Short-term plasticity in the spinal nociceptive system.


Journal

Pain
ISSN: 1872-6623
Titre abrégé: Pain
Pays: United States
ID NLM: 7508686

Informations de publication

Date de publication:
01 Nov 2023
Historique:
received: 21 07 2022
accepted: 08 06 2023
pubmed: 14 8 2023
medline: 14 8 2023
entrez: 14 8 2023
Statut: ppublish

Résumé

Somatosensory information is delivered to neuronal networks of the dorsal horn (DH) of the spinal cord by the axons of primary afferent neurons that encode the intensity of peripheral sensory stimuli under the form of a code based on the frequency of action potential firing. The efficient processing of these messages within the DH involves frequency-tuned synapses, a phenomenon linked to their ability to display activity-dependent forms of short-term plasticity (STP). By affecting differently excitatory and inhibitory synaptic transmissions, these STP properties allow a powerful gain control in DH neuronal networks that may be critical for the integration of nociceptive messages before they are forwarded to the brain, where they may be ultimately interpreted as pain. Moreover, these STPs can be finely modulated by endogenous signaling molecules, such as neurosteroids, adenosine, or GABA. The STP properties of DH inhibitory synapses might also, at least in part, participate in the pain-relieving effect of nonpharmacological analgesic procedures, such as transcutaneous electrical nerve stimulation, electroacupuncture, or spinal cord stimulation. The properties of target-specific STP at inhibitory DH synapses and their possible contribution to electrical stimulation-induced reduction of hyperalgesic and allodynic states in chronic pain will be reviewed and discussed.

Identifiants

pubmed: 37578501
doi: 10.1097/j.pain.0000000000002999
pii: 00006396-990000000-00376
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2411-2424

Informations de copyright

Copyright © 2023 International Association for the Study of Pain.

