VR study with zebrafish shows surroundings influence developing biology of the eye

The environment experienced by young zebrafish influences both the shape and electrical activity of the neurons in the eye, which affects subsequent behavior.

Neuroscientists at King’s College London studied the fish in the first five days of their lives to investigate whether visual features of the environment they grow up in affect how the cells in the eye develop. The study, published in Neuron, found that fish growing up surrounded by horizontal stripes develop neurons with different shapes and responses compared with fish growing up surrounded by vertical stripes.

Using a virtual reality behavioral test, developed in collaboration with the University of Konstanz, researchers showed these structural and functional differences in the neurons influence how the fish behave. Zebrafish have an innate preference to swim toward stripes that are parallel to the orientation of their body. The study used virtual reality to test the strength of that preference and found that this instinct is greatly reduced in fish that grow up in a horizontally striped environment, whereas it is retained by those that grow up surrounded by vertical lines.

Plasticity reaches the retina

This is the first time research has shown different environments influence the overall shape of neurons in the eye and that this maps onto subsequent behavior. These changes were shown in the retina, a structure at the back of the eye that is responsible for detecting light and basic visual processing.

“We were extremely surprised and excited to find experience-based plasticity at this level in a primary sensory organ—the retina,” comments Robert Hindges, senior author of the study and professor of developmental neurobiology at the Institute of Psychiatry, Psychology & Neuroscience (IoPPN), King’s College London.

“Neither humans nor fish are born with a fully developed eye and brain. Many neurons are physically present but will be refined further—through a process known as plasticity—before adulthood. Classically, the retina has been portrayed as ‘hardware,’ and refinement was previously thought to occur mostly inside highly adaptable parts of the brain such as the cerebral cortex.”

This research adds to a growing body of evidence showing the retina pre-processes the visual scene before passing it on to the rest of the brain for further processing. It is the first study to show this pre-processing is dependent on the visual environment in which the retina and the fish are developing.

Growing up among stripes

To understand whether the environment could influence how the eye develops, researchers placed fish in striped environments that were either horizontal or vertical in the first five days of their lives. Stripes are highly salient visual features that all animals use to help understand what they are looking at.

“People actually use horizontal and vertical features to make sense of more complex images like faces, where the nose is a strong vertical line and the brow is a clear horizontal line,” explains Hindges.

Half the fish grew up in a world full of horizontal stripes. The other half experienced a world with only vertical lines. Using a microscope to image neurons in the retina, the researchers discovered the two groups of fish had differently shaped neurons in their retinas. The neural activity sent from the eye to the rest of the brain in the retina was also biased toward the stripes the fish had seen in these first few days since birth.

“This has a striking potential to suggest that the places we grow up influence how we see the world,” comments Hindges. “This is in keeping with studies in humans that have shown that people who grow up in different visual environments perceive optical illusions differently. What wasn’t known was that these changes are being at least partially driven by changes in the earliest stage of visual processing: in the retina.”

Behavior shifts in virtual reality

The scientists tested whether these changes in the retina affected how the fish behaved after five days. This behavioral test leveraged the zebrafish’s innate preference to turn toward stripes parallel to their body, which relies on the ability to discern between different orientations of stripes.

Using a virtual reality system that tracks movements as they occur, the fish were given a choice between turning toward stripes parallel or perpendicular to them. The zebrafish that grew up in the horizontal world failed to display this innate preference for parallel stripes, behaving as if they had more difficulty differentiating between horizontal and vertical stripes, whereas the fish that grew up in the vertically striped world retained this preference.

“We wanted to explore how these changes that are happening in the eye can impact the actual behavior of the fish,” explains Dr. Phoebe Reynolds, first author of the study, who carried out the research as part of her Ph.D. at King’s. “To do this, we developed a novel behavioral test in virtual reality where the fish can display a preference for lines of certain orientations. This let us test whether their innate preferences were affected by the environment they were raised in.”

“The design of the tracking setup and the behavioral paradigms were inspired by our observations of the structural and functional changes in the retina. Whether these features would also impact the ability to distinguish stripe patterns during behavior was completely unclear. We were therefore very surprised that the conditions in which the animals were raised indeed had a major impact on performance,” says Armin Bahl of the Centre for the Advanced Study of Collective Behavior at the University of Konstanz, who led the behavioral experiments in this study.

Isolating the eye’s role

Using a genetic manipulation, researchers were able to isolate the contribution of retinal plasticity to this behavior. Without the influence of plasticity in the retina, the fish from both environments behaved the same, demonstrating that the changes in the biology of the eye are driving how they behave.

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Gaby Clark

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Robert Egan

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