How does morphology relate to function in sensory arbors?

Sensory dendrites fall into many different morphological and functional classes. Polymodal nociceptors are one subclass of sensory neurons, which are of particular note owing to their elaborate dendritic arbors. Complex developmental programs are required to form these arbors and there is striking conservation of morphology, function and molecular determinants between vertebrate and invertebrate polymodal nociceptors. Based on these studies, we argue that arbor morphology plays an important role in the function of polymodal nociceptors. Similar associations between form and function might explain the plethora of dendrite morphologies seen among all sensory neurons.

[1]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[2]  Y. Jan,et al.  Genes regulating dendritic outgrowth, branching, and routing in Drosophila. , 1999, Genes & development.

[3]  M. Chalfie,et al.  Extracellular Proteins Needed for C. elegans Mechanosensation , 1996, Neuron.

[4]  H. E. Torebjörk,et al.  Innervation territories of mechano-insensitive C nociceptors in human skin. , 2002, Journal of neurophysiology.

[5]  M. Chalfie,et al.  Organization of neuronal microtubules in the nematode Caenorhabditis elegans , 1979, The Journal of cell biology.

[6]  Gilles Laurent,et al.  painless, a Drosophila Gene Essential for Nociception , 2003, Cell.

[7]  Zaven Kaprielian,et al.  C. elegans bicd-1, homolog of the Drosophila dynein accessory factor Bicaudal D, regulates the branching of PVD sensory neuron dendrites , 2011, Development.

[8]  E. Perl.  Chapter 2. Cutaneous polymodal receptors: characteristics and plasticity , 1996 .

[9]  Y. Jan,et al.  Growing Dendrites and Axons Differ in Their Reliance on the Secretory Pathway , 2007, Cell.

[10]  Yukako Hattori,et al.  Selective expression of Knot/Collier, a transcriptional regulator of the EBF/Olf‐1 family, endows the Drosophila sensory system with neuronal class‐specific elaborated dendritic patterns , 2007, Genes to cells : devoted to molecular & cellular mechanisms.

[11]  N. Cauna.  The free penicillate nerve endings of the human hairy skin. , 1973, Journal of anatomy.

[12]  M. Chalfie,et al.  The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. , 1989, Genes & development.

[13]  E. Smith,et al.  Nociceptors: a phylogenetic view , 2009, Journal of Comparative Physiology A.

[14]  G. Tavosanis,et al.  Slit and Robo regulate dendrite branching and elongation of space-filling neurons in Drosophila. , 2008, Developmental biology.

[15]  D. Satoh,et al.  Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes , 2008, Nature Cell Biology.

[16]  Tzumin Lee,et al.  Drosophila Sensory Neurons Require Dscam for Dendritic Self-Avoidance and Proper Dendritic Field Organization , 2007, Neuron.

[17]  Miriam B Goodman,et al.  Nanoscale Organization of the MEC-4 DEG/ENaC Sensory Mechanotransduction Channel in Caenorhabditis elegans Touch Receptor Neurons , 2007, The Journal of Neuroscience.

[18]  Y. Jan,et al.  The Coiled-Coil Protein Shrub Controls Neuronal Morphogenesis in Drosophila , 2006, Current Biology.

[19]  Feng Zhang,et al.  Nociceptive Neurons Protect Drosophila Larvae from Parasitoid Wasps , 2007, Current Biology.

[20]  E. Perl,et al.  Fine structure of myelinated mechanical nociceptor endings in cat hairy skin , 1981, The Journal of comparative neurology.

[21]  A. Patapoutian,et al.  TRPA1 Contributes to Cold Hypersensitivity , 2010, The Journal of Neuroscience.

[22]  G. Stent,et al.  Developmental arborization of sensory neurons in the leech Haementeria ghilianii. I. Origin of natural variations in the branching pattern , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  Y. Jan,et al.  Different Levels of the Homeodomain Protein Cut Regulate Distinct Dendrite Branching Patterns of Drosophila Multidendritic Neurons , 2003, Cell.

[24]  Wendy M. Knowlton,et al.  TRPM8, but not TRPA1, is required for neural and behavioral responses to acute noxious cold temperatures and cold-mimetics in vivo , 2010, PAIN.

[25]  Rajesh Ranganathan,et al.  C. elegans Locomotory Rate Is Modulated by the Environment through a Dopaminergic Pathway and by Experience through a Serotonergic Pathway , 2000, Neuron.

[26]  P. McIntyre,et al.  A TRP Channel that Senses Cold Stimuli and Menthol , 2002, Cell.

[27]  J. Sulston,et al.  Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. , 1981, Developmental biology.

[28]  C. Woolf,et al.  Sensory innervation of the hairs of the rat hindlimb: A light microscopic analysis , 1988, The Journal of comparative neurology.

