Excitatory synaptic transmission and network activity are depressed following mechanical injury in cortical neurons

Journal of Neurophysiology

Volumn 105, Issue 5, 2011, Pages 2350-2363

  Goforth, Paulette B ^a   Ren, Jianhua ^a   Schwartz, Benjamin S ^a   Satin, Leslie S ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

amino 3 hydroxyl 5 methyl 4 isoxazolepropionate receptors; N methyl D aspartate; Oscillations; Traumatic brain injury

Indexed keywords

CALCIUM; CHLORPHENIRAMINE MALEATE PLUS PHENYLEPHRINE; N METHYL DEXTRO ASPARTIC ACID;

AMPLITUDE MODULATION; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CONTROLLED STUDY; LONG TERM DEPRESSION; NERVE CELL LESION; NERVE CELL NETWORK; NERVE CELL STIMULATION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SYNAPTIC TRANSMISSION; TRAUMATIC BRAIN INJURY;

ANIMALS; ANIMALS, NEWBORN; CALCIUM SIGNALING; CELLS, CULTURED; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM SYNAPTIC DEPRESSION; NEOCORTEX; NERVE NET; NEURONAL PLASTICITY; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION;

EID: 79956260642     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00467.2010     Document Type: Article

References (72)

1. Ashman TA, Gordon WA, Cantor JB, Hibbard MR. Neurobehavioral consequences of traumatic brain injury. Mt Sinai J Med 73: 999-1005, 2006.
2. Atkins CM, Chen S, Alonso OF, Dietrich WD, Hu BR. Activation of calcium/calmodulin-dependent protein kinases after traumatic brain injury. J Cereb Blood Flow Metab 26: 1507-1518, 2006.
3. Avramescu S, Timofeev I. Synaptic strength modulation after cortical trauma: a role in epileptogenesis. J Neurosci 28: 6760-6772, 2008.
4. Bell JD, Ai J, Chen Y, Baker AJ. Mild in vitro trauma induces rapid Glur2 endocytosis, robustly augments calcium permeability and enhances susceptibility to secondary excitotoxic insult in cultured Purkinje cells. Brain 130: 2528-2542, 2007.
5. Bell JD, Park E, Ai J, Baker AJ. PICK1-mediated GluR2 endocytosis contributes to cellular injury after neuronal trauma. Cell Death Differ 16: 1665-1680, 2009.
6. Biegon A, Fry PA, Paden CM, Alexandrovich A, Tsenter J, Shohami E. Dynamic changes in N-methyl-D-aspartate receptors after closed head injury in mice: implications for treatment of neurological and cognitive deficits. Proc Natl Acad Sci USA 101: 5117-5122, 2004.
7. Calderone A, Jover T, Noh KM, Tanaka H, Yokota H, Lin Y, Grooms SY, Regis R, Bennett MV, Zukin RS. Ischemic insults derepress the gene silencer REST in neurons destined to die. J Neurosci 23: 2112-2121, 2003.
8. Chung HJ, Steinberg JP, Huganir RL, Linden DJ. Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression. Science 300: 1751-1755, 2003.
9. Cohen AS, Pfister BJ, Schwarzbach E, Grady MS, Goforth PB, Satin LS. Injury-induced alterations in CNS electrophysiology. Prog Brain Res 161: 143-169, 2007.
10. Cole JT, Mitala CM, Kundu S, Verma A, Elkind JA, Nissim I, Cohen AS. Dietary branched chain amino acids ameliorate injury-induced cognitive impairment. Proc Natl Acad Sci USA 107: 366-371, 2010.
11. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr Opin Neurobiol 16: 288-297, 2006.
12. Cull-Candy SG, Leszkiewicz DN. Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004 (255): re16, 2004.
13. D'Ambrosio R, Maris DO, Grady MS, Winn HR, Janigro D. Selective loss of hippocampal long-term potentiation, but not depression, following fluid percussion injury. Brain Res 786: 64-79, 1998.
