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Ala Morshedian, Gordon L Fain; Single-Photon Sensitivity of Lamprey Rods with Cone-like Outer Segments. Invest. Ophthalmol. Vis. Sci. 2015;56(7 ):5731.
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© ARVO (1962-2015); The Authors (2016-present)
Lamprey have two kinds of photoreceptors, called “short” and “long” and the outer segments of both have an identical cone-like morphology of stacks of lamellae without a continuous surrounding plasma membrane. As a result some workers have argued that the features of ‘true’ rod transduction in jawed vertebrates evolved after the separation of gnathostomes from lampreys. To test this hypothesis we characterized some of the electrophysiological properties of the two cell types in Petromyzon marinus.
The Lamprey were generously provided by the Great Lake Fishery Commission, and suction electrode recordings were made from single cells.
Short photoreceptors had responses resembling amphibian rods and a spectral sensitivity peaking at about 520 nm. We therefore identify these cells as lamprey rods. The long photoreceptors had responses rising and decaying much more rapidly with a spectral sensitivity peaking at about 570 nm. We identify these cells as lamprey cones. The ratio of the values of sensitivity at the maximum wavelegth of the pigments, calculated by plotting the mean response amplitude and fitting them to the equations of the form r = rmax [1 - exp(-kI)] was approximately 70. When small amplitude responses were fitted to a single exponential decay function, the time constant of decay τREC gave a value of 54 ± 4 ms (SEM, n=8) for cones and 841 ± 59 ms (n=12), for rods. To see if lamprey rods respond to single photons of light, we gave a series of dim flashes and calculated the mean single-photon response from the squared mean and variance. Our results demonstrate that 4-5% of the channels of the outer segment are closed by a single photon in lamprey rods. The peak response in lamprey is well within the range of single-photon response amplitudes of other vertebrate rods.
Our results show that the lamprey retina has two physiological classes of photoreceptors closely resembling the rods and cones of other vertebrates. Photoreceptors with many of the features of rods emerged before the split between agnatha and gnathostomata, and a rod-like outer segment with cytosolic disks surrounded by a continuous plasma membrane is not necessary for high sensitivity visual detection. We hypothesize that disks evolved in jawed vertebrates after the split from jawless vertebrates, not to improve sensitivity, but in order to provide a more systematic renewal of rod outer segment protein.
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