[29]  W. Schafer,et al.  Lateral Facilitation between Primary Mechanosensory Neurons Controls Nose Touch Perception in C. elegans , 2011, Neuron.

[30]  Ellen A. Lumpkin,et al.  Mechanisms of sensory transduction in the skin , 2007, Nature.

[31]  L. Looger,et al.  Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall , 2010, Nature.

[32]  Manuela Schmidt,et al.  Piezo1 and Piezo2 Are Essential Components of Distinct Mechanically Activated Cation Channels , 2010, Science.

[33]  R. Yuste,et al.  Linear Summation of Excitatory Inputs by CA1 Pyramidal Neurons , 1999, Neuron.

[34]  D. McKemy,et al.  Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1 , 2004, Nature.

[35]  M. Lazdunski,et al.  Knockout of the ASIC2 channel in mice does not impair cutaneous mechanosensation, visceral mechanonociception and hearing , 2004, The Journal of physiology.

[36]  D. Corey,et al.  Transport and Localization of the DEG/ENaC Ion Channel BNaC1α to Peripheral Mechanosensory Terminals of Dorsal Root Ganglia Neurons , 2001, The Journal of Neuroscience.

[37]  D. McKemy,et al.  Identification of a cold receptor reveals a general role for TRP channels in thermosensation , 2002, Nature.

[38]  W. Schafer,et al.  Caenorhabditis elegans TRPA-1 functions in mechanosensation , 2007, Nature Neuroscience.

[39]  Control of dendritic development by the Drosophila fragile X-related gene involves the small GTPase Rac1 , 2003, Development.

[40]  I. Parnas,et al.  Physiological responses, receptive fields and terminal arborizations of nociceptive cells in the leech. , 1982, The Journal of physiology.

[41]  John B. Thomas,et al.  A sensory feedback circuit coordinates muscle activity in Drosophila , 2007, Molecular and Cellular Neuroscience.

[42]  Jay Z. Parrish,et al.  The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance , 2006, Nature.

[43]  M. Häusser,et al.  The single dendritic branch as a fundamental functional unit in the nervous system , 2010, Current Opinion in Neurobiology.

[44]  David Julius,et al.  TRPA1 Mediates the Inflammatory Actions of Environmental Irritants and Proalgesic Agents , 2006, Cell.

[45]  M. Chalfie,et al.  mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans , 1988, Cell.

[46]  S. Cajal,et al.  Histology of the Nervous System , 1911 .

[47]  W. Schafer,et al.  Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors , 2010, Nature Neuroscience.

[48]  M. Galko,et al.  Cytokine Signaling Mediates UV-Induced Nociceptive Sensitization in Drosophila Larvae , 2009, Current Biology.

[49]  William R. Schafer,et al.  C. elegans TRP Family Protein TRP-4 Is a Pore-Forming Subunit of a Native Mechanotransduction Channel , 2010, Neuron.

[50]  Huajun Wang,et al.  The Establishment of Peripheral Sensory Arbors in the Leech:In Vivo Time-Lapse Studies Reveal a Highly Dynamic Process , 1997, The Journal of Neuroscience.

[51]  J Rinzel,et al.  Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. , 1973, Biophysical journal.

[52]  M. Treinin,et al.  Mutations in the extracellular domain and in the membrane-spanning domains interfere with nicotinic acetylcholine receptor maturation. , 2002, Biochemistry.

[53]  J. N. Thomson,et al.  Mutant sensory cilia in the nematode Caenorhabditis elegans. , 1986, Developmental biology.

[54]  L. Avery,et al.  LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. elegans nervous system. , 2003, Developmental biology.

[55]  C. Belmonte,et al.  Properties of the nociceptive neurons of the leech segmental ganglion. , 1996, Journal of neurophysiology.

[56]  S. Weintraub,et al.  Heat generates oxidized linoleic acid metabolites that activate TRPV1 and produce pain in rodents. , 2010, The Journal of clinical investigation.

[57]  C. Montell,et al.  Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade , 2008, Nature Neuroscience.

[58]  M. Chalfie,et al.  MEC-2 regulates C. elegans DEG/ENaC channels needed for mechanosensation , 2002, Nature.

[59]  Dror G. Feitelson,et al.  C. elegans multi-dendritic sensory neurons: Morphology and function , 2011, Molecular and Cellular Neuroscience.

[60]  A I Basbaum,et al.  Impaired nociception and pain sensation in mice lacking the capsaicin receptor. , 2000, Science.

[61]  Lily Yeh Jan,et al.  Branching out: mechanisms of dendritic arborization , 2010, Nature Reviews Neuroscience.

[62]  Rachel I. Wilson,et al.  The Force Be With You: A Mechanoreceptor Channel in Proprioception and Touch , 2010, Neuron.

[63]  K. Messlinger.  Functional morphology of nociceptive and other fine sensory endings (free nerve endings) in different tissues. , 1996, Progress in brain research.

