Spontaneous Activity in the Zebrafish Tectum Reorganizes over Development and Is Influenced by Visual Experience

Spontaneous patterns of activity in the developing visual system may play an important role in shaping the brain for function. During the period 4-9 dpf (days post-fertilization), larval zebrafish learn to hunt prey, a behavior that is critically dependent on the optic tectum. However, how spontaneous activity develops in the tectum over this period and the effect of visual experience are unknown. Here we performed two-photon calcium imaging of GCaMP6s zebrafish larvae at all days from 4 to 9 dpf. Using recently developed graph theoretic techniques, we found significant changes in both single-cell and population activity characteristics over development. In particular, we identified days 5-6 as a critical moment in the reorganization of the underlying functional network. Altering visual experience early in development altered the statistics of tectal activity, and dark rearing also caused a long-lasting deficit in the ability to capture prey. Thus, tectal development is shaped by both intrinsic factors and visual experience.

[1]  Martin P Meyer,et al.  Evidence from In Vivo Imaging That Synaptogenesis Guides the Growth and Branching of Axonal Arbors by Two Distinct Mechanisms , 2006, The Journal of Neuroscience.

[2]  M. Crair,et al.  Retinal waves coordinate patterned activity throughout the developing visual system , 2012, Nature.

[3]  R. Wong,et al.  Retinal waves and visual system development. , 1999, Annual review of neuroscience.

[4]  J. Tiago Gonçalves,et al.  Circuit level defects in the developing neocortex of fragile X mice , 2013, Nature Neuroscience.

[5]  David J. Field,et al.  Innate Visual Learning through Spontaneous Activity Patterns , 2008, PLoS Comput. Biol..

[6]  Florian Engert,et al.  Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons , 2002, Nature.

[7]  H. Tao,et al.  Functional Elimination of Excitatory Feedforward Inputs Underlies Developmental Refinement of Visual Receptive Fields in Zebrafish , 2011, Journal of Neuroscience.

[8]  Germán Sumbre,et al.  The Emergence of the Spatial Structure of Tectal Spontaneous Activity Is Independent of Visual Inputs , 2017, Cell reports.

[9]  Florian Engert,et al.  Emergence of binocular functional properties in a monocular neural circuit , 2008, Nature Neuroscience.

[10]  Mark Hübener,et al.  Critical-period plasticity in the visual cortex. , 2012, Annual review of neuroscience.

[11]  Jitendra Malik,et al.  Normalized cuts and image segmentation , 1997, Proceedings of IEEE Computer Society Conference on Computer Vision and Pattern Recognition.

[12]  A. Grinvald,et al.  Spontaneously emerging cortical representations of visual attributes , 2003, Nature.

[13]  Drew N. Robson,et al.  Brain-wide neuronal dynamics during motor adaptation in zebrafish , 2012, Nature.

[14]  Kenneth D. Miller,et al.  Adaptive filtering enhances information transmission in visual cortex , 2006, Nature.

[15]  M. Feller,et al.  Mechanisms underlying spontaneous patterned activity in developing neural circuits , 2010, Nature Reviews Neuroscience.

[16]  Gesine Reinert,et al.  Estimating the number of communities in a network , 2016, Physical review letters.

[17]  R. Yuste,et al.  Visual stimuli recruit intrinsically generated cortical ensembles , 2014, Proceedings of the National Academy of Sciences.

[18]  Stephen J. Smith,et al.  Neural activity and the dynamics of central nervous system development , 2004, Nature Neuroscience.

[19]  Mark E. J. Newman,et al.  Stochastic blockmodels and community structure in networks , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[20]  K. Pratt,et al.  Development and spike timing–dependent plasticity of recurrent excitation in the Xenopus optic tectum , 2008, Nature Neuroscience.

[21]  Tobias Bonhoeffer,et al.  Neuronal Plasticity: Beyond the Critical Period , 2014, Cell.

[22]  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.

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

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

[25]  Ethan K. Scott,et al.  Focusing on optic tectum circuitry through the lens of genetics , 2010, BMC Biology.

[26]  M. Feller,et al.  Mechanisms underlying development of visual maps and receptive fields. , 2008, Annual review of neuroscience.

[27]  Ethan K. Scott,et al.  Topographic wiring of the retinotectal connection in zebrafish , 2015, Developmental neurobiology.

[28]  Johann H. Bollmann,et al.  Classification of Object Size in Retinotectal Microcircuits , 2014, Current Biology.