Références

Adrian ED. The recovery process of excitable tissues: part I. J Physiol 1920;54:1–31.
Adrian ED, Zotterman Y. The impulses produced by sensory nerve endings: part 3. Impulses set up by touch and pressure. J Physiol 1926;61:465–83.
Alles SRA, Smith PA. Peripheral voltage-gated cation channels in neuropathic pain and their potential as therapeutic targets. Front Pain Res (Lausanne) 2021;2:750583.
Andrew D, Greenspan JD. Peripheral coding of tonic mechanical cutaneous pain: comparison of nociceptor activity in rat and human psychophysics. J Neurophysiol 1999;82:2641–8.
Anwar H, Li X, Bucher D, Nadim F. Functional roles of short-term synaptic plasticity with an emphasis on inhibition. Curr Opin Neurobiol 2017;43:71–8.
Arendt-Nielsen L, Petersen-Felix S, Fischer M, Bak P, Bjerring P, Zbinden AM. The effect of N-methyl-D-aspartate antagonist (ketamine) on single and repeated nociceptive stimuli: a placebo-controlled experimental human study. Anesth Analg 1995;81:63–8.
Aziz Q, Botha C, Willert R. Pharmacology of visceral pain: central factors. Dig Dis 2009;27(suppl 1):31–41.
Baba H, Kohno T, Okamoto M, Goldstein PA, Shimoji K, Yoshimura M. Muscarinic facilitation of GABA release in substantia gelatinosa of the rat spinal dorsal horn. J Physiol 1998;508:83–93.
Baba H, Yoshimura M, Nishi S, Shimoji K. Synaptic responses of substantia gelatinosa neurones to dorsal column stimulation in rat spinal cord in vitro. J Physiol 1994;478:87–99.
Ballarin M, Fredholm BB, Ambrosio S, Mahy N. Extracellular levels of adenosine and its metabolites in the striatum of awake rats: inhibition of uptake and metabolism. Acta Physiol Scand 1991;142:97–103.
Bao J, Reim K, Sakaba T. Target-dependent feedforward inhibition mediated by short-term synaptic plasticity in the cerebellum. J Neurosci 2010;30:8171–9.
Baraldi PG, Zaid AN, Lampronti I, Fruttarolo F, Pavani MG, Tabrizi MA, Shryock JC, Leung E, Romagnoli R. Synthesis and biological effects of a new series of 2-amino-3-benzoylthiophenes as allosteric enhancers of A1-adenosine receptor. Bioorg Med Chem Lett 2000;10:1953–7.
Bartley AF, Dobrunz LE. Short-term plasticity regulates the excitation/inhibition ratio and the temporal window for spike integration in CA1 pyramidal cells. Eur J Neurosci 2015;41:1402–15.
Battaglia G, Rustioni A. Coexistence of glutamate and substance P in dorsal root ganglion neurons of the rat and monkey. J Comp Neurol 1988;277:302–12.
Beierlein M, Gibson JR, Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 2003;90:2987–3000.
Betelli C, MacDermott AB, Bardoni R. Transient, activity dependent inhibition of transmitter release from low threshold afferents mediated by GABAA receptors in spinal cord lamina III/IV. Mol Pain 2015;11:64.
Branchereau P, Cattaert D, Delpy A, Allain AE, Martin E, Meyrand P. Depolarizing GABA/glycine synaptic events switch from excitation to inhibition during frequency increases. Sci Rep 2016;6:21753.
Brezina V, Church PJ, Weiss KR. Temporal pattern dependence of neuronal peptide transmitter release: models and experiments. J Neurosci 2000;20:6760–72.
Budai D, Larson AA. Role of substance P in the modulation of C-fiber-evoked responses of spinal dorsal horn neurons. Brain Res 1996;710:197–203.
Buonomano DV. Decoding temporal information: a model based on short-term synaptic plasticity. J Neurosci 2000;20:1129–41.
Buonomano DV. The biology of time across different scales. Nat Chem Biol 2007;3:594–7.
Campero M, Serra J, Ochoa JL. C-polymodal nociceptors activated by noxious low temperature in human skin. J Physiol 1996;497:565–72.
Castro-Lopes JM, Tavares I, Tolle TR, Coito A, Coimbra A. Increase in GABAergic cells and GABA levels in the spinal cord in unilateral inflammation of the hindlimb in the rat. Eur J Neurosci 1992;4:296–301.
Cathenaut L, Leonardon B, Kuster R, Inquimbert P, Schlichter R, Hugel S. Inhibitory interneurons with differential plasticities at their connections tune excitatory/inhibitory balance in the spinal nociceptive system. PAIN 2022;163:e675–88.
