Roles of synaptic metaplasticity in the recovery after spinal cord injury

Abstract

Abstract: The term synaptic plasticity describes the ability of excitatory synapse to undergo activity-dependent long-term changes in the efficacy of synaptic transmission. This change includes LTP and LTD. Metaplasticity is a high-order form of synaptic plasticity that regulates the expressions of LTP and LTD through prime stimulation. The synaptic plasticity in spinal cord and its role in the recovery after spinal cord injury have been widely reported in recent years, research on mechanism underlying metaplasticity and its role in the recovery after spinal cord injury has become a hotspot. And it will be focused in this review.

Key words: spinal cord injury, synaptic plasticity, metaplasticity

CLC Number:

R744

QIN Wen, ZHANG Yan, WANG Meng-ya. Roles of synaptic metaplasticity in the recovery after spinal cord injury[J]. Chinese Journal of Clinical Pharmacology and Therapeutics, 2014, 19(11): 1288-1293.

References 57

[1]	Lynskey JV, Belanger A, Jung R.Activity-dependent plasticity in spinal cord injury[J]. J Rehabil Res Dev, 2008, 45(2): 229-240.
[2]	Bliss TV, Lomo T.Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path[J]. J Physiol, 1973, 232(2):331-356.
[3]	Izquierdo I, Cammarota M, Da Silva WC, et al.The evidence for hippocampal long-term potentiation as a basis of memory for simple tasks[J]. An Acad Bras Ciênc, 2008, 80(1):115-127.
[4]	Ikeda H, Kiritoshi T, Murase K.Synaptic plasticity in the spinal dorsal horn[J]. Neurosci Res, 2009, 64(2):133-136.
[5]	Kniffki KD, Schomburg ED, Steffens H.Synaptic effects from chemically activated fine muscle afferents upon alpha-motoneurones in decerebrate and spinal cats[J]. Brain Res, 1981, 206(2):361-370.
[6]	Wolpaw JR, Tennissen AM.Activity-dependent spinal cord plasticity in health and disease[J]. Annu Rev Neurosci, 2001, 24:807-843.
[7]	江潇, 汪萌芽. 对侧腹外侧索强直刺激在脊髓运动神经元诱发的长时程增强[J]. 皖南医学院学报, 2008, 27(6): 391-394, 398.
[8]	Briggman KL, Kristan WB.Multifunctional pattern-generating circuits[J]. Annu Rev Neurosci, 2008, 31: 271-294.
[9]	Rossignol S, Frigon A, Barrière G, et al.Spinal plasticity in the recovery of locomotion[J]. Prog Brain Res, 2011, 188: 229-241.
[10]	Joynes RL, Grau JW.Mechanisms of Pavolovian conditioning: role of protection from habituation in spinal conditioning[J]. Behav Neurosci, 1996, 110(6):1375-1387.
[11]	Grau JW, Barstow DG, Joynes RL.Instrumental learning within the spinal cord: I. Behavioral properties[J]. Behav Neurosci, 1998, 112(6): 1366-1386.
[12]	Wolpaw JR.Spianl cord plasticity in acquisition and maintenance of motor skills[J]. Acta Physiol(Oxf), 2007, 189(2): 155-169.
[13]	Barriere G, Leblond H, Provencher J, et al.Prominent role of the spinal central pattern generator in the recovery of locomotion after partial spinal cord injuries[J]. J Neurosci, 2008, 28(15): 3976-3987.
[14]	Abraham WC.Metaplasticity: turning synapses and networks for plasticity[J]. Nat Rev Neurosci, 2008, 9(5):387.
[15]	Grau JW, Crown ED, Ferguson AR, et al.Instrumental learning within the spinal cord: underlying mechanisms and implications for recovery after injury[J]. Behav Cogn Neurosci Rev, 2006, 5(4): 191-239.
[16]	Bartlett TE, Bannister NJ, Collett VJ, et al.Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-Week old rat hippocampus[J]. Neuropharmacology, 2007, 52(1): 60-70.
[17]	Moser EI, Krobert KA, Moser MB, et al.Impaired spatial learning after saturation of long-term potentiation[J]. Science, 1998, 281(5385): 2038-2042.
[18]	Zorumski CF, Izumi Y.NMDA receptors and metaplasticity: Mechanisms and possible roles in neuropsychiatric disorders[J]. Neurosci Biobehav Rev, 2012, 36(3): 989-1000.
