Cross Talk of BDNF and GDNF in Spinal Substantia Gelatinosa (Lamina II): Focus on Circuitry.
BDNF
Chronic pain
GDNF
Neuropathic pain
Nociception
Spinal dorsal horn
Journal
Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103
Informations de publication
Date de publication:
2021
2021
Historique:
entrez:
28
8
2021
pubmed:
29
8
2021
medline:
1
9
2021
Statut:
ppublish
Résumé
BDNF and GDNF display the notable qualities of undergoing a regulated secretion in neurons and being anterogradely transported to nerve terminals, where they can modulate fast synaptic transmission. That BDNF positively modulates nociception and/or pain is today widely accepted, as the growth factor can start and maintain physiological and pathological pain. The contribution of GDNF to nociception is by far most elusive, but evidence is accumulating that the molecule displays analgesic activity, at least in rodents. Here I resume the current knowledge on the spinal cord circuits in which these two factors may act as modulators of pain-related synaptic transmission, focusing on their structural and functional interplay in the regulation of nociception and pain.
Identifiants
pubmed: 34453301
doi: 10.1007/978-3-030-74046-7_14
doi:
Substances chimiques
Brain-Derived Neurotrophic Factor
0
Glial Cell Line-Derived Neurotrophic Factor
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
215-229Informations de copyright
© 2021. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Adelson D, Lao L, Zhang G, Kim W, Marvizòn JC (2009) Substance P release and neurokinin 1 receptor activation in the rat spinal cord increases with the firing frequency of C-fibers. Neuroscience 161:538–553
pubmed: 19336248
doi: 10.1016/j.neuroscience.2009.03.058
pmcid: 19336248
Airaksinen MS, Saarma M (2002) The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 3:383–394
pubmed: 11988777
doi: 10.1038/nrn812
pmcid: 11988777
Averill S, McMahon SB, Clary DO, Reichardt LF, Priestley JV (1995) Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci 7(7):1484–1494
pubmed: 7551174
pmcid: 2758238
doi: 10.1111/j.1460-9568.1995.tb01143.x
Bardoni R, Merighi A (2009) BDNF and trkB mediated mechanisms in the spinal cord. In: Malcangio M (ed) Synaptic plasticity in pain. Springer, New York
Bardoni R, Ghirri A, Salio C, Prandini M, Merighi A (2007) BDNF-mediated modulation of GABA and glycine release in dorsal horn lamina II from postnatal rats. Dev Neurobiol 67:960–975
pubmed: 17506495
doi: 10.1002/dneu.20401
pmcid: 17506495
Bennett GJ, Abdelmoumene M, Hayashi H, Dubner R (1980) Physiology and morphology of substantia gelatinosa neurons intracellularly stained with horseradish peroxidase. J Comp Neurol 194:809–827
pubmed: 6162863
doi: 10.1002/cne.901940407
pmcid: 6162863
Bennett GJ, Ruda MA, Gobel S, Dubner R (1982) Enkephalin immunoreactive stalked cells and islet cells in lamina IIb of the cat substantia gelatinosa. Brain Res 240:162–166
pubmed: 7093716
doi: 10.1016/0006-8993(82)90656-4
pmcid: 7093716
Bennett DL, Michael GJ, Ramachandran N, Munson JB, Averill S, Yan Q, McMahon SB, Priestley JV (1998) A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J Neurosci 18:3059–3072
pubmed: 9526023
pmcid: 6792585
doi: 10.1523/JNEUROSCI.18-08-03059.1998
Bennett DL, Boucher TJ, Armanini MP, Poulsen KT, Michael GJ, Priestley JV, Phillips HS, McMahon SB, Shelton DL (2000) The glial cell line-derived neurotrophic factor family receptor components are differentially regulated within sensory neurons after nerve injury. J Neurosci 20:427–437
