Putative excitatory and putative inhibitory inputs are localised in different dendritic domains in a Drosophila flight motoneuron

Input–output computations of individual neurons may be affected by the three‐dimensional structure of their dendrites and by the location of input synapses on specific parts of their dendrites. However, only a few examples exist of dendritic architecture which can be related to behaviorally relevant computations of a neuron. By combining genetic, immunohistochemical and confocal laser scanning methods this study estimates the location of the spike‐initiating zone and the dendritic distribution patterns of putative synaptic inputs on an individually identified Drosophila flight motorneuron, MN5. MN5 is a monopolar neuron with > 4000 dendritic branches. The site of spike initiation was estimated by mapping sodium channel immunolabel onto geometric reconstructions of MN5. Maps of putative excitatory cholinergic and of putative inhibitory GABAergic inputs on MN5 dendrites were created by charting tagged Dα7 nicotinic acetylcholine receptors and Rdl GABAA receptors onto MN5 dendritic surface reconstructions. Although these methods provide only an estimate of putative input synapse distributions, the data indicate that inhibitory and excitatory synapses were located preferentially on different dendritic domains of MN5 and, thus, computed mostly separately. Most putative inhibitory inputs were close to spike initiation, which was consistent with sharp inhibition, as predicted previously based on recordings of motoneuron firing patterns during flight. By contrast, highest densities of putative excitatory inputs at more distant dendritic regions were consistent with the prediction that, in response to different power demands during flight, tonic excitatory drive to flight motoneuron dendrites must be smoothly translated into different tonic firing frequencies.

[1]  N. Spruston,et al.  Synapse Distribution Suggests a Two-Stage Model of Dendritic Integration in CA1 Pyramidal Neurons , 2009, Neuron.

[2]  K. E. Machin,et al.  The physiology of insect fibrillar muscle - II Mechanical properties of a beetle flight muscle , 1959, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[3]  J F Evers,et al.  Developmental relocation of presynaptic terminals along distinct types of dendritic filopodia. , 2006, Developmental biology.

[4]  Subhabrata Sanyal,et al.  Genomic mapping and expression patterns of C380, OK6 and D42 enhancer trap lines in the larval nervous system of Drosophila. , 2009, Gene expression patterns : GEP.

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

[6]  D. Sattelle,et al.  Immunocytochemical mapping of a C-terminus anti-peptide antibody to the GABA receptor subunit, RDL in the nervous system of Drosophila melanogaster , 1996, Cell and Tissue Research.

[7]  R. ffrench-Constant,et al.  Isolation of dieldrin resistance from field populations of Drosophila melanogaster (Diptera: Drosophilidae). , 1990, Journal of economic entomology.

[8]  Stefanie Ryglewski,et al.  Dendrite elongation and dendritic branching are affected separately by different forms of intrinsic motoneuron excitability. , 2008, Journal of neurophysiology.

[9]  D. Sattelle,et al.  Novel Putative Nicotinic Acetylcholine Receptor Subunit Genes , D 5 , D 6 and D 7 , in Drosophila melanogaster Identify a New and Highly Conserved Target of Adenosine Deaminase Acting on RNA-Mediated A-toI Pre-mRNA Editing , 2002 .

[10]  R. Wyman,et al.  Neurophysiology of flight in wild-type and a mutant Drosophila. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[11]  K. Ikeda,et al.  Neural interactions controlling timing of flight muscle activity in Drosophila. , 1980, The Journal of experimental biology.

[12]  D. O'Dowd,et al.  Fast Synaptic Currents in Drosophila Mushroom Body Kenyon Cells Are Mediated by α-Bungarotoxin-Sensitive Nicotinic Acetylcholine Receptors and Picrotoxin-Sensitive GABA Receptors , 2003, The Journal of Neuroscience.

[13]  F. Diao,et al.  SIDL interacts with the dendritic targeting motif of Shal (Kv4) K+ channels in Drosophila , 2010, Molecular and Cellular Neuroscience.

[14]  M. S. Tu,et al.  The Function of Dipteran Flight Muscle , 1997 .

[15]  P. Somogyi,et al.  The hippocampal CA3 network: An in vivo intracellular labeling study , 1994, The Journal of comparative neurology.

[16]  K. Ikeda,et al.  Interspike interval relationship among flight muscle fibres in Drosophila. , 1980, The Journal of experimental biology.

[17]  P. Somogyi,et al.  Salient features of synaptic organisation in the cerebral cortex 1 Published on the World Wide Web on 3 March 1998. 1 , 1998, Brain Research Reviews.

