Single-Photon Sensitivity of Lamprey Rods with Cone-like Outer Segments

Most vertebrates have a duplex retina containing rods for dim light vision and cones for bright lights and color detection. Photoreceptors like cones are present in many invertebrate phyla as well as in chordata, and rods evolved from cones [1, 2], but the sequence of events is not well understood. Since duplex retinas are present in both agnatha and gnathostomata, which diverged more than 400 million years ago, some properties of ancestral rods may be inferred from a comparison of cells in these two groups. Lamprey have two kinds of photoreceptors, called short'' and long'' [39], which seem to be rods and cones; however, the outer segments of both have an identical cone-like morphology of stacks of lamellae without a continuous surrounding plasma membrane [3, 4, 6, 7]. This observation and other aspects of the cellular and molecular biology of the photoreceptors have convinced several investigators [2, 10-12] that the features of 'true' rod transduction in jawed vertebrates, which permit the reliable detection of single photons of light, evolved after the separation of gnathostomes from lampreys'' [12]. To test this hypothesis, we recorded from photoreceptors of the sea lamprey Petromyzon marinus and show that their rods have a single-photon sensitivity similar to that of rods in other vertebrates. Thus, photoreceptors with many of the features of rodsemerged before the split between-agnatha and gnathostomata, and a rod-like outer segment with cytosolic disks surrounded by a plasma membrane is not necessary for high-sensitivity visual detection.