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The brain circuits that allow us to see in 3D already existed in our fish ancestors

The eyes are connected to the brain by the two optic nerves. What we see is captured by the retina that lines the back of our eyes and then sent along the nerves to regions of the brain that analyse and interpret the perceived images. In the retina, the neurons whose extensions (or axons) form the optic nerve are the ganglion cells. In many animal species, such as mammals (and therefore humans), the two optic nerves intersect at a structure called the optic chiasm.

This anatomical peculiarity had already struck early anatomists, including Leonardo da Vinci (In the picture: Drawing by Leonardo da Vinci (1508) showing the eyes (1), the two optic nerves (2) and the chiasma (3))

In humans, as well as in most animals with two eyes, vision is stereoscopic, i.e. we perceive relief and depth. Although our two eyes see largely the same region of the visual field, the distance between the eyes and their inclination means that the image perceived by the two eyes is slightly different.

Drawing by Leonardo da Vinci (1508) showing the eyes (1), the two optic nerves (2) and the chiasma (3)
The central part of the visual field is seen by both eyes (binocular). In each eye, the retina on the lateral side (green for the left eye) is connected to visual centres of the brain on the same side, while the medial retina (purple) projects to the opposite side

This difference allows the brain to generate a three-dimensional (3D) image of our environment. How is this visual comparison achieved? Almost a century ago it was discovered that the axons of the ganglion cells located in the lateral or medial half of each retina separate at the optic chiasm. Those originating in the medial region continue to the brain in the opposite optic nerve, while those originating in the lateral region of the retina remain in the optic nerve on the same side and remain there until the brain. As a result, the visual centres on each side of the brain are binocular: they receive information from both eyes. It is the comparison of the two images that allows the brain to see in 3D. In certain pathologies, such as albinism, the proportion of retinal axons projecting to the opposite side is abnormally high, which disturbs the vision of relief (In the picture: The central part of the visual field is seen by both eyes (binocular). In each eye, the retina on the lateral side (green for the left eye) is connected to visual centres of the brain on the same side, while the medial retina (purple) projects to the opposite side).

Comparative study of the visual system of many mammalian species has revealed that the ratio of retinal neurons connected to the opposite side of the brain is highly variable: it is about 50% in primates, 85% in a ferret, and 97% in a mouse, so that the binocular vision of primates is more developed than that of rodents, and more generally it is more developed in species that are predators, which would correlate with a better ability to catch prey.

Further comparative anatomy work has shown that this bilateral organisation of visual projections is also found in birds, reptiles and amphibians, which together with mammals make up the tetrapods (vertebrates with four limbs).30 years ago, studies suggested that this was not the case in fish, and that their eyes projected only into the half of the brain on the opposite side. Therefore, it was thought that the development of bilateral visual projections was one of the major evolutionary events that, together with the appearance of limbs and lungs, allowed the emergence of fish from the water (320 million years ago).

Work carried out at the Institut de la Vision by the teams of Filippo Del Bene and Alain Chédotal, and published in the American journal Science (DOI: 10.1126/science.abe7790), has completely challenged this model.

Light-sheet microscopy image of a lepisote brain. The visual projections from the left eye are shown in green and those from the right eye in magenta. They project from both sides of the brain

The researchers used modern 3D imaging techniques, including light-sheet laser microscopy, to study the organisation of visual projections in many fish species (In the picture: Light-sheet microscopy image of a lepisote brain. The visual projections from the left eye are shown in green and those from the right eye in magenta. They project from both sides of the brain).

There are currently about 30,000 species of fish, almost half of all vertebrate species. Fish have colonised all oceans and continents, and live in both fresh and salt water.

Fish are our distant cousins and have evolved over hundreds of millions of years. Of all fish, tetrapods are closest to coelacanths and lungfish, such as the Australian lungfish, having diverged from their common ancestor only about 450 million years ago. evolutionThese ancient fish, sometimes referred to as living fossils (which is inaccurate because they have continued to evolve since their appearance in the Silurian), are much rarer than the so-called teleost fish, which together account for more than 95% of present-day fish. Other 'relict' fish species, the lepisostes, separated from the other fish 300-340 million years ago, before the appearance of teleosts. There are now only seven species of lepisostes left in the world, found mainly in American lakes.

The teams of Dr Del Bene and Dr Chédotal collaborated with Australian, American and Spanish researchers to map the visual pathways of ancient fish and teleost fish. To their surprise, they found that ancient fish (including sturgeons) all have bilateral visual projections like tetrapods and that only teleosts have visual projections that only innervate the opposite side of the brain. This shows that a bilateral/binocular organisation of the visual pathways already existed in fish, long before they emerged from the water, and that it disappeared in teleosts. The researchers also showed that the molecular mechanisms that control the establishment of bilateral visual projections differ between tetrapods and ancient fish. Further work is underway to better understand the origin and function of laterality of visual projections and to discover the underlying molecular mechanisms. This work is leading to a better understanding of how the eyes connect to the brain, which could ultimately lead to the discovery of new therapeutic avenues for reconnecting the eye to the brain in patients with optic nerve damage (as is the case in glaucoma).


Original Publication

Bilateral visual projections predate the emergence of tetrapods
Full Title: Bilateral visual projections exist in non-teleost bony fish and predate the emergence of tetrapods
Robin J. Vigouroux, Karine Duroure, Juliette Vougny, Shahad Albadri, Peter Kozulin, Eloisa Herrera, Kim Nguyen-Ba-Charvet, Ingo Braasch, Rodrigo Suárez, Filippo Del Bene* and Alain Chédotal*
Science 09 Apr 2021 | Vol. 372, Issue 6538, pp. 150-156
DOI: 10.1126/science.abe7790

Contacts:
filippo.del-bene[at]inserm.fr
alain.chedotal[at]inserm.fr

Watch the excellent and very didactic video by Science which summarises the main findings of this paper => https://youtu.be/p4K0CRAPXGI