A positive feedback synapse from retinal horizontal cells to cone photoreceptors

• Published in: PLoS biology Vol. 9; no. 5; p. e1001057
• Main Authors: Jackman, Skyler L, Babai, Norbert, Chambers, James J, Thoreson, Wallace B, Kramer, Richard H
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.05.2011; Public Library of Science (PLoS)
• Subjects: alpha -Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors; alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - pharmacology; Ambystoma; Animals; Biology; Brain; Calcium; Calcium (intracellular); Calcium - metabolism; Calcium Signaling - drug effects; Cameras; Color vision; Cones; Digital cameras; Experiments; Eye lens; Feedback; Feedback, Physiological; Glutamic Acid - metabolism; Horizontal cells; In Vitro Techniques; Light intensity; Lizards; Membrane potential; Membrane Potentials - drug effects; Motor task performance; Neurotransmitter release; Nitric oxide; Perception; Photoreceptors; Quinoxalines - pharmacology; Rabbits; Receptors, AMPA - antagonists & inhibitors; Receptors, AMPA - metabolism; Receptors, Glutamate - metabolism; Retina; Retina - cytology; Retina - drug effects; Retina - physiology; Retinal Cone Photoreceptor Cells - drug effects; Retinal Cone Photoreceptor Cells - metabolism; Retinal Cone Photoreceptor Cells - physiology; Retinal Horizontal Cells - drug effects; Retinal Horizontal Cells - metabolism; Retinal Horizontal Cells - physiology; Rods; Synapses; Synapses - drug effects; Synapses - metabolism; Synapses - physiology; Visual system; Zebrafish; Receptors, Glutamate; alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid; Rabbits; Retinal Cone Photoreceptor Cells; Calcium; Retinal Horizontal Cells; Quinoxalines; Retina; Zebrafish; Glutamic Acid; Feedback, Physiological; Animals; Membrane Potentials; Lizards; Ambystoma; Receptors, AMPA; Calcium Signaling; Synapses
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.1001057

Cone photoreceptors and horizontal cells (HCs) have a reciprocal synapse that underlies lateral inhibition and establishes the antagonistic center-surround organization of the visual system. Cones transmit to HCs through an excitatory synapse and HCs feed back to cones through an inhibitory synapse. Here we report that HCs also transmit to cone terminals a positive feedback signal that elevates intracellular Ca(2+) and accelerates neurotransmitter release. Positive and negative feedback are both initiated by AMPA receptors on HCs, but positive feedback appears to be mediated by a change in HC Ca(2+), whereas negative feedback is mediated by a change in HC membrane potential. Local uncaging of AMPA receptor agonists suggests that positive feedback is spatially constrained to active HC-cone synapses, whereas the negative feedback signal spreads through HCs to affect release from surrounding cones. By locally offsetting the effects of negative feedback, positive feedback may amplify photoreceptor synaptic release without sacrificing HC-mediated contrast enhancement.