Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn

Journal of Physiology

Volumn 592, Issue 4, 2014, Pages 759-776

  Punnakkal, Pradeep ^a,c   von Schoultz, Carolin ^a,b   Haenraets, Karen ^a,b   Wildner, Hendrik ^a   Zeilhofer, Hanns Ulrich ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c SREE CHITRA TIRUNAL INSTITUTE FOR MEDICAL SCIENCES AND TECHNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIALS; ANIMALS; GABAERGIC NEURONS; INTERNEURONS; MICE; POSTERIOR HORN CELLS; SYNAPSES; SYNAPTIC POTENTIALS;

EID: 84894095373     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.264937     Document Type: Article

References (64)

1. 2 selectively blocks inhibitory glycinergic neurotransmission onto rat superficial dorsal horn neurons. Nat Neurosci 5, 34-40.
2. Al-Khater KM, Kerr R & Todd AJ (2008). A quantitative study of spinothalamic neurons in laminae I, III, and IV in lumbar and cervical segments of the rat spinal cord. J Comp Neurol 511, 1-18.
3. Alvarez FJ, Villalba RM, Zerda R & Schneider SP (2004). Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses. J Comp Neurol 472, 257-280.
4. 3H-d-aspartate in the dorsal horn of the rat spinal cord. J Comp Neurol 314, 114-124.
5. Baba H, Ji RR, Kohno T, Moore KA, Ataka T, Wakai A, Okamoto M & Woolf CJ (2003). Removal of GABAergic inhibition facilitates polysynaptic A fibre-mediated excitatory transmission to the superficial spinal dorsal horn. Mol Cell Neurosci 24, 818-830.
6. Barber RP, Vaughn JE & Roberts E (1982). The cytoarchitecture of GABAergic neurons in rat spinal cord. Brain Res 238, 305-328.
7. Celio MR (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375-475.
8. Chaudhry FA, Boulland JL, Jenstad M, Bredahl MK & Edwards RH (2008). Pharmacology of neurotransmitter transport into secretory vesicles. Handb Exp Pharmacol, 77-106.
9. Cheng L, Arata A, Mizuguchi R, Qian Y, Karunaratne A, Gray PA, Arata S, Shirasawa S, Bouchard M, Luo P, Chen CL, Busslinger M, Goulding M, Onimaru H & Ma Q (2004). Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat Neurosci 7, 510-517.
10. A receptor-mediated IPSCs in identified lamina I neurons of the adult rat spinal cord. J Neurosci 19, 7342-7355.
11. Cui L, Kim YR, Kim HY, Lee SC, Shin HS, Szabo G, Erdelyi F, Kim J & Kim SJ (2011). Modulation of synaptic transmission from primary afferents to spinal substantia gelatinosa neurons by group III mGluRs in GAD65-EGFP transgenic mice. J Neurophysiol 105, 1102-1111.
12. Daniele CA & MacDermott AB (2009). Low-threshold primary afferent drive onto GABAergic interneurons in the superficial dorsal horn of the mouse. J Neurosci 29, 686-695.
13. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
14. Gassner M, Ruscheweyh R & Sandkühler J (2009). Direct excitation of spinal GABAergic interneurons by noradrenaline. Pain 145, 204-210.
15. Gobel S (1975). Golgi studies in the substantia gelatinosa neurons in the spinal trigeminal nucleus. J Comp Neurol 162, 397-415.
16. Gobel S (1978). Golgi studies of the neurons in layer II of the dorsal horn of the medulla (trigeminal nucleus caudalis). J Comp Neurol 180, 395-413.
17. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME & Heintz N (2003). A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425, 917-925.
18. Graham BA, Brichta AM & Callister RJ (2007). Moving from an averaged to specific view of spinal cord pain processing circuits. J Neurophysiol 98, 1057-1063.
19. Grudt TJ & Perl ER (2002). Correlations between neuronal morphology and electrophysiological features in the rodent superficial dorsal horn. J Physiol 540, 189-207.
20. Hantman AW, van den Pol AN & Perl ER (2004). Morphological and physiological features of a set of spinal substantia gelatinosa neurons defined by green fluorescent protein expression. J Neurosci 24, 836-842.
