Hypoxia-induced neonatal seizures diminish silent synapses and long-term potentiation in hippocampal CA1 neurons

Journal of Neuroscience

Volumn 31, Issue 50, 2011, Pages 18211-18222

  Zhou, Chengwen ^a,b   Bell, Jocelyn J Lippman ^a,b   Sun, Hongyu ^a,b   Jensen, Frances E ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 NITRO 7 SULFAMOYLBENZO [F] QUINOXALINE 2, 3 DIONE; AMPA RECEPTOR; GLUTAMATE RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPAL CA1 REGION; HYPOXIA INDUCED SEIZURE; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RAT; SEIZURE; SILENT SYNAPSE; SYNAPSE; SYNAPTIC COLOCALIZATION;

ANIMALS; ANOXIA; CA1 REGION, HIPPOCAMPAL; LONG-TERM POTENTIATION; MALE; NEURONS; RATS; RATS, LONG-EVANS; RECEPTORS, N-METHYL-D-ASPARTATE; SEIZURES; SYNAPSES;

EID: 83455163684     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4838-11.2011     Document Type: Article

References (67)

1. Asaka Y, Jugloff DG, Zhang L, Eubanks JH, Fitzsimonds RM (2006) Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol Dis 21:217-227
2. Bassell GJ, Warren ST (2008) Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60:201-214
3. Benke TA, Lüthi A, Isaac JT, Collingridge GL (1998) Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393:793-797
4. Berg AT (2011) Epilepsy, cognition, and behavior: the clinical picture. Epilepsia 52 [Suppl 1]:7-12
5. Bittigau P, Sifringer M, Genz K, Reith E, Pospischil D, Govindarajalu S, Dzietko M, Pesditschek S, Mai I, Dikranian K, Olney JW, Ikonomidou C (2002) Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. Proc Natl Acad Sci U S A 99:15089-15094
6. Boehm J, Kang MG, Johnson RC, Esteban J, Huganir RL, Malinow R (2006) Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 51:213-225
7. Busetto G, Higley MJ, Sabatini BL (2008) Developmental presence and disappearance of postsynaptically silent synapses on dendritic spines of rat layer 2/3 pyramidal neurons. J Physiol 586:1519-1527
8. Carreño M, Donaire A, Sánchez-Carpintero R (2008) Cognitive disorders associated with epilepsy: diagnosis and treatment. Neurologist 14:S26-34
9. Cornejo BJ, Mesches MH, Benke TA (2008) A single early-life seizure impairs short-term memory but does not alter spatial learning, recognition memory, or anxiety. Epilepsy Behav 13:585-592
10. Crump FT, Dillman KS, Craig AM (2001) CAMP-dependent protein kinase mediates activity-regulated synaptic targeting ofNMDAreceptors. J Neurosci 21:5079-5088
11. Dodrill CB (2002) Progressive cognitive decline in adolescents and adults with epilepsy. Prog Brain Res 135:399-407
12. Dumas TC (2005) Late postnatal maturation of excitatory synaptic transmission permits adult-like expression of hippocampal-dependent behaviors. Hippocampus 15:562-578
13. Durand GM, Kovalchuk Y, Konnerth A (1996) Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381:71-75
14. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143
15. Hayashi T, Huganir RL (2004) Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases. J Neurosci 24:6152-6160
16. Hoeffer CA, Klann E (2010) MTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci 33:67-75
17. Holmes GL, Ben-Ari Y (2007) A single episode of neonatal seizures permanently alters glutamatergic synapses. Ann Neurol 61:379-381
18. Hoppe C, Elger CE, Helmstaedter C (2007) Long-term memory impairment in patients with focal epilepsy. Epilepsia 48 [Suppl 9]:26-29
19. Huang LT, Yang SN, Liou CW, Hung PL, Lai MC, Wang CL, Wang TJ (2002) Pentylenetetrazol-induced recurrent seizures in rat pups: time course on spatial learning and long-term effects. Epilepsia 43:567-573
20. Huttenlocher PR, Wollmann RL (1991) Cellular neuropathology of tuberous sclerosis. Ann NY Acad Sci 615:140-148
