In vivo evidence for an activity-independent maturation of AMPA/NMDA signaling in the developing hippocampus

Neuroscience

Volumn 121, Issue 1, 2003, Pages 65-72

  Groc, L ^a   Gustafsson, B ^a   Hanse, E ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Glutamate synapse; Maturation; Neonate hippocampus; Neural activity

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; N METHYL DEXTRO ASPARTIC ACID; TETANUS TOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN SLICE; CONTROLLED STUDY; GROWTH RETARDATION; HIPPOCAMPUS; NERVE CELL; NERVE CONDUCTION; NONHUMAN; PERINATAL PERIOD; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION;

EID: 0141795222     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00366-X     Document Type: Article

References (49)

1. Barth A.L., Malenka R.C. NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses. Nat Neurosci. 4:2001;235-236.
2. Ben Ari Y., Cherubini E., Corradetti R., Gaiarsa J.L. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol (Lond). 416:1989;303-325.
3. Ben-Ari Y., Khazipov R., Leinekugel X., Caillard O., Gaiarsa J.L. GABAA, NMDA and AMPA receptors a developmentally regulated 'menage a trois . Trends Neurosci. 20:1997;523-529.
4. Burrone J., O'Byrne M., Murthy V.N. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature. 420:2002;414-418.
5. 2+ partially rescues synaptic transmission in hippocampal cultures treated with botulinum toxin A and C, but not tetanus toxin. J Neurosci. 17:1997;7190-7202.
6. Carmignoto G., Vicini S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science. 258:1992;1007-1011.
7. Chavis P., Westbrook G. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature. 411:2001;317-321.
8. Constantine-Paton M., Cline H.T. LTP and activity-dependent synaptogenesis the more alike they are, the more different they become . Curr Opin Neurobiol. 8:1998;139-148.
9. Durand G.M., Kovalchuk Y., Konnerth A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature. 381:1996;71-75.
10. Featherstone D.E., Rushton E., Broadie K. Developmental regulation of glutamate receptor field size by nonvesicular glutamate release. Nat Neurosci. 5:2002;141-146.
11. Ferrer I., Tortosa A., Blanco R., Martin F., Serrano T., Planas A., Macaya A. Naturally occurring cell death in the developing cerebral cortex of the rat evidence of apoptosis-associated internucleosomal DNA fragmentation . Neurosci Lett. 182:1994;77-79.
12. Fiala J.C., Feinberg M., Popov V., Harris K.M. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci. 18:1998;8900-8911.
13. Friedman H.V., Bresler T., Garner C.C., Ziv N.E. Assembly of new individual excitatory synapses time course and temporal order of synaptic molecule recruitment . Neuron. 27:2000;57-69.
14. Garaschuk O., Hanse E., Konnerth A. Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J Physiol (Lond). 507:1998;219-236.
15. Goodman C.S., Shatz C.J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell. 72:(Suppl):1993;77-98.
16. Groc L., Gustafsson B., Hanse E. Spontaneous unitary synaptic activity in CA1 pyramidal neurons during early postnatal development constant contribution of AMPA and NMDA receptors . J Neurosci. 22:2002;5552-5562.
17. Groc L., Petanjek Z., Gustafsson B., Ben Ari Y., Hanse E., Khazipov R. In vivo blockade of neural activity alters dendritic development of neonatal CA1 pyramidal cells. Eur J Neurosci. 16:2002;1931-1938.
18. Hanse E., Gustafsson B. Vesicle release probability and pre-primed pool at glutamatergic synapses in area CA1 of the rat neonatal hippocampus. J Physiol (Lond). 531:2001;481-493.
19. Hanse E., Gustafsson B. Quantal variability at glutamatergic synapses in area CA1 of the rat neonatal hippocampus. J Physiol (Lond). 531:2001;467-480.
20. Hanse E., Durand G.M., Garaschuk O., Konnerth A. Activity-dependent wiring of the developing hippocampal neuronal circuit. Seminars Cell Dev Biol. 8:1997;35-42.
21. Hestrin S. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature. 357:1992;686-689.
22. Hohnke C.D., Oray S., Sur M. Activity-dependent patterning of retinogeniculate axons proceeds with a constant contribution from AMPA and NMDA receptors. J Neurosci. 20:2000;8051-8060.
23. Hsia A.Y., Malenka R.C., Nicoll R.A. Development of excitatory circuitry in the hippocampus. J Neurophysiol. 79:1998;2013-2024.