Chery N, De Koninck Y. GABA(B) receptors are the first target of released GABA at lamina I inhibitory synapses in the adult rat spinal cord. J Neurophysiol 2000;84:1006–11.
Cordero-Erausquin M, Coull JA, Boudreau D, Rolland M, De Koninck Y. Differential maturation of GABA action and anion reversal potential in spinal lamina I neurons: impact of chloride extrusion capacity. J Neurosci 2005;25:9613–23.
Cordero-Erausquin M, Inquimbert P, Schlichter R, Hugel S. Neuronal networks and nociceptive processing in the dorsal horn of the spinal cord. Neuroscience 2016;338:230–47.
Coste J, Voisin DL, Miraucourt LS, Dallel R, Luccarini P. Dorsal horn NK1-expressing neurons control windup of downstream trigeminal nociceptive neurons. PAIN 2008;137:340–51.
Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sik A, De Koninck P, De Koninck Y. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 2003;424:938–42.
Craig AD, Andrew D. Responses of spinothalamic lamina I neurons to repeated brief contact heat stimulation in the cat. J Neurophysiol 2002;87:1902–14.
Cui JG, Meyerson BA, Sollevi A, Linderoth B. Effect of spinal cord stimulation on tactile hypersensitivity in mononeuropathic rats is potentiated by simultaneous GABA(B) and adenosine receptor activation. Neurosci Lett 1998;247:183–6.
Cui JG, O'Connor WT, Ungerstedt U, Linderoth B, Meyerson BA. Spinal cord stimulation attenuates augmented dorsal horn release of excitatory amino acids in mononeuropathy via a GABAergic mechanism. PAIN 1997;73:87–95.
Cui JG, Sollevi A, Linderoth B, Meyerson BA. Adenosine receptor activation suppresses tactile hypersensitivity and potentiates spinal cord stimulation in mononeuropathic rats. Neurosci Lett 1997;223:173–6.
D'Mello R, Dickenson AH. Spinal cord mechanisms of pain. Br J Anaesth 2008;101:8–16.
Dai QX, Huang LP, Mo YC, Yu LN, Du WW, Zhang AQ, Geng WJ, Wang JL, Yan M. Role of spinal adenosine A1 receptors in the analgesic effect of electroacupuncture in a rat model of neuropathic pain. J Int Med Res 2020;48:300060519883748.
Davies SN, Lodge D. Evidence for involvement of N-methylaspartate receptors in 'wind-up' of class 2 neurones in the dorsal horn of the rat. Brain Res 1987;424:402–6.
De Koninck Y, Henry JL. Peripheral vibration causes an adenosine-mediated postsynaptic inhibitory potential in dorsal horn neurons of the cat spinal cord. Neuroscience 1992;50:435–43.
Dickenson AH. A cure for wind up: NMDA receptor antagonists as potential analgesics. Trends Pharmacol Sci 1990;11:307–9.
Dickenson AH, Sullivan AF. Evidence for a role of the NMDA receptor in the frequency dependent potentiation of deep rat dorsal horn nociceptive neurones following C fibre stimulation. Neuropharmacology 1987;26:1235–8.
Dickhaus H, Pauser G, Zimmermann M. Tonic descending inhibition affects intensity coding of nociceptive responses of spinal dorsal horn neurones in the cat. PAIN 1985;23:145–58.
Dickie A, Tabasam G, Tashani O, Marchant P, Johnson MI. A preliminary investigation into the effect of coffee on hypolagesia associated with transcutaneous electrical nerve stimulation. Clin Physiol Funct Imaging 2009;29:293–9.
Dickie AC, McCormick B, Lukito V, Wilson KL, Torsney C. Inflammatory pain reduces C fiber activity-dependent slowing in a sex-dependent manner, amplifying nociceptive input to the spinal cord. J Neurosci 2017;37:6488–502.
Dorgans K, Demais V, Bailly Y, Poulain B, Isope P, Doussau F. Short-term plasticity at cerebellar granule cell to molecular layer interneuron synapses expands information processing. Elife 2019;8:e41586.
Doyon N, Prescott SA, Castonguay A, Godin AG, Kroger H, De Koninck Y. Efficacy of synaptic inhibition depends on multiple, dynamically interacting mechanisms implicated in chloride homeostasis. PLoS Comput Biol 2011;7:e1002149.
Draper-Joyce CJ, Bhola R, Wang J, Bhattarai A, Nguyen ATN, Cowie-Kent I, O'Sullivan K, Chia LY, Venugopal H, Valant C, Thal DM, Wootten D, Panel N, Carlsson J, Christie MJ, White PJ, Scammells P, May LT, Sexton PM, Danev R, Miao Y, Glukhova A, Imlach WL, Christopoulos A. Positive allosteric mechanisms of adenosine A1 receptor-mediated analgesia. Nature 2021;597:571–6.
