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5 Publications

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    08/19/13 | Spinal projection neurons control turning behaviors in zebrafish.
    Huang K, Ahrens MB, Dunn TW, Engert F
    Current Biology. 2013 Aug 19;23(16):1566-73. doi: 10.1016/j.cub.2013.06.044

    Discrete populations of brainstem spinal projection neurons (SPNs) have been shown to exhibit behavior-specific responses during locomotion [1-9], suggesting that separate descending pathways, each dedicated to a specific behavior, control locomotion. In an alternative model, a large variety of motor outputs could be generated from different combinations of a small number of basic motor pathways. We examined this possibility by studying the precise role of ventromedially located hindbrain SPNs (vSPNs) in generating turning behaviors. We found that unilateral laser ablation of vSPNs reduces the tail deflection and cycle period specifically during the first undulation cycle of a swim bout, whereas later tail movements are unaffected. This holds true during phototaxic [10], optomotor [11], dark-flash-induced [12], and spontaneous turns [13], suggesting a universal role of these neurons in controlling turning behaviors. Importantly, we found that the ablation not only abolishes turns but also results in a dramatic increase in the number of forward swims, suggesting that these neurons transform forward swims into turns by introducing turning kinematics into a basic motor pattern of symmetric tail undulations. Finally, we show that vSPN activity is direction specific and graded by turning angle. Together, these results provide a clear example of how a specific motor pattern can be transformed into different behavioral events by the graded activation of a small set of SPNs.

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    06/06/13 | Two-photon calcium imaging during fictive navigation in virtual environments.
    Ahrens MB, Huang KH, Narayan S, Mensh BD, Engert F
    Frontiers in Neural Circuits. 2013 Jun 6;7:104. doi: 10.3389/fncir.2013.00104 *equal contribution

    A full understanding of nervous system function requires recording from large populations of neurons during naturalistic behaviors. Here we enable paralyzed larval zebrafish to fictively navigate two-dimensional virtual environments while we record optically from many neurons with two-photon imaging. Electrical recordings from motor nerves in the tail are decoded into intended forward swims and turns, which are used to update a virtual environment displayed underneath the fish. Several behavioral features-such as turning responses to whole-field motion and dark avoidance-are well-replicated in this virtual setting. We readily observed neuronal populations in the hindbrain with laterally selective responses that correlated with right or left optomotor behavior. We also observed neurons in the habenula, pallium, and midbrain with response properties specific to environmental features. Beyond single-cell correlations, the classification of network activity in such virtual settings promises to reveal principles of brainwide neural dynamics during behavior.

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    05/01/13 | Whole-brain functional imaging at cellular resolution using light-sheet microscopy.
    Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ
    Nature Methods. 2013 May;10(5):413-20. doi: 10.1038/nmeth.2434

    Brain function relies on communication between large populations of neurons across multiple brain areas, a full understanding of which would require knowledge of the time-varying activity of all neurons in the central nervous system. Here we use light-sheet microscopy to record activity, reported through the genetically encoded calcium indicator GCaMP5G, from the entire volume of the brain of the larval zebrafish in vivo at 0.8 Hz, capturing more than 80% of all neurons at single-cell resolution. Demonstrating how this technique can be used to reveal functionally defined circuits across the brain, we identify two populations of neurons with correlated activity patterns. One circuit consists of hindbrain neurons functionally coupled to spinal cord neuropil. The other consists of an anatomically symmetric population in the anterior hindbrain, with activity in the left and right halves oscillating in antiphase, on a timescale of 20 s, and coupled to equally slow oscillations in the inferior olive.

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    02/27/13 | Identification of nonvisual photomotor response cells in the vertebrate hindbrain.
    Kokel D, Dunn TW, Ahrens MB, Alshut R, Cheung CY, Saint-Amant L, Bruni G, Mateus R, van Ham TJ, Shiraki T, Fukada Y, Kojima D, Yeh JJ, Mikut R, von Lintig J, Engert F, Peters RT
    The Journal of Neuroscience. 2013 Feb 27;33(9):3834-43. doi: 10.1523/JNEUROSCI.3689-12.2013

    Nonvisual photosensation enables animals to sense light without sight. However, the cellular and molecular mechanisms of nonvisual photobehaviors are poorly understood, especially in vertebrate animals. Here, we describe the photomotor response (PMR), a robust and reproducible series of motor behaviors in zebrafish that is elicited by visual wavelengths of light but does not require the eyes, pineal gland, or other canonical deep-brain photoreceptive organs. Unlike the relatively slow effects of canonical nonvisual pathways, motor circuits are strongly and quickly (seconds) recruited during the PMR behavior. We find that the hindbrain is both necessary and sufficient to drive these behaviors. Using in vivo calcium imaging, we identify a discrete set of neurons within the hindbrain whose responses to light mirror the PMR behavior. Pharmacological inhibition of the visual cycle blocks PMR behaviors, suggesting that opsin-based photoreceptors control this behavior. These data represent the first known light-sensing circuit in the vertebrate hindbrain.

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    02/01/13 | Optogenetics in a transparent animal: circuit function in the larval zebrafish.
    Portugues R, Severi KE, Wyart C, Ahrens MB
    Current Opinion in Neurobiology. 2013 Feb;23(1):119-26. doi: 10.1016/j.conb.2012.11.001

    Optogenetic tools can be used to manipulate neuronal activity in a reversible and specific manner. In recent years, such methods have been applied to uncover causal relationships between activity in specified neuronal circuits and behavior in the larval zebrafish. In this small, transparent, genetic model organism, noninvasive manipulation and monitoring of neuronal activity with light is possible throughout the nervous system. Here we review recent work in which these new tools have been applied to zebrafish, and discuss some of the existing challenges of these approaches.

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