Identifying local and descending inputs for primary sensory neurons

Journal of Clinical Investigation

Volumn 125, Issue 10, 2015, Pages 3782-3794

  Zhang, Yi ^a   Zhao, Shengli ^a   Rodriguez, Erica ^a   Takatoh, Jun ^a   Han, Bao Xia ^a   Zhou, Xiang ^b   Wang, Fan ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ENKEPHALIN; 4 AMINOBUTYRIC ACID RECEPTOR; NERVE PROTEIN;

ADULT; ANIMAL CELL; ARTICLE; BRAIN REGION; CONTROLLED STUDY; GANGLION; HEAT; MECHANICAL STIMULATION; MOUSE; NONHUMAN; PAIN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RABIES VIRUS; ROSTROVENTRAL MEDULLA; SENSORY NERVE CELL; SENSORY STIMULATION; SEROTONINERGIC NERVE CELL; SPINAL CORD; SPINAL CORD DORSAL HORN; TOUCH; ANIMAL; CLASSIFICATION; CYTOLOGY; EFFERENT NERVE; FORELIMB; HYPERALGESIA; INNERVATION; INTERNEURON; NERVE CELL NETWORK; NERVE CONDUCTION; NERVE ENDING; NOCICEPTION; PAIN RECEPTOR; PATHOPHYSIOLOGY; PHYSIOLOGY; POSTERIOR HORN CELL; SATELLITE VIRUS; SENSORY NERVE; SKIN; SPINAL GANGLION; ULTRASTRUCTURE; VIROLOGY; VIRUS REPLICATION;

AFFERENT PATHWAYS; ANIMALS; DEFECTIVE VIRUSES; EFFERENT PATHWAYS; ENKEPHALINS; FORELIMB; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; GANGLIA, SPINAL; HYPERALGESIA; INTERNEURONS; NERVE NET; NERVE TISSUE PROTEINS; NEURAL CONDUCTION; NEURONS, AFFERENT; NEURONS, EFFERENT; NOCICEPTION; NOCICEPTORS; POSTERIOR HORN CELLS; PRESYNAPTIC TERMINALS; RABIES VIRUS; SENSORY RECEPTOR CELLS; SKIN; SPINAL CORD DORSAL HORN; VIRUS REPLICATION;

EID: 84943254180     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI81156     Document Type: Article

References (79)