Duan B, Wu LJ, Yu YQ, Ding Y, Jing L, Xu L, Chen J, Xu TL. Upregulation of acid-sensing ion channel ASIC1a in spinal dorsal horn neurons contributes to inflammatory pain hypersensitivity. J Neurosci 2007;27:11139–48.
Dunwiddie TV, Masino SA. The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 2001;24:31–55.
Eide PK. Wind-up and the NMDA receptor complex from a clinical perspective. Eur J Pain 2000;4:5–15.
Fan W, Sdrulla AD. Differential modulation of excitatory and inhibitory populations of superficial dorsal horn neurons in lumbar spinal cord by Abeta-fiber electrical stimulation. PAIN 2020;161:1650–60.
Ferrini F, Perez-Sanchez J, Ferland S, Lorenzo LE, Godin AG, Plasencia-Fernandez I, Cottet M, Castonguay A, Wang F, Salio C, Doyon N, Merighi A, De Koninck Y. Differential chloride homeostasis in the spinal dorsal horn locally shapes synaptic metaplasticity and modality-specific sensitization. Nat Commun 2020;11:3935.
Fleischer E, Handwerker HO, Joukhadar S. Unmyelinated nociceptive units in two skin areas of the rat. Brain Res 1983;267:81–92.
Fossat P, Sibon I, Le Masson G, Landry M, Nagy F. L-type calcium channels and NMDA receptors: a determinant duo for short-term nociceptive plasticity. Eur J Neurosci 2007;25:127–35.
Fredholm BB, IJzerman AP, Jacobson KA, Linden J, Muller CE. International union of basic and clinical pharmacology. LXXXI. Nomenclature and classification of adenosine receptors—an update. Pharmacol Rev 2011;63:1–34.
Fredholm BB, Battig K, Holmen J, Nehlig A, Zvartau EE. Actions of caffeine in the brain with special reference to factors that contribute to its widespread use. Pharmacol Rev 1999;51:83–133.
Froemke RC, Merzenich MM, Schreiner CE. A synaptic memory trace for cortical receptive field plasticity. Nature 2007;450:425–9.
Fukuhara K, Katafuchi T, Yoshimura M. Effects of baclofen on mechanical noxious and innocuous transmission in the spinal dorsal horn of the adult rat: in vivo patch-clamp analysis. Eur J Neurosci 2013;38:3398–407.
Gale JR, Gedeon JY, Donnelly CJ, Gold MS. Local translation in primary afferents and its contribution to pain. PAIN 2022;163:2302–14.
Gee MD, Lynn B, Cotsell B. Activity-dependent slowing of conduction velocity provides a method for identifying different functional classes of C-fibre in the rat saphenous nerve. Neuroscience 1996;73:667–75.
Gemes G, Koopmeiners A, Rigaud M, Lirk P, Sapunar D, Bangaru ML, Vilceanu D, Garrison SR, Ljubkovic M, Mueller SJ, Stucky CL, Hogan QH. Failure of action potential propagation in sensory neurons: mechanisms and loss of afferent filtering in C-type units after painful nerve injury. J Physiol 2013;591:1111–31.
Giere C, Melchior M, Dufour A, Poisbeau P. Spinal integration of hot and cold nociceptive stimuli by wide-dynamic-range neurons in anesthetized adult rats. Pain Rep 2021;6:e983.
Grudt TJ, Perl ER. Correlations between neuronal morphology and electrophysiological features in the rodent superficial dorsal horn. J Physiol 2002;540:189–207.
Handwerker HO, Anton F, Reeh PW. Discharge patterns of afferent cutaneous nerve fibers from the rat's tail during prolonged noxious mechanical stimulation. Exp Brain Res 1987;65:493–504.
Harding EK, Zamponi GW. Central and peripheral contributions of T-type calcium channels in pain. Mol Brain 2022;15:39.
Hartell NA, Headley PM. The effect of naloxone on spinal reflexes to electrical and mechanical stimuli in the anaesthetized, spinalized rat. J Physiol 1991;442:513–26.
Herrero JF, Laird JM, Lopez-Garcia JA. Wind-up of spinal cord neurones and pain sensation: much ado about something? Prog Neurobiol 2000;61:169–203.
Hugel S, Schlichter R. Convergent control of synaptic GABA release from rat dorsal horn neurones by adenosine and GABA autoreceptors. J Physiol 2003;551:479–89.
Imlach WL, Bhola RF, May LT, Christopoulos A, Christie MJ. A positive allosteric modulator of the adenosine A1 receptor selectively inhibits primary afferent synaptic transmission in a neuropathic pain model. Mol Pharmacol 2015;88:460–8.
Ingram RA, Fitzgerald M, Baccei ML. Developmental changes in the fidelity and short-term plasticity of GABAergic synapses in the neonatal rat dorsal horn. J Neurophysiol 2008;99:3144–50.
