Topography of a Visuomotor Transformation

The brain converts perceptual information into appropriate patterns of muscle activity depending on the categorization and localization of sensory cues. Sensorimotor information might either be encoded by distributed networks or by "labeled lines" connecting sensory channels to dedicated behavioral pathways. Here we investigate, in the context of natural behavior, how the tectum of larval zebrafish can inform downstream premotor areas. Optogenetic mapping revealed a tectal motor map underlying locomotor maneuvers for escape and approach. Single-cell reconstructions and high-resolution functional imaging showed that two spatially segregated and uncrossed descending axon tracts selectively transmit approach and escape signals to the hindbrain. Moreover, the approach pathway conveys information about retinotopic target coordinates to specific premotor ensembles via spatially ordered axonal projections. This topographic organization supports a tectum-generated space code sufficient to steer orienting movements. We conclude that specific labeled lines guide object-directed behavior in the larval zebrafish brain.

[1]  A. Kinkhabwala,et al.  A structural and functional ground plan for neurons in the hindbrain of zebrafish , 2011, Proceedings of the National Academy of Sciences.

[2]  Ziad M Hafed,et al.  Goal Representations Dominate Superior Colliculus Activity during Extrafoveal Tracking , 2008, The Journal of Neuroscience.

[3]  D. Sparks.  The brainstem control of saccadic eye movements , 2002, Nature Reviews Neuroscience.

[4]  K. Cullen,et al.  Local Population Synchrony and the Encoding of Eye Position in the Primate Neural Integrator , 2015, The Journal of Neuroscience.

[5]  P. May,et al.  Reticular Formation Connections Underlying Horizontal Gaze: The Central Mesencephalic Reticular Formation (cMRF) as a Conduit for the Collicular Saccade Signal , 2017, Front. Neuroanat..

[6]  Herwig Baier,et al.  The Retinal Projectome Reveals Brain-Area-Specific Visual Representations Generated by Ganglion Cell Diversity , 2014, Current Biology.

[7]  K. Uematsu,et al.  Identification of the midbrain locomotor nuclei and their descending pathways in the teleost carp, Cyprinus carpio , 1997, Brain Research.

[8]  Herwig Baier,et al.  Descending Control of Swim Posture by a Midbrain Nucleus in Zebrafish , 2014, Neuron.

[9]  Masanori Murayama,et al.  Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats. , 2007, Journal of neurophysiology.

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

[11]  W Pieter Medendorp,et al.  Three-dimensional transformations for goal-directed action. , 2011, Annual review of neuroscience.

[12]  Jennifer M Groh,et al.  Auditory signals evolve from hybrid- to eye-centered coordinates in the primate superior colliculus. , 2012, Journal of neurophysiology.

[13]  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.

[14]  Herwig Baier,et al.  A Visual Pathway for Looming-Evoked Escape in Larval Zebrafish , 2015, Current Biology.

[15]  D. Sparks,et al.  Combined eye-head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. , 1996, Journal of neurophysiology.

[16]  Talia N. Lerner,et al.  Communication in Neural Circuits: Tools, Opportunities, and Challenges , 2016, Cell.

[17]  Lilach Avitan,et al.  Limitations of Neural Map Topography for Decoding Spatial Information , 2016, The Journal of Neuroscience.

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

[19]  Herwig Baier,et al.  Targeting neural circuitry in zebrafish using GAL4 enhancer trapping , 2007, Nature Methods.

[20]  Malcolm A. MacIver,et al.  Visually guided gradation of prey capture movements in larval zebrafish , 2013, Journal of Experimental Biology.

[21]  Sten Grillner,et al.  Tectal microcircuit generating visual selection commands on gaze-controlling neurons , 2015, Proceedings of the National Academy of Sciences.

[22]  Gunnar Blohm,et al.  Intrinsic Reference Frames of Superior Colliculus Visuomotor Receptive Fields during Head-Unrestrained Gaze Shifts , 2011, The Journal of Neuroscience.

[23]  Felix Effenberger,et al.  Universal features of dendrites through centripetal branch ordering , 2017, PLoS Comput. Biol..

[24]  E. Ito,et al.  Periventricular efferent neurons in the optic tectum of rainbow trout , 2006, The Journal of comparative neurology.

[25]  M. Orger,et al.  Whole-Brain Activity Maps Reveal Stereotyped, Distributed Networks for Visuomotor Behavior , 2014, Neuron.

[26]  J. K. Harting,et al.  Connectional organization of the superior colliculus , 1984, Trends in Neurosciences.

[27]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[28]  I. Temizer.  Looming-Evoked Escape Behavior and its Visual Pathway in the Larval Zebrafish , 2016 .

[29]  L M Optican,et al.  Superior colliculus neurons mediate the dynamic characteristics of saccades. , 1991, Journal of neurophysiology.

[30]  James D. Manton,et al.  NeuroAnatomy Toolbox v1.5.2 , 2014 .

[31]  E. Pnevmatikakis,et al.  NoRMCorre: An online algorithm for piecewise rigid motion correction of calcium imaging data , 2017, Journal of Neuroscience Methods.

[32]  B. Torres,et al.  Connectivity of the goldfish optic tectum with the mesencephalic and rhombencephalic reticular formation , 2003, Experimental Brain Research.

[33]  Yang Li,et al.  Divergent midbrain circuits orchestrate escape and freezing responses to looming stimuli in mice , 2018, Nature Communications.

[34]  M. A. Basso,et al.  Circuits for Action and Cognition: A View from the Superior Colliculus. , 2017, Annual review of vision science.

[35]  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.

