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

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.