[19]	Oh MC, Derkach VA, Guire ES, et al.Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation[J]. J Biol Chem, 2006, 281(2): 752-758.
[20]	Tenorio G, Connor SA, Guévremont D, et al.'Silent' priming of translation-dependent LTP by β-adrenergic receptors involves phosphorylation and recruitment of AMPA receptors[J]. Learn Mem, 2010, 17(12): 627-638.
[21]	Ren SQ, Yan JZ, Zhang XY, et al.PKCλ is critical in AMPA receptor phosphorylation and synaptic incorporation during LTP[J]. EMBO J, 2013, 32(10): 1365-1380.
[22]	Ugolini A, Corsi M, Bordi F.Potentiation of NMDA and AMPA responses by group I mGluR in spinal cord motoneurons[J]. Neuropharmacology, 1997, 36(8): 1047-1055.
[23]	Guo W, Wei F, Zou S, et al.Group I metabotropic glutamate receptor NMDA receptor coupling and signaling cascade mediate s pinal dorsal horn NMDA receptor 2B tyrosine phosphorylation associated with inflammatory hyperalgesia[J]. J Neurosci, 2004, 24(41): 9161-9173.
[24]	Castro-Lopes JM, Malcangio M, Pan BH, et al.Complex changes of GABAA and GABAB receptor binding in the spinal cord dorsal horn following peripheral inflammation or neurectomy[J]. Brain Res, 1995, 679(2): 289-297.
[25]	Miletic G, Miletic V.Contribution of GABA-A receptors to metaplasticity in the spinal dorsal horn[J]. Pain, 2001, 90(1/2): 157-162.
[26]	Kvarta MD, Harris-Warrick RM, Johnson BR.Neuronmodulator-evoked synaptic metaplasticity within a central pattern generator network[J]. J Neurophysiol, 2012, 108(10): 2846-2856.
[27]	Parker D, Grillner S.Activity-dependent metaplasticity of inhibitory and excitatory synaptic transmission in the lamprey spinal cord locomotor network[J]. J Neurosci, 1999, 19(5): 1647-1656.
[28]	Parker D.Spinal-Cord plasticity: independent and interactive effects of neuromodulator and activity-dependent plasticity[J]. Mol Neurobiol, 2000, 22(1/2/3): 55-80.
[29]	Bevan S, Parker D.Metaplastic facilitation and ultrastructural changes in synaptic properties are associated with long-term modulation of the lamprey locomotor network[J]. J Neurosci, 2004, 24(42): 9458-9468.
[30]	Coba MP, Pocklington AJ, Collins MO, et al. Neurotransmitters drive combinatorial multistate postsynaptic density networks[J]. Sci Signal, 2009, 2(68): ral 19.
[31]	Young JZ, Isiegas C, Abel T, et al.Metaplasticity of the late-phase of long-term potentiation: a critical role for protein kinase A in synaptic tagging[J]. Eur J Neurosci, 2006, 23(7): 1784-1794.
[32]	Sweatt JD.Mitogen-activated protein kinases in synaptic plasticity and memory[J]. Curr Opin Neurobiol, 2004, 14(3): 311-317.
[33]	Anwyl R.Induction and expression mechanisms of postsynaptic NMDA receptor-independent homosynaptic long-term depression[J]. Prog Neurobiol, 2006, 78(1):17-37.
[34]	Zhu Y, Pak D, Qin Y, et al.Rap-2-JNK removes synaptic AMPA receptors during depotentiation[J]. Neuron, 2005, 46(6): 905-916.
[35]	Flynn JR, Dunn LR, Galea MP, et al.Exercise training after spinal cord injury selectively alters synaptic properties in neurons in adult mouse spinal cord[J]. J Neurotrauma, 2013, 30(10): 891-896.
[36]	Grau JW, Crown ED, Ferguson AR, et al.Instrumental learning within the spinal cord: underlying mechanisms and implications for recovery after injury[J]. Behav Cogn Neurosci Rev, 2006, 5(4): 191-239.
[37]	Baumbauer KM, Hoy KC Jr, Huie JR, et al.Timing in the absence of supraspinal input I: variable, but not fixed, spaced stimulation of the sciatic nerve undermines spinally-mediated instrumental learning[J]. Neuroscience, 2008, 155(4): 1030-1047.