Inquimbert P, Rodeau JL, Schlichter R. Regional differences in the decay kinetics of GABA(A) receptor-mediated miniature IPSCs in the dorsal horn of the rat spinal cord are determined by mitochondrial transport of cholesterol. J Neurosci 2008;28:3427–37.
Isaacson JS, Solis JM, Nicoll RA. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 1993;10:165–75.
Jacobson KA, Tosh DK, Jain S, Gao ZG. Historical and current adenosine receptor agonists in preclinical and clinical development. Front Cell Neurosci 2019;13:124.
Jean-Xavier C, Mentis GZ, O'Donovan MJ, Cattaert D, Vinay L. Dual personality of GABA/glycine-mediated depolarizations in immature spinal cord. Proc Natl Acad Sci U S A 2007;104:11477–82.
Jeftinija S, Urban L. Repetitive stimulation induced potentiation of excitatory transmission in the rat dorsal horn: an in vitro study. J Neurophysiol 1994;71:216–28.
Kataoka K, Hara K, Haranishi Y, Terada T, Sata T. The antinociceptive effect of SNAP5114, a gamma-aminobutyric acid transporter-3 inhibitor, in rat experimental pain models. Anesth Analg 2013;116:1162–9.
Keller AF, Breton JD, Schlichter R, Poisbeau P. Production of 5alpha-reduced neurosteroids is developmentally regulated and shapes GABA(A) miniature IPSCs in lamina II of the spinal cord. J Neurosci 2004;24:907–15.
Khasabov SG, Rogers SD, Ghilardi JR, Peters CM, Mantyh PW, Simone DA. Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci 2002;22:9086–98.
Kimura S, Kontani H. Separate recording of A-delta and C fiber-mediated nociceptive flexor reflex responses of mouse hindlimb using electromyography and the characteristics of wind-up appearing in the responses. J Pharmacol Sci 2008;108:172–8.
Kimura S, Tanabe M, Honda M, Ono H. Enhanced wind-up of the C-fiber-mediated nociceptive flexor reflex movement following painful diabetic neuropathy in mice. J Pharmacol Sci 2005;97:195–202.
Kloc ML, Pradier B, Chirila AM, Kauer JA. NMDA receptor activation induces long-term potentiation of glycine synapses. PLoS One 2019;14:e0222066.
Klyachko VA, Stevens CF. Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains. PLoS Biol 2006;4:e207.
Koltzenburg M, Handwerker HO. Differential ability of human cutaneous nociceptors to signal mechanical pain and to produce vasodilatation. J Neurosci 1994;14:1756–65.
Koyanagi S, Kusunose N, Taniguchi M, Akamine T, Kanado Y, Ozono Y, Masuda T, Kohro Y, Matsunaga N, Tsuda M, Salter MW, Inoue K, Ohdo S. Glucocorticoid regulation of ATP release from spinal astrocytes underlies diurnal exacerbation of neuropathic mechanical allodynia. Nat Commun 2016;7:13102.
Kuhlman SJ, Olivas ND, Tring E, Ikrar T, Xu X, Trachtenberg JT. A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature 2013;501:543–6.
Labrakakis C, Lorenzo LE, Bories C, Ribeiro-da-Silva A, De Koninck Y. Inhibitory coupling between inhibitory interneurons in the spinal cord dorsal horn. Mol Pain 2009;5:24.
Labrakakis C, Rudolph U, De Koninck Y. The heterogeneity in GABAA receptor-mediated IPSC kinetics reflects heterogeneity of subunit composition among inhibitory and excitatory interneurons in spinal lamina II. Front Cell Neurosci 2014;8:424.
Letzkus JJ, Wolff SB, Meyer EM, Tovote P, Courtin J, Herry C, Luthi A. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 2011;480:331–5.
Lever I, Cunningham J, Grist J, Yip PK, Malcangio M. Release of BDNF and GABA in the dorsal horn of neuropathic rats. Eur J Neurosci 2003;18:1169–74.
Li DP, Chen SR, Pan YZ, Levey AI, Pan HL. Role of presynaptic muscarinic and GABA(B) receptors in spinal glutamate release and cholinergic analgesia in rats. J Physiol 2002;543:807–18.
Li J, Baccei ML. Functional organization of cutaneous and muscle afferent synapses onto immature spinal lamina I projection neurons. J Neurosci 2017;37:1505–17.
Lin Q, Peng YB, Willis WD. Role of GABA receptor subtypes in inhibition of primate spinothalamic tract neurons: difference between spinal and periaqueductal gray inhibition. J Neurophysiol 1996;75:109–23.
