Dopamine Modulates the Kinetics of Ion Channels Gated by Excitatory Amino Acids in Retinal Horizontal Cells

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 87; no. 2; pp. 767 - 771
• Main Authors: Knapp, Andrew G., Schmidt, Karl F., Dowling, John E.
• Format: Journal Article
• Language: English
• Published: Washington, DC National Academy of Sciences of the United States of America 01.01.1990; National Acad Sciences
• Subjects: Agonists; Analysis of Variance; Animals; Biological and medical sciences; Brackish; Cells, Cultured; Dopamine - pharmacology; Electric current; Excitatory amino acids; Eye and associated structures. Visual pathways and centers. Vision; Freshwater; Fundamental and applied biological sciences. Psychology; Glutamate receptors; Glutamates - pharmacology; Glutamic Acid; Haloperidol - pharmacology; Ion channels; Ion Channels - drug effects; Ion Channels - physiology; Kainic Acid - pharmacology; Kinetics; Marine; Morone americana; Neurons; Neurotransmitter Agents - pharmacology; Perches; Photoreceptors; Pipettes; Retina - cytology; Retina - drug effects; Retina - physiology; Statistical variance; Teleostei; Vertebrates: nervous system and sense organs; Eye; Visual system; Cell culture; Vertebrata; Dopamine; Pisces; Excitatory aminoacid; Neurotransmitter; Horizontal neuron; Retina; Ionic channel
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.87.2.767

Upon exposure to dopamine, cultured teleost retinal horizontal cells become more responsive to the putative photoreceptor neurotransmitter L-glutamate and to its analog kainate. We have recorded unitary and whole-cell currents to determine the mechanism by which dopamine enhances ion channels activated by these agents. In single-channel recordings from cell-attached patches with agonist in the patch pipette, the frequency of 5- to 10-pS unitary events, but not their amplitude, increased by as much as 150% after application of dopamine to the rest of the cell. The duration of channel openings also increased somewhat, by 20-30%. In whole-cell experiments, agonists with and without dopamine were applied to voltage-clamped horizontal cells by slow superfusion. Analysis of whole-cell current variance as a function of mean current indicated that dopamine increased the probability of channel opening for a given agonist concentration without changing the amount of current passed by an individual channel. For kainate, noise analysis additionally demonstrated that dopamine did not alter the number of functional channels. Dopamine also increased a slow spectral component of whole-cell currents elicited by kainate or glutamate, suggesting a change in the open-time kinetics of the channels. This effect was more pronounced for currents induced by glutamate than for those induced by kainate. We conclude that dopamine potentiates the activity of horizontal cell glutamate receptors by altering the kinetics of the ion channel to favor the open state.