Control of a specific motor program by a small brain area in zebrafish

Complex motor behaviors are thought to be coordinated by networks of brain nuclei that may control different elementary motor programs. Transparent zebrafish larvae offer the opportunity to analyze the functional organization of motor control networks by optical manipulations of neuronal activity during behavior. We examined motor behavior in transgenic larvae expressing channelrhodopsin-2 throughout many neurons in the brain. Wide-field optical stimulation triggered backward and rotating movements caused by the repeated execution of J-turns, a specific motor program that normally occurs during prey capture. Although optically-evoked activity was widespread, behavioral responses were highly coordinated and lateralized. 3-D mapping of behavioral responses to local optical stimuli revealed that J-turns can be triggered specifically in the anterior-ventral optic tectum (avOT) and/or the adjacent pretectum. These results suggest that the execution of J-turns is controlled by a small group of neurons in the midbrain that may act as a command center. The identification of a brain area controlling a defined motor program involved in prey capture is a step toward a comprehensive analysis of neuronal circuits mediating sensorimotor behaviors of zebrafish.

[1]  Toshihiko Hosoya,et al.  Genetic Single-Cell Mosaic Analysis Implicates ephrinB2 Reverse Signaling in Projections from the Posterior Tectum to the Hindbrain in Zebrafish , 2007, The Journal of Neuroscience.

[2]  Herwig Baier,et al.  Visuomotor Behaviors in Larval Zebrafish after GFP-Guided Laser Ablation of the Optic Tectum , 2003, The Journal of Neuroscience.

[3]  S. Grillner,et al.  Neural bases of goal-directed locomotion in vertebrates—An overview , 2008, Brain Research Reviews.

[4]  Donald M. O’Malley,et al.  Prey Capture by Larval Zebrafish: Evidence for Fine Axial Motor Control , 2002, Brain, Behavior and Evolution.

[5]  Ewert Jp.  Electric stimulation of the retinal projection field in the midbrain of the terrestrial toad (Bufo bufo L.) , 1967 .

[6]  H. Burgess,et al.  Modulation of locomotor activity in larval zebrafish during light adaptation , 2007, Journal of Experimental Biology.

[7]  T Radil-Weiss,et al.  Electrical stimulation of the tectum in freely moving cats. , 1971, Brain Research.

[8]  Sebastian Kraves,et al.  OFF ganglion cells cannot drive the optokinetic reflex in zebrafish , 2007, Proceedings of the National Academy of Sciences.

[9]  Yoshihiro Yoshihara,et al.  Mutually Exclusive Glomerular Innervation by Two Distinct Types of Olfactory Sensory Neurons Revealed in Transgenic Zebrafish , 2005, The Journal of Neuroscience.

[10]  Karl Deisseroth,et al.  Neuronal filtering of multiplexed odour representations , 2011, Nature.

[11]  Karel Svoboda,et al.  ScanImage: Flexible software for operating laser scanning microscopes , 2003, Biomedical engineering online.

[12]  B E Stein,et al.  Control of pinna movements and sensorimotor register in cat superior colliculus. , 1981, Brain, behavior and evolution.

[13]  M B Sterman,et al.  Modification of locomotor performance by reticular formation and basal forebrain stimulation in the cat: evidence for reciprocal systems. , 1966, Brain research.

[14]  F. Del Bene,et al.  Optogenetics: A new enlightenment age for zebrafish neurobiology , 2012, Developmental neurobiology.

[15]  D. O'Malley,et al.  Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. , 2000, The Journal of experimental biology.

[16]  Melina E. Hale,et al.  Swimming of larval zebrafish: fin–axis coordination and implications for function and neural control , 2004, Journal of Experimental Biology.

[17]  David W. Tank,et al.  Regression-Based Identification of Behavior-Encoding Neurons During Large-Scale Optical Imaging of Neural Activity at Cellular Resolution , 2010, Journal of neurophysiology.

[18]  N. Schellart,et al.  A golgi study of goldfish optic tectum , 1978, The Journal of comparative neurology.

[19]  Ethan K. Scott,et al.  Optogenetic dissection of a behavioral module in the vertebrate spinal cord , 2009, Nature.

[20]  M. L. Shik,et al.  On the descending control of the lumbosacral spinal cord from the "mesencephalic locomotor region". , 1973, Acta physiologica Scandinavica.

[21]  Rainer W. Friedrich,et al.  Circuit Neuroscience in Zebrafish , 2010, Current Biology.

[22]  Junichi Nakai,et al.  Real-Time Visualization of Neuronal Activity during Perception , 2013, Current Biology.

[23]  William A. Harris,et al.  Genetic Disorders of Vision Revealed by a Behavioral Screen of 400 Essential Loci in Zebrafish , 1999, The Journal of Neuroscience.

[24]  Donald M. O’Malley,et al.  Prey Tracking by Larval Zebrafish: Axial Kinematics and Visual Control , 2005, Brain, Behavior and Evolution.

[25]  N. J. Gandhi,et al.  Motor functions of the superior colliculus. , 2011, Annual review of neuroscience.

[26]  Herwig Baier,et al.  Optical control of zebrafish behavior with halorhodopsin , 2009, Proceedings of the National Academy of Sciences.

[27]  Barry E. Stein,et al.  Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters , 1982, Brain Research.

[28]  Leonard Maler,et al.  Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice , 1988, Journal of Comparative Physiology A.

[29]  Mark T. Waters,et al.  This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited.Thislicensedoesnot permit commercial exploitation or the creation of derivative works without sp , 2009 .