Lind G, Meyerson BA, Winter J, Linderoth B. Intrathecal baclofen as adjuvant therapy to enhance the effect of spinal cord stimulation in neuropathic pain: a pilot study. Eur J Pain 2004;8:377–83.
Lind G, Schechtmann G, Winter J, Meyerson BA, Linderoth B. Baclofen-enhanced spinal cord stimulation and intrathecal baclofen alone for neuropathic pain: long-term outcome of a pilot study. Eur J Pain 2008;12:132–6.
Liu P, Zhang X, He X, Jiang Z, Wang Q, Lu Y. Spinal GABAergic neurons are under feed-forward inhibitory control driven by Adelta and C fibers in Gad2 td-Tomato mice. Mol Pain 2021;17:1744806921992620.
Liu X, Sandkuhler J. Characterization of long-term potentiation of C-fiber-evoked potentials in spinal dorsal horn of adult rat: essential role of NK1 and NK2 receptors. J Neurophysiol 1997;78:1973–82.
Lovett-Barron M, Turi GF, Kaifosh P, Lee PH, Bolze F, Sun XH, Nicoud JF, Zemelman BV, Sternson SM, Losonczy A. Regulation of neuronal input transformations by tunable dendritic inhibition. Nat Neurosci 2012;15:423–30, S421–3.
Lu Y, Perl ER. A specific inhibitory pathway between substantia gelatinosa neurons receiving direct C-fiber input. J Neurosci 2003;23:8752–8.
Lundberg LE, Jorum E, Holm E, Torebjork HE. Intra-neural electrical stimulation of cutaneous nociceptive fibres in humans: effects of different pulse patterns on magnitude of pain. Acta Physiol Scand 1992;146:41–8.
Malan TP, Mata HP, Porreca F. Spinal GABA(A) and GABA(B) receptor pharmacology in a rat model of neuropathic pain. Anesthesiology 2002;96:1161–7.
Marchand S, Li J, Charest J. Effects of caffeine on analgesia from transcutaneous electrical nerve stimulation. N Engl J Med 1995;333:325–6.
Markram H, Wang Y, Tsodyks M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A 1998;95:5323–8.
Mazo I, Roza C, Zamanillo D, Merlos M, Vela JM, Lopez-Garcia JA. Effects of centrally acting analgesics on spinal segmental reflexes and wind-up. Eur J Pain 2015;19:1012–20.
Mendell LM. Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol 1966;16:316–32.
Mendell LM, Wall PD. Responses of single dorsal cord cells to peripheral cutaneous unmyelinated fibres. Nature 1965;206:97–9.
Moreno A, Morris RGM, Canals S. Frequency-dependent gating of hippocampal-neocortical interactions. Cereb Cortex 2016;26:2105–14.
Morisset V, Nagy F. Plateau potential-dependent windup of the response to primary afferent stimuli in rat dorsal horn neurons. Eur J Neurosci 2000;12:3087–95.
Motanis H, Seay MJ, Buonomano DV. Short-term synaptic plasticity as a mechanism for sensory timing. Trends Neurosci 2018;41:701–11.
Muschol M, Salzberg BM. Dependence of transient and residual calcium dynamics on action-potential patterning during neuropeptide secretion. J Neurosci 2000;20:6773–80.
Nakatsuka T, Ataka T, Kumamoto E, Tamaki T, Yoshimura M. Alteration in synaptic inputs through C-afferent fibers to substantia gelatinosa neurons of the rat spinal dorsal horn during postnatal development. Neuroscience 2000;99:549–56.
Nakatsuka T, Furue H, Yoshimura M, Gu JG. Activation of central terminal vanilloid receptor-1 receptors and alpha beta-methylene-ATP-sensitive P2X receptors reveals a converged synaptic activity onto the deep dorsal horn neurons of the spinal cord. J Neurosci 2002;22:1228–37.
Patel R, Dickenson AH. Neuropharmacological basis for multimodal analgesia in chronic pain. Postgrad Med 2022;134:245–59.
Perrier JF, Alaburda A, Hounsgaard J. Spinal plasticity mediated by postsynaptic L-type Ca2+ channels. Brain Res Brain Res Rev 2002;40:223–9.
Petitjean H, Rodeau JL, Schlichter R. Interactions between superficial and deep dorsal horn spinal cord neurons in the processing of nociceptive information. Eur J Neurosci 2012;36:3500–8.
Poisbeau P, Patte-Mensah C, Keller AF, Barrot M, Breton JD, Luis-Delgado OE, Freund-Mercier MJ, Mensah-Nyagan AG, Schlichter R. Inflammatory pain upregulates spinal inhibition via endogenous neurosteroid production. J Neurosci 2005;25:11768–76.
Pouille F, Scanziani M. Routing of spike series by dynamic circuits in the hippocampus. Nature 2004;429:717–23.