pubmed: 10627618
pmcid: 6774134
doi: 10.1523/JNEUROSCI.20-01-00427.2000
Blum R, Konnerth A (2005) Neurotrophin-mediated rapid signaling in the central nervous system: mechanisms and functions. Physiology 20:70–78
pubmed: 15653842
doi: 10.1152/physiol.00042.2004
pmcid: 15653842
Borsook D, Becerra L (2011) CNS animal fMRI in pain and analgesia. Neurosci Biobehav Rev 35:1125–1143
pubmed: 21126534
doi: 10.1016/j.neubiorev.2010.11.005
pmcid: 21126534
Bradbury EJ, Burnstock G, McMahon SB (1998) The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol Cell Neurosci 12:256–268
pubmed: 9828090
doi: 10.1006/mcne.1998.0719
pmcid: 9828090
Brown AG, Fyffe RE (1981) Form and function of dorsal horn neurones with axons ascending the dorsal columns in cat. J Physiol 321:31–47
pubmed: 7338813
pmcid: 1249612
doi: 10.1113/jphysiol.1981.sp013970
Bushnell MC, Duncan GH (1989) Sensory and affective aspects of pain perception: is medial thalamus restricted to emotional issues? Exp Brain Res 78(2):415–418
pubmed: 2599050
doi: 10.1007/BF00228914
pmcid: 2599050
Cervero F, Connell LA (1984) Distribution of somatic and visceral primary afferent fibres within the thoracic spinal cord of the cat. J Comp Neurol 230:88–98
pubmed: 6096416
doi: 10.1002/cne.902300108
pmcid: 6096416
Cervero F, Laird JMA (1999) Visceral pain. Lancet 353:2145–2148
pubmed: 10382712
doi: 10.1016/S0140-6736(99)01306-9
pmcid: 10382712
Chao MV, Hempstead BL (1995) p75 and Trk: a two-receptor system. Trends Neurosci 18:321–326
pubmed: 7571013
doi: 10.1016/0166-2236(95)93922-K
pmcid: 7571013
Coimbra A, Sodré-Borges BP, Magalhaes MM (1974) The substantia gelatinosa Rolandi of the rat. Fine structure, cytochemistry (acid phosphatase) and changes after dorsal root section. J Neurocytol 3:199–217
pubmed: 4366333
doi: 10.1007/BF01098389
pmcid: 4366333
Coimbra A, Ribeiro-Da-Silva A, Pignatelli D (1984) Effects of dorsal rhizotomy on the several types of primary afferent terminals in laminae I-III of the rat spinal cord. An electron microscope study. Anat Embryol (Berl) 170:279–287
doi: 10.1007/BF00318731
Conner JM, Lauterborn JC, Yan Q, Gall CM, Varon S (1997) Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J Neurosci 17:2295–2313
pubmed: 9065491
pmcid: 6573520
doi: 10.1523/JNEUROSCI.17-07-02295.1997
Cruz L, Basbaum AI (1985) Multiple opioid peptides and the modulation of pain: immunohistochemical analysis of dynorphin and enkephalin in the trigeminal nucleus caudalis and spinal cord of the cat. J Comp Neurol 240:331–348
pubmed: 2907522
doi: 10.1002/cne.902400402
pmcid: 2907522
Duan B, Cheng L, Bourane S, Britz O, Padilla C, Garcia-Campmany L, Krashes M, Knowlton W, Velasquez T, Ren X, S-á R, B-á L, Wang Y, Goulding M, Ma Q (2014) Identification of spinal circuits transmitting and gating mechanical pain. Cell 159:1417–1432
pubmed: 25467445
pmcid: 4258511
doi: 10.1016/j.cell.2014.11.003
Ernfors P, Merlio JP, Persson H (1992) Cells expressing mRNA for Neurotrophins and their receptors during embryonic rat development. Eur J Neurosci 4:1140–1158
pubmed: 12106420
doi: 10.1111/j.1460-9568.1992.tb00141.x
pmcid: 12106420
Gebhart GF (2000) J.J. Bonica lecture--2000: physiology, pathophysiology, and pharmacology of visceral pain. Reg Anesth Pain Med 25:632–638
pubmed: 11097673
pmcid: 11097673
Gibon J, Barker PA (2017) Neurotrophins and proneurotrophins: focus on synaptic activity and plasticity in the brain. Neuroscientist 23:587–604
pubmed: 28303740
doi: 10.1177/1073858417697037