1. Prescott SA, Ratte S. Pain processing by spinal microcircuits: afferent combinatorics. Curr Opin Neurobiol. 2012;22(4):631-639.
2. Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell. 2009;139(2):267-284.
3. Braz J, Solorzano C, Wang X, Basbaum AI. Transmitting pain and itch messages: a contemporary view of the spinal cord circuits that generate gate control. Neuron. 2014;82(3):522-536.
4. Todd AJ. Neuronal circuitry for pain processing in the dorsal horn. Nat Rev Neurosci. 2010;11(12):823-836.
5. Ribeiro-da-Silva A, Coimbra A. Two types of synaptic glomeruli and their distribution in laminae I-III of the rat spinal cord. J Comp Neurol. 1982;209(2):176-186.
6. Rethelyi M, Light AR, Perl ER. Synaptic complexes formed by functionally defined primary afferent units with fine myelinated fibers. J Comp Neurol. 1982;207(4):381-393.
7. Todd AJ. GABA and glycine in synaptic glomeruli of the rat spinal dorsal horn. Eur J Neurosci. 1996;8(12):2492-2498.
8. Rudomin P, Engberg I, Jimenez I. Mechanisms involved in presynaptic depolarization of group I and rubrospinal fibers in cat spinal cord. J Neurophysiol. 1981;46(3):532-548.
9. Kullmann DM, Ruiz A, Rusakov DM, Scott R, Semyanov A, Walker MC. Presynaptic, extrasynaptic and axonal GABAA receptors in the CNS: where and why? Prog Biophys Mol Biol. 2005;87(1):33-46.
10. Witschi R, et al. Presynaptic α2-GABAA receptors in primary afferent depolarization and spinal pain control. J Neurosci. 2011;31(22):8134-8142.
11. Wall PD. The laminar organization of dorsal horn and effects of descending impulses. J Physiol. 1967;188(3):403-423.
12. Oliveras JL, Besson JM, Guilbaud G, Liebeskind JC. Behavioral and electrophysiological evidence of pain inhibition from midbrain stimulation in the cat. Exp Brain Res. 1974;20(1):32-44.
13. Oliveras JL, Redjemi F, Guilbaud G, Besson JM. Analgesia induced by electrical stimulation of the inferior centralis nucleus of the raphe in the cat. Pain. 1975;1(2):139-145.
14. Reynolds DV. Surgery in the rat during electrical analgesia induced by focal brain stimulation. Science. 1969;164(3878):444-445.
15. Liebeskind JC, Guilbaud G, Besson JM, Oliveras JL. Analgesia from electrical stimulation of the periaqueductal gray matter in the cat: behavioral observations and inhibitory effects on spinal cord interneurons. Brain Res. 1973;50(2):441-446.
16. Heinricher MM, Tavares I, Leith JL, Lumb BM. Descending control of nociception: Specificity, recruitment and plasticity. Brain Res Rev. 2009;60(1):214-225.
17. Ossipov MH, Dussor GO, Porreca F. Central modulation of pain. J Clin Invest. 2010;120(11):3779-3787.
18. Fields HL, Bry J, Hentall I, Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci. 1983;3(12):2545-2552.
19. Mason P. Central mechanisms of pain modulation. Curr Opin Neurobiol. 1999;9(4):436-441.
20. Gebhart GF. Descending modulation of pain. Neurosci Biobehav Rev. 2004;27(8):729-737.
21. Budai D, Fields HL. Endogenous opioid peptides acting at mu-opioid receptors in the dorsal horn contribute to midbrain modulation of spinal nociceptive neurons. J Neurophysiol. 1998;79(2):677-687.
22. Wickersham IR, et al. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron. 2007;53(5):639-647.
23. Callaway EM. Transneuronal circuit tracing with neurotropic viruses. Curr Opin Neurobiol. 2008;18(6):617-623.
24. Tsiang H, Lycke E, Ceccaldi PE, Ermine A, Hirardot X. The anterograde transport of rabies virus in rat sensory dorsal root ganglia neurons. J Gen Virol. 1989;70(pt 8):2075-2085.
25. Zampieri N, Jessell TM, Murray AJ. Mapping sensory circuits by anterograde transsynaptic transfer of recombinant rabies virus. Neuron. 2014;81(4):766-778.
26. Coulon P, Derbin C, Kucera P, Lafay F, Prehaud C, Flamand A. Invasion of the peripheral nervous systems of adult mice by the CVS strain of rabies virus and its avirulent derivative AvO1. J Virol. 1989;63(8):3550-3554.
27. Stanek E IV, Cheng S, Takatoh J, Han B-X, Wang F. Monosynaptic premotor circuit tracing reveals neural substrates for oro-motor coordination. Elife. 2014;3:e02511.
28. Takatoh J, et al. New modules are added to vibrissal premotor circuitry with the emergence of exploratory whisking. Neuron. 2013;77(2):346-360.
29. da Silva S, et al. Proper formation of whisker barrelettes requires periphery-derived Smad4-dependent TGF-β signaling. Proc Natl Acad Sci U S A. 2011;108(8):3395-3400.