Price DD, Hu JW, Dubner R, Gracely RH. Peripheral suppression of first pain and central summation of second pain evoked by noxious heat pulses. PAIN 1977;3:57–68.
Price DD, Hull CD, Buchwald NA. Intracellular responses of dorsal horn cells to cutaneous and sural nerve A and C fiber stimuli. Exp Neurol 1971;33:291–309.
Puente B, Nadal X, Portillo-Salido E, Sanchez-Arroyos R, Ovalle S, Palacios G, Muro A, Romero L, Entrena JM, Baeyens JM, Lopez-Garcia JA, Maldonado R, Zamanillo D, Vela JM. Sigma-1 receptors regulate activity-induced spinal sensitization and neuropathic pain after peripheral nerve injury. PAIN 2009;145:294–303.
Puig S, Sorkin LS. Formalin-evoked activity in identified primary afferent fibers: systemic lidocaine suppresses phase-2 activity. PAIN 1996;64:345–55.
Ratté S, Zhu Y, Lee KY, Prescott SA. Criticality and degeneracy in injury-induced changes in primary afferent excitability and the implications for neuropathic pain. Elife 2014;3:e02370.
Romero L, Merlos M, Vela JM. Antinociception by sigma-1 receptor antagonists: central and peripheral effects. Adv Pharmacol 2016;75:179–215.
Royer S, Zemelman BV, Losonczy A, Kim J, Chance F, Magee JC, Buzsaki G. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat Neurosci 2012;15:769–75.
Russo RE, Hounsgaard J. Short-term plasticity in turtle dorsal horn neurons mediated by L-type Ca2+ channels. Neuroscience 1994;61:191–7.
Saini A, Tucci M, Tampellini M, Maina D, Bouraouia K, Giuliano PL, Termine A, Castellano M, Campagna S, Laciura P, Berruti A. Circadian variation of breakthrough pain in cancer patients. Eur J Pain 2013;17:264–70.
Salio C, Merighi A, Bardoni R. GABAB receptors-mediated tonic inhibition of glutamate release from Abeta fibers in rat laminae III/IV of the spinal cord dorsal horn. Mol Pain 2017;13:1744806917710041.
Santos SF, Luz LL, Szucs P, Lima D, Derkach VA, Safronov BV. Transmission efficacy and plasticity in glutamatergic synapses formed by excitatory interneurons of the substantia gelatinosa in the rat spinal cord. PLoS One 2009;4:e8047.
Sawynok J. Adenosine receptor targets for pain. Neuroscience 2016;338:1–18.
Schlichter R, Keller AF, De Roo M, Breton JD, Inquimbert P, Poisbeau P. Fast nongenomic effects of steroids on synaptic transmission and role of endogenous neurosteroids in spinal pain pathways. J Mol Neurosci 2006;28:33–51.
Schouenborg J. Functional and topographical properties of field potentials evoked in rat dorsal horn by cutaneous C-fibre stimulation. J Physiol 1984;356:169–92.
Schouenborg J, Sjolund BH. Activity evoked by A- and C-afferent fibers in rat dorsal horn neurons and its relation to a flexion reflex. J Neurophysiol 1983;50:1108–21.
Schuler V, Luscher C, Blanchet C, Klix N, Sansig G, Klebs K, Schmutz M, Heid J, Gentry C, Urban L, Fox A, Spooren W, Jaton AL, Vigouret J, Pozza M, Kelly PH, Mosbacher J, Froestl W, Kaslin E, Korn R, Bischoff S, Kaupmann K, van der Putten H, Bettler B. Epilepsy, hyperalgesia, impaired memory, and loss of pre- and postsynaptic GABA(B) responses in mice lacking GABA(B(1)). Neuron 2001;31:47–58.
Seagrove LC, Suzuki R, Dickenson AH. Electrophysiological characterisations of rat lamina I dorsal horn neurones and the involvement of excitatory amino acid receptors. PAIN 2004;108:76–87.
Serra J, Campero M, Ochoa J, Bostock H. Activity-dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin. J Physiol 1999;515(Pt 3):799–811.
Shim B, Ringkamp M, Lambrinos GL, Hartke TV, Griffin JW, Meyer RA. Activity-dependent slowing of conduction velocity in uninjured L4 C fibers increases after an L5 spinal nerve injury in the rat. PAIN 2007;128:40–51.
Smith TM, Lee D, Bradley K, McMahon SB. Methodology for quantifying excitability of identified projection neurons in the dorsal horn of the spinal cord, specifically to study spinal cord stimulation paradigms. J Neurosci Methods 2020;330:108479.
Staley KJ, Proctor WR. Modulation of mammalian dendritic GABA(A) receptor function by the kinetics of Cl- and HCO3- transport. J Physiol 1999;519:693–712.
Staud R. Predictors of clinical pain intensity in patients with fibromyalgia syndrome. Curr Pain Headache Rep 2005;9:316–21.