pmcid: 28303740
Giesler GJ Jr, Cannon JT, Urca G, Liebeskind JC (1978) Long ascending projections from substantia gelatinosa Rolandi and the subjacent dorsal horn in the rat. Science 202:984–986
pubmed: 715454
doi: 10.1126/science.715454
pmcid: 715454
Gobel S (1975) Golgi studies of the substantia gelatinosa neurons in the spinal trigeminal nucleus. J Comp Neurol 162:397–416
pubmed: 50333
doi: 10.1002/cne.901620308
pmcid: 50333
Gobel S (1978a) Golgi studies of the neurons in layer I of the dorsal horn of the medulla (trigeminal nucleus caudalis). J Comp Neurol 180:375–394
pubmed: 659667
doi: 10.1002/cne.901800212
pmcid: 659667
Gobel S (1978b) Golgi studies of the neurons in layer II of the dorsal horn of the medulla (trigeminal nucleus caudalis). J Comp Neurol 180:395–413
pubmed: 659668
doi: 10.1002/cne.901800213
pmcid: 659668
Gold MS, Gebhart GF (2010) Nociceptor sensitization in pain pathogenesis. Nat Med 16(11):1248–1257
pubmed: 20948530
pmcid: 5022111
doi: 10.1038/nm.2235
Golden JP, Hoshi M, Nassar MA, Enomoto H, Wood JN, Milbrandt J, Gereau RW, Johnson EM Jr, Jain S (2010) RET signaling is required for survival and normal function of nonpeptidergic nociceptors. J Neurosci 30:3983–3994
pubmed: 20237269
pmcid: 2850282
doi: 10.1523/JNEUROSCI.5930-09.2010
Groenewegen HJ (1988) Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography. Neuroscience 24:379–431
pubmed: 2452377
doi: 10.1016/0306-4522(88)90339-9
pmcid: 2452377
Grudt TJ, Perl ER (2002) Correlations between neuronal morphology and electrophysiological features in the rodent superficial dorsal horn. J Physiol 540:189–207
pubmed: 11927679
pmcid: 2290200
doi: 10.1113/jphysiol.2001.012890
Guo Y, Yao FR, Cao DY, Pickar JG, Zhang Q, Wang HS, Zhao Y (2008) Somatostatin inhibits activation of dorsal cutaneous primary afferents induced by antidromic stimulation of primary afferents from an adjacent thoracic segment in the rat. Brain Res 1229:61–71
pubmed: 18640104
doi: 10.1016/j.brainres.2008.06.111
pmcid: 18640104
Hantman AW, Perl ER (2005) Molecular and genetic features of a labeled class of spinal substantia gelatinosa neurons in a transgenic mouse. J Comp Neurol 492:90–100
pubmed: 16175558
doi: 10.1002/cne.20709
pmcid: 16175558
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
pubmed: 14749428
pmcid: 6729829
doi: 10.1523/JNEUROSCI.4221-03.2004
Hiura A, Ishizuka H, Villalobos EL (1991) GABAergic neurons in the mouse superficial dorsal horn with special emphasis on their relation to primary afferent central terminals. Arch Histol Cytol 54:195–206
pubmed: 1873076
doi: 10.1679/aohc.54.195
pmcid: 1873076
Holstege JC, Jongen JL, Kennis JH, Rooyen-Boot AA, Vecht CJ (1998) Immunocytochemical localization of GDNF in primary afferents of the lumbar dorsal horn. Neuroreport 9:2893–2897
pubmed: 9760141
doi: 10.1097/00001756-199808240-00039
pmcid: 9760141
Huang J, Polgár E, HJr S, Mishra SK, Tseng PY, Iwagaki N, Boyle KA, Dickie AC, Kriegbaum MC, Wildner H, Zeilhofer HU, Watanabe M, Riddell JS, Todd AJ, Hoon MA (2018) Circuit dissection of the role of somatostatin in itch and pain. Nat Neurosci 21:707–716
pubmed: 29556030
pmcid: 5923877
doi: 10.1038/s41593-018-0119-z
Jongen JL, Jaarsma D, Hossaini M, Natarajan D, Haasdijk ED, Holstege JC (2007) Distribution of RET immunoreactivity in the rodent spinal cord and changes after nerve injury. J Comp Neurol 500:1136–1153
pubmed: 17183535
doi: 10.1002/cne.21234
pmcid: 17183535
