Spherical Arena Reveals Optokinetic Response Tuning to Stimulus Location

RESEARCH ARTICLE Spherical arena reveals optokinetic response tuning to stimulus location, size, and frequency across entire visual field of larval zebrafish Florian A Dehmelt1†, Rebecca Meier1†, Julian Hinz1†‡, Takeshi Yoshimatsu2, Clara A Simacek1, Ruoyu Huang1, Kun Wang1, Tom Baden2, Aristides B Arrenberg1* 1University of Tu¨ bingen, Werner Reichardt Centre for Integrative Neuroscience and Institute of Neurobiology, Tu¨ bingen, Germany; 2Sussex Neuroscience, School of Life Sciences, University of Sussex, Sussex, United Kingdom Abstract Many animals have large visual fields, and sensory circuits may sample those regions of visual space most relevant to behaviours such as gaze stabilisation and hunting. Despite this, relatively small displays are often used in vision neuroscience. To sample stimulus locations across most of the visual field, we built a spherical stimulus arena with 14,848 independently controllable LEDs. We measured the optokinetic response gain of immobilised zebrafish larvae to stimuli of *For correspondence: different steradian size and visual field locations. We find that the two eyes are less yoked than aristides.arrenberg@uni- previously thought and that spatial frequency tuning is similar across visual field positions. tuebingen.de However, zebrafish react most strongly to lateral, nearly equatorial stimuli, consistent with † previously reported spatial densities of red, green, and blue photoreceptors. Upside-down These authors contributed equally to this work experiments suggest further extra-retinal processing. Our results demonstrate that motion vision circuits in zebrafish are anisotropic, and preferentially monitor areas with putative behavioural ‡ Present address: Friedrich relevance. Miescher Institute for Biomedical Research (FMI), Basel, Switzerland Competing interests: The Introduction authors declare that no The layout of the retina, and the visual system as a whole, evolved to serve specific behavioural tasks competing interests exist. that animals perform to survive in their respective habitats. A well-known example is the position of Funding: See page 22 the eyes in the head which varies between hunting animals (frontal eyes) and animals that frequently Received: 22 September 2020 need to avoid predation (lateral eyes) (Cronin et al., 2014). Hunting animals keep the prey within Accepted: 07 June 2021 particular visual field regions to maximise behavioural performance (Hoy et al., 2016; Bianco et al., Published: 08 June 2021 2011; Yoshimatsu et al., 2020). To avoid predation, however, it is useful to observe a large propor- tion of visual space, especially those regions in which predators are most likely to appear Reviewing editor: Kristin Tessmar-Raible, University of (Smolka et al., 2011; Zhang et al., 2012). The ecological significance of visual stimuli thus depends Vienna, Austria on their location within the visual field, and it is paralleled by non-uniform processing channels across the retina. This non-uniformity manifests as an area centralis or a fovea in many species, which is a Copyright Dehmelt et al. This region of heightened photoreceptor density in the central retina and serves to increase visual perfor- article is distributed under the mance in the corresponding visual field regions. Photoreceptor densities put a direct physical limit terms of the Creative Commons Attribution License, which on performance parameters such as spatial resolution (Haug et al., 2010; Merigan and Katz, 1990). permits unrestricted use and In addition to these restrictions mediated by the peripheral sensory circuitry, an animal’s use of cer- redistribution provided that the tain visual field regions is also affected by behaviour-specific neural pathways, for example pathways original author and source are dedicated to feeding and stabilisation behaviour. The retinal and extra-retinal circuit anisotropies credited. can in turn effect a dependence of behavioural performance on visual field location (Hoy et al., Dehmelt, Meier, Hinz, et al. eLife 2021;10:e63355. DOI: https://doi.org/10.7554/eLife.63355 1 of 26 Research article Neuroscience 2016; Bianco et al., 2011; Murasugi and Howard, 1989; Shimizu et al., 2010; Yang and Guo, 2013; Zimmermann et al., 2018; Baden et al., 2013). Investigating behavioural performance limits and non-uniformities can offer insights into the processing capabilities and ecological adaptations of animal brains, especially if they can be studied and quantitatively understood at each processing step. The larval zebrafish is a promising vertebrate organism for such an endeavour, since its brain is small and a wide array of experimental techniques are available (Baier and Scott, 2009; McLean and Fetcho, 2011). Zebrafish are lateral-eyed animals and