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Volume 16, Number 10, Issue of May 15, 1996 pp. 3178-3188
Copyright ©1996 Society for Neuroscience

Selective, Activity-Dependent Uptake of Histamine into an Arthropod Photoreceptor

Received Oct. 19, 1995; revised Feb. 7, 1996; accepted Feb. 19, 1996.

Ann E. Stuart, Jennifer R. Morgan, Harold E. Mekeel, Elizabeth Kempter, and Joseph C. Callaway

Department of Physiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7545

The synapses made by many arthropod photoreceptors are disinhibitory and use histamine as their transmitter. Because decreases and not increases in the cleft concentration of transmitter constitute the important event at these synapses, a transporter to clear the cleft of histamine would seem particularly crucial to signal transfer. We report here that ³H-histamine is taken up selectively into barnacle photoreceptors by a Na⁺-dependent mechanism, presumably a transporter. Using light microscopic autoradiography, we observe heavy label over axons and presynaptic terminals of these neurons when they are stimulated during uptake. The radioactivity taken up was identified as ³H-histamine by thin layer chromatography; no metabolites were detected, even after 5 hr. Radiolabeled 5-hydroxytryptamine and GABA are not taken up by the photoreceptor. ³H-histamine uptake into photoreceptors is decreased markedly by an excess of unlabeled histamine and by chlorpromazine and phenoxybenzamine. Unexpectedly for uptake dependent on the Na⁺ gradient, photoreceptor terminals label more intensely in the light (when depolarized) than in the dark (when hyperpolarized). Glia label more strongly than photoreceptors in dark-incubated preparations. The presence of presynaptic uptake strengthens the evidence that histamine is the neurotransmitter of arthropod photoreceptors and provides a mechanism by which this synapse could recycle transmitter, control its steady-state cleft concentration, and clear it from the cleft in response to decreases in its release from the photoreceptors.

Key words: histamine; photoreceptor; arthropod; transporter; barnacle; autoradiography; neurotransmitter; synapse; disinhibition

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