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Genetic identification of a prey detector circuit in zebrafish

›•“‘ Κ / Akira Muto:1,2@μγ _ˆκ / Koichi Kawakami:1,2@ 1:‘—§ˆβ“`Œ€ŒΒ‘Μˆβ“`‰Šϊ”­Ά / National Institute of Genetics (NIG), Shizuoka, Japan@2:‘Œ€‘ε‰@ˆβ“`Šw / SOKENDAI, Mishima, Japan@

Genetic identification of a prey-detector neural circuit in zebrafish
In diurnal animals, vision is the primary sensory modality used to find food or detect their prey. Prey detection is an innate function of the brain in lower vertebrates that have no parental care at the larval stage1. The initial step of visual recognition of possible prey or a small object starts in the retina. However, the neural substrate of prey detection at the later stage of visual processing has not yet been identified. The activity of prey-detecting neurons is expected to be invariant with respect to objects' apparent size and speed that change with distance from the animal. Here, we explored the brain of zebrafish larvae by using calcium imaging to discover neural activity related to the presence of prey, regardless of its location in the visual field or its motion direction. The Gal4-UAS system was used to express GCaMP, a calcium indicator, in a subpopulation of neurons2,3. We showed that a genetically identified population of neurons in the pretectal area served as the prey detector in zebrafish larvae. These neurons were activated when a paramecium approached the larva regardless of its motion direction. This neuronal activity was observed as early as 4 days post-fertilization, the day that zebrafish larvae start to swim, suggesting that it did not require any prior feeding experience. These neurons responded to an artificial moving spot in a wide range of sizes and speeds. Laser-ablation of these neurons specifically abolished prey-capture behavior, whereas the optokinetic response (eye movements in response to a large-field motion stimulus)4 remained unaffected. Furthermore, we discovered that the inferior lobe of the hypothalamus, known to be a target of pretectal projections in some teleost fish, also showed paramecium-driven neuronal activity similar to that in the pretectal neurons. Our results suggest that the pretectum and the inferior lobe of the hypothalamus are essential parts of the neural circuit that is responsible for prey recognition in zebrafish larvae. Our studies also suggest that prey detection was hard-wired in the brain to assure survival of zebrafish larvae.

References
1. Muto and Kawakami. Front Neural Circuits. 2013;7:110.
2. Muto et al. Curr Biol. 2013;23(4):307-11.
3. Muto et al. Proc Natl Acad Sci U S A. 2011;108(13):5425-30.
4. Muto et al. PLoS Genet. 2005;1(5):e66.