24. Isaac J.T., Nicoll R.A., Malenka R.C. Evidence for silent synapses implications for the expression of LTP . Neuron. 15:1995;427-434.
25. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science. 274:1996;1133-1138.
26. 2+ block of N-methyl-D-aspartate receptor channels during postnatal development of hippocampal CA3 pyramidal neurons. Neuroscience. 69:1995;1057-1065.
27. Kirson E.D., Yaari Y. Synaptic NMDA receptors in developing mouse hippocampal neurones functional properties and sensitivity to ifenprodil . J Physiol (Lond). 497:1996;437-455.
28. Kutsuwada T., Sakimura K., Manabe T., Takayama C., Katakura N., Kushiya E., Natsume R., Watanabe M., Inoue Y., Yagi T., Aizawa S., Arakawa M., Takahashi T., Nakamura Y., Mori H., Mishina M. Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor epsilon 2 subunit mutant mice. Neuron. 16:1996;333-344.
29. Lee C.L., Hrachovy R.A., Smith K.L., Frost J.D. Jr, Swann J.W. Tetanus toxin-induced seizures in infant rats and their effects on hippocampal excitability in adulthood. Brain Res. 677:1995;97-109.
30. Liao D., Hessler N.A., Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature. 375:1995;400-404.
31. Malinow R., Mainen Z.F., Hayashi Y. LTP mechanisms from silence to four-lane traffic . Curr Opin Neurobiol. 10:2000;352-357.
32. Martinez-Arca S., Coco S., Mainguy G., Schenk U., Alberts P., Bouille P., Mezzina M., Prochiantz A., Matteoli M., Louvard D., Galli T. A common exocytotic mechanism mediates axonal and dendritic outgrowth. J Neurosci. 21:2001;3830-3838.
33. McKinney R.A., Capogna M., Durr R., Gahwiler B.H., Thompson S.M. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci. 2:1999;44-49.
34. Monyer H., Burnashev N., Laurie D.J., Sakmann B., Seeburg P.H. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron. 12:1994;529-540.
35. Muller D., Oliver M., Lynch G. Developmental changes in synaptic properties in hippocampus of neonatal rats. Brain Res Dev Brain Res. 49:1989;105-114.
36. Rao A., Craig A.M. Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron. 19:1997;801-812.
37. Renger J.J., Egles C., Liu G. A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation. Neuron. 29:2001;469-484.
38. Shi J., Townsend M., Constantine-Paton M. Activity-dependent induction of tonic calcineurin activity mediates a rapid developmental downregulation of NMDA receptor currents. Neuron. 28:2000;103-114.
39. Schiavo G., Matteoli M., Montecucco C. Neurotoxins affecting neuroexocytosis. Physiol Rev. 80:2000;717-766.
40. Schiavo G., Benfenati F., Poulain B., Rossetto O., Polverino de Laureto P., DasGupta B.R., Montecucco C. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature. 359:1992;832-835.
41. Schoch S., Deak F., Konigstorfer A., Mozhayeva M., Sara Y., Sudhof T.C., Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science. 294:2001;1117-1122.
42. + currents . J Neurophysiol. 68:1992;55-69.
43. Steward O., Falk P.M. Selective localization of polyribosomes beneath developing synapses a quantitative analysis of the relationships between polyribosomes and developing synapses in the hippocampus and dentate gyrus . J Comp Neurol. 314:1991;545-557.
44. Tyzio R., Represa A., Jorquera I., Ben-Ari Y., Gozlan H., Aniksztejn L. The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J Neurosci. 19:1999;10372-10382.
45. Varoqueaux F., Sigler A., Rhee J.S., Brose N., Enk C., Reim K., Rosenmund C. Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc Natl Acad Sci USA. 99:2002;9037-9042.
46. Wasling P., Hanse E., Gustafsson B. Long-term depression in the developing hippocampus low induction threshold and synapse nonspecificity . J Neurosci. 22:2002;1823-1830.
47. Watt A.J., van Rossum M.C., MacLeod K.M., Nelson S.B., Turrigiano G.G. Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron. 26:2000;659-670.
48. Verderio C., Coco S., Bacci A., Rossetto O., De Camilli P., Montecucco C., Matteoli M. Tetanus toxin blocks the exocytosis of synaptic vesicles clustered at synapses but not of synaptic vesicles in isolated axons. J Neurosci. 19:1999;6723-6732.
49. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., Toonen R.F., Hammer R.E., van den Berg T.K., Missler M., Geuze H.J., Sudhof T.C. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science. 287:2000;864-869.