Using field work, state-of-the-art electrical recordings and sub-micron precision anatomy, Carola Yovanovich and Tom Baden will unravel which colour information is available to frogs and how it is processed to reach the limits of colour discrimination performance available to the vertebrate eye
Colour vision at night is out of reach for most vertebrates due to the division of labour between the cone and rod photoreceptor cells that react to light reaching the retina. There are usually several populations of cones that are preferentially sensitive to different parts of the spectrum of visible light. Comparison of the signals produced by different types of these cones allows for colour discrimination, however there is one fundamental limitation: cones usually operate only when light intensity is relatively high. On the contrary, the higher sensitivity of rods allows them to perform well in dim light levels, but all rods tend to have the same spectral sensitivity and therefore they do not by themselves allow for colour discrimination in the dark. Accordingly, vertebrates including humans are generally thought to use cones for colour vision during the daytime and rods for colour-blind ‘black-and-white’ vision at night.
Amphibians are the only known exception to this rule because unlike any fish, reptile, bird or mammal, frogs and some salamanders possess a second type of rod. This raises the potential for colour vision at night, relying purely on spectral comparisons from the two rod types. Indeed, recent behavioural work demonstrated that frogs can tell apart green from blue even in extremely dim light when our own eyes can barely tell there is anything there to see at all! However, beyond this behavioural demonstration, we still know very little about how the retinas and brains of these amphibians actually extract this additional information. Moreover, we also do not really know what use frogs actually draw from their little superpower.
In this project we will therefore establish the purpose, underlying retinal physiology and circuit implementation of this unique ability. We will use a multidisciplinary approach spanning natural scene imaging, simultaneous recordings of electrical activity from 1,000s of retinal neurons and high-resolution anatomy of the rod circuitry, down to the level of nano-scale synaptic connections. We will tackle questions such as: what is there to be seen in the dark with rod-based colour vision? How does the retinal output encode rod–rod spectral comparisons? How is the frogs’ unique second rod type wired into the retinal circuitry?
Besides the colour discrimination abilities that it enables, the amphibians’ second rod is a key puzzle piece in the evolution of vertebrate visual cells: while rods in general are derived from ancestral cones, this specific type has retained cone-like features that are absent in the typical rods, suggesting that it represents an intermediate stage in the divergence of rods from cones. Thus, by using frogs as our experimental model and leveraging on their complex life cycle and intermediate position in the vertebrate tree of life we will be able to dig into two evolutionary axes: one at the organismic level, going from aquatic ancestors to derived terrestrial vertebrates; and the other at the cell lineage level, going from the ancestral cones to the more novel rods. The typically aquatic tadpoles and the more terrestrially drawn adults will give us the insight that we are searching for in terms of phylogenetic and ecological evolutionary transitions and also provide a deeper understanding about the purpose and reach of nocturnal colour vision in these different environments.