30. Zhou X, et al. Deletion of PIK3C3/Vps34 in sensory neurons causes rapid neurodegeneration by disrupting the endosomal but not the autophagic pathway. Proc Natl Acad Sci U S A. 2010;107(20):9424-9429.
31. Mishra SK, Tisel SM, Orestes P, Bhangoo SK, Hoon MA. TRPV1-lineage neurons are required for thermal sensation. EMBO J. 2011;30(3):582-593.
32. Ribeiro-da-Silva A, Tagari P, Cuello AC. Morphological characterization of substance P-like immunoreactive glomeruli in the superficial dorsal horn of the rat spinal cord and trigeminal subnucleus caudalis: a quantitative study. J Comp Neurol. 1989;281(4):497-515.
33. Ugolini G. Advances in viral transneuronal tracing. J Neurosci Methods. 2010;194(1):2-20.
34. Rudy B, Fishell G, Lee S, Hjerling-Leffler J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol. 2011;71(1):45-61.
35. Duan B, et al. Identification of spinal circuits transmitting and gating mechanical pain. Cell. 2014;159(6):1417-1432.
36. Huang J, et al. Neurochemical properties of enkephalinergic neurons in lumbar spinal dorsal horn revealed by preproenkephalin-green fluorescent protein transgenic mice. J Neurochem. 2010;113(6):1555-1564.
37. Sardella TC, Polgar E, Watanabe M, Todd AJ. A quantitative study of neuronal nitric oxide synthase expression in laminae I-III of the rat spinal dorsal horn. Neuroscience. 2011;192:708-720.
38. Watkins LR, Suberg SN, Thurston CL, Culhane ES. Role of spinal cord neuropeptides in pain sensitivity and analgesia: thyrotropin releasing hormone and vasopressin. Brain Res. 1986;362(2):308-317.
39. Freire MA, Guimaraes JS, Leal WG, Pereira A. Pain modulation by nitric oxide in the spinal cord. Front Neurosci. 2009;3(2):175-181.
40. Fields H. State-dependent opioid control of pain. Nat Rev Neurosci. 2004;5(7):565-575.
41. Marinelli S, Vaughan CW, Schnell SA, Wessendorf MW, Christie MJ. Rostral ventromedial medulla neurons that project to the spinal cord express multiple opioid receptor phenotypes. J Neurosci. 2002;22(24):10847-10855.
42. Antal M, Petko M, Polgar E, Heizmann CW, Storm-Mathisen J. Direct evidence of an extensive GABAergic innervation of the spinal dorsal horn by fibres descending from the rostral ventromedial medulla. Neuroscience. 1996;73(2):509-518.
43. Fields HL, Malick A, Burstein R. Dorsal horn projection targets of ON and OFF cells in the rostral ventromedial medulla. J Neurophysiol. 1995;74(4):1742-1759.
44. Mason P, Fields HL. Axonal trajectories and terminations of on-and off-cells in the cat lower brainstem. J Comp Neurol. 1989;288(2):185-207.
45. Adamantidis AR, Zhang F, de Lecea L, Deisseroth K. Optogenetics: opsins and optical interfaces in neuroscience. Cold Spring Harb Protoc. 2014;2014(8):815-822.
46. Rudomin P, Schmidt RF. Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res. 1999;129(1):1-37.
47. Alvarez-Leefmans FJ. Chloride transporters in presynaptic inhibition, pain and neurogenic inflammation. In: Alvarez-Leefmans F, Delpire E, eds. Physiology and Pathology of Chloride Transporters and Channels in the Nervous System: From Molecules to Diseases. San Diego, California, USA: Elsevier-Academic Press; 2009:439-470.
48. Link E, et al. Tetanus toxin action: inhibition of neurotransmitter release linked to synaptobrevin proteolysis. Biochem Biophys Res Commun. 1992;189(2):1017-1023.
49. Schiavo G, et al. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature. 1992;359(6398):832-835.
50. Navone F, Di Gioia G, Jahn R, Browning M, Greengard P, De Camilli P. Microvesicles of the neurohypophysis are biochemically related to small synaptic vesicles of presynaptic nerve terminals. J Cell Biol. 1989;109(6 pt 2):3425-3433.
51. Sweeney ST, Broadie K, Keane J, Niemann H, O'Kane CJ. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron. 1995;14(2):341-351.
52. Jones BE, Holmes CJ, Rodriguezveiga E, Mainville L. GABA-synthesizing neurons in the medulla: their relationship to serotonin-containing and spinally projecting neurons in the rat. J Comp Neurol. 1991;313(2):349-367.
53. Yang CF, et al. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell. 2013;153(4):896-909.
54. Alexander GM, et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron. 2009;63(1):27-39.
55. Schnell MJ, McGettigan JP, Wirblich C, Papaneri A. The cell biology of rabies virus: using stealth to reach the brain. Nat Rev Microbiol. 2010;8(1):51-61.