14. Ellis EF, McKinney JS, Willoughby KA, Liang S, Povlishock JT. A new model for rapid stretch-induced injury of cells in culture: characterization of the model using astrocytes. J Neurotrauma 12: 325-339, 1995.
15. Goforth PB, Ellis EF, Satin LS. Enhancement of AMPA-mediated current after traumatic injury in cortical neurons. J Neurosci 19: 7367-7374, 1999.
16. Goforth PB, Ellis EF, Satin LS. Mechanical injury modulates AMPA receptor kinetics via an NMDA receptor-dependent pathway. J Neurotrauma 21: 719-732, 2004.
17. Golarai G, Greenwood AC, Feeney DM, Connor JA. Physiological and structural evidence for hippocampal involvement in persistent seizure susceptibility after traumatic brain injury. J Neurosci 21: 8523-8537, 2001.
18. Grosskreutz J, Zoerner A, Schlesinger F, Krampfl K, Dengler R, Bufler J. Kinetic properties of human AMPA-type glutamate receptors expressed in HEK293 cells. Eur J Neurosci 17: 1173-1178, 2003.
19. Guire ES, Oh MC, Soderling TR, Derkach VA. Recruitment of calciumpermeable AMPA receptors during synaptic potentiation is regulated by CaM-kinase I. J Neurosci 28: 6000-6009, 2008.
20. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391: 85-100, 1981.
21. Herrington J, Bookman RJ. Pulse control v4.3: Igor XOP's for patch clamp data acquisition. Miami, FL: Univ of Miami Press, 1994.
22. Hoffman SN, Salin PA, Prince DA. Chronic neocortical epileptogenesis in vitro. J Neurophysiol 71: 1762-1773, 1994.
23. Huettner JE, Baughman RW. Primary culture of identified neurons from the visual cortex of postnatal rats. J Neurosci 6: 3044-3060, 1986.
24. Isaac JT, Ashby M, McBain CJ. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54: 859-871, 2007.
25. Jin X, Prince DA, Huguenard JR. Enhanced excitatory synaptic connectivity in layer v pyramidal neurons of chronically injured epileptogenic neocortex in rats. J Neurosci 26: 4891-4900, 2006.
26. Jones TL, Sorkin LS. Calcium-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid/kainate receptors mediate development, but not maintenance, of secondary allodynia evoked by first-degree burn in the rat. J Pharmacol Exp Ther 310: 223-229, 2004.
27. Ju W, Morishita W, Tsui J, Gaietta G, Deerinck TJ, Adams SR, Garner CC, Tsien RY, Ellisman MH, Malenka RC. Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat Neurosci 7: 244-253, 2004.
28. Kampfl A, Posmantur RM, Zhao X, Schmutzhard E, Clifton GL, Hayes RL. Mechanisms of calpain proteolysis following traumatic brain injury: implications for pathology and therapy: implications for pathology and therapy: a review and update. J Neurotrauma 14: 121-134, 1997.
29. A currents after mechanical injury of cortical neurons. J Neurotrauma 21: 259-270, 2004.
30. 2+-permeable AMPA receptors in cultured rat hippocampal neurons. Neurosci Res 29: 27-36, 1997.
31. Kumar A, Zou L, Yuan X, Long Y, Yang K. N-methyl-D-aspartate receptors: transient loss of NR1/NR2A/NR2B subunits after traumatic brain injury in a rodent model. J Neurosci Res 67: 781-786, 2002.
32. Kurz JE, Hamm RJ, Singleton RH, Povlishock JT, Churn SB. A persistent change in subcellular distribution of calcineurin following fluid percussion injury in the rat. Brain Res 1048: 153-160, 2005.
33. Kwak S, Weiss JH. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr Opin Neurobiol 16: 281-287, 2006.
