Correction: From water to land: Evolution of photoreceptor circuits for vision in air.

[This corrects the article DOI: 10.1371/journal.pbio.3002422.].

From water to land: Evolution of photoreceptor circuits for vision in air.

When vertebrates first conquered the land, they encountered a visual world that was radically distinct from that of their aquatic ancestors. Fish exploit the strong wavelength-dependent interactions of light with water by differentially feeding the signals from up to 5 spectral photoreceptor types into distinct behavioural programmes. However, above the water the same spectral rules do not apply, and this called for an update to visual circuit strategies. Early tetrapods soon evolved the double cone, a still poorly understood pair of new photoreceptors that brought the "ancestral terrestrial" complement from 5 to 7. Subsequent nonmammalian lineages differentially adapted this highly parallelised retinal input strategy for their diverse visual ecologies. By contrast, mammals shed most ancestral photoreceptors and converged on an input strategy that is exceptionally general. In eutherian mammals including in humans, parallelisation emerges gradually as the visual signal traverses the layers of the retina and into the brain.

New twists in the evolution of retinal direction selectivity.

In mammals, starburst amacrine cells are centrally involved in motion vision and a new study in PLOS Biology, by Yan and colleagues finds that zebrafish have them, too. They coexist with a second pair of starburst-like neurons, but neither appears to be strongly motion selective.

Ancestral photoreceptor diversity as the basis of visual behaviour.

Animal colour vision is based on comparing signals from different photoreceptors. It is generally assumed that processing different spectral types of photoreceptor mainly serves colour vision. Here I propose instead that photoreceptors are parallel feature channels that differentially support visual-motor programmes like motion vision behaviours, prey capture and predator evasion. Colour vision may have emerged as a secondary benefit of these circuits, which originally helped aquatic vertebrates to visually navigate and segment their underwater world. Specifically, I suggest that ancestral vertebrate vision was built around three main systems, including a high-resolution general purpose greyscale system based on ancestral red cones and rods to mediate visual body stabilization and navigation, a high-sensitivity specialized foreground system based on ancestral ultraviolet cones to mediate threat detection and prey capture, and a net-suppressive system based on ancestral green and blue cones for regulating red/rod and ultraviolet circuits. This ancestral strategy probably still underpins vision today, and different vertebrate lineages have since adapted their original photoreceptor circuits to suit their diverse visual ecologies.

The vertebrate retina: a window into the evolution of computation in the brain.

Animal brains are probably the most complex computational machines on our planet, and like everything in biology, they are the product of evolution. Advances in developmental and palaeobiology have been expanding our general understanding of how nervous systems can change at a molecular and structural level. However, how these changes translate into altered function - that is, into 'computation' - remains comparatively sparsely explored. What, concretely, does it mean for neuronal computation when neurons change their morphology and connectivity, when new neurons appear or old ones disappear, or when transmitter systems are slowly modified over many generations? And how does evolution use these many possible knobs and dials to constantly tune computation to give rise to the amazing diversity in animal behaviours we see today? Addressing these major gaps of understanding benefits from choosing a suitable model system. Here, I present the vertebrate retina as one perhaps unusually promising candidate. The retina is ancient and displays highly conserved core organisational principles across the entire vertebrate lineage, alongside a myriad of adjustments across extant species that were shaped by the history of their visual ecology. Moreover, the computational logic of the retina is readily interrogated experimentally, and our existing understanding of retinal circuits in a handful of species can serve as an anchor when exploring the visual circuit adaptations across the entire vertebrate tree of life, from fish deep in the aphotic zone of the oceans to eagles soaring high up in the sky.

A microRNA that controls the emergence of embryonic movement.

Movement is a key feature of animal systems, yet its embryonic origins are not fully understood. Here, we investigate the genetic basis underlying the embryonic onset of movement in Drosophila focusing on the role played by small non-coding RNAs (microRNAs, miRNAs). To this end, we first develop a quantitative behavioural pipeline capable of tracking embryonic movement in large populations of fly embryos, and using this system, discover that the Drosophila miRNA miR-2b-1 plays a role in the emergence of movement. Through the combination of spectral analysis of embryonic motor patterns, cell sorting and RNA in situs, genetic reconstitution tests, and neural optical imaging we define that miR-2b-1 influences the emergence of embryonic movement by exerting actions in the developing nervous system. Furthermore, through the combination of bioinformatics coupled to genetic manipulation of miRNA expression and phenocopy tests we identify a previously uncharacterised (but evolutionarily conserved) chloride channel encoding gene - which we term Movement Modulator (Motor) - as a genetic target that mechanistically links miR-2b-1 to the onset of movement. Cell-specific genetic reconstitution of miR-2b-1 expression in a null miRNA mutant background, followed by behavioural assays and target gene analyses, suggest that miR-2b-1 affects the emergence of movement through effects in sensory elements of the embryonic circuitry, rather than in the motor domain. Our work thus reports the first miRNA system capable of regulating embryonic movement, suggesting that other miRNAs are likely to play a role in this key developmental process in Drosophila as well as in other species.

Restoration of cone-circuit functionality in the regenerating adult zebrafish retina.

Unlike humans, teleosts like zebrafish exhibit robust retinal regeneration after injury from endogenous stem cells. However, it is unclear if regenerating cone photoreceptors regain physiological function and integrate correctly into post-synaptic circuits. We used two-photon calcium imaging of living adult retina to examine photoreceptor responses before and after light-induced lesions. To assess functional recovery of cones and downstream outer retinal circuits, we exploited color opponency; UV cones exhibit intrinsic Off-response to blue light, but On-response to green light, which depends on feedback signals from outer retinal circuits. Accordingly, we assessed the presence and quality of Off- vs. On-responses and found that regenerated UV cones regain both Off-responses to short-wavelength and On-responses to long-wavelength light within 3 months after lesion. Therefore, physiological circuit functionality is restored in regenerated cone photoreceptors, suggesting that inducing endogenous regeneration is a promising strategy for human retinal repair.

Ancient origin of the rod bipolar cell pathway in the vertebrate retina.

Vertebrates rely on rod photoreceptors for vision in low-light conditions. The specialized downstream circuit for rod signalling, called the primary rod pathway, is well characterized in mammals, but circuitry for rod signalling in non-mammals is largely unknown. Here we demonstrate that the mammalian primary rod pathway is conserved in zebrafish, which diverged from extant mammals ~400 million years ago. Using single-cell RNA sequencing, we identified two bipolar cell types in zebrafish that are related to mammalian rod bipolar cell (RBCs), the only bipolar type that directly carries rod signals from the outer to the inner retina in the primary rod pathway. By combining electrophysiology, histology and ultrastructural reconstruction of the zebrafish RBCs, we found that, similar to mammalian RBCs, both zebrafish RBC types connect with all rods in their dendritic territory and provide output largely onto amacrine cells. The wiring pattern of the amacrine cells postsynaptic to one RBC type is strikingly similar to that of mammalian RBCs and their amacrine partners, suggesting that the cell types and circuit design of the primary rod pathway emerged before the divergence of teleost fish and mammals. The second RBC type, which forms separate pathways, was either lost in mammals or emerged in fish.