ATP consumption by mammalian rod photoreceptors in darkness and in light.
Why do vertebrates use rods and cones that hyperpolarize, when in insect eyes a single depolarizing photoreceptor can function at all light levels? We answer this question at least in part with a comprehensive assessment of ATP consumption for mammalian rods from voltages and currents and recently published physiological and biochemical data. In darkness, rods consume 10(8) ATP s(-1), about the same as Drosophila photoreceptors. Ion fluxes associated with phototransduction and synaptic transmission dominate; as in CNS, the contribution of enzymes of the second-messenger cascade is surprisingly small. Suppression of rod responses in daylight closes light-gated channels and reduces total energy consumption by >75%, but in Drosophila light opens channels and increases consumption 5-fold. Rods therefore provide an energy-efficient mechanism not present in rhabdomeric photoreceptors. Rods are metabolically less "costly" than cones, because cones do not saturate in bright light and use more ATP s(-1) for transducin activation and rhodopsin phosphorylation. This helps to explain why the vertebrate retina is duplex, and why some diurnal animals like primates have a small number of cones, concentrated in a region of high acuity.
Okawa
Haruhisa
H
Neuroscience Graduate Program, Zilkha Neurogenetic Institute, USC Keck School of Medicine, Los Angeles, CA 90089, USA.
Sampath
Alapakkam P
AP
Laughlin
Simon B
SB
Fain
Gordon L
GL
D000255:Adenosine Triphosphate / Q000378:metabolism*; D000818:Animals; D003624:Darkness; D066298:In Vitro Techniques; D017136:Ion Transport; D008027:Light; D008322:Mammals; D051379:Mice; D010101:Oxygen Consumption; D018408:Patch-Clamp Techniques; D012160:Retina / Q000378:metabolism; D017949:Retinal Cone Photoreceptor Cells / Q000378:metabolism; D055211:Retinal Photoreceptor Cell Inner Segment / Q000378:metabolism; D017948:Retinal Rod Photoreceptor Cells / Q000378:metabolism* / Q000528:radiation effects*; D012374:Rod Cell Outer Segment / Q000378:metabolism; D000254:Sodium-Potassium-Exchanging ATPase / Q000378:metabolism
D000255:Adenosine Triphosphate; D000254:Sodium-Potassium-Exchanging ATPase