have a large visual field, which increases during early development and in individual 4-day-old larvae has been reported to cover about 163˚ per eye (Easter and Nicola, 1996), although little is known about interindividual variability. Their retina contains four different cone photoreceptor types (Nawrocki et al., 1985), each distributed differently across the retina. UV photoreceptors are dens- est in the ventro-temporal retina (area temporalis ventralis), whereas the red, green, and blue photoreceptors cover more central retinal regions (Zimmermann et al., 2018). Zebrafish larvae perform a wide range of visually mediated behaviours, ranging from prey capture (Trivedi and Bollmann, 2013; Mearns et al., 2020) and escape behaviour (Heap et al., 2018) to stabilisation behaviour (Kubo et al., 2014; Orger et al., 2008); however, the importance of stimulus location within the visual field for the execution of the respective behaviours has only recently been recognized and is still not well understood (Hoy et al., 2016; Zimmermann et al., 2018; Mearns et al., 2020; Kist and Portugues, 2019; Wang et al., 2020; Johnson et al., 2020; Lagogiannis et al., 2020). During visually mediated stabilisation behaviours, such as optokinetic and optomotor responses, animals move their eyes and bodies, respectively, in order to stabilise the retinal image and/or the body position relative to the visual surround. The optokinetic response (OKR) consists of reflexively executed stereotypical eye movements, in which phases of stimulus ‘tracking’ (slow phase) are inter- rupted by quick phases (Figure 1a). In the quick phases, eye position is reset by a saccade in the direction opposite to stimulus motion. In humans, optokinetic responses are strongest in the central visual field (Howard and Ohmi, 1984). Furthermore, lower visual field locations of the stimulus evoke stronger OKR than upper visual field locations, which likely represents an adaptation to the rich optic flow information available from the structures on the ground in the natural environments of primates (Murasugi and Howard, 1989; Hafed and Chen, 2016). In zebrafish larvae, OKR behaviour has been used extensively to assess visual function in geneti- cally altered animals (Brockerhoff et al., 1995; Muto et al., 2005; Neuhauss et al., 1999). OKR tuning to velocity, frequency, and contrast of grating stimuli has been measured (Clark, 1981; Cohen et al., 1977; Huang and Neuhauss, 2008; Rinner et al., 2005), and, more recently, zebrafish are used as a model for investigating vertebrate sensorimotor transformations (Kubo et al., 2014; Portugues et al., 2014). While zebrafish can distinguish rotational from translational optic flow to evoke appropriate optokinetic and optomotor responses (Kubo et al., 2014; Naumann et al., 2016; Wang et al., 2019), it is still unclear which regions of the visual field zebrafish preferentially observe in these behaviours. The aquatic lifestyle, in combination with the preferred swimming depths (Lindsey et al., 2010), might cause the lower visual field to contain less relevant information when compared to terrestrial animals. This in turn might result in behavioural biases to other – more infor- mative – visual field regions. A corresponding systematic behavioural quantification in zebrafish or other aquatic species, which would relate OKR behaviour to naturally occurring motion statistics and the underlying neuronal representations in retina and retino-recipient brain structures, has been pre- vented by technical limitations. Specifically, little is known about (i) the dependence of OKR gain on stimulus location or (ii) on stimulus sizes, (iii) possible interactions between stimulus location, size and frequency, (iv) putative asymmetries between the left and right hemispheres of the visual field, and (v) the relationship between a putative dependence of OKR on stimulus location and zebrafish retinal architecture. In other species with large visual fields, such as Drosophila, full-surround stimulation setups have been designed and used successfully (Reiser and Dickinson, 2008; Kim et al., 2017; Maisak et al., 2013), but to date, none has been used for fish. This is at least partly due to their aquatic environ- ment and the associated difficulties regarding the refraction of stimulus light at the air-water inter- face. Such distortions of shape can be partially compensated by pre-emptively altering the shape of the stimulus. However, using regular computer screens or video projection, the resulting luminance profiles remain anisotropic unless compensated, potentially biasing the response toward brighter Dehmelt, Meier, Hinz, et al. eLife 2021;10:e63355. DOI: https://doi.org/10.7554/eLife.63355 2 of 26 Research article Neuroscience Figure 1. Presenting visual

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