21. Isaac JT (2003) Postsynaptic silent synapses: evidence and mechanisms. Neuropharmacology 45:450-460
22. Isaac JT, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434
23. Isaac JT, Hjelmstad GO, Nicoll RA, Malenka RC (1996) Long-term potentiation at single fiber inputs to hippocampal CA1 pyramidal cells. Proc Natl Acad Sci U S A 93:8710-8715
24. Isaac JT, Crair MC, Nicoll RA, Malenka RC (1997) Silent synapses during development of thalamocortical inputs. Neuron 18:269-280
25. Jensen FE (2009) Introduction-epileptogenic cortical dysplasia: emerging trends in diagnosis, treatment, and pathogenesis. Epilepsia 50 [Suppl 9]:1-2
26. Jensen FE, Holmes GL, Lombroso CT, Blume HK, Firkusny IR (1992) Agedependent changes in long-term seizure susceptibility and behavior after hypoxia in rats. Epilepsia 33:971-980
27. Jensen FE, Blume H, Alvarado S, Firkusny I, Geary C (1995) NBQX blocks acute and late epileptogenic effects of perinatal hypoxia. Epilepsia 36:966-972
28. Jensen FE, Wang C, Stafstrom CE, Liu Z, Geary C, Stevens MC (1998) Acute and chronic increases in excitability in rat hippocampal slices after perinatal hypoxia in vivo. J Neurophysiol 79:73-81
29. Karnam HB, Zhao Q, Shatskikh T, Holmes GL (2009) Effect of age on cognitive sequelae following early life seizures in rats. Epilepsy Res 85:221-230
30. Kerchner GA, Nicoll RA (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9:813-825
31. Koh S, Tibayan FD, Simpson JN, Jensen FE (2004) NBQX or topiramate treatment following perinatal hypoxia-induced seizures prevents later increases in seizure-induced neuronal injury. Epilepsia 45:569-575
32. Kullmann DM (1994) Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: Implications for long-term potentiation. Neuron 12:1111-1120
33. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400-404
34. Liao D, Scannevin RH, Huganir R (2001) Activation of silent synapses by rapid activity-dependent synaptic recruitment ofAMPAreceptors. J Neurosci 21:6008-6017
35. Lin JW, Ju W, Foster K, Lee SH, Ahmadian G, Wyszynski M, Wang YT, Sheng M (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat Neurosci 3:1282-1290
36. Lisman J, Raghavachari S (2006) A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE 356:re11.
37. Losi G, Prybylowski K, Fu Z, Luo JH, Vicini S (2002) Silent synapses in developing cerebellar granule neurons. J Neurophysiol 87:1263-1270
38. Makino Y, Johnson RC, Yu Y, Takamiya K, Huganir RL (2011) Enhanced synaptic plasticity in mice with phosphomimetic mutation of the GluA1 AMPA receptor. Proc Natl Acad Sci U S A 108:8450-8455
39. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126
40. Marie H, Morishita W, Yu X, Calakos N, Malenka RC (2005) Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45:741-752
41. Mikati MA, Zeinieh MP, Kurdi RM, Harb SA, El Hokayem JA, Daderian RH, Shamseddine A, Obeid M, Bitar FF, El Sabban M (2005) Long-term effects of acute and of chronic hypoxia on behavior and on hippocampal histology in the developing brain. Brain Res Dev Brain Res 157:98-102
42. Mokin M, Keifer J (2006) Quantitative analysis of immunofluorescent punctate staining of synaptically localized proteins using confocal microscopy and stereology. J Neurosci Methods 157:218-224
43. Mokin M, Zheng Z, Keifer J (2007) Conversion of silent synapses into the active pool by selective GluR1-3 and GluR4 AMPAR trafficking during in vitro classical conditioning. J Neurophysiol 98:1278-1286
44. Moretti P, Levenson JM, Battaglia F, Atkinson R, Teague R, Antalffy B, Armstrong D, Arancio O, Sweatt JD, Zoghbi HY (2006) Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J Neurosci 26:319-327
45. Nie D, Di Nardo A, Han JM, Baharanyi H, Kramvis I, Huynh T, Dabora S, Codeluppi S, Pandolfi PP, Pasquale EB, Sahin M (2010) Tsc2-Rheb signaling regulates EphA-mediated axon guidance. Nat Neurosci 13:163-172