[36]  P. Grobstein,et al.  The organization of descending tectofugal pathways underlying orienting in the frog, Rana pipiens , 2004, Experimental Brain Research.

[37]  Chie Satou,et al.  Hindbrain V2a Neurons in the Excitation of Spinal Locomotor Circuits during Zebrafish Swimming , 2013, Current Biology.

[38]  Jonathan W. Peirce,et al.  PsychoPy—Psychophysics software in Python , 2007, Journal of Neuroscience Methods.

[39]  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.

[40]  C. Comer,et al.  Visually elicited turning behavior in Rana pipiens: comparative organization and neural control of escape and prey capture , 1996, Journal of Comparative Physiology A.

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

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

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

[44]  Ethan K. Scott,et al.  Integrative whole-brain neuroscience in larval zebrafish , 2018, Current Opinion in Neurobiology.

[45]  Alessandro Filosa,et al.  Feeding State Modulates Behavioral Choice and Processing of Prey Stimuli in the Zebrafish Tectum , 2016, Neuron.

[46]  H. Vanegas,et al.  Projections of the optic tectum in two teleost species , 1976, The Journal of comparative neurology.

[47]  W. K. Metcalfe,et al.  T reticular interneurons: A class of serially repeating cells in the zebrafish hindbrain , 1985, The Journal of comparative neurology.

[48]  M. Goodale,et al.  A functional analysis of the collicular output pathways: a dissociation of deficits following lesions of the dorsal tegmental decussation and the ipsilateral collicular efferent bundle in the Mongolian gerbil , 2004, Experimental Brain Research.

[49]  Aristides B. Arrenberg,et al.  A Structural and Genotypic Scaffold Underlying Temporal Integration , 2015, The Journal of Neuroscience.

[50]  Aristides B. Arrenberg,et al.  Optogenetic Localization and Genetic Perturbation of Saccade-Generating Neurons in Zebrafish , 2010, The Journal of Neuroscience.

[51]  Gregory S.X.E. Jefferis,et al.  NBLAST: Rapid, Sensitive Comparison of Neuronal Structure and Construction of Neuron Family Databases , 2016, Neuron.

[52]  F. Engert,et al.  Visuomotor Transformations Underlying Hunting Behavior in Zebrafish , 2015, Current Biology.

[53]  Pengcheng Zhou,et al.  CaImAn an open source tool for scalable calcium imaging data analysis , 2019, eLife.

[54]  Xiaogang Yan,et al.  Spatial transformations between superior colliculus visual and motor response fields during head‐unrestrained gaze shifts , 2015, The European journal of neuroscience.

[55]  Aristides B. Arrenberg,et al.  Functional Architecture of an Optic Flow-Responsive Area that Drives Horizontal Eye Movements in Zebrafish , 2014, Neuron.

[56]  Herwig Baier,et al.  Sensorimotor Decision Making in the Zebrafish Tectum , 2015, Current Biology.

[57]  H. Baier,et al.  A dedicated visual pathway for prey detection in larval zebrafish , 2014, eLife.

[58]  V. Tropepe,et al.  Visual Experience Facilitates BDNF-Dependent Adaptive Recruitment of New Neurons in the Postembryonic Optic Tectum , 2018, The Journal of Neuroscience.

[59]  B. Torres,et al.  Afferent and efferent connections of the mesencephalic reticular formation in goldfish , 2008, Brain Research Bulletin.

[60]  Torsten Rohlfing,et al.  Nonrigid image registration in shared-memory multiprocessor environments with application to brains, breasts, and bees , 2003, IEEE Transactions on Information Technology in Biomedicine.

[61]  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.

[62]  Florian Engert,et al.  Neural Control and Modulation of Swimming Speed in the Larval Zebrafish , 2014, Neuron.

[63]  P. Grobstein,et al.  Neuronal organization underlying visually elicited prey orienting in the frog—III. Evidence for the existence of an uncrossed descending tectofugal pathway , 1987, Neuroscience.

[64]  P. Dean,et al.  Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties , 2006, Experimental Brain Research.

[65]  A. Kinkhabwala,et al.  Mapping a sensory-motor network onto a structural and functional ground plan in the hindbrain , 2011, Proceedings of the National Academy of Sciences.

[66]  Eliana M. Klier,et al.  The superior colliculus encodes gaze commands in retinal coordinates , 2001, Nature Neuroscience.

[67]  Gidon Felsen,et al.  Midbrain contributions to sensorimotor decision making. , 2012, Journal of neurophysiology.

[68]  D. Ingle.  Brain Mechanisms of Visual Localization by Frogs and Toads , 1983 .

[69]  Herwig Baier,et al.  Linking Neurons to Network Function and Behavior by Two-Photon Holographic Optogenetics and Volumetric Imaging , 2017, Neuron.

[70]  S. Lisberger,et al.  A tale of two species: Neural integration in zebrafish and monkeys , 2015, Neuroscience.

[71]  P. Dean,et al.  Head and body movements produced by electrical stimulation of superior colliculus in rats: Effects of interruption of crossed tectoreticulospinal pathway , 1986, Neuroscience.

[72]  Philipp J. Keller,et al.  Light-sheet functional imaging in fictively behaving zebrafish , 2014, Nature Methods.

[73]  J. Meek,et al.  Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum , 1983, Brain Research Reviews.

[74]  Hongying Wang,et al.  Three-dimensional eye-head coordination is implemented downstream from the superior colliculus. , 2003, Journal of neurophysiology.

[75]  P. Dean,et al.  Event or emergency? Two response systems in the mammalian superior colliculus , 1989, Trends in Neurosciences.