Josephson A, Widenfalk J, Trifunovski A, Widmer HR, Olson L, Spenger C (2001) GDNF and NGF family members and receptors in human fetal and adult spinal cord and dorsal root ganglia. J Comp Neurol 440:204–217
pubmed: 11745618
doi: 10.1002/cne.1380
pmcid: 11745618
Kashiba H, Uchida Y, Senba E (2003) Distribution and colocalization of NGF and GDNF family ligand receptor mRNAs in dorsal root and nodose ganglion neurons of adult rats. Brain Res Mol Brain Res 110:52
pubmed: 12573533
doi: 10.1016/S0169-328X(02)00584-3
pmcid: 12573533
Kato G, Kawasaki Y, Ji RR, Strassman AM (2007) Differential wiring of local excitatory and inhibitory synaptic inputs to islet cells in rat spinal lamina II demonstrated by laser scanning photostimulation. J Physiol 580:815–833
pubmed: 17289782
pmcid: 2075465
doi: 10.1113/jphysiol.2007.128314
Khan N, Smith MT (2015) Neurotrophins and neuropathic pain: role in pathobiology. Molecules 20:10657–10688
pubmed: 26065639
pmcid: 6272404
doi: 10.3390/molecules200610657
Koerber HR (2009) Nociceptors: adequate stimulus. In: Binder MD, Hirokawa N, Windhorst U (eds) Encyclopedia of neuroscience. Springer, Berlin, Heidelberg, pp 2873–2876
doi: 10.1007/978-3-540-29678-2_3999
Li L, Rutlin M, Abraira VE, Cassidy C, Kus L, Gong S, M-á J, Luo W, Heintz N, Koerber H, Woodbury C, Ginty DD (2011) The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147:1615–1627
pubmed: 22196735
pmcid: 3262167
doi: 10.1016/j.cell.2011.11.027
Light AR, Kavookjian AM (1988) Morphology and ultrastructure of physiologically identified substantia gelatinosa (lamina II) neurons with axons that terminate in deeper dorsal horn laminae (III-V). J Comp Neurol 267:172–189
pubmed: 3343395
doi: 10.1002/cne.902670203
pmcid: 3343395
Light AR, Perl ER (1979) Reexamination of the dorsal root projection to the spinal dorsal horn including observations on the differential termination of coarse and fine fibers. J Comp Neurol 186:117–131
pubmed: 447880
doi: 10.1002/cne.901860202
pmcid: 447880
Liu XG, Sandkühler J (1995) The effects of extrasynaptic substance P on nociceptive neurons in laminae I and II in rat lumbar spinal dorsal horn. Neuroscience 68:1207–1218
pubmed: 8544994
doi: 10.1016/0306-4522(95)00187-N
pmcid: 8544994
Lorenzo LE, Ramien M, St.Louis M, De Koninck Y, Ribeiro-da-Silva A (2008) Postnatal changes in the Rexed lamination and markers of nociceptive afferents in the superficial dorsal horn of the rat. J Comp Neurol 508:592–604
pubmed: 18383051
doi: 10.1002/cne.21691
pmcid: 18383051
Lu Y, Perl ER (2003) A specific inhibitory pathway between substantia gelatinosa neurons receiving direct C-fiber input. J Neurosci 23:8752–8758
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
pubmed: 15829642
pmcid: 6724918
doi: 10.1523/JNEUROSCI.0102-05.2005
Luo R, Guo Y, Cao DY, Pickar JG, Li L, Wang J, Zhao Y (2010) Local effects of octreotide on glutamate-evoked activation of Aδ and C afferent fibers in rat hairy skin. Brain Res 1322:50–58
pubmed: 20117102
doi: 10.1016/j.brainres.2010.01.058
pmcid: 20117102
Malcangio M, Getting SJ, Grist J, Cunningham JR, Bradbury EJ, Charbel IP, Lever IJ, Pezet S, Perretti M (2002) A novel control mechanism based on GDNF modulation of somatostatin release from sensory neurones. FASEB J 16:730–732
pubmed: 11978739
doi: 10.1096/fj.01-0971fje
pmcid: 11978739
Marker CL, Lujan R, Colon J, Wickman K (2006) Distinct populations of spinal cord lamina II interneurons expressing G-protein-gated potassium channels. J Neurosci 26:12251–12259
pubmed: 17122050
pmcid: 6675441
