Fast near-whole brain imaging in adult Drosophila during responses to stimuli and behavior

Whole brain recordings give us a global perspective of the brain in action. In this study, we describe a method using light field microscopy to record near-whole brain calcium and voltage activity, at high speed, in behaving adult flies. We first obtained global activity maps for various stimuli and behaviors. Notably, we found that brain activity increased on a global scale when the fly walked but not when it groomed. This global increase with walking was particularly strong in dopamine neurons. Second, we extracted maps of spatially distinct sources of activity as well as their time series using principal component analysis and independent component analysis. The characteristic shapes in the maps matched the anatomy of sub-neuropil regions and in some cases a specific neuron type. Brain structures that responded to light and odor were consistent with previous reports, confirming the new technique’s validity. We also observed previously uncharacterized behavior-related activity, as well as patterns of spontaneous voltage activity.

[1]  John Wright,et al.  RASL: Robust alignment by sparse and low-rank decomposition for linearly correlated images , 2010, 2010 IEEE Computer Society Conference on Computer Vision and Pattern Recognition.

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

[3]  Benjamin F. Grewe,et al.  High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor , 2015, Science.

[4]  Kevin J Mann,et al.  Whole-Brain Calcium Imaging Reveals an Intrinsic Functional Network in Drosophila , 2017, Current Biology.

[5]  Ryohei Kanzaki,et al.  Information flow through neural circuits for pheromone orientation , 2014, Nature Communications.

[6]  Julie H. Simpson,et al.  A Systematic Nomenclature for the Insect Brain , 2014, Neuron.

[7]  Joshua W Shaevitz,et al.  Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans , 2015, Proceedings of the National Academy of Sciences.

[8]  Michael B. Reiser,et al.  Walking Modulates Speed Sensitivity in Drosophila Motion Vision , 2010, Current Biology.

[9]  Andrea Giovannucci,et al.  NoRMCorre: An online algorithm for piecewise rigid motion correction of calcium imaging data , 2017 .

[10]  Todd Anderson,et al.  Elastic source selection for in vivo imaging of neuronal ensembles , 2009, 2009 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[11]  Nicolas Chenouard,et al.  Icy: an open bioimage informatics platform for extended reproducible research , 2012, Nature Methods.

[12]  Mark J. Schnitzer,et al.  Automated Analysis of Cellular Signals from Large-Scale Calcium Imaging Data , 2009, Neuron.

[13]  George Loizou,et al.  Computer vision and pattern recognition , 2007, Int. J. Comput. Math..

[14]  Johannes D. Seelig,et al.  Neural dynamics for landmark orientation and angular path integration , 2015, Nature.

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

[16]  Johannes D. Seelig,et al.  Video-rate volumetric functional imaging of the brain at synaptic resolution , 2016, Nature Neuroscience.

[17]  Elizabeth M. C. Hillman,et al.  SCAPE Microscopy for High Speed, 3D Whole-Brain Imaging in Drosophila Melanogaster , 2016 .

[18]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[19]  Nathan W. Gouwens,et al.  Signal Propagation in Drosophila Central Neurons , 2009, The Journal of Neuroscience.

[20]  Vikas Bhandawat,et al.  Organization of descending neurons in Drosophila melanogaster , 2016, Scientific Reports.

[21]  Jamey S. Kain,et al.  Neuronal control of locomotor handedness in Drosophila , 2014, Proceedings of the National Academy of Sciences.

[22]  Ann-Shyn Chiang,et al.  A comprehensive wiring diagram of the protocerebral bridge for visual information processing in the Drosophila brain. , 2013, Cell reports.

[23]  Surya Ganguli,et al.  Identification of cellular-activity dynamics across large tissue volumes in the mammalian brain , 2017, bioRxiv.

[24]  Michael Broxton,et al.  SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function , 2015, Cell.

[25]  Damon A. Clark,et al.  Processing properties of ON and OFF pathways for Drosophila motion detection , 2014, Nature.

[26]  Kristin Branson,et al.  Whole-central nervous system functional imaging in larval Drosophila , 2015, Nature Communications.

[27]  A. Vaziri,et al.  Video rate volumetric Ca2+ imaging across cortex using seeded iterative demixing (SID) microscopy , 2017, Nature Methods.

[28]  G. Rubin,et al.  Neuroarchitecture and neuroanatomy of the Drosophila central complex: A GAL4-based dissection of protocerebral bridge neurons and circuits , 2014, The Journal of comparative neurology.

[29]  Aaron S. Andalman,et al.  Wave optics theory and 3-D deconvolution for the light field microscope. , 2013, Optics express.

[30]  Marie P Suver,et al.  An Array of Descending Visual Interneurons Encoding Self-Motion in Drosophila , 2016, The Journal of Neuroscience.

[31]  Rachel I. Wilson,et al.  Origins of correlated activity in an olfactory circuit , 2009, Nature Neuroscience.

[32]  Zeguan Wang,et al.  Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (Danio rerio) , 2017, bioRxiv.

[33]  Michael B. Reiser,et al.  Mapping the Neural Substrates of Behavior , 2017, Cell.

[34]  G. Rubin,et al.  The neuronal architecture of the mushroom body provides a logic for associative learning , 2014, eLife.

[35]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[36]  E. Boyden,et al.  Simultaneous whole-animal 3D-imaging of neuronal activity using light-field microscopy , 2014, Nature Methods.

[37]  Rachel I. Wilson.  Early olfactory processing in Drosophila: mechanisms and principles. , 2013, Annual review of neuroscience.

[38]  Vincent A. Pieribone,et al.  Single Action Potentials and Subthreshold Electrical Events Imaged in Neurons with a Fluorescent Protein Voltage Probe , 2012, Neuron.

[39]  Aapo Hyvärinen,et al.  Fast and robust fixed-point algorithms for independent component analysis , 1999, IEEE Trans. Neural Networks.

[40]  Dal Hyung Kim,et al.  Pan-neuronal calcium imaging with cellular resolution in freely swimming zebrafish , 2017, Nature Methods.

[41]  R W Cox,et al.  Real‐time 3D image registration for functional MRI , 1999, Magnetic resonance in medicine.

[42]  V. Pieribone,et al.  Genetically Targeted Optical Electrophysiology in Intact Neural Circuits , 2013, Cell.

[43]  Peter T Weir,et al.  Functional divisions for visual processing in the central brain of flying Drosophila , 2015, Proceedings of the National Academy of Sciences.

[44]  Markus Knaden,et al.  Decoding odor quality and intensity in the Drosophila brain , 2014, eLife.

[45]  Michael Z. Lin,et al.  Subcellular Imaging of Voltage and Calcium Signals Reveals Neural Processing In Vivo , 2016, Cell.

[46]  Marc Levoy,et al.  Light field microscopy , 2006, ACM Trans. Graph..

[47]  Nicholas Burton,et al.  The Virtual Fly Brain browser and query interface , 2012, Bioinform..