Elevated energy requirement of cone photoreceptors

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 117; no. 32; pp. 19599 - 19603
• Main Authors: Ingram, Norianne T., Fain, Gordon L., Sampath, Alapakkam P.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 11.08.2020
• Subjects: Adenosine triphosphate; Adenosine Triphosphate - metabolism; Animals; ATP; Biological Sciences; Calcium - metabolism; Calcium channels; Calcium channels (voltage-gated); Calcium ions; Channels; Cones; Cyclic GMP - metabolism; Cyclic Nucleotide-Gated Cation Channels - metabolism; Darkness; Daylight; Eye; Fovea; Fovea Centralis - cytology; Fovea Centralis - metabolism; Humans; Hyperpolarization; Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels - metabolism; Ion Channel Gating; Ion channels (cyclic nucleotide-gated); Ion transport; Light; Mice; Nucleotides; Photoreceptors; Presynaptic Terminals - metabolism; Primates; Retina; Retina - cytology; Retina - metabolism; Retinal cells; Retinal Cone Photoreceptor Cells - metabolism; Retinal Rod Photoreceptor Cells - metabolism; Rod outer segment membranes; Rods; Sodium - metabolism; Synapses; Utilization; fovea; metabolism; retina; degeneration; photoreceptor
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2001776117

We have used recent measurements of mammalian cone light responses and voltage-gated currents to calculate cone ATP utilization and compare it to that of rods. The largest expenditure of ATP results from ion transport, particularly from removal of Na⁺ entering outer segment light-dependent channels and inner segment hyperpolarization-activated cyclic nucleotide-gated channels, and from ATP-dependent pumping of Ca2+ entering voltage-gated channels at the synaptic terminal. Single cones expend nearly twice as much energy as single rods in darkness, largely because they make more synapses with second-order retinal cells and thus must extrude more Ca2+. In daylight, cone ATP utilization per cell remains high because cones never remain saturated and must continue to export Na⁺ and synaptic Ca2+ even in bright illumination. In mouse and human retina, rods greatly outnumber cones and consume more energy overall even in background light. In primates, however, the high density of cones in the fovea produces a pronounced peak of ATP utilization, which becomes particularly prominent in daylight and may make this part of the retina especially sensitive to changes in energy availability.