Passive signal propagation and membrane properties in median photoreceptors of the giant barnacle

Abstract

The light-induced electrical responses of barnacle photoreceptors spread decrementally along the cells'' axons. The decay of the depolarizing and hyperpolarizing components of the visual signal was studied by recording intracellularly from single receptor axons of the median ocellus of the giant barnacle [Balanus nubilus]. The resistance of the photoreceptor neuron decreases markedly when the cell is depolarized with respect to its dark resting potential of -60 mV. This rectification results in differential attenuation of the depolarizing and hyperpolarizing components of the visual signal as they spread down the axon. Consequently, the visual signal entering the synaptic region is conspicuously distorted. Bathing the photoreceptor axons in Na-free or Ca-free saline or in isotonic sucrose does not significantly affect the spread of the visual signal to the terminals. The signal is not amplified by an ionic mechanism along the axon. Membrane characteristics of the photoreceptor for hyperpolarizing voltage changes were estimated from the ratio of the amplitudes of the visual signals recorded simultaneously in the axon and in the soma; the time constant and the input resistance of the cell. All 3 independent measurements are consistent with a length constant 1-2 times the total length of the cell (.lambda. = 10-18 mm) and an unusually high membrane resistivity of about 300 k.OMEGA. cm2. This resistivity enables the receptor potential to spread passively to the terminal region. EM examination of receptor axons reveals an investment of glial lamellae, but demonstrates neither unusual structures which would lead to a high apparent membrane resistivity, nor junctions between cells which would seal off the extracellular space. The observed high resistivity appears to be an intrinsic property of the receptor membrane.