Gaze stabilisation behaviour is anisotropic across visual field locations in zebrafish

Abstract

Many animals have large visual fields, allowing them to observe almost any stimulus in their surround. The underlying sensory circuits have evolved to sample those visual field regions most informative to the animal. These regions can vary between different visually mediated behaviours, such as stabilisation and hunting behaviour. Despite this, relatively small displays are often used in vision neuroscience, making it difficult to study the tuning of the visual system to specific visual field locations. To overcome these technical limitations and reveal the organisation of motion circuits with respect to visual space, we built a spherical stimulus arena with 14,848 independently controllable LEDs and used it to stimulate almost the entire visual surround of immobilised zebrafish larvae. We measured the gain of the optokinetic response at different stimulus positions relative to the fish, and related behavioural performance to photoreceptor densities in the retina. We report that zebrafish larvae react most strongly and consistently to stimuli located laterally and near the equator of their visual space. The OKR appears to be symmetric between both eyes, although individual animals oftentimes have a dominant eye. For small stimuli, the OKR gain depends on stimulus size in a logarithmic fashion. OKR to our mostly green stimuli was tuned to the higher spatial densities of red, green and blue photoreceptors in the central retina. In addition, experiments in animals mounted upside-down suggest that extra-retinal processing affects the preferred OKR stimulus location. The tuning to stimulus size and spatial frequency was similar across different visual field positions. During monocular motion stimulation, the non-stimulated eye was strongly yoked if a low-contrast stimulus was present, and less so if a high-contrast stimulus was presented. Our results provide a precise analysis of OKR responses across the whole visual field, and relate sensory performance both to the architecture of the retina and to downstream neural pathways. Our results suggest that motion vision circuits in zebrafish are highly anisotropic. We hypothesize that they monitor specific positions in visual space that are relevant for behaviour in nature, and specifically, that the observed variation of OKR performance across visual field locations is caused by retinal and central adaptations of the zebrafish brain to behavioural needs during visual orientation and stabilisation.Author summaryThe visual system of larval zebrafish mirrors many features, present in the visual system of other vertebrates, including its ability to mediate optomotor and optokinetic behaviour. Although the presence of such behaviours and some of the underlying neural correlates have been firmly established, previous experiments did not consider the large visual field of zebrafish, which covers more than 160° for each eye. Given that different parts of the visual field likely carry unequal amount of behaviourally relevant information for the animal, this raises the question whether optic flow is integrated across the entire visual field or just parts of it, and how this shapes behaviour such as the optokinetic response. We constructed a spherical LED arena to present visual stimuli almost anywhere across their visual field, while tracking horizontal eye movements. By displaying moving gratings on this LED arena, we demonstrate that the optokinetic response, one of the most prominent visually induced behaviours of zebrafish, indeed strongly depends on stimulus location and stimulus size, as well as on other parameters such as the spatial and temporal frequency of the gratings. This location dependence is consistent with areas of high retinal photoreceptor densities.BlurbStimulation across entire visual field reveals that zebrafish optokinetic behaviour is most strongly driven by lateral stimulus locations. This anisotropy is a result of retinal and extra-retinal effects.

Understanding the retinal basis of vision across species

“…Recent studies have started to reveal the extent to which the retinas of some species are adapted to the statistics of the visual information that they receive, such as the distribution of spatial, temporal and spectral information, as well as to their specific behavioural demands 3,[6][7][8][9][10][11][12] . These studies have demonstrated that retinal circuits may differ even between closely related species 1,2 .…”

Spherical arena reveals optokinetic response tuning to stimulus location, size, and frequency across entire visual field of larval zebrafish

“…More importantly, several gaps in LED coverage, resulting from structural elements of the arena, were restricted mainly to the back, the top, and bottom of the animal. The ‘keel’ behind and in front of the fish supports the horizontal ‘ribs’, and the circular openings in the top and bottom accommodate the optical path for eye tracking or scanning microscopy (also see discussion of arena geometry in our data repository [ Dehmelt et al, 2020 ; https://gin.g-node.org/Arrenberg_Lab/spherical_arena ]).…”

“…Azimuth sign is opposite to the conventional mathematical notation of angles when looking top-down onto the fish. In our data repository, we provide a detailed description of the coordinate systems used, including transformations between Cartesian and geographic coordinate systems ( Dehmelt et al, 2020 , https://gin.g-node.org/Arrenberg_Lab/spherical_arena ).…”

Simultaneous analysis of neuroactive compounds in zebrafish

“…Zebrafish larvae and embryos have long been used to assay environmental toxicants. 2,3,8,30 They have also made waves in neuroscience as models for vision, 7,9,21,37,49 threat response, 38 memory, 52 algesia, 6,14,44 and sleep. 35,39,43 In a rare example of bench-to-bedside, the FDA approved the drug lorcaserin as an antiepileptic, based mostly on evidence in zebrafish.…”