Wiring variations that enable and constrain neural computation in a sensory microcircuit

Neural network function can be shaped by varying the strength of synaptic connections. One way to achieve this is to vary connection structure. To investigate how structural variation among synaptic connections might affect neural computation, we examined primary afferent connections in the Drosophila olfactory system. We used large-scale serial section electron microscopy to reconstruct all the olfactory receptor neuron (ORN) axons that target a left-right pair of glomeruli, as well as all the projection neurons (PNs) postsynaptic to these ORNs. We found three variations in ORN→PN connectivity. First, we found a systematic co-variation in synapse number and PN dendrite size, suggesting total synaptic conductance is tuned to postsynaptic excitability. Second, we discovered that PNs receive more synapses from ipsilateral than contralateral ORNs, providing a structural basis for odor lateralization behavior. Finally, we found evidence of imprecision in ORN→PN connections that can diminish network performance. DOI: http://dx.doi.org/10.7554/eLife.24838.001

[1]  B. Katz,et al.  On the factors which determine the amplitude of the ‘miniature end‐plate potential’ , 1957, The Journal of physiology.

[2]  Wilfrid Rall,et al.  Theoretical significance of dendritic trees for neuronal input-output relations , 1964 .

[3]  A. van Harreveld,et al.  Changes in extracellular space of the mouse cerebral cortex during hydroxyadipaldehyde fixation and osmium tetroxide post-fixation. , 1969, Journal of cell science.

[4]  J. Weakly,et al.  Correlation between nerve terminal size and transmitter release at the neuromuscular junction of the frog , 1971, The Journal of physiology.

[5]  S. Ward,et al.  Electron microscopical reconstruction of the anterior sensory anatomy of the nematode caenorhabditis elegans , 1975, The Journal of comparative neurology.

[6]  C. Goodman Isogenic grasshoppers: Genetic variability in the morphology of identified neurons , 1978, The Journal of comparative neurology.

[7]  J Walton,et al.  Lead asparate, an en bloc contrast stain particularly useful for ultrastructural enzymology. , 1979, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[8]  D. Purves,et al.  Visualization of neuromuscular junctions over periods of several months in living mice , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  RJ Balice-Gordon,et al.  In vivo visualization of the growth of pre- and postsynaptic elements of neuromuscular junctions in the mouse , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  I. Meinertzhagen,et al.  Ultrastructure and quantification of synapses in the insect nervous system , 1996, Journal of Neuroscience Methods.

[11]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[12]  Richard Axel,et al.  An Olfactory Sensory Map in the Fly Brain , 2000, Cell.

[13]  John R. Carlson,et al.  Odor Coding in the Drosophila Antenna , 2001, Neuron.

[14]  Bert Sakmann,et al.  Reciprocal intraglomerular excitation and intra‐ and interglomerular lateral inhibition between mouse olfactory bulb mitral cells , 2002, The Journal of physiology.

[15]  George H. Patterson,et al.  A Photoactivatable GFP for Selective Photolabeling of Proteins and Cells , 2002, Science.

[16]  Dmitri B. Chklovskii,et al.  Wiring Optimization in Cortical Circuits , 2002, Neuron.

[17]  Gero Miesenböck,et al.  Transmission of Olfactory Information between Three Populations of Neurons in the Antennal Lobe of the Fly , 2002, Neuron.

[18]  Kei Ito,et al.  Integration of Chemosensory Pathways in the Drosophila Second-Order Olfactory Centers , 2004, Current Biology.

[19]  E. Marder,et al.  Similar network activity from disparate circuit parameters , 2004, Nature Neuroscience.

[20]  E. Hallem,et al.  The odor coding system of Drosophila. , 2004, Trends in genetics : TIG.

[21]  Ariane Ramaekers,et al.  Developmental origin of wiring specificity in the olfactory system of Drosophila , 2004, Development.

[22]  Alexander Borst,et al.  Computation of olfactory signals inDrosophila melanogaster , 1983, Journal of comparative physiology.

[23]  Barry J. Dickson,et al.  Molecular, Anatomical, and Functional Organization of the Drosophila Olfactory System , 2005, Current Biology.

[24]  M. Dickinson,et al.  Free-flight responses of Drosophila melanogaster to attractive odors , 2006, Journal of Experimental Biology.

[25]  I. Meinertzhagen,et al.  Development and structure of synaptic contacts in Drosophila. , 2006, Seminars in cell & developmental biology.

[26]  R. Angus Silver,et al.  neuroConstruct: A Tool for Modeling Networks of Neurons in 3D Space , 2007, Neuron.

[27]  Shawn R. Olsen,et al.  Lateral presynaptic inhibition mediates gain control in an olfactory circuit , 2008, Nature.

[28]  Barry J. Dickson,et al.  The Drosophila pheromone cVA activates a sexually dimorphic neural circuit , 2008, Nature.

[29]  Hokto Kazama,et al.  Homeostatic Matching and Nonlinear Amplification at Identified Central Synapses , 2008, Neuron.