doi: 10.1523/JNEUROSCI.3693-06.2006
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
pubmed: 17717012
pmcid: 2277171
doi: 10.1113/jphysiol.2007.140996
McMahon SB, Dmitrieva N, Koltzenburg M (1995) Visceral pain. Br J Anaesth 75:132–144
pubmed: 7577247
doi: 10.1093/bja/75.2.132
pmcid: 7577247
Melzack R, Wall PD (1965) Pain mechanisms: a new theory. Science 150:971–980
pubmed: 5320816
doi: 10.1126/science.150.3699.971
pmcid: 5320816
Merighi A (2016) Targeting the glial-derived neurotrophic factor and related molecules for controlling normal and pathologic pain. Exp Opin Ther Targets 20:193–208
Merighi A (2017) Neuropeptides and Coexistence. In: Reference module in neuroscience and biobehavioral psychology. Elsevier. isbn:9780128093245, Amsterdam. https://doi.org/10.1016/B978-0-12-809324-5.02310-5
doi: 10.1016/B978-0-12-809324-5.02310-5
Merighi A (2018) The histology, physiology, neurochemistry and circuitry of the substantia gelatinosa Rolandi (lamina II) in mammalian spinal cord. Prog Neurobiol 169:91–134
pubmed: 29981393
doi: 10.1016/j.pneurobio.2018.06.012
pmcid: 29981393
Merighi A, Carmignoto G, Gobbo S, Lossi L, Salio C, Vergnano AM, Zonta M (2004) Neurotrophins in spinal cord nociceptive pathways. Prog Brain Res 146:291–321
pubmed: 14699971
doi: 10.1016/S0079-6123(03)46019-6
pmcid: 14699971
Merighi A, Bardoni R, Salio C, Lossi L, Ferrini F, Prandini M, Zonta M, Gustincich S, Carmignoto G (2008a) Presynaptic functional trkB receptors mediate the release of excitatory neurotransmitters from primary afferent terminals in lamina II (substantia gelatinosa) of postnatal rat spinal cord. Dev Neurobiol 68:457–475
pubmed: 18172890
doi: 10.1002/dneu.20605
pmcid: 18172890
Merighi A, Salio C, Ghirri A, Lossi L, Ferrini F, Betelli C, Bardoni R (2008b) BDNF as a pain modulator. Prog Neurobiol 85:297–317
pubmed: 18514997
doi: 10.1016/j.pneurobio.2008.04.004
pmcid: 18514997
Michael GJ, Averill S, Nitkunan A, Rattray M, Bennett DLH, Yan Q, Priestley JV (1997) Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in trk-a expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J Neurosci 17:8476–8490
pubmed: 9334420
pmcid: 6573719
doi: 10.1523/JNEUROSCI.17-21-08476.1997
Mogil JS (2019) The translatability of pain across species. Phil Trans R Soc London B374:20190286
doi: 10.1098/rstb.2019.0286
Molliver DC, Snider WD (1997) Nerve growth factor receptor TrkA is down-regulated during postnatal development by a subset of dorsal root ganglion neurons. J Comp Neurol 381:428–438
pubmed: 9136800
doi: 10.1002/(SICI)1096-9861(19970519)381:4<428::AID-CNE3>3.0.CO;2-4
pmcid: 9136800
Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K, Wen D, Yan Q, Snider WD (1997) IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19:849–861
pubmed: 9354331
doi: 10.1016/S0896-6273(00)80966-6
pmcid: 9354331
Ohta K, Inokuchi T, Gen E, Chang J (2001) Ultrastructural study of anterograde transport of glial cell line-derived neurotrophic factor from dorsal root ganglion neurons of rats towards the nerve terminal. Cells Tiss Organs 169:410–421
doi: 10.1159/000047909
Ortega-de San Luis C, Pascual A (2016) Simultaneous detection of both GDNF and GFRα1 expression patterns in the mouse central nervous system. Front Neuroanat 10:73
pubmed: 27445711
pmcid: 4919337
doi: 10.3389/fnana.2016.00073
Ossipov MH (2011) Growth factors and neuropathic pain. Curr Pain Headache Rep 15:185–192
pubmed: 21327569
doi: 10.1007/s11916-011-0183-5
pmcid: 21327569