21. Heinke B, Ruscheweyh R, Forsthuber L, Wunderbaldinger G & Sandkühler J (2004). Physiological, neurochemical and morphological properties of a subgroup of GABAergic spinal lamina II neurones identified by expression of green fluorescent protein in mice. J Physiol 560, 249-266.
22. + channels primarily in excitatory neurons of the spinal dorsal horn. J Neurophysiol. 105, 3010-3021.
23. Hu J, Huang T, Li T, Guo Z & Cheng L (2012). c-Maf is required for the development of dorsal horn laminae III/IV neurons and mechanoreceptive DRG axon projections. J Neurosci 32, 5362-5373.
24. Kato A, Punnakkal P, Pernía-Andrade AJ, von Schoultz C, Sharopov S, Nyilas R, Katona I & Zeilhofer HU (2012). Endocannabinoid-dependent plasticity at spinal nociceptor synapses. J Physiol 590, 4717-4733.
25. Kim YH, Back SK, Davies AJ, Jeong H, Jo HJ, Chung G, Na HS, Bae YC, Kim SJ, Kim JS, Jung SJ & Oh SB (2012). TRPV1 in GABAergic interneurons mediates neuropathic mechanical allodynia and disinhibition of the nociceptive circuitry in the spinal cord. Neuron 74, 640-647.
26. Labrakakis C, Lorenzo LE, Bories C, Ribeiro-da-Silva A & De Koninck Y (2009). Inhibitory coupling between inhibitory interneurons in the spinal cord dorsal horn. Mol Pain 5, 24.
27. Littlewood NK, Todd AJ, Spike RC, Watt C, Shehab SA (1995). The types of neuron in spinal dorsal horn which possess neurokinin-1 receptors. Neuroscience 66, 597-608.
28. Lu Y, Dong H, Gao Y, Gong Y, Ren Y, Gu N, Zhou S, Xia N, Sun YY, Ji RR & Xiong L (2013). A feed-forward spinal cord glycinergic neural circuit gates mechanical allodynia. J Clin Invest. 123, 4050-4062.
29. Lu Y & Perl ER (2003). A specific inhibitory pathway between substantia gelatinosa neurons receiving direct C-fibre input. J Neurosci 23, 8752-8758.
30. Lu Y & Perl ER (2005). Modular organization of excitatory circuits between neurons of the spinal superficial dorsal horn (laminae I and II). J Neurosci 25, 3900-3907.
31. Mackie M, Hughes DI, Maxwell DJ, Tillakaratne NJ & Todd AJ (2003). Distribution and colocalisation of glutamate decarboxylase isoforms in the rat spinal cord. Neuroscience 119, 461-472.
32. McMahon SB & Wall PD (1985). Electrophysiological mapping of brainstem projections of spinal cord lamina I cells in the rat. Brain Res 333, 19-26.
33. Malet M, Vieytes CA, Lundgren KH, Seal RP, Tomasella E, Seroogy KB, Hökfelt T, Gebhart GF & Brumovsky PR (2013). Transcript expression of vesicular glutamate transporters in lumbar dorsal root ganglia and the spinal cord of mice - Effects of peripheral axotomy or hindpaw inflammation. Neuroscience 248, 95-111.
34. Maricich SM & Herrup K (1999). Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 41, 281-294.
35. Marshall GE, Shehab SA, Spike RC & Todd AJ (1996). Neurokinin-1 receptors on lumbar spinothalamic neurons in the rat. Neuroscience 72, 255-263.
36. Martin WJ, Liu H, Wang H, Malmberg AB & Basbaum AI (1999). Inflammation-induced up-regulation of protein kinase Cgamma immunoreactivity in rat spinal cord correlates with enhanced nociceptive processing. Neuroscience 88, 1267-1274.
37. Maxwell DJ, Belle MD, Cheunsuang O, Stewart A & Morris R (2007). Morphology of inhibitory and excitatory interneurons in superficial laminae of the rat dorsal horn. J Physiol 584, 521-533.
38. Melzack R & Wall PD (1965). Pain mechanisms: a new theory. Science 150, 971-979.
39. Moussaoui SM, Hermans E, Mathieu AM, Bonici B, Clerc F, Guinet F, Garret C & Laduron PM (1992). Polyclonal antibodies against the rat NK1 receptor: characterization and localization in the spinal cord. Neuroreport 3, 1073-1076.
40. Mullen RJ, Buck CR & Smith AM (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201-211.
41. Oliva AA Jr, Jiang M, Lam T, Smith KL & Swann JW (2000). Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20, 3354-3368.
42. Oliveira AL, Hydling F, Olsson E, Shi T, Edwards RH, Fujiyama F, Kaneko T, Hökfelt T, Cullheim S & Meister B (2003). Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root ganglia. Synapse 50, 117-129.