[64]  D. Hall,et al.  The Fusogen EFF-1 Controls Sculpting of Mechanosensory Dendrites , 2010, Science.

[65]  K. Nagata,et al.  Nociceptor and Hair Cell Transducer Properties of TRPA1, a Channel for Pain and Hearing , 2005, The Journal of Neuroscience.

[66]  H. Horvitz,et al.  A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[67]  M. Kondo,et al.  Homophilic Dscam Interactions Control Complex Dendrite Morphogenesis , 2007, Neuron.

[68]  Bernd Nilius,et al.  TRPM3 Is a Nociceptor Channel Involved in the Detection of Noxious Heat , 2011, Neuron.

[69]  S. Blackshaw.  Morphology and distribution of touch cell terminals in the skin of the leech. , 1981, The Journal of physiology.

[70]  E. Perl,et al.  Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. , 1969, Journal of neurophysiology.

[71]  M. Caterina,et al.  Nociceptors Lacking TRPV1 and TRPV2 Have Normal Heat Responses , 2004, The Journal of Neuroscience.

[72]  Cori Bargmann,et al.  OSM-9, A Novel Protein with Structural Similarity to Channels, Is Required for Olfaction, Mechanosensation, and Olfactory Adaptation inCaenorhabditis elegans , 1997, The Journal of Neuroscience.

[73]  M. Chalfie,et al.  The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals , 2005, Nature Neuroscience.

[74]  A. Moqrich,et al.  TRPV3 in keratinocytes transmits temperature information to sensory neurons via ATP , 2009, Pflügers Archiv - European Journal of Physiology.

[75]  Kara L. Marshall,et al.  The cell biology of touch , 2010, The Journal of cell biology.

[76]  Ramanathan Arvind,et al.  Knot/Collier and Cut Control Different Aspects of Dendrite Cytoskeleton and Synergize to Define Final Arbor Shape , 2007, Neuron.

[77]  E. Jorgensen,et al.  The C.elegans ric‐3 gene is required for maturation of nicotinic acetylcholine receptors , 2002, The EMBO journal.

[78]  G. Stent,et al.  Developmental arborization of sensory neurons in the leech Haementeria ghilianii. II. Experimentally induced variations in the branching pattern , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  A. Coulson,et al.  mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. , 1989, Genes & development.

[80]  Yuh Nung Jan,et al.  Tiling of the Drosophila epidermis by multidendritic sensory neurons. , 2002, Development.

[81]  Y. Jan,et al.  Control of Dendritic Branching and Tiling by the Tricornered-Kinase/Furry Signaling Pathway in Drosophila Sensory Neurons , 2004, Cell.

[82]  R. Meyer,et al.  Electrophysiological assessment of the cutaneous arborization of Adelta-fiber nociceptors. , 1999, Journal of neurophysiology.

[83]  M. Gold,et al.  Nociceptor sensitization in pain pathogenesis , 2010, Nature Medicine.

[84]  P. Sternberg,et al.  A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue , 2006, Nature.

[85]  David H. Hall,et al.  C. elegans Atlas , 2008 .

[86]  Millet Treinin,et al.  Time-lapse imaging and cell-specific expression profiling reveal dynamic branching and molecular determinants of a multi-dendritic nociceptor in C. elegans. , 2010, Developmental biology.

[87]  E. Mccleskey,et al.  Cell damage excites nociceptors through release of cytosolic ATP , 2002, Pain.

[88]  Richard Y. Hwang,et al.  Pickpocket Is a DEG/ENaC Protein Required for Mechanical Nociception in Drosophila Larvae , 2010, Current Biology.

[89]  J. C. Clemens,et al.  Dendrite Self-Avoidance Is Controlled by Dscam , 2007, Cell.

[90]  D. Cockayne,et al.  Acid‐sensing ion channels ASIC2 and ASIC3 do not contribute to mechanically activated currents in mammalian sensory neurones , 2004, The Journal of physiology.

[91]  Peter McIntyre,et al.  ANKTM1, a TRP-like Channel Expressed in Nociceptive Neurons, Is Activated by Cold Temperatures , 2003, Cell.

[92]  H. Handwerker,et al.  Bradykinin and serotonin effects on various types of cutaneous nerve fibres , 1974, Pflügers Archiv.

[93]  David Julius,et al.  The menthol receptor TRPM8 is the principal detector of environmental cold , 2007, Nature.

[94]  W. A. Johnson,et al.  Ripped Pocket and Pickpocket, Novel Drosophila DEG/ENaC Subunits Expressed in Early Development and in Mechanosensory Neurons , 1998, The Journal of cell biology.

[95]  Cori Bargmann,et al.  Combinatorial Expression of TRPV Channel Proteins Defines Their Sensory Functions and Subcellular Localization in C. elegans Neurons , 2002, Neuron.