[18]  Michael Bate,et al.  Electrophysiological Development of Central Neurons in theDrosophila Embryo , 1998, The Journal of Neuroscience.

[19]  Dimitrios Kadas,et al.  Constitutive Activation of Ca2+/Calmodulin-Dependent Protein Kinase II during Development Impairs Central Cholinergic Transmission in a Circuit Underlying Escape Behavior in Drosophila , 2012, The Journal of Neuroscience.

[20]  Deborah J. Baro,et al.  Differential Expression and Targeting of K+ Channel Genes in the Lobster Pyloric Central Pattern Generatora , 1998 .

[21]  Vann Bennett,et al.  AnkyrinG Is Required for Clustering of Voltage-gated Na Channels at Axon Initial Segments and for Normal Action Potential Firing , 1998, The Journal of cell biology.

[22]  D. Sattelle,et al.  Acetylcholine receptor/channel molecules of insects. , 1993, EXS.

[23]  Alexander Borst,et al.  Synaptic Organization of Lobula Plate Tangential Cells in Drosophila: Dα7 Cholinergic Receptors , 2009, Journal of neurogenetics.

[24]  J. B. Duffy,et al.  GAL4 system in drosophila: A fly geneticist's swiss army knife , 2002, Genesis.

[25]  P. Hiesinger,et al.  The Nicotinic Acetylcholine Receptor Dα7 Is Required for an Escape Behavior inDrosophila , 2006, PLoS biology.

[26]  R. ffrench-Constant,et al.  A point mutation in a Drosophila GABA receptor confers insecticide resistance , 1993, Nature.

[27]  C Duch,et al.  Postembryonic development of the dorsal longitudinal flight muscle and its innervation in Manduca sexta , 2000, The Journal of comparative neurology.

[28]  Kevin G. Moffat,et al.  Article Title: Regulation of Neuronal Excitability through Pumilio- Dependent Control of a Sodium Channel Gene Regulation of Neuronal Excitability through Pumilio- Dependent Control of a Sodium Channel Gene Materials and Methods , 2022 .

[29]  M. Bate,et al.  Development of larval muscle properties in the embryonic myotubes of Drosophila melanogaster , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  Peter Shrager,et al.  Neurofascin assembles a specialized extracellular matrix at the axon initial segment , 2007, The Journal of cell biology.

[31]  Carsten Duch,et al.  Correlative electron and confocal microscopy assessment of synapse localization in the central nervous system of an insect , 2008, Journal of Neuroscience Methods.

[32]  S. Redman,et al.  Statistical analysis of amplitude fluctuations in EPSCs evoked in rat CA1 pyramidal neurones in vitro. , 1996, The Journal of physiology.

[33]  G. Boulianne,et al.  Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Kevin L. Briggman,et al.  Towards neural circuit reconstruction with volume electron microscopy techniques , 2006, Current Opinion in Neurobiology.

[35]  R. Levine,et al.  Dendritic Remodeling and Growth of Motoneurons during Metamorphosis of Drosophila melanogaster , 2002, The Journal of Neuroscience.

[36]  M. Ramaswami,et al.  Evidence for cell autonomous AP1 function in regulation of Drosophila motor-neuron plasticity , 2003, BMC Neuroscience.

[37]  Christof Koch,et al.  The role of single neurons in information processing , 2000, Nature Neuroscience.

[38]  Karel Svoboda,et al.  Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs , 2004, Nature Neuroscience.

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

[40]  A. S. French,et al.  Na+-Dependent neuritic spikes initiate Ca2+-dependent somatic plateau action potentials in insect dorsal paired median neurons. , 1998, Journal of neurophysiology.

[41]  D. Sattelle,et al.  Novel putative nicotinic acetylcholine receptor subunit genes, Dalpha5, Dalpha6 and Dalpha7, in Drosophila melanogaster identify a new and highly conserved target of adenosine deaminase acting on RNA-mediated A-to-I pre-mRNA editing. , 2002, Genetics.

[42]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.

[43]  Y. Hamasaka,et al.  γ‐Aminobutyric acid (GABA) signaling components in Drosophila: Immunocytochemical localization of GABAB receptors in relation to the GABAA receptor subunit RDL and a vesicular GABA transporter , 2007, The Journal of comparative neurology.

[44]  Andreas Prokop,et al.  Are dendrites in Drosophila homologous to vertebrate dendrites? , 2005, Developmental biology.

[45]  Fengqiu Diao,et al.  Fast inactivation of Shal (Kv4) K+ channels is regulated by the novel interactor SKIP3 in Drosophila neurons , 2009, Molecular and Cellular Neuroscience.

