Unusual dopamine-mediated regulation of the phototransduction in lamprey compared to jawed vertebrates

Abstract

The vertebrate retina uses neurotransmitters to regulate its various functions and adjust vision according to the day/night cycle. Dopamine is probably one of the most important of these neurotransmitters. It is released by dopaminergic amacrine cells in the retina and exerts its regulatory effects, in part, through the cAMP pathway. It has been demonstrated that dopamine affects the phototransduction cascade in isolated amphibian rods. Furthermore, elevated intracellular levels of cAMP increase the light sensitivity of vertebrate rods and modulate the response of vertebrate cones. These effects can be triggered by dopamine receptors and adjust vision to daily light variations. Therefore, the evolution of dopamine loops in the retina is of interest, and the lamprey, being the most primitive vertebrate, could be valuable in this regard. In the present study, we examined whether the photoresponse properties of long (cone-like) and short (rod-like) photoreceptors in the river lamprey could be regulated by dopamine or cAMP level modulation. Using suction pipette recording, we demonstrated that dopamine slightly increased short photoreceptors sensitivity and it slowed the rising and falling phases of photoresponses in long photoreceptors and increased the integration time, with no effect on the sensitivity to brief flashes. The second part of our study -- an immunohistochemical analysis of the lamprey retina -- revealed that both D1 and D2 dopamine receptors are expressed in both types of lamprey photoreceptors. Our results suggest that the regulation of photoreceptor functions by the neurotransmitter dopamine originated in the early stages of vertebrate evolution, specifically during the Cambrian period. SummaryThe lamprey, a primitive vertebrate, is a valuable object for studying the evolution of dopamine loops in the vertebrate retina. This study shows that photoresponse properties of lamprey photoreceptors are regulated by dopamine in a different way compared to gnathostomes.