[30]  Matthias Landgraf,et al.  Structural Homeostasis: Compensatory Adjustments of Dendritic Arbor Geometry in Response to Variations of Synaptic Input , 2008, PLoS biology.

[31]  Jing W. Wang,et al.  A Presynaptic Gain Control Mechanism Fine-Tunes Olfactory Behavior , 2008, Neuron.

[32]  Ju Lu,et al.  The Interscutularis Muscle Connectome , 2009, PLoS biology.

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

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

[35]  Stephan Saalfeld,et al.  CATMAID: collaborative annotation toolkit for massive amounts of image data , 2009, Bioinform..

[36]  J. Carlson,et al.  Olfactory Perception: Receptors, Cells, and Circuits , 2009, Cell.

[37]  L. Luo,et al.  Diversity and Wiring Variability of Olfactory Local Interneurons in the Drosophila Antennal Lobe , 2010, Nature Neuroscience.

[38]  Michael L. Hines,et al.  NeuroML: A Language for Describing Data Driven Models of Neurons and Networks with a High Degree of Biological Detail , 2010, PLoS Comput. Biol..

[39]  Michael H. Dickinson,et al.  Olfactory modulation of flight in Drosophila is sensitive, selective and rapid , 2010, Journal of Experimental Biology.

[40]  E. Yaksi,et al.  Electrical Coupling between Olfactory Glomeruli , 2010, Neuron.

[41]  Arthur W. Wetzel,et al.  Network anatomy and in vivo physiology of visual cortical neurons , 2011, Nature.

[42]  Tzumin Lee,et al.  Lineage Analysis of Drosophila Lateral Antennal Lobe Neurons Reveals Notch-Dependent Binary Temporal Fate Decisions , 2012, PLoS biology.

[43]  Kei Ito,et al.  Organization of antennal lobe‐associated neurons in adult Drosophila melanogaster brain , 2012, The Journal of comparative neurology.

[44]  Ronald L Calabrese,et al.  Animal-to-animal variability of connection strength in the leech heartbeat central pattern generator. , 2012, Journal of neurophysiology.

[45]  Rachel I. Wilson,et al.  Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system , 2013, Proceedings of the National Academy of Sciences.

[46]  Jamey S. Kain,et al.  Asymmetric neurotransmitter release enables rapid odor lateralization in Drosophila , 2012, Nature.

[47]  Michael H. Dickinson,et al.  Plume-Tracking Behavior of Flying Drosophila Emerges from a Set of Distinct Sensory-Motor Reflexes , 2014, Current Biology.

[48]  L. Luo,et al.  Synaptic organization of the Drosophila antennal lobe and its regulation by the Teneurins , 2014, eLife.

[49]  G. Knott,et al.  Ultrastructural analysis of adult mouse neocortex comparing aldehyde perfusion with cryo fixation , 2015, eLife.

[50]  T. Sejnowski,et al.  Nanoconnectomic upper bound on the variability of synaptic plasticity , 2015, eLife.

[51]  Louis K. Scheffer,et al.  Synaptic circuits and their variations within different columns in the visual system of Drosophila , 2015, Proceedings of the National Academy of Sciences.

[52]  James M. Jeanne,et al.  Convergence, Divergence, and Reconvergence in a Feedforward Network Improves Neural Speed and Accuracy , 2015, Neuron.

[53]  Bill S Hansson,et al.  Digital in vivo 3D atlas of the antennal lobe of Drosophila melanogaster , 2015, The Journal of comparative neurology.

[54]  Casey M. Schneider-Mizell,et al.  Quantitative neuroanatomy for connectomics in Drosophila , 2015, bioRxiv.

[55]  Rachel I. Wilson,et al.  Behavior Reveals Selective Summation and Max Pooling among Olfactory Processing Channels , 2016, Neuron.

[56]  Rafael Cantera,et al.  Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster , 2016, The Journal of comparative neurology.

[57]  Aravinthan D. T. Samuel,et al.  The wiring diagram of a glomerular olfactory system , 2016, bioRxiv.

[58]  Katherine I Nagel,et al.  Mechanisms Underlying Population Response Dynamics in Inhibitory Interneurons of the Drosophila Antennal Lobe , 2016, The Journal of Neuroscience.

[59]  Brett J. Graham,et al.  Anatomy and function of an excitatory network in the visual cortex , 2016, Nature.

[60]  Bill S Hansson,et al.  Elucidating the Neuronal Architecture of Olfactory Glomeruli in the Drosophila Antennal Lobe. , 2016, Cell reports.

[61]  Zhiyuan Lu,et al.  The CNS connectome of a tadpole larva of Ciona intestinalis (L.) highlights sidedness in the brain of a chordate sibling , 2016, eLife.

[62]  E. Marder,et al.  Sloppy morphological tuning in identified neurons of the crustacean stomatogastric ganglion , 2017, eLife.