Neurobiology of Aging
Volume 31, Issue 5 , Pages 813-825 , May 2010

Synaptic strength and postsynaptically silent synapses through advanced aging in rat hippocampal CA1 pyramidal neurons

  • Evgeny A. Sametsky

      Affiliations

    • Department of Physiology, Northwestern University, Feinberg School of Medicine, 303 East Chicago Avenue, Chicago, IL 60611, USA
  • ,
  • John F. Disterhoft

      Affiliations

    • Department of Physiology, Northwestern University, Feinberg School of Medicine, 303 East Chicago Avenue, Chicago, IL 60611, USA
  • ,
  • Yuri Geinisman

      Affiliations

    • Department of Cell and Molecular Biology, Northwestern University, Feinberg School of Medicine, 303 East Chicago Avenue, Chicago, IL 60611, USA
  • ,
  • Daniel A. Nicholson

      Affiliations

    • Department of Cell and Molecular Biology, Northwestern University, Feinberg School of Medicine, 303 East Chicago Avenue, Chicago, IL 60611, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 312 503 3759; fax: +1 312 503 7912.

Received 10 January 2008 ,Revised 28 May 2008 ,Accepted 30 May 2008.

References 

  1. Barnes CA, Rao G, Foster TC, McNaughton BL. Region-specific age effects on AMPA sensitivity: electrophysiological evidence for loss of synaptic contacts in hippocampal field CA1. Hippocampus. 1992;2:457–468
  2. Barnes CA, Rao G, Shen J. Age-related decrease in the N-methyl-D-aspartate receptor-mediated excitatory postsynaptic potential in hippocampal region CA1. Neurobiol. Aging. 1997;18:445–452
  3. Bourne J, Harris KM. Do thin spines learn to be mushroom spines that remember?. Curr. Opin. Neurobiol. 2007;17:381–386
  4. Bourne JN, Kirov SA, Sorra KE, Harris KM. Warmer preparation of hippocampal slices prevents synapse proliferation that might obscure LTP-related structural plasticity. Neuropharmacology. 2007;52:55–59
  5. Bredt DS, Nicoll RA. AMPA receptor trafficking at excitatory synapses. Neuron. 2003;40:361–379
  6. Burke SN, Barnes CA. Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 2006;7:30–40
  7. Calhoun ME, Fletcher BR, Yi S, Zentko DC, Gallagher M, Rapp PR. Age-related spatial learning impairment is unrelated to spinophilin immunoreactive spine number and protein levels in hippocampus. Neurobiol. Aging. 2007;29:1256–1264
  8. Disterhoft JF, Oh MM. Learning, aging, and intrinsic neuronal plasticity. Trends Neurosci. 2006;29:587–599
  9. Dumas TC, Foster TC. Developmental increase in CA3-CA1 presynaptic function in the hippocampal slice. J. Neurophysiol. 1995;73:1821–1828
  10. Durand GM, Kovalchuk Y, Konnerth A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature. 1996;381:71–75
  11. Foster TC. Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell. 2007;6:319–325
  12. Gallagher M, Colantuoni C, Eichenbaum H, Haberman RP, Rapp PR, Tanila H, et al. Individual difference in neurocognitive aging of the medial temporal lobe. Age. 2006;28:221–223
  13. Ganeshina O, Berry RW, Petralia RS, Nicholson DA, Geinisman Y. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J. Comp. Neurol. 2004;468:86–95
  14. Gant JC, Sama MM, Landfield PW, Thibault O. Early and simultaneous emergence of multiple hippocampal biomarkers of aging is mediated by Ca2+-induced Ca2+ release. J. Neurosci. 2006;26:3482–3490
  15. Gasparini S, Saviane C, Voronin LL, Cherubini E. Silent synapses in developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release?. Proc. Natl. Acad. Sci. U.S.A. 2000;97:9741–9746
  16. Geinisman Y. Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb. Cortex. 2000;10:952–962
  17. Geinisman Y, Ganeshina O, Yoshida R, Berry RW, Disterhoft JF, Gallagher M. Aging, spatial learning, and total synapse number in the rat CA1 stratum radiatum. Neurobiol. Aging. 2004;25:407–416
  18. Harris KM, Kater SB. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci. 1994;17:341–371
  19. Hsia AY, Malenka RC, Nicoll RA. Development of excitatory circuitry in the hippocampus. J. Neurophysiol. 1998;79:2013–2024
  20. Isaac JT, Nicoll RA, Malenka RC. Evidence for silent synapses: implications for the expression of LTP. Neuron. 1995;15:427–434
  21. Isaac JT, Hjelmstad GO, Nicoll RA, Malenka RC. Long-term potentiation at single fiber inputs to hippocampal CA1 pyramidal cells. Proc. Natl. Acad. Sci. U.S.A. 1996;93:8710–8715
  22. Isaac JT, Crair MC, Nicoll RA, Malenka RC. Silent synapses during development of thalamocortical inputs. Neuron. 1997;18:269–280
  23. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H. Structure-stability-function relationships of dendritic spines. Trends Neurosci. 2003;26:360–368