56. Pagadala P, et al. Loss of NR1 subunit of NMDARs in primary sensory neurons leads to hyperexcitability and pain hypersensitivity: involvement of Ca(2+)-activated small conductance potassium channels. J Neurosci. 2013;33(33):13425-13430.
57. Kung LH, et al. Evidence for glutamate as a neuroglial transmitter within sensory ganglia. PLoS One. 2013;8(7):e68312.
58. Bráz JM, Ackerman L, Basbaum AI. Sciatic nerve transection triggers release and intercellular transfer of a genetically expressed macromolecular tracer in dorsal root ganglia. J Comp Neurol. 2011;519(13):2648-2657.
59. Zhang X, Chen Y, Wang C, Huang LY. Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc Natl Acad Sci U S A. 2007;104(23):9864-9869.
60. Ceruti S, et al. Calcitonin gene-related peptidemediated enhancement of purinergic neuron/glia communication by the algogenic factor bradykinin in mouse trigeminal ganglia from wild-type and R192Q Cav2.1 Knock-in mice: implications for basic mechanisms of migraine pain. J Neurosci. 2011;31(10):3638-3649.
61. Purkiss J, Welch M, Doward S, Foster K. Capsaicin-stimulated release of substance P from cultured dorsal root ganglion neurons: involvement of two distinct mechanisms. Biochem Pharmacol. 2000;59(11):1403-1406.
62. Hathway GJ, Vega-Avelaira D, Fitzgerald M. A critical period in the supraspinal control of pain: Opioid-dependent changes in brainstem rostroventral medulla function in preadolescence. Pain. 2012;153(4):775-783.
63. Lee CJ, et al. Functional expression of AMPA receptors on central terminals of rat dorsal root ganglion neurons and presynaptic inhibition of glutamate release. Neuron. 2002;35(1):135-146.
64. Lorenzo LE, et al. Gephyrin clusters are absent from small diameter primary afferent terminals despite the presence of GABA(A) receptors. J Neurosci. 2014;34(24):8300-8317.
65. Wei F, et al. Molecular depletion of descending serotonin unmasks its novel facilitatory role in the development of persistent pain. J Neurosci. 2010;30(25):8624-8636.
66. Kim YS, et al. Central terminal sensitization of TRPV1 by descending serotonergic facilitation modulates chronic pain. Neuron. 2014;81(4):873-887.
67. Duggan AW, Hall JG, Headley PM. Morphine, enkephalin and the substantia gelatinosa. Nature. 1976;264(5585):456-458.
68. Besse D, Lombard MC, Besson JM. Autoradiographic distribution of mu, delta and kappa opioid binding sites in the superficial dorsal horn, over the rostrocaudal axis of the rat spinal cord. Brain Res. 1991;548(1-2):287-291.
69. Arvidsson U, et al. delta-Opioid receptor immunoreactivity: distribution in brainstem and spinal cord, and relationship to biogenic amines and enkephalin. J Neurosci. 1995;15(2):1215-1235.
70. Arvidsson U, et al. Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. J Neurosci. 1995;15(5 pt 1):3328-3341.
71. Mansour A, Fox CA, Burke S, Akil H, Watson SJ. Immunohistochemical localization of the cloned mu opioid receptor in the rat CNS. J Chem Neuroanat. 1995;8(4):283-305.
72. Rudomin P, Lomeli J, Quevedo J. Tonic differential supraspinal modulation of PAD and PAH of segmental and ascending intraspinal collaterals of single group I muscle afferents in the cat spinal cord. Exp Brain Res. 2004;159(2):239-250.
73. Scherrer G, et al. Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell. 2009;137(6):1148-1159.
74. Bardoni R, et al. Delta opioid receptors presynaptically regulate cutaneous mechanosensory neuron input to the spinal cord dorsal horn. Neuron. 2014;81(6):1312-1327.
75. Fields HL, Bry J, Hentall I, Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci. 1983;3(12):2545-2552.
76. Cerri M, et al. The inhibition of neurons in the central nervous pathways for thermoregulatory cold defense induces a suspended animation state in the rat. J Neurosci. 2013;33(7):2984-2993.
77. Arenkiel BR, et al. Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS One. 2011;6(12):e29423.
78. Osakada F, Callaway EM. Design and generation of recombinant rabies virus vectors. Nat Protoc. 2013;8(8):1583-1601.
79. Wall NR, Wickersham IR, Cetin A, De La Parra M, Callaway EM. Monosynaptic circuit tracing in vivo through Cre-dependent targeting and complementation of modified rabies virus. Proc Natl Acad Sci U S A. 2010;107(50):21848-21853.