [Cl-](o) acts through the dendritic steady-state chloride conductance to shift the membrane potential further from the reversal potential for K+. Submicromolar concentrations of hyperpolarizing odorants added to an excitatory (depolarizing) mixture were sufficient to attenuate not only the magnitude but also the rate of depolarization. Attenuation of excitation was dose dependent. These results confirm that at least one odor-activated K+ conductance is colocalized and coactivated with excitatory odor-activated conductance(s) on lobster olfactory receptor cells. Coactivation of the K+ conductance shunts the (net) excitatory depolarization evoked by other components of complex mixtures, thereby modulating both the magnitude (frequency) and time course (latency) of the output. The implication of these findings is that, in the lobster at least, processing of olfactory information begins in the receptor cell dendrites before the initiation of action potentials.

Original languageEnglish
Pages (from-to)446-453
Number of pages8
JournalJournal of Neurophysiology
Volume65
Issue number3
DOIs
StatePublished - 1991

ASJC Scopus subject areas

  • Neuroscience (all)
  • Physiology

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