[30]  N. Sankrithi,et al.  Activation of a multisensory, multifunctional nucleus in the zebrafish midbrain during diverse locomotor behaviors , 2010, Neuroscience.

[31]  M. Ryan,et al.  Sex-specific perceptual spaces for a vertebrate basal social aggregative behavior , 2008, Proceedings of the National Academy of Sciences.

[32]  Tomomi Sato,et al.  HuC:Kaede, a useful tool to label neural morphologies in networks in vivo , 2006, Genesis.

[33]  Florian Engert,et al.  The neural basis of visual behaviors in the larval zebrafish , 2009, Current Opinion in Neurobiology.

[34]  Herwig Baier,et al.  Retinotopic order in the absence of axon competition , 2008, Nature.

[35]  T. Prescott,et al.  Is there a brainstem substrate for action selection? , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[36]  Florian Engert,et al.  Prey Capture Behavior Evoked by Simple Visual Stimuli in Larval Zebrafish , 2011, Front. Syst. Neurosci..

[37]  Shiva R. Sinha,et al.  Orienting responses and vocalizations produced by microstimulation in the superior colliculus of the echolocating bat, Eptesicus fuscus , 2002, Journal of Comparative Physiology A.

[38]  E I Knudsen,et al.  Neural maps of head movement vector and speed in the optic tectum of the barn owl. , 1990, Journal of neurophysiology.

[39]  Sebastian T. Bundschuh,et al.  Optogenetic Dissection of Neuronal Circuits in Zebrafish using Viral Gene Transfer and the Tet System , 2009, Front. Neural Circuits.

[40]  B. Torres,et al.  Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish , 1998, Experimental Brain Research.

[41]  Herwig Baier,et al.  A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection , 2005, Development.

[42]  Matthew C Smear,et al.  Perception of Fourier and non-Fourier motion by larval zebrafish , 2000, Nature Neuroscience.

[43]  Michael H. Dickinson,et al.  Motmot, an open-source toolkit for realtime video acquisition and analysis , 2009, Source Code for Biology and Medicine.

[44]  J. Ewert,et al.  Neural modulation of visuomotor functions underlying prey-catching behaviour in anurans: perception, attention, motor performance, learning. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[45]  Tobias Breuninger,et al.  Eyecup scope—optical recordings of light stimulus-evoked fluorescence signals in the retina , 2009, Pflügers Archiv - European Journal of Physiology.

[46]  M A Goodale,et al.  Visuomotor modules in the vertebrate brain. , 1996, Canadian journal of physiology and pharmacology.

[47]  Kristen E. Severi,et al.  Control of visually guided behavior by distinct populations of spinal projection neurons , 2008, Nature Neuroscience.

[48]  C. Niell,et al.  Functional Imaging Reveals Rapid Development of Visual Response Properties in the Zebrafish Tectum , 2005, Neuron.

[49]  D. M. Guthrie,et al.  Motor responses to localized electrical stimulation of the tectum in the freshwater perch (perca fluviatilis) , 1986, Neuroscience.

[50]  Herwig Baier,et al.  Characterization of Genetically Targeted Neuron Types in the Zebrafish Optic Tectum , 2011, Front. Neural Circuits.

[51]  Herwig Baier,et al.  Channeling of red and green cone inputs to the zebrafish optomotor response , 2005, Visual Neuroscience.

[52]  Shih-Chii Liu,et al.  Oculomotor Instabilities in Zebrafish Mutant belladonna: A Behavioral Model for Congenital Nystagmus Caused by Axonal Misrouting , 2006, The Journal of Neuroscience.

[53]  Ethan K. Scott,et al.  The cellular architecture of the larval zebrafish tectum , as revealed by Gal 4 enhancer trap lines , 2022 .

[54]  K. Schaefer.  Unit analysis and electrical stimulation in the optic tectum of rabbits and cats. , 1970, Brain, behavior and evolution.

[55]  B. Torres,et al.  Tectal codification of eye movements in goldfish studied by electrical microstimulation , 1997, Neuroscience.

[56]  Herwig Baier,et al.  Visual Prey Capture in Larval Zebrafish Is Controlled by Identified Reticulospinal Neurons Downstream of the Tectum , 2005, The Journal of Neuroscience.

[57]  Ethan K. Scott,et al.  Filtering of Visual Information in the Tectum by an Identified Neural Circuit , 2010, Science.

[58]  J. Fetcho,et al.  Laser Ablations Reveal Functional Relationships of Segmental Hindbrain Neurons in Zebrafish , 1999, Neuron.

[59]  S. Easter,et al.  Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio) , 1994, The Journal of comparative neurology.

[60]  S. Easter,et al.  The development of vision in the zebrafish (Danio rerio). , 1996, Developmental biology.

[61]  M. Ekker,et al.  A Highly Conserved Enhancer in the Dlx5/Dlx6Intergenic Region is the Site of Cross-Regulatory Interactions betweenDlx Genes in the Embryonic Forebrain , 2000, The Journal of Neuroscience.

[62]  S. Grillner,et al.  Tectal control of locomotion, steering, and eye movements in lamprey. , 2007, Journal of neurophysiology.

[63]  Vijay Iyer,et al.  Ephus: Multipurpose Data Acquisition Software for Neuroscience Experiments , 2010, Front. Neural Circuits.

[64]  S. Easter,et al.  The role of the optic tectum in various visually mediated behaviors of goldfish , 1977, Brain Research.

[65]  Rainer W Friedrich,et al.  High-resolution optical control of spatiotemporal neuronal activity patterns in zebrafish using a digital micromirror device , 2012, Nature Protocols.