[29]  Malik Magdon-Ismail,et al.  Measuring Similarity between Sets of Overlapping Clusters , 2010, 2010 IEEE Second International Conference on Social Computing.

[30]  Ethan K. Scott,et al.  The influence of activity on axon pathfinding in the optic tectum , 2015, Developmental neurobiology.

[31]  J. Tiago Gonçalves,et al.  Internally Mediated Developmental Desynchronization of Neocortical Network Activity , 2009, The Journal of Neuroscience.

[32]  T. Hensch Critical period plasticity in local cortical circuits , 2005, Nature Reviews Neuroscience.

[33]  I. Thompson,et al.  A Systems-Based Dissection of Retinal Inputs to the Zebrafish Tectum Reveals Different Rules for Different Functional Classes during Development , 2013, The Journal of Neuroscience.

[34]  M E J Newman,et al.  Community structure in social and biological networks , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Edoardo M. Airoldi,et al.  A Survey of Statistical Network Models , 2009, Found. Trends Mach. Learn..

[36]  S. Easter,et al.  The development of eye movements in the zebrafish (Danio rerio). , 1997, Developmental psychobiology.

[37]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

[38]  Arseny S Khakhalin,et al.  Visual Experience-Dependent Maturation of Correlated Neuronal Activity Patterns in a Developing Visual System , 2011, The Journal of Neuroscience.

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

[40]  Daniel Durstewitz,et al.  Cell assemblies at multiple time scales with arbitrary lag constellations , 2017, eLife.

[41]  Arseny S Khakhalin,et al.  Excitation and inhibition in recurrent networks mediate collision avoidance in Xenopus tadpoles , 2014, The European journal of neuroscience.

[42]  J. Rauschecker,et al.  Mechanisms of visual plasticity: Hebb synapses, NMDA receptors, and beyond. , 1991, Physiological reviews.

[43]  Dario L Ringach,et al.  Spontaneous and driven cortical activity: implications for computation , 2009, Current Opinion in Neurobiology.

[44]  Vítor Lopes-dos-Santos,et al.  Detecting cell assemblies in large neuronal populations , 2013, Journal of Neuroscience Methods.

[45]  Martin P Meyer,et al.  In vivo imaging of synapse formation on a growing dendritic arbor , 2004, Nature Neuroscience.

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

[47]  Timothy W. Dunn,et al.  Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish , 2016, Neuron.

[48]  Arseny S Khakhalin,et al.  Multivariate analysis of electrophysiological diversity of Xenopus visual neurons during development and plasticity , 2015, eLife.

[49]  Adriano B. L. Tort,et al.  Neuronal Assembly Detection and Cell Membership Specification by Principal Component Analysis , 2011, PloS one.

[50]  C. Desplan,et al.  Deterministic or Stochastic Choices in Retinal Neuron Specification , 2012, Neuron.

[51]  József Fiser,et al.  Spontaneous Cortical Activity Reveals Hallmarks of an Optimal Internal Model of the Environment , 2011, Science.

[52]  K. Kawakami,et al.  Stereotyped initiation of retinal waves by bipolar cells via presynaptic NMDA autoreceptors , 2016, Nature Communications.

[53]  Michael R. Taylor,et al.  Hardwiring of fine synaptic layers in the zebrafish visual pathway , 2008, Neural Development.

[54]  A. Barabasi,et al.  Network biology: understanding the cell's functional organization , 2004, Nature Reviews Genetics.

[55]  Marla B. Feller,et al.  Spatiotemporal Features of Retinal Waves Instruct the Wiring of the Visual Circuitry , 2016, Front. Neural Circuits.

[56]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[57]  Jing Shen,et al.  Development of Activity in the Mouse Visual Cortex , 2016, The Journal of Neuroscience.

[58]  Ulrike von Luxburg,et al.  A tutorial on spectral clustering , 2007, Stat. Comput..

[59]  Béla Bollobás,et al.  Modern Graph Theory , 2002, Graduate Texts in Mathematics.

[60]  Germán Sumbre,et al.  Spontaneous Neuronal Network Dynamics Reveal Circuit’s Functional Adaptations for Behavior , 2015, Neuron.

[61]  Nathalie L Rochefort,et al.  Sparsification of neuronal activity in the visual cortex at eye-opening , 2009, Proceedings of the National Academy of Sciences.