46. Palmer MJ, Isaac JT, Collingridge GL (2004) Multiple, developmentally regulated expression mechanisms of long-term potentiation at CA1 synapses. J Neurosci 24:4903-4911
47. Patrikelis P, Angelakis E, Gatzonis S (2009) Neurocognitive and behavioral functioning in frontal lobe epilepsy: a review. Epilepsy Behav 14:19-26
48. Petralia RS, Esteban JA, Wang YX, Partridge JG, Zhao HM, Wenthold RJ, Malinow R (1999) Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci 2:31-36
49. Rakhade SN, Jensen FE (2009) Epileptogenesis in the immature brain: emerging mechanisms. Nat Rev Neurol 5:380-391
50. Rakhade SN, Zhou C, Aujla PK, Fishman R, Sucher NJ, Jensen FE (2008) Early alterations of AMPA receptors mediate synaptic potentiation induced by neonatal seizures. J Neurosci 28:7979-7990
51. Rakhade SN, Klein PM, Huynh T, Hilario-Gomez C, Kosaras B, Rotenberg A, Jensen FE (2011) Development of later life spontaneous seizures in a rodent model of hypoxia-induced neonatal seizures. Epilepsia 52:753-765
52. Ronen GM, Buckley D, Penney S, Streiner DL (2007) Long-term prognosisin children with neonatal seizures: a population-based study. Neurology 69:1816-1822
53. Rumpel S, Kattenstroth G, Gottmann K (2004) Silent synapses in the immature visual cortex: layer-specific developmental regulation. J Neurophysiol 91:1097-1101
54. Sanchez RM, Koh S, Rio C, Wang C, Lamperti ED, Sharma D, Corfas G, Jensen FE (2001) Decreased glutamate receptor 2 expression and enhanced epileptogenesis in immature rat hippocampus after perinatal hypoxia-induced seizures. J Neurosci 21:8154-8163
55. Sanchez RM, Dai W, Levada RE, Lippman JJ, Jensen FE (2005) AMPA/ kainate receptor-mediated downregulation of GABAergic synaptic transmission by calcineurin after seizures in the developing rat brain. J Neurosci 25:3442-3451
56. Scantlebury MH, Galanopoulou AS, Chudomelova L, Raffo E, Betancourth D, Moshé SL (2010) A model of symptomatic infantile spasms syndrome. Neurobiol Dis 37:604-612
57. Shepherd JD, Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23:613-643
58. Silverstein FS, Jensen FE (2007) Neonatal seizures. Ann Neurol 62:112-120
59. Spence SJ, Schneider MT (2009) The role of epilepsy and epileptiform EEGs in autism spectrum disorders. Pediatr Res 65:599-606
60. Talos DM, Follett PL, Folkerth RD, Fishman RE, Trachtenberg FL, Volpe JJ, Jensen FE (2006) Developmental regualtion of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-proprionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. II. Human cerebral white matter and cortex. J Comp Neurol 497:61-77
61. Thiagarajan TC, Lindskog M, Malgaroli A, Tsien RW (2007) LTP and adaptation to inactivity: overlapping mechanisms and implications for metaplasticity. Neuropharmacology 52:156-175
62. Tuchman R, Alessandri M, Cuccaro M (2010) Autism spectrum disorders and epilepsy: moving towards a comprehensive approach to treatment. Brain Dev 32:719-730
63. Vingerhoets G (2006) Cognitive effects of seizures. Seizure 15:221-226
64. von der Brelie C, Waltereit R, Zhang L, Beck H, Kirschstein T (2006) Impaired synaptic plasticity in a rat model of tuberous sclerosis. Eur J Neurosci 23:686-692
65. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097
66. Yang SN, Huang CB, Yang CH, Lai MC, Chen WF, Wang CL, Wu CL, Huang LT (2004) Impaired SynGAP expression and long-term spatial learning and memory in hippocampal CA1 area from rats previously exposed to perinatal hypoxia-induced insults: beneficial effects of A68930. Neurosci Lett 371:73-78
67. Zhou C, Jensen FE, Sucher NJ (2009) Altered development of glutamatergic synapses in layer V pyramidal neurons in NR3A knockout mice. Mol Cell Neurosci 42:419-426.