  24. Kennedy MJ, Ehlers MD. Organelles and trafficking machinery for postsynaptic plasticity Annu. Rev. Neurosci. 2006;29:325–362
  25. Khachaturian ZS. Hypothesis on the regulation of cytosol calcium concentration and the aging brain. Neurobiol. Aging. 1987;8:345–346
  26. Kirov SA, Petrak LJ, Fiala JC, Harris KM. Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus. Neuroscience. 2004;127:69–80
  27. Knuttinen MG, Gamelli AE, Weiss C, Power JM, Disterhoft JF. Age-related effects on eyeblink conditioning in the F344 x BN F1 hybrid rat. Neurobiol. Aging. 2001;22:1–8
  28. Kullmann DM, Asztely F. Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends Neurosci. 1998;21:8–14
  29. Kumar A, Thinschmidt JS, Foster TC, King MA. Aging effects on the limits and stability of long-term synaptic potentiation and depression in rat hippocampal area CA1. J Neurophysiol. 2007;98:594–601
  30. Landfield PW. ‘Increased calcium-current’ hypothesis of brain aging. Neurobiol. Aging. 1987;8:346–347
  31. Liao D, Hessler NA, Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature. 1995;375:400–404
  32. Magee JC, Cook EP. Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat. Neurosci. 2000;3:895–903
  33. Malinow R, Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu. Rev Neurosci. 2002;25:103–126
  34. McNaughton BL, Barnes CA, Andersen P. Synaptic efficacy and EPSP summation in granule cells of rat fascia dentate studied in vitro. J. Neurophysiol. 1981;46:952–966
  35. Nicholson, D.A., Geinisman, Y. Synaptic subtype-specific differences in structure, size, strength and connectivity in apical dendritic regions of rat hippocampal CA1 pyramidal neurons. J. Comp. Neurol., in press.
  36. Nicholson DA, Yoshida R, Berry RW, Gallagher M, Geinisman Y. Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J. Neurosci. 2004;24:7648–7653
  37. Nicholson DA, Trana R, Katz Y, Kath WL, Spruston N, Geinisman Y. Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron. 2006;50:431–442
  38. Nicoll RA. Expression mechanisms underlying long-term potentiation: a postsynaptic view. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003;358:721–726
  39. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron. 1998;21:545–559
  40. Petralia RS, Esteban JA, Wang YX, Partridge JG, Zhao HM, Wenthold RJ, et al. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat. Neurosci. 1999;2:31–36
  41. Racca C, Stephenson FA, Streit P, Roberts JD, Somogyi P. NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J. Neurosci. 2000;20:2512–2522
  42. Saviane C, Savtchenko LP, Raffaelli G, Voronin LL, Cherubini E. Frequency-dependent shift from paired-pulse facilitation to paired-pulse depression at unitary CA3-CA3 synapses in the rat hippocampus. J. Physiol. 2002;544:469–476
  43. Sorra KE, Harris KM. Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1. J. Neurosci. 1993;13:3736–3748
  44. Spruston N, McBain CJ. Structural and functional properties of hippocampal neurons. In:  Andersen P,  Morris RG,  Amaral D,  Bliss T,  O’Keefe J editor. The Hippocampus Book. Oxford: Oxford University Press; 2007;p. 133–201
  45. Spruston N, Jonas P, Sakmann B. Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J. Physiol. 1995;482:325–352
  46. Stevens CF, Wang Y. Facilitation and depression at single central synapses. Neuron. 1995;14:795–802
  47. Takumi Y, Ramírez-León V, Laake P, Rinvik E, Ottersen OP. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat. Neurosci. 1999;2:618–624
  48. Toescu EC, Verkhratsky A. The importance of being subtle: small changes in calcium homeostasis control cognitive decline in normal aging. Aging Cell. 2007;6:267–273
  49. Toescu EC, Verkhratsky A, Landfield PW. Ca2+ regulation and gene expression in normal brain aging. Trends Neurosci. 2004;27:614–620
  50. Voronin LL, Cherubini E. ‘Deaf, mute, and whispering’ silent synapses: their role in plasticity. J. Physiol. 2004;557:3–12
  51. Voronin LL, Altinbaev RS, Bayazitov IT, Gasparini S, Kasyanov AV, Saviane C, et al. Postsynaptic depolarization enhances transmitter release and causes the appearance of responses at “silent” synapses in rat hippocampus. Neuroscience. 2004;126:45–59
  52. Wilson IA, Gallagher M, Eichenbaum H, Tanila H. Neurocognitive aging: prior memories hinder new hippocampal encoding. Trends Neurosci. 2006;29:662–670
  53. Yankova M, Hart SA, Woolley CS. Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron- microscopic study. Proc. Natl. Acad. Sci. U.S.A. 2001;98:3525–3530

PII: S0197-4580(08)00206-6

doi: 10.1016/j.neurobiolaging.2008.05.029

Neurobiology of Aging
Volume 31, Issue 5 , Pages 813-825 , May 2010