Staud R, Cannon RC, Mauderli AP, Robinson ME, Price DD, Vierck CJ Jr. Temporal summation of pain from mechanical stimulation of muscle tissue in normal controls and subjects with fibromyalgia syndrome. PAIN 2003;102:87–95.
Stiller CO, Cui JG, O'Connor WT, Brodin E, Meyerson BA, Linderoth B. Release of gamma-aminobutyric acid in the dorsal horn and suppression of tactile allodynia by spinal cord stimulation in mononeuropathic rats. Neurosurgery 1996;39:367–74. discussion 374–5.
Sullivan SJ, Sdrulla AD. Excitatory and inhibitory neurons of the spinal cord superficial dorsal horn diverge in their somatosensory responses and plasticity in vivo. J Neurosci 2022;42:1958–73.
Suzuki R, Dickenson A. Spinal and supraspinal contributions to central sensitization in peripheral neuropathy. Neurosignals 2005;14:175–81.
Suzuki R, Hunt SP, Dickenson AH. The coding of noxious mechanical and thermal stimuli of deep dorsal horn neurones is attenuated in NK1 knockout mice. Neuropharmacology 2003;45:1093–100.
Suzuki R, Morcuende S, Webber M, Hunt SP, Dickenson AH. Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways. Nat Neurosci 2002;5:1319–26.
Thalhammer JG, Raymond SA, Popitz-Bergez FA, Strichartz GR. Modality-dependent modulation of conduction by impulse activity in functionally characterized single cutaneous afferents in the rat. Somatosensory Mot Res 1994;11:243–57.
Thompson SW, King AE, Woolf CJ. Activity-dependent changes in rat ventral horn neurons in vitro; summation of prolonged afferent evoked postsynaptic depolarizations produce a d-2-amino-5-phosphonovaleric acid sensitive windup. Eur J Neurosci 1990;2:638–49.
Tian L, Ji G, Wang C, Bai X, Lu Y, Xiong L. Excitatory synaptic transmission in the spinal substantia gelatinosa is under an inhibitory tone of endogenous adenosine. Neurosci Lett 2010;477:28–32.
Torebjork HE, Hallin RG. Responses in human A and C fibres to repeated electrical intradermal stimulation. J Neurol Neurosurg Psychiatry 1974;37:653–64.
Vierck CJ Jr, Cannon RL, Fry G, Maixner W, Whitsel BL. Characteristics of temporal summation of second pain sensations elicited by brief contact of glabrous skin by a preheated thermode. J Neurophysiol 1997;78:992–1002.
Wan YH, Hu SJ. Short-term depression at primary afferent synapses in rat substantia gelatinosa region. Neuroreport 2003;14:197–200.
Wan YH, Jian Z, Wang WT, Xu H, Hu SJ, Ju G. Short-term plasticity at primary afferent synapse in rat spinal dorsal horn and its biological function. Neurosignals 2006;15:74–90.
Waxman SG, Cummins TR, Dib-Hajj S, Fjell J, Black JA. Sodium channels, excitability of primary sensory neurons, and the molecular basis of pain. Muscle Nerve 1999;22:1177–87.
Woda A, Blanc O, Voisin DL, Coste J, Molat JL, Luccarini P. Bidirectional modulation of windup by NMDA receptors in the rat spinal trigeminal nucleus. Eur J Neurosci 2004;19:2009–16.
Woolf CJ. Windup and central sensitization are not equivalent. PAIN 1996;66:105–8.
Xu-Friedman MA, Regehr WG. Structural contributions to short-term synaptic plasticity. Physiol Rev 2004;84:69–85.
Xu XJ, Dalsgaard CJ, Wiesenfeld-Hallin Z. Spinal substance P and N-methyl-D-aspartate receptors are coactivated in the induction of central sensitization of the nociceptive flexor reflex. Neuroscience 1992;51:641–8.
Yoon KW, Rothman SM. The modulation of rat hippocampal synaptic conductances by baclofen and gamma-aminobutyric acid. J Physiol 1991;442:377–90.
Yoshimura M. Slow synaptic transmission in the spinal dorsal horn. Prog Brain Res 1996;113:443–62.
Zemoura K, Ralvenius WT, Malherbe P, Benke D. The positive allosteric GABAB receptor modulator rac-BHFF enhances baclofen-mediated analgesia in neuropathic mice. Neuropharmacology 2016;108:172–8.
Zhang W, Schneider SP. Short-term modulation at synapses between neurons in laminae II-V of the rodent spinal dorsal horn. J Neurophysiol 2011;105:2920–30.
Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 2002;64:355–405.

Auteurs

Lou Cathenaut (L)

Centre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives, Strasbourg, France.

Classifications MeSH