[38]	Grau JW, Washbum SN, Hook MA, et al.Uncontrollable stimulation undermines recovery after spinal cord injury[J]. J Neurotrauma, 2004, 21(12): 1795-1817.
[39]	Gwak YS, Hulsebosch CE.GABA and central neuropathic pain following spinal cord injury[J]. Neuropharmacology, 2011, 60(5): 799-808.
[40]	Martinez M, Delivet-Mongrain H, Leblond H, et al.Recovery of hindlimb locomotion after incomplete spinal cord injury in the cat involves spontaneous compensatory changes within the spinal locomotor circuitry[J]. J Neurophysiol, 2011, 106(4): 1969-1984.
[41]	Acevedo JM, Díaz-Ríos M.Removing sensory input disrupts spinal locomotor activity in the early postnatal period[J]. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 2013, 199(12): 1105-1116.
[42]	Martinez M, Rossignol S.A dual spinal cord lesion paradigm to study spinal locomotor plasticity in the cat[J]. Ann N Y Acad Sci, 2013, 1279: 127-134.
[43]	Ma L, Shen YQ, Khatri HP, et al.The asparaginyl endopeptidase legumain is essential for functional recovery after spinal cord injury in adult zebrafish[J]. PLoS One,2014, 9(4): e95098.
[44]	Pan HC, Lin JF, Ma LP, et al.Major vault protein promotes locomotor recovery and regeneration after spinal cord injury in adult zebrafish[J]. Eur J Neurosci, 2013, 37(2): 203-211.
[45]	Gwak YS, Hulsebosch CE.GABA and central neuropathic pain following spinal cord injury[J]. Neuropharmacology, 2011, 60(5): 799-808.
[46]	Ferguson AR, Bolding KA, Huie JR, et al.Group I metabotropic glutamate receptors control metaplasticity of spinal cord learning through a protein kinase C-dependent mechanism[J]. J Neurosci, 2008, 28(46):11939-11949.
[47]	Gwak YS, Kang J, Unabia GC, et al.Spatial and temporal activation of spinal glial cells: role of gliopathy in central neuropathic pain following spinal cord injury in rats[J]. Exp Neurol, 2012, 234(2): 362-372.
[48]	Carlton SM, Du J, Tan HY, et al.Peripheral and central sensitization in remote spinal cord regions contribute to central neuropathic pain after spinal cord injury[J]. Pain, 2009, 147(1/2/3): 265-276.
[49]	Gwak YS, Hulsebosch CE.Remote astrocytic and microglial activation modulates neuronal hyperexcitability and below-level neuropathic pain after spinal injury in rat[J]. Neuroscience, 2009, 161(3): 895-903.
[50]	Huie JR, Baumbauer KM, Lee KH, et al.Glial tumor necrosis factor alpha (TNFα) generates metaplastic inhibition of spinal learning[J]. PLoS One, 2012, 7(6): e39751.
[51]	Harkema S, Gerasimenko Y, Hodes J, et al.Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study[J]. Lancet, 2011, 377(9781): 1938-1947.
[52]	Zhang HM, Zhang H, Dougherty PM.Dynamic effects of TNF-α on synaptic transmission in mice over time following sciatic nerve chronic constriction injury[J]. J Neurophysiol, 2013, 110(7):1663-1671.
[53]	Zhou LJ, Zhong Y, Ren WJ, et al.BDNF induces late-phase LTP of C-fiber evoked field potentials in rat spinal dorsal horn[J]. Exp Neurol, 2008, 212(2): 507-514.
[54]	Huie JR, Garraway SM, Baumbauer KM, et al.Brain-derived neurotrophic factor promotes adaptive plasticity within the spinal cord and mediates the beneficial effects of controllable stimulation[J]. Neuroscience, 2012, 200: 74-90.
[55]	Bramham CR, Messaoudi E.BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis[J]. Prog Neurobiol, 2005, 76(2): 99-125.
[56]	Park BN, Kim SW, Cho SR, et al.Epigenetic regulation in the brain after spinal cord injury: a comparative study[J]. J Korean Neurosurg Soc, 2013, 53(6): 337-341.
[57]	Huang J, Zhang Y, Lu L, et al.Electrical stimulation accelerates nerve regeneration and functional recovery in delayed peripheral nerve injury in rats[J]. Eur J Neurosci, 2013, 38(12):3691-3701.