Miniature synaptic currents become neurotoxic to chronically silenced neurons

Cerebral Cortex

Volumn 17, Issue 6, 2007, Pages 1292-1306

  Fishbein, Ianai ^a   Segal, Menahem ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

AMPA receptors; Ca2+ clearance; Cortical culture; Neurotoxicity; Tetrodotoxin

Indexed keywords

6,7 DINITRO 2,3 QUINOXALINEDIONE; AMPA RECEPTOR ANTAGONIST; TETRODOTOXIN; AMINO ACID RECEPTOR BLOCKING AGENT; AMPA RECEPTOR; CALCIUM; GLUTAMIC ACID; LOCAL ANESTHETIC AGENT; QUINOXALINE DERIVATIVE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; NERVE CELL; NERVE CELL DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; ACTION POTENTIAL; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; NERVE DEGENERATION; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPTIC TRANSMISSION; ULTRASTRUCTURE; WISTAR RAT;

ACTION POTENTIALS; ANESTHETICS, LOCAL; ANIMALS; APOPTOSIS; CALCIUM; CELLS, CULTURED; DENDRITIC SPINES; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; NERVE DEGENERATION; NEURONS; QUINOXALINES; RATS; RATS, WISTAR; RECEPTORS, AMPA; SYNAPTIC TRANSMISSION; TETRODOTOXIN;

EID: 34347273812     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhl037     Document Type: Article

References (47)

