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      Prey Capture Behavior Evoked by Simple Visual Stimuli in Larval Zebrafish

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          Abstract

          Understanding how the nervous system recognizes salient stimuli in the environment and selects and executes the appropriate behavioral responses is a fundamental question in systems neuroscience. To facilitate the neuroethological study of visually guided behavior in larval zebrafish, we developed “virtual reality” assays in which precisely controlled visual cues can be presented to larvae whilst their behavior is automatically monitored using machine vision algorithms. Freely swimming larvae responded to moving stimuli in a size-dependent manner: they directed multiple low amplitude orienting turns (∼20°) toward small moving spots (1°) but reacted to larger spots (10°) with high-amplitude aversive turns (∼60°). The tracking of small spots led us to examine how larvae respond to prey during hunting routines. By analyzing movie sequences of larvae hunting paramecia, we discovered that all prey capture routines commence with eye convergence and larvae maintain their eyes in a highly converged position for the duration of the prey-tracking and capture swim phases. We adapted our virtual reality assay to deliver artificial visual cues to partially restrained larvae and found that small moving spots evoked convergent eye movements and J-turns of the tail, which are defining features of natural hunting. We propose that eye convergence represents the engagement of a predatory mode of behavior in larval fish and serves to increase the region of binocular visual space to enable stereoscopic targeting of prey.

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          Most cited references26

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          Optogenetic dissection of a behavioral module in the vertebrate spinal cord

          Locomotion relies on neural networks called central pattern generators (CPGs) that generate periodic motor commands for rhythmic movements1. We have identified a spinal input to the CPG that drives spontaneous locomotion using a combination of intersectional gene expression and optogenetics2 in zebrafish larvae. The photo-stimulation of one specific cell type was sufficient to induce a symmetrical tail beating sequence that mimics spontaneous slow forward swimming. This neuron is the Kolmer-Agduhr (KA) cell3, which extends cilia into the central cerebrospinal fluid containing canal of the spinal cord and has an ipsilateral ascending axon that terminates in a series of consecutive segments4. Genetically silencing KA cells reduced the frequency of spontaneous free swimming, indicating that KA cell activity provides necessary tone for spontaneous forward swimming. KA cells have been known for over 75 years, but their function has been mysterious. Our results reveal that during early development in low vertebrates these cells provide a positive drive to the spinal CPG for spontaneous locomotion.
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            Sensorimotor gating in larval zebrafish.

            Control of behavior in the natural environment where sensory stimuli are abundant requires superfluous information to be ignored. In part, this is achieved through selective transmission, or gating of signals to motor systems. A quantitative and clinically important measure of sensorimotor gating is prepulse inhibition (PPI) of the startle response, impairments in which have been demonstrated in several neuropsychiatric disorders, including schizophrenia. Here, we show for the first time that the acoustic startle response in zebrafish larvae is modulated by weak prepulses in a manner similar to mammalian PPI. We demonstrate that, like in mammals, antipsychotic drugs can suppress disruptions in zebrafish PPI induced by dopamine agonists. Because genetic factors underlying PPI are not well understood, we performed a screen and isolated mutant lines with reduced PPI. Analysis of Ophelia mutants demonstrates that they have normal sensory acuity and startle performance, but reduced PPI, suggesting that Ophelia is critical for central processing of sensory information. Thus, our results provide the first evidence for sensorimotor gating in larval zebrafish and report on the first unbiased screen to identify genes regulating this process.
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              The development of vision in the zebrafish (Danio rerio).

              We studied the development and maturation of the visual system by determining when zebrafish begin to see and to move their eyes. This information was correlated with the time courses of the development of the retina, the retinofugal projection, the retinal image, and the extraocular muscles, to obtain an integrated picture of early visual development. Two visual behaviors were monitored over 48-96 hr postfertilization (hpf). The startle response (body twitch) was evoked by an abrupt decrease in light intensity. The optokinetic response (tracking eye movements) was evoked by rotation of a striped drum. Visually evoked startle developed over 68-79 hpf, more than 20 hr after the onset of a touch-evoked startle. It was not seen in eyeless fish, excluding a role for nonretinal light senses. Tracking eye movements developed over 73-80 hpf. They were always in the direction of drum rotation, even when the fish had been light deprived from blastula stage, ruling out a "trial and error" period of learning to track the drum. The image formed by the ocular lens was examined in intact fish made transparent by suppressing the formation of melanin. The eye was initially far sighted and gradually improved, so that by 72 hpf the image plane coincided with the photoreceptor layer. The extraocular muscles assumed their adult configuration between 66 and 72 hpf. Thus, the retinal image and functional extraocular muscles appeared nearly simultaneously with the onset of tracking eye movements and probably represent the last events in the construction of this behavior.
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                Author and article information

                Journal
                Front Syst Neurosci
                Front. Syst. Neurosci.
                Frontiers in Systems Neuroscience
                Frontiers Research Foundation
                1662-5137
                16 December 2011
                2011
                : 5
                Affiliations
                [1] 1simpleDepartment of Molecular and Cellular Biology, Center for Brain Science, Harvard University Cambridge, MA, USA
                [2] 2simpleChampalimaud Neuroscience Programme, Champalimaud Centre for the Unknown Lisbon, Portugal
                Author notes

                Edited by: Federico Bermudez-Rattoni, Universidad Nacional Autónoma de México, Mexico

                Reviewed by: James W. Grau, Texas A&M University, USA; Stephan C. F. Neuhauss, University of Zürich, Switzerland

                *Correspondence: Isaac H. Bianco, Department of Molecular and Cellular Biology, Harvard University, BioLabs-2073, 16 Divinity Avenue, Cambridge, MA 02138, USA. e-mail: ibianco@ 123456mcb.harvard.edu
                Article
                10.3389/fnsys.2011.00101
                3240898
                22203793
                f7682bde-e89c-4f6e-852d-34e14e439d99
                Copyright © 2011 Bianco, Kampff and Engert.

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.

                Page count
                Figures: 6, Tables: 0, Equations: 0, References: 35, Pages: 13, Words: 10130
                Categories
                Neuroscience
                Original Research

                Neurosciences
                prey capture,binocular vision,zebrafish,ocular vergence,behavior
                Neurosciences
                prey capture, binocular vision, zebrafish, ocular vergence, behavior

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