Design and implementation of multi-signal and time-varying neural reconstructions

Several efficient procedures exist to digitally trace neuronal structure from light microscopy, and mature community resources have emerged to store, share, and analyze these datasets. In contrast, the quantification of intracellular distributions and morphological dynamics is not yet standardized. Current widespread descriptions of neuron morphology are static and inadequate for subcellular characterizations. We introduce a new file format to represent multichannel information as well as an open-source Vaa3D plugin to acquire this type of data. Next we define a novel data structure to capture morphological dynamics, and demonstrate its application to different time-lapse experiments. Importantly, we designed both innovations as judicious extensions of the classic SWC format, thus ensuring full back-compatibility with popular visualization and modeling tools. We then deploy the combined multichannel/time-varying reconstruction system on developing neurons in live Drosophila larvae by digitally tracing fluorescently labeled cytoskeletal components along with overall dendritic morphology as they changed over time. This same design is also suitable for quantifying dendritic calcium dynamics and tracking arbor-wide movement of any subcellular substrate of interest.

[1]  Giorgio A. Ascoli,et al.  A Comparative Computer Simulation of Dendritic Morphology , 2008, PLoS Comput. Biol..

[2]  Luis Sullivan,et al.  Functional Genomic Analyses of Two Morphologically Distinct Classes of Drosophila Sensory Neurons: Post-Mitotic Roles of Transcription Factors in Dendritic Patterning , 2013, PloS one.

[3]  Michael S Smirnov,et al.  Automated Remote Focusing, Drift Correction, and Photostimulation to Evaluate Structural Plasticity in Dendritic Spines , 2016, bioRxiv.

[4]  Serge Charpak,et al.  Spectral Unmixing: Analysis of Performance in the Olfactory Bulb In Vivo , 2009, PloS one.

[5]  Cyrille Alexandre,et al.  Flybow: genetic multicolor cell labeling for neural circuit analysis in Drosophila melanogaster , 2011, Nature Methods.

[6]  Christian Götze,et al.  Wide-Field Multi-Parameter FLIM: Long-Term Minimal Invasive Observation of Proteins in Living Cells , 2011, PloS one.

[7]  Fred H. Gage,et al.  In-vivo imaging of dendritic pruning in dentate granule cells , 2016, Nature Neuroscience.

[8]  J F Evers,et al.  Progress in functional neuroanatomy: precise automatic geometric reconstruction of neuronal morphology from confocal image stacks. , 2005, Journal of neurophysiology.

[9]  G. Ascoli,et al.  NeuroMorpho.Org: A Central Resource for Neuronal Morphologies , 2007, The Journal of Neuroscience.

[10]  Randy H Kardon,et al.  Effect of enriching the diet with menhaden oil or daily treatment with resolvin D1 on neuropathy in a mouse model of type 2 diabetes. , 2015, Journal of neurophysiology.

[11]  Herwig Baier,et al.  An optogenetic toolbox for unbiased discovery of functionally connected cells in neural circuits , 2017, Nature Communications.

[12]  Arne V. Blackman,et al.  Neuronal morphometry directly from bitmap images , 2014, Nature Methods.

[13]  G. Ascoli,et al.  Neuronal Morphology Goes Digital: A Research Hub for Cellular and System Neuroscience , 2013, Neuron.

[14]  E. S. Ruthazer,et al.  In vivo time-lapse imaging of neuronal development in Xenopus. , 2013, Cold Spring Harbor protocols.

[15]  Stephen J. Smith,et al.  Array Tomography: A New Tool for Imaging the Molecular Architecture and Ultrastructure of Neural Circuits , 2007, Neuron.

[16]  Carlos Portera-Cailliau,et al.  In vivo imaging of axonal and dendritic structures in neonatal mouse cortex. , 2014, Cold Spring Harbor protocols.

[17]  R. C Cannon,et al.  An on-line archive of reconstructed hippocampal neurons , 1998, Journal of Neuroscience Methods.

[18]  Erik De Schutter,et al.  STEPS: efficient simulation of stochastic reaction–diffusion models in realistic morphologies , 2012, BMC Systems Biology.

[19]  Giorgio A. Ascoli,et al.  Digital Reconstructions of Neuronal Morphology: Three Decades of Research Trends , 2012, Front. Neurosci..

[20]  Hollis T. Cline,et al.  Diadem X: Automated 4 Dimensional Analysis of Morphological Data , 2011, Neuroinformatics.

[21]  Kristina D. Micheva,et al.  Array tomography of physiologically-characterized CNS synapses , 2016, Journal of Neuroscience Methods.

[22]  Giorgio A. Ascoli,et al.  Structural Plasticity in Dendrites: Developmental Neurogenetics, Morphological Reconstructions, and Computational Modeling , 2017 .