1. Baker RE, Ruijter JM. 1991. Chronic blockade of bioelectric activity in neonatal rat neocortex in vitro: physiological effects. Int J Dev Neurosci 9:321-329.
2. Balkowiec A, Katz DM. 2002. Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J Neurosci 22:10399-10407.
3. Bickler PE, Fahlman CS. 2004. Moderate increases in intracellular calcium activate neuroprotective signals in hippocampal neurons. Neuroscience 127:673-683.
4. Bravin M, Morando L, Vercelli A, Rossi F, Strata P. 1999. Control of spine formation by electrical activity in the adult rat cerebellum. Proc Natl Acad Sci USA 96:1704-1709.
5. Cameron HA, McKay RD. 2001. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406-417.
6. Capurso SA, Calhoun ME, Sukhov RR, Mouton PR, Price DL, Koliatsos VE. 1997. Deafferentation causes apoptosis in cortical sensory neurons in the adult rat. J Neurosci 17:7372-7384.
7. Collin C, Miyaguchi K, Segal M. 1997. Dendritic spine density and LTP induction in cultured hippocampal slices. J Neurophysiol 77:1614-1623.
8. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. 2003. Shortterm and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572.
9. De Lima AD, Opitz T, Voigt T. 2004. Irreversible loss of a subpopulation of cortical interneurons in the absence of glutamatergic network activity. Eur J Neurosci 19:2931-2943.
10. Dirnagl U, Iadecola C, Moskowitz Michael A. 1999. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391-397.
11. Flores G, Alquicer G, Silva-Gomez AB, Zaldivar G, Stewart J, Quirion R, Srivastava LK. 2005. Alterations in dendritic morphology of prefrontal cortical and nucleus accumbens neurons in post-pubertal rats after neonatal excitotoxic lesions of the ventral hippocampus. Neurosci 133:463-470.
12. Galvan CD, Hrachovy RA, Smith KL, Swann JW. 2000. Blockade of neuronal activity during hippocampal development produces a chronic focal epilepsy in the rat. J Neurosci 20:2904-2916.
13. Ghosh A, Carnahan J, Greenberg ME. 1994. Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263:1618-1623.
14. Goldin M, Segal M, Avignone E. 2001. Functional plasticity triggers formation and pruning of dendritic spines in cultured hippocampal networks. J Neurosci 21:186-193.
15. Gorba T, Klostermann O, Wahle P. 1999. Development of neuronal activity and activity-dependent expression of brain-derived neurotrophic factor mRNA in organotypic cultures of rat visual cortex. Cereb Cortex 9:864-877.
16. Gould E, Vail N, Wagers M, Gross CG. 2001. Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA 98:10910-10917.
17. Hardingham GE, Bading HU. 2003. The yin and yang of NMDA receptor signalling. Trends Neurosci 26:81-89.
18. Harmon KM, Wellman CL. 2003. Differential effects of cholinergic lesions on dendritic spines in frontal cortex of young adult and aging rats. Brain Res 992:60-68.
19. Ichisaka S, Katoh_Semba R, Hata Y, Ohshima M, Kameyama K, Tsumoto T. 2003. Activity-dependent change in the protein level of brain-derived neurotrophic factor but no change in other neurotrophins in the visual cortex of young and adult ferrets. Neurosci 117:361-371.
20. Jensen JB, Lund TM, Timmermann DB, Schousboe A, Pickering DS. 2001. Role of GluR2 expression in AMPA-induced toxicity in cultured murine cerebral cortical neurons. J Neurosci Res 65:267-277.
21. Johnson F, Hohmann SE, DiStefano PS, Bottjer SW. 1997. Neurotrophins suppress apoptosis induced by deafferentation of an avian motorcortical region. J Neurosci 17:2101-2111.
22. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
23. Kempermann G, Kuhn HG, Gage FH. 1997. More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
24. Kohara K, Kitamura A, Morishima M, Tsumoto T. 2001. Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 291:2419-2423.
25. Liu S, Lau L, Wei J, Zhu D, Zou S, Sun HS, Fu Y, Liu F, Lu Y. 2004. Expression of Ca(2+)-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 43:43-55.
26. Lu YM, Yin HZ, Chiang J, Weiss JH. 1996. Ca2+-permeable AMPA/Kainate and NMDA channels: high rate of Ca2+ influx underlies potent induction of injury. J Neurosci 16:5457-5465.
27. Nakayama K, Kiyosue K, Taguchi T. 2005. Diminished neuronal activity increases neuron-neuron connectivity underlying silent synapse formation and the rapid conversion of silent to functional synapses. J Neurosci 25:4040-4051.
28. Ott A, van Rossum CT, van Harskamp F, van de Mheen H, Hofman A, Breteler MM. 1999. Education and the incidence of dementia in a large population-based study: the Rotterdam study. Neurology 52:663-666.
29. Papa M, Bundman M, Greenberger V, Segal M. 1995. Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. J Neurosci 15:1-11.
30. Papadia S, Stevenson P, Hardingham NR, Bading H, Hardingham GE. 2005. Nuclear Ca2+ and the cAMP response element-binding protein family mediate a late phase of activity-dependent neuroprotection. J Neurosci 25:4279-4287.
31. Pellegrini-Giampietro DE, Gorter JA, Bennett MV, Zukin RS. 1997. The GluR2 (GluR-B) hypothesis: Ca(2+)-permeable AMPA receptors in neurological disorders. Trends Neurosci 20:464-470.
32. Petreanu L, Alvarez-Buylla A. 2002. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22:6106-6113.
33. Pivovarova NB, Nguyen HV, Winters CA, Brantner CA, Smith CL, Andrews SB. 2004. Excitotoxic calcium overload in a subpopulation of mitochondria triggers delayed death in hippocampal neurons. J Neurosci 24:5611-5622.
34. Ramakers GJ, Raadsheer FC, Corner MA, Ramaekers FC, Van Leeuwen FW. 1991. Development of neurons and glial cells in cerebral cortex, cultured in the presence or absence of bioelectric activity: morphological observations. Eur J Neurosci 3:140-153.
35. Ruijter JM, Baker RE, De Jong BM, Romijn HJ. 1991. Chronic blockade of bioelectric activity in neonatal rat cortex grown in vitro: morphological effects. Int J Dev Neurosci 9:331-338.
36. Scheetz AJ, Williams RW, Dubin MW. 1995. Severity of ganglion cell death during early postnatal development is modulated by both neuronal activity and binocular competition. Vis Neurosci 12:605-610.
37. Sun W, Gould TW, Newbern J, Milligan C, Choi SY, Kim H, Oppenheim RW. 2005. Phosphorylation of c-Jun in avian and mammalian motoneurons in vivo during programmed cell death: an early reversible event in the apoptotic cascade. J Neurosci 25:5595-5603.
38. Sutton MA, Wall NR, Aakalu GN, Schuman EM. 2004. Regulation of dendritic protein synthesis by miniature synaptic events. Science 304:1979-1983.
39. Thayer SA, Usachev YM, Pottorf WJ. 2002. Modulating Ca2+ clearance from neurons. Front Biosci 7:d1255-d1279.
40. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB. 1998. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892-896.
41. Turrigiano GG, Nelson SB. 2004. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107.
42. Tyler WJ, Pozzo-Miller L. 2003. Miniature synaptic transmission and BDNF modulate dendritic spine growth and form in rat CA1 neurons. J Physiol 553:497-509.
43. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ, Takasu MA, Tao X, Greenberg ME. 2001. Calcium regulation of neuronal gene expression. Proc Natl Acad Sci USA 98:11024-11031.
44. Wilson RS, Bennett DA, Bienias JL, Aggarwal NT, Mendes De Leon CF, Morris MC, Schneider JA, Evans DA. 2002. Cognitive activity and incident AD in a population-based sample of older persons. Neurology 59:1910-1914.
45. Young D, Lawlor PA, Leone P, Dragunow M, During MJ. 1999. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat Med 5:448-453.
46. Zhang LI, Poo MM. 2001. Electrical activity and development of neural circuits. Nat Neurosci 4(Suppl):1207-1214.
47. Zhang Y, Lipton P. 1999. Cytosolic Ca2+ changes during in vitro ischemia in rat hippocampal slices: major roles for glutamate and Na+-dependent Ca2+ release from mitochondria. J Neurosci 19:3307-3315.