43. A receptor subtypes in mouse spinal dorsal horn neurons and primary afferents. J Comp Neurol 520, 3895-3911.
44. Pernía-Andrade AJ, Kato A, Witschi R, Nyilas R, Katona I, Freund TF, Watanabe M, Filitz J, Koppert W, Schüttler J, Ji G, Neugebauer V, Marsicano G, Lutz B, Vanegas H & Zeilhofer HU (2009). Spinal endocannabinoids and CB1 receptors mediate C-fibre-induced heterosynaptic pain sensitization. Science 325, 760-764.
45. Polgár E, Fowler JH, McGill MM & Todd AJ (1999). The types of neuron which contain protein kinase C gamma in rat spinal cord. Brain Res 833, 71-80.
46. Polgár E, Sardella TC, Tiong SY, Locke S, Watanabe M & Todd AJ (2013). Functional differences between neurochemically defined populations of inhibitory interneurons in the rat spinal dorsal horn. Pain 154, 2606-2615.
47. Rexed B (1952). The cytoarchitectonic organization of the spinal cord in the cat. J Comp Neurol 96, 414-495.
48. Rudomin P & Schmidt RF (1999). Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129, 1-37.
49. Schneider SP & Walker TM (2007). Morphology and electrophysiological properties of hamster spinal dorsal horn neurons that express VGLUT2 and enkephalin. J Comp Neurol 501, 790-809.
50. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K & Kaneko T (2003). Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467, 60-79.
51. Todd AJ (2010). Neuronal circuitry for pain processing in the dorsal horn. Nat Rev Neurosci 11, 823-836.
52. Todd AJ, Hughes DI, Polgár E, Nagy GG, Mackie M, Ottersen OP & Maxwell DJ (2003). The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17, 13-27.
53. Todd AJ, McGill MM & Shehab SA (2000). Neurokinin 1 receptor expression by neurons in laminae I, III and IV of the rat spinal dorsal horn that project to the brainstem. Eur J Neurosci 12, 689-700.
54. Todd AJ & McKenzie J (1989). GABA-immunoreactive neurons in the dorsal horn of the rat spinal cord. Neuroscience 31, 799-806.
55. Todd AJ & Spike RC (1993). The localization of classical transmitters and neuropeptides within neurons in laminae I-III of the mammalian spinal dorsal horn. Prog Neurobiol 41, 609-645.
56. Torsney C & MacDermott AB (2006). Disinhibition opens the gate to pathological pain signalling in superficial neurokinin 1 receptor-expressing neurons in rat spinal cord. J Neurosci 26, 1833-1843.
57. Wang X, Zhang J, Eberhart D, Urban R, Meda K, Solorzano C, Yamanaka H, Rice D & Basbaum AI (2013). Excitatory superficial dorsal horn interneurons are functionally heterogeneous and required for the full behavioral expression of pain and itch. Neuron 78, 312-324.
58. Willis WD, Jr (1999). Dorsal root potentials and dorsal root reflexes: a double-edged sword. Exp Brain Res 124, 395-421.
59. Yamamoto T, Carr PA, Baimbridge KG & Nagy JI (1989). Parvalbumin- and calbindin D28k-immunoreactive neurons in the superficial layers of the spinal cord dorsal horn of rat. Brain Res Bull 23, 493-508.
60. Yasaka T, Kato G, Furue H, Rashid MH, Sonohata M, Tamae A, Murata Y, Masuko S & Yoshimura M (2007). Cell-type-specific excitatory and inhibitory circuits involving primary afferents in the substantia gelatinosa of the rat spinal dorsal horn in vitro. J Physiol 581, 603-618.
61. Yasaka T, Tiong SY, Hughes DI, Riddell JS & Todd AJ (2010). Populations of inhibitory and excitatory interneurons in lamina II of the adult rat spinal dorsal horn revealed by a combined electrophysiological and anatomical approach. Pain 151, 475-488.
62. Zeilhofer HU, Benke D & Yévenes GE (2012a). Chronic pain states: pharmacological strategies to restore diminished inhibitory spinal pain control. Annu Rev Pharmacol Toxicol 52, 111-133.
63. Zeilhofer HU, Studler B, Arabadzisz D, Schweizer C, Ahmadi S, Layh B, Bösl MR & Fritschy JM (2005). Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J Comp Neurol 482, 123-141.
64. Zeilhofer HU, Wildner H & Yévenes GE (2012b). Fast synaptic inhibition in spinal sensory processing and pain control. Physiol Rev 92, 193-235.