Zebrafish study shows how visual surroundings reshape the eye’s retina

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

Neuroscientists at King’s College London studied the fish in the first five days of their life 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 to 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 towards stripes that are parallel to the orientation of their body. The study used virtual reality to test the strength of preference and found that this instinct is greatly reduced in fish who grow up in a horizontally striped environment whereas it is retained by those who grow up surrounded by vertical lines. 

This is the first time that 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. 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.” 

Robert Hindges, senior author on the study and Professor of Developmental Neurobiology, Institute of Psychiatry, Psychology & Neuroscience (IoPPN) King’s College London

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

To understand whether the environment could influence how the eye develops, researchers placed fish in striped environments which were either horizontal or vertical in the first 5 days of their lives. Stripes are highly salient visual features which 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 Professor 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 that the two groups of fish had differently shaped neurons in their retinas. The neural activity that is sent from the eye to the rest of the brain in the retina was also biased towards 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 Professor 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.” 

The scientists tested whether these changes in the retina affected how the fish behaved after 5 days. This behavioral test leveraged the zebrafishes’ innate preference to turn towards 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 towards 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 on the study, who carried out the research as part of her PhD 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 behaviour 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 Professor Armin Bahl from the “Centre for the Advanced Study of Collective Behaviour” of the University of Konstanz, who led the behavioural experiments in this study. 

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 that are driving how they behave. 

The research was primarily funded by the Medical Research Council (MRC), the Leverhulme Trust, The Biotechnology and Biological Sciences Research Council, and the Emmy Noether Program. 

Dr Phoebe Reynolds is now a postdoctoral researcher at the Friedrich Miescher Institute of Biomedical Research in Basel, Switzerland.

This article was originally published on news-medical