Pan YZ, Pan HL (2004) Primary afferent stimulation differentially potentiates excitatory and inhibitory inputs to spinal lamina II outer and inner neurons. J Neurophysiol 91:2413–2421
pubmed: 14749303
doi: 10.1152/jn.01242.2003
pmcid: 14749303
Pintér E, Helyes Z, Szolcsanyi J (2006) Inhibitory effect of somatostatin on inflammation and nociception. Pharmacol Ther 112:440–456
pubmed: 16764934
doi: 10.1016/j.pharmthera.2006.04.010
pmcid: 16764934
Polgár E, Al Ghamdi KS, Todd AJ (2010) Two populations of neurokinin 1 receptor-expressing projection neurons in lamina I of the rat spinal cord that differ in AMPA receptor subunit composition and density of excitatory synaptic input. Neuroscience 167:1192–1204
pubmed: 20303396
doi: 10.1016/j.neuroscience.2010.03.028
pmcid: 20303396
Punnakkal P, von Schoultz C, Haenraets K, Wildner H, Zeilhöfer HU (2014) Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn. J Physiol 592:759–776
pubmed: 24324003
pmcid: 3934713
doi: 10.1113/jphysiol.2013.264937
Reichardt LF (2006) Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B 361:1545–1564
doi: 10.1098/rstb.2006.1894
Rexed B (1952) The cytoarchitectonic organisation of the spinal cord of the cat. J Comp Neurol 96:415–496
doi: 10.1002/cne.900960303
Rexed B (1954) A cytoarchitectonic atlas of the spinal cord in the cat. J Comp Neurol 100:297–379
pubmed: 13163236
doi: 10.1002/cne.901000205
pmcid: 13163236
Ribeiro-da-Silva A (2015) Chapter 7 – Substantia gelatinosa of the spinal cord – Paxinos, George. In: The rat nervous system, 4th edn. Academic Press, San Diego, pp 97–114
Ribeiro-Da-Silva A, Coimbra A (1982) Two types of synaptic glomeruli and their distribution in laminae I-III of the rat spinal cord. J Comp Neurol 209:176–186
pubmed: 6890076
doi: 10.1002/cne.902090205
pmcid: 6890076
Ribeiro-Da-Silva A, De Koninck Y (2008) Morphological and neurochemical organization of the spinal dorsal horn. In: Albright TD, Albright TD, Masland RH et al (eds) The senses: a comprehensive reference. Academic Press, New York, pp 279–310
Ribeiro-Da-Silva A, Pignatelli D, Coimbra A (1985) Synaptic architecture of glomeruli in superficial dorsal horn of rat spinal cord, as shown in serial reconstructions. J Neurocytol 14:203–220
pubmed: 4045504
doi: 10.1007/BF01258448
pmcid: 4045504
Ribeiro-Da-Silva A, Pioro EP, Cuello AC (1991) Substance P- and enkephalin-like immunoreactivities are colocalized in certain neurons of the substantia gelatinosa of the rat spinal cord: an ultrastructural double-labeling study. J Neurosci 11:1068–1080
pubmed: 1707094
pmcid: 6575373
doi: 10.1523/JNEUROSCI.11-04-01068.1991
Salio C, Ferrini F (2016) BDNF and GDNF expression in discrete populations of nociceptors. Ann Anat 207:55–61
pubmed: 26706106
doi: 10.1016/j.aanat.2015.12.001
pmcid: 26706106
Salio C, Lossi L, Ferrini F, Merighi A (2005) Ultrastructural evidence for a pre- and post-synaptic localization of full length trkB receptors in substantia gelatinosa (lamina II) of rat and mouse spinal cord. Eur J Neurosci 22:1951–1966
pubmed: 16262634
doi: 10.1111/j.1460-9568.2005.04392.x
pmcid: 16262634
Salio C, Averill S, Priestley JV, Merighi A (2007) Costorage of BDNF and neuropeptides within individual dense-core vesicles in central and peripheral neurons. Dev Neurobiol 67:326–338
pubmed: 17443791
doi: 10.1002/dneu.20358
pmcid: 17443791
Salio C, Ferrini F, Muthuraju S, Merighi A (2014) Presynaptic modulation of spinal nociceptive transmission by glial cell line-derived neurotrophic factor (GDNF). J Neurosci 34:13819–13833