[23]  Chih-Yang Lin,et al.  Computer Aided Alignment and Quantitative 4D Structural Plasticity Analysis of Neurons , 2013, Neuroinformatics.

[24]  Erik De Schutter,et al.  Context-aware modeling of neuronal morphologies , 2014, Front. Neuroanat..

[25]  Reinhard Guthke,et al.  Regulatory interactions for iron homeostasis in Aspergillus fumigatus inferred by a Systems Biology approach , 2012, BMC Systems Biology.

[26]  Jianli Li,et al.  In Vivo Time-Lapse Imaging and Serial Section Electron Microscopy Reveal Developmental Synaptic Rearrangements , 2011, Neuron.

[27]  Louis K. Scheffer,et al.  A connectome of a learning and memory center in the adult Drosophila brain , 2017, eLife.

[28]  Michael Scholz,et al.  New methods for the computer-assisted 3-D reconstruction of neurons from confocal image stacks , 2004, NeuroImage.

[29]  Giorgio A. Ascoli,et al.  NeuroMorpho.Org Implementation of Digital Neuroscience: Dense Coverage and Integration with the NIF , 2008, Neuroinformatics.

[30]  Giorgio A Ascoli,et al.  Computational models of neuronal biophysics and the characterization of potential neuropharmacological targets. , 2008, Current medicinal chemistry.

[31]  Peter Stratton,et al.  Calcium signalling in medial intercalated cell dendrites and spines , 2017, The Journal of physiology.

[32]  Rebecca Chen,et al.  Fast Spatiotemporal Smoothing of Calcium Measurements in Dendritic Trees , 2012, PLoS Comput. Biol..

[33]  Jonas Ranft,et al.  An aggregation-removal model for the formation and size determination of post-synaptic scaffold domains , 2017, PLoS Comput. Biol..

[34]  Hanchuan Peng,et al.  Extensible visualization and analysis for multidimensional images using Vaa3D , 2014, Nature Protocols.

[35]  Hollis T. Cline,et al.  Experience-Dependent Bimodal Plasticity of Inhibitory Neurons in Early Development , 2016, Neuron.

[36]  Eugene W. Myers,et al.  BlastNeuron for Automated Comparison, Retrieval and Clustering of 3D Neuron Morphologies , 2015, Neuroinformatics.

[37]  Ryohei Yasuda,et al.  Automated remote focusing, drift correction, and photostimulation to evaluate structural plasticity in dendritic spines , 2016 .

[38]  Randal A. Koene,et al.  NETMORPH: A Framework for the Stochastic Generation of Large Scale Neuronal Networks With Realistic Neuron Morphologies , 2009, Neuroinformatics.

[39]  Guan-Yu Chen,et al.  Three-Dimensional Reconstruction of Brain-wide Wiring Networks in Drosophila at Single-Cell Resolution , 2011, Current Biology.

[40]  Andreas Frick,et al.  Three-dimensional tracking and analysis of ion channel signals across dendritic arbors , 2013, Front. Neural Circuits.

[41]  A. Pestronk Histology of the Nervous System of Man and Vertebrates , 1997, Neurology.

[42]  D F Wann,et al.  An on-line digital-computer system for the semiautomatic analysis of Golgi-impregnated neurons. , 1973, IEEE transactions on bio-medical engineering.

[43]  Sridevi Polavaram,et al.  Win–win data sharing in neuroscience , 2017, Nature Methods.

[44]  M. Liset Rietman,et al.  Source (or Part of the following Source): Type Article Title Candidate Genes in Ocular Dominance Plasticity Author(s) Hypothesis and Theory Article Candidate Genes in Ocular Dominance Plasticity , 2022 .

[45]  J. Capowski Computer-aided reconstruction of neuron trees from several serial sections. , 1977, Computers and biomedical research, an international journal.

[46]  James G. King,et al.  Reconstruction and Simulation of Neocortical Microcircuitry , 2015, Cell.

[47]  Hanchuan Peng,et al.  mGRASP enables mapping mammalian synaptic connectivity with light microscopy , 2011, Nature Methods.

[48]  Kaspar Podgorski,et al.  Rapid Hebbian axonal remodeling mediated by visual stimulation , 2014, Science.

[49]  E Pannese,et al.  The Golgi Stain: invention, diffusion and impact on neurosciences. , 1999, Journal of the history of the neurosciences.

[50]  Marvin Goodfriend,et al.  Early Development , 1994 .

[51]  Jinhyun Kim,et al.  neuTube 1.0: A New Design for Efficient Neuron Reconstruction Software Based on the SWC Format 123 , 2015, eNeuro.

[52]  G. Ascoli,et al.  L-Measure: a web-accessible tool for the analysis, comparison and search of digital reconstructions of neuronal morphologies , 2008, Nature Protocols.

[53]  Hausser Michael,et al.  One rule to grow them all: A general theory of neuronal branching and its practical application , 2010 .