34. Lea PM, Custer SJ, Vicini S, Faden AI. Neuronal and glial mGluR5 modulation prevents stretch-induced enhancement of NMDA receptor current. Pharmacol Biochem Behav 73: 287-298, 2002.
35. Lea PM 4th, Custer SJ, Stoica BA, Faden AI. Modulation of stretch-induced enhancement of neuronal NMDA receptor current by mGluR1 depends upon presence of glia. J Neurotrauma 20: 1233-1249, 2003.
36. Li G, Pei W, Niu L. Channel-opening kinetics of GluR2Q(flip) AMPA receptor: a laser-pulse photolysis study. Biochemistry 42: 12358-12366, 2003.
37. Li H, Prince DA. Synaptic activity in chronically injured, epileptogenic sensory-motor neocortex. J Neurophysiol 88: 2-12, 2002.
38. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci 30: 126-134, 2007.
39. Malinow R, Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126, 2002.
40. McKinney JS, Willoughby KA, Liang S, Ellis EF. Stretch-induced injury of cultured neuronal, glial, and endothelial cells. Effect of polyethylene glycolconjugated superoxide dismutase. Stroke 27: 934-940, 1996.
41. Miyazaki S, Katayama Y, Lyeth BG, Jenkins LW, DeWitt DS, Goldberg SJ, Newlon PG, Hayes RL. Enduring suppression of hippocampal longterm potentiation following traumatic brain injury in rat. Brain Res 585: 335-339, 1992.
42. Murphy TH, Blatter LA, Wier WG, Baraban JM. Spontaneous synchronous synaptic calcium transients in cultured cortical neurons. J Neurosci 12: 4834-4845, 1992.
43. Nakanishi K, Kukita F. Functional synapses in synchronized bursting of neocortical neurons in culture. Brain Res 795: 137-146, 1998.
44. Oh MC, Derkach VA. Dominant role of the GluR2 subunit in regulation of AMPA receptors by CaMKII. Nat Neurosci 8: 853-854, 2005.
45. Osteen CL, Giza CC, Hovda DA. Injury-induced alterations in N-methyl-Daspartate receptor subunit composition contribute to prolonged 45calcium accumulation following lateral fluid percussion. Neuroscience 128: 305-322, 2004.
46. Park E, Bell JD, Baker AJ. Traumatic brain injury: can the consequences be stopped? CMAJ 178: 1163-1170, 2008.
47. Prince DA, Tseng GF. Epileptogenesis in chronically injured cortex: in vitro studies. J Neurophysiol 69: 1276-1291, 1993.
48. Reeves TM, Kao CQ, Phillips LL, Bullock MR, Povlishock JT. Presynaptic excitability changes following traumatic brain injury in the rat. J Neurosci Res 60: 370-379, 2000.
49. Reeves TM, Lyeth BG, Povlishock JT. Long-term potentiation deficits and excitability changes following traumatic brain injury. Exp Brain Res 106: 248-256, 1995.
50. Robinson HP, Kawahara M, Jimbo Y, Torimitsu K, Kuroda Y, Kawana A. Periodic synchronized bursting and intracellular calcium transients elicited by low magnesium in cultured cortical neurons. J Neurophysiol 70: 1606-1616, 1993.
51. Rogawski MA, Donevan SD. AMPA receptors in epilepsy and as targets for antiepileptic drugs. Adv Neurol 79: 947-963, 1999.
52. Salin P, Tseng GF, Hoffman S, Parada I, Prince DA. Axonal sprouting in layer V pyramidal neurons of chronically injured cerebral cortex. J Neurosci 15: 8234-8245, 1995.
53. Sanders MJ, Sick TJ, Perez-Pinzon MA, Dietrich WD, Green EJ. Chronic failure in the maintenance of long-term potentiation following fluid percussion injury in the rat. Brain Res 861: 69-76, 2000.
54. Santhakumar V, Ratzliff AD, Jeng J, Toth Z, Soltesz I. Long-term hyperexcitability in the hippocampus after experimental head trauma. Ann Neurol 50: 708-717, 2001.