pubmed: 25297108
pmcid: 6608376
doi: 10.1523/JNEUROSCI.0808-14.2014
Schoenen J (1982) Dendritic organization of the human spinal cord: the dorsal horn. Neuroscience 7:2057–2087
pubmed: 7145088
doi: 10.1016/0306-4522(82)90120-8
pmcid: 7145088
Sengupta JN (2009) Visceral pain: the neurophysiological mechanism. Handbook Exp Pharmacol 194:31–74
doi: 10.1007/978-3-540-79090-7_2
Seybold VS (2009) The role of peptides in central sensitization. In: Canning BJ, Spina D (eds) Sensory nerves. Springer, Berlin, Heidelberg, pp 451–491
doi: 10.1007/978-3-540-79090-7_13
Sugiura Y, Terui N, Hosoya Y (1989) Difference in distribution of central terminals between visceral and somatic unmyelinated (C) primary afferent fibers. J Neurophysiol 62:834–840
pubmed: 2809705
doi: 10.1152/jn.1989.62.4.834
pmcid: 2809705
Surmeier DJ, Honda CN, Willis WD Jr (1988) Natural groupings of primate spinothalamic neurons based on cutaneous stimulation. Physiological and anatomical features. J Neurophysiol 59:833–860
pubmed: 3367200
doi: 10.1152/jn.1988.59.3.833
pmcid: 3367200
Thompson SJ, Bushnell MC (2012) Rodent functional and anatomical imaging of pain. Neurosci Lett 520:131–139
pubmed: 22445887
doi: 10.1016/j.neulet.2012.03.015
pmcid: 22445887
Todd AJ, McKenzie J (1989) GABA-immunoreactive neurons in the dorsal horn of the rat spinal cord. Neuroscience 31:799–806
pubmed: 2594201
doi: 10.1016/0306-4522(89)90442-9
pmcid: 2594201
Todd AJ, Hughes DI, Polgàr 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
pubmed: 12534965
doi: 10.1046/j.1460-9568.2003.02406.x
pmcid: 12534965
Wang J, Guo Y, Cao DY, Luo R, Ma SJ, Wang HS, Pickar JG, Zhao Y (2009) Tonic inhibition of somatostatin on C and Aδ afferent fibers in rat dorsal skin in vivo. Brain Res 1288:50–59
pubmed: 19596279
doi: 10.1016/j.brainres.2009.06.088
pmcid: 19596279
Widenfalk J, Lundstromer K, Jubran M, Brene S, Olson L (2001) Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J Neurosci 21:3457–3475
pubmed: 11331375
pmcid: 6762497
doi: 10.1523/JNEUROSCI.21-10-03457.2001
Willis WD Jr, Coggeshall RE (2004) Structure of the dorsal horn. In: Sensory mechanisms of the spinal cord – primary afferent neurons and the spinal dorsal horn, 3rd edn. Kluver Academic/Plenum Publisher, New York, pp 155–186
doi: 10.1007/978-1-4615-0037-7_5
Willis WD, Leonard RB, Kenshalo DRJ (1978) Spinothalamic tract neurons in the substantia gelatinosa. Science 202:986–988
pubmed: 102034
doi: 10.1126/science.102034
pmcid: 102034
Woodbury CJ, Ritter AM, Koerber HR (2000) On the problem of lamination in the superficial dorsal horn of mammals: a reappraisal of the substantia gelatinosa in postnatal life. J Comp Neurol 417:88–102
pubmed: 10660890
doi: 10.1002/(SICI)1096-9861(20000131)417:1<88::AID-CNE7>3.0.CO;2-U
pmcid: 10660890
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
pubmed: 17347278
pmcid: 2075204
doi: 10.1113/jphysiol.2006.123919
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
pubmed: 20817353
pmcid: 3170912
doi: 10.1016/j.pain.2010.08.008
Yasaka T, Tiong SY, PolgÃr E, Watanabe M, Kumamoto E, Riddell JS, Todd AJ (2014) A putative relay circuit providing low-threshold mechanoreceptive input to lamina I projection neurons via vertical cells in lamina II of the rat dorsal horn. Mol Pain 10:1744–8069
Zheng J, Lu Y, Perl ER (2010) Inhibitory neurones of the spinal substantia gelatinosa mediate interaction of signals from primary afferents. J Physiol 588:2065–2075
pubmed: 20403977
pmcid: 2911212
doi: 10.1113/jphysiol.2010.188052