[46]  Carsten Duch,et al.  Activity Affects Dendritic Shape and Synapse Elimination during Steroid Controlled Dendritic Retraction in Manduca sexta , 2004, The Journal of Neuroscience.

[47]  Matthew N. Rasband,et al.  The axon initial segment and the maintenance of neuronal polarity , 2010, Nature Reviews Neuroscience.

[48]  Vann Bennett,et al.  A Common Ankyrin-G-Based Mechanism Retains KCNQ and NaV Channels at Electrically Active Domains of the Axon , 2006, The Journal of Neuroscience.

[49]  Ronald L. Davis,et al.  GABAA Receptor RDL Inhibits Drosophila Olfactory Associative Learning , 2007, Neuron.

[50]  M L Hines,et al.  Neuron: A Tool for Neuroscientists , 2001, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[51]  A. S. French,et al.  Immunocytochemical localization of sodium channels in an insect central nervous system using a site-directed antibody. , 1993, Journal of neurobiology.

[52]  R. Levine,et al.  Cav2 channels mediate low and high voltage‐activated calcium currents in Drosophila motoneurons , 2012, The Journal of physiology.

[53]  Alexander Borst,et al.  Synaptic organization of lobula plate tangential cells in Drosophila: γ‐Aminobutyric acid receptors and chemical release sites , 2007, The Journal of comparative neurology.

[54]  C. Duch,et al.  A steroid hormone affects sodium channel expression in Manduca central neurons , 2006, Cell and Tissue Research.

[55]  R. Harris-Warrick,et al.  Differential expression and targeting of K+ channel genes in the lobster pyloric central pattern generator. , 1998, Annals of the New York Academy of Sciences.

[56]  K. Ikeda,et al.  Morphological identification of the motor neurons innervating the dorsal longitudinal flight muscle of Drosophila melanogaster , 1988, The Journal of comparative neurology.

[57]  C Duch,et al.  Remodeling of Membrane Properties and Dendritic Architecture Accompanies the Postembryonic Conversion of a Slow into a Fast Motoneuron , 2000, The Journal of Neuroscience.

[58]  R. Wyman,et al.  Output pattern generation by Drosophila flight motoneurons. , 1977, Journal of neurophysiology.

[59]  Bartlett W. Mel,et al.  Dendrites: bug or feature? , 2003, Current Opinion in Neurobiology.

[60]  Jan Felix Evers,et al.  Developmental changes in dendritic shape and synapse location tune single-neuron computations to changing behavioral functions. , 2009, Journal of neurophysiology.

[61]  E. Giniger,et al.  Cdk5 Regulates the Size of an Axon Initial Segment-Like Compartment in Mushroom Body Neurons of the Drosophila Central Brain , 2011, The Journal of Neuroscience.

[62]  Y. Okamura,et al.  Ion Channel Clustering at the Axon Initial Segment and Node of Ranvier Evolved Sequentially in Early Chordates , 2008, PLoS genetics.

[63]  G. Matthews,et al.  Polarized distribution of ion channels within microdomains of the axon initial segment , 2007, The Journal of comparative neurology.

[64]  Stephan J. Sigrist,et al.  Bruchpilot, a Protein with Homology to ELKS/CAST, Is Required for Structural Integrity and Function of Synaptic Active Zones in Drosophila , 2006, Neuron.

[65]  Michael H Dickinson,et al.  Role of calcium in the regulation of mechanical power in insect flight. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[66]  F. Vonhoff,et al.  Tiling among stereotyped dendritic branches in an identified Drosophila motoneuron , 2010, The Journal of comparative neurology.

[67]  Kendal Broadie,et al.  Activity-dependent development of the neuromuscular synapse during drosophila embryogenesis , 1993, Neuron.

[68]  C. Duch,et al.  Shaker and Shal mediate transient calcium-independent potassium current in a Drosophila flight motoneuron. , 2009, Journal of neurophysiology.

[69]  C. Duch,et al.  Average shape standard atlas for the adult Drosophila ventral nerve cord , 2010, The Journal of comparative neurology.

[70]  D. Amaral,et al.  Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat , 1990, The Journal of comparative neurology.

[71]  Robert M. Brownstone,et al.  Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior , 2003, Trends in Neurosciences.

[72]  M. London,et al.  Dendritic computation. , 2005, Annual review of neuroscience.

[73]  M. Rosbash,et al.  Modulation of GABAA receptor desensitization uncouples sleep onset and maintenance in Drosophila , 2008, Nature Neuroscience.

[74]  M. Scanziani,et al.  Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition , 2001, Science.

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