MEMBRANE CONDUCTANCES INVOLVED IN AMPLIFICATION OF SMALL SIGNALS BY SODIUM-CHANNELS IN PHOTORECEPTORS OF DRONE HONEY-BEE

A M VALLET, J A COLES, J C EILBECK, Alwyn C. Scott

Research output: Contribution to journalArticle

Abstract

1. Voltage signals of about 1 mV evoked in photoreceptors of the drone honey bee by shallow modulation of a background illumination of an intensity useful for behaviour are thought to be amplified by voltage-dependent Na+ channels. To elucidate the roles of the various membrane conductances in this amplification we have studied the effects of the Na+ channel blocker tetrodotoxin (TTX) and various putative K+ channel blockers on the membrane potential, V(m).

2. Superfusion of a slice of retina with 0.5-10 mM-4-aminopyridine (4-AP) depolarized the membrane and, in fifty of sixty-three cells induced repetitive action potentials. Ionophoretic injection of tetraethylammonium produced similar effects.

3. In order to measure the depolarization caused by 4-AP, action potentials were prevented by application of TTX: 4-AP was applied when the membrane was depolarized to different levels by light. 4-AP induced an additional depolarization at all membrane potentials tested (-64 to -27 mV). We conclude that there are 4-AP-sensitive K+ channels that are open at constant voltage over this range.

4. 4-AP slowed down the recovery phase of the action potential induced by a light flash by a factor that ranged from 0.51 to 0.16. This reduction could be accounted for by the reduction in a voltage-independent K+ conductance estimated from the steady-state depolarization.

5. After the voltage-gated Na+ channels had been blocked by TTX, exposure to 4-AP further changed the amplitude of the response to a small (almost-equal-to 10%) decremental light stimulus. The change was an increase when the background illumination brought V(m) to potentials more negative than about -40 mV; it was a decrease when V(m) > -40 mV. The data could be fitted by a circuit representation of the membrane with a light-activated conductance and a K+ conductance (E(K) = -66 mV) that was partly blocked by 4-AP. The voltage range studied was from -52 to -27 mV; neither conductance in the model was voltage dependent.

6. The responses to small changes in light intensity in the absence of TTX were mimicked by a model. We conclude that a voltage-dependent Na+ conductance described by the Hodgkin-Huxley equations can amplify small voltage changes in a cell membrane that is also capable of generating action potentials; the magnitude of the K+ conductance is critical for optimization of signals while avoiding membrane instability.

Original languageEnglish
Pages (from-to)303-324
Number of pages22
JournalJournal of Physiology
Volume456
Publication statusPublished - Oct 1992

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