55. Santos SD, Carvalho AL, Caldeira MV, Duarte CB. Regulation of AMPA receptors and synaptic plasticity. Neuroscience 158: 105-125, 2009.
56. Schumann J, Alexandrovich GA, Biegon A, Yaka R. Inhibition of NR2B phosphorylation restores alterations in NMDA receptor expression and improves functional recovery following traumatic brain injury in mice. J Neurotrauma 25: 945-957, 2008.
57. Schwarzbach E, Bonislawski DP, Xiong G, Cohen AS. Mechanisms underlying the inability to induce area CA1 LTP in the mouse after traumatic brain injury. Hippocampus 16: 541-550, 2006.
58. Seidenman KJ, Steinberg JP, Huganir R, Malinow R. Glutamate receptor subunit 2 Serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells. J Neurosci 23: 9220-9228, 2003.
59. Spaethling JM, Klein DM, Singh P, Meaney DF. Calcium-permeable AMPA receptors appear in cortical neurons after traumatic mechanical injury and contribute to neuronal fate. J Neurotrauma 25: 1207-1216, 2008.
60. Sutton MA, Ito HT, Cressy P, Kempf C, Woo JC, Schuman EM. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 125: 785-799, 2006.
61. Swanson GT, Kamboj SK, Cull-Candy SG. Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17: 58-69, 1997.
62. Takazawa A, Yamazaki O, Kanai H, Ishida N, Kato N, Yamauchi T. Potent and long-lasting anticonvulsant effects of 1-naphthylacetyl spermine, an analogue of Joro spider toxin, against amygdaloid kindled seizures in rats. Brain Res 706: 173-176, 1996.
63. Terashima A, Pelkey KA, Rah JC, Suh YH, Roche KW, Collingridge GL, McBain CJ, Isaac JT. An essential role for PICK1 in NMDA receptordependent bidirectional synaptic plasticity. Neuron 57: 872-882, 2008.
64. Topolnik L, Steriade M, Timofeev I. Hyperexcitability of intact neurons underlies acute development of trauma-related electrographic seizures in cats in vivo. Eur J Neurosci 18: 486-496, 2003.
65. Turrigiano GG. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135: 422-435, 2008.
66. 2+-permeable AMPA and reduced NR2B NMDA receptor-mediated neurotransmission at dorsal horn nociceptive synapses during inflammatory pain in the rat. J Physiol 586: 515-527, 2008.
67. 2+ oscillations in cortical neurons. Brain Res 767: 239-249, 1997.
68. Witgen BM, Lifshitz J, Smith ML, Schwarzbach E, Liang SL, Grady MS, Cohen AS. Regional hippocampal alteration associated with cognitive deficit following experimental brain injury: a systems, network and cellular evaluation. Neuroscience 133: 1-15, 2005.
69. Yaka R, Biegon A, Grigoriadis N, Simeonidou C, Grigoriadis S, Alexandrovich AG, Matzner H, Schumann J, Trembovler V, Tsenter J, Shohami E. D-cycloserine improves functional recovery and reinstates long-term potentiation (LTP) in a mouse model of closed head injury. Faseb J 21: 2033-2041, 2007.
70. Yang K, Taft WC, Dixon CE, Todaro CA, Yu RK, Hayes RL. Alterations of protein kinase C in rat hippocampus following traumatic brain injury. J Neurotrauma 10: 287-295, 1993.
71. Yang L, Benardo LS, Valsamis H, Ling DS. Acute injury to superficial cortex leads to a decrease in synaptic inhibition and increase in excitation in neocortical layer V pyramidal cells. J Neurophysiol 97: 178-187, 2007.
72. Zhang L, Rzigalinski BA, Ellis EF, Satin LS. Reduction of voltage-dependent Mg2+ blockade of NMDA current in mechanically injured neurons. Science 274: 1921-1923, 1996.