Synapse specificity of long-term potentiation breaks down with aging

[en] Memory shows age-related decline. According to the current prevailing theoretical model, encoding of memories relies on modifications in the strength of the synapses connecting the different cells within a neuronal network. The selective increases in synaptic weight are thought to be biologically implemented by long-term potentiation (LTP). Here, we report that tetanic stimulation of afferent fibers in slices from 12-mo-old mice triggers an LTP not restricted to the activated synapses. This phenomenon, which can be anticipated to hinder memory encoding, is suppressed by blocking either L-type Ca++ channels or Ca++-induced Ca++ release, both well known to become disregulated with aging.

Disciplines :

Neurology

Author, co-author :

Ris, Laurence

Godaux, Emile ; Université de Mons > Faculté de Médecine et de Pharmacie > Neurosciences

Language :

English

Title :

Synapse specificity of long-term potentiation breaks down with aging

Publication date :

01 March 2007

Journal title :

Learning and Memory

ISSN :

1072-0502

Publisher :

Cold Spring Harbor Laboratory Press, United States - New York

Volume :

Issue :

Pages :

185-189

Peer reviewed :

Peer Reviewed verified by ORBi

Research unit :

M119 - Neurosciences

Available on ORBi UMONS :

since 10 June 2010

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Bibliography

Abel, T., Nguyen, P.V., Barad, M., Deuel, T.A., Kandel, E.R., and Bourtchouladze, R. 1997. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus based long-term memory. Cell 88: 615-626.
Andersen, P., Sundberg, S.H., Sveen, O., and Wigstrom, H. 1977. Specific long-lasting potentiation of synaptic transmission in hippocampal slices. Nature 266: 736-737.
Bach, M.E., Barad, M., Son, H., Zhuo, M., Lu, Y.F., Shih, R., Mansuy, I., Hawkins, R.D., and Kandel, E.R. 1999. Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc. Natl. Acad. Sci. 96: 5280-5285.
Barnes, C.A., Rao, G., Foster, T.C., and McNaughton, B.L. 1992. Region specific age effects on AMPA sensitivity: Electrophysiological evidence for loss of synaptic contacts in hippocampal field CA1. Hippocampus 2: 457-468.
Bliss, T.V. and Lomo, T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232: 331-356.
Brody, H. 1955. Organization of the cerebral cortex. III. A study of aging in the human cerebral cortex. J. Comp. Neurol. 102: 511-516.
Burke, S.N. and Barnes, C.A. 2006. Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 7: 30-40.
Cavus, I. and Teyler, T. 1996. Two forms of long-term potentiation in area CA1 activate different signal transduction cascades. J. Neurophysiol. 76: 3038-3047.
Deupree, D.L., Bradley, J., and Turner, D.A. 1993. Age-related alterations in potentiation in the CA1 region in F344 rats. Neurobiol. Aging 14: 249-258.
Engert, F. and Bonhoeffer, T. 1997. Synapse specificity of long-term potentiation breaks down at short distances. Nature 388: 279-284.
Gant, J.C., Sama, M.M., Landfield, P.W., and Thibault, O. 2006. Early and simultaneous emergence of multiple hippocampal biomarkers of aging is mediated by Ca2+- induced Ca2+ release. J. Neurosci. 26: 3482-3490.
Huang, Y.Y. and Kandel, E.R. 1994. Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn. Mem. 1: 74-82.
Huang, Y.Y. and Kandel, E.R. 2006. Age-related enhancement of a protein synthesis-dependent late phase of LTP induced by low frequency paired-pulse stimulation in hippocampus. Learn. Mem. 13: 298-306.
Jaffe, D.B. and Brown, T.H. 1994. Metabotropic glutamate receptor activation induces calcium waves within hippocampal dendrites. J. Neurophysiol. 72: 471-474.
Jäger, T., Behnisch, T., and Reymann, K.G. 2002. High frequency stimulation-induced dendritic calcium waves in rat hippocampal neurons. Neurosci. Lett. 335: 103-106.
Kumar, A. and Foster, T.C. 2004. Enhanced long-term potentiation during aging is masked by processes involving intracellular calcium stores. J. Neurophysiol. 91: 2437-2444.
Landfield, P.W. and Pitler, T.A. 1984. Prolonged Ca2+- dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science 226: 1089-1092.
Landfield, P.W., Pitler, T.A., and Applegate, M.D. 1986. The effects of high Mg2+-to-Ca2+ ratios on frequency potentiation in hippocampal slices of young and aged rats. J. Neurophysiol. 56: 797-811.
Moore, C.I., Browning, M.D., and Rose, G.M. 1993. Hippocampal plasticity induced by primed burst, but not long-term potentiation, stimulation is impaired in area CA1 of aged Fischer 344 rats. Hippocampus 3: 57-66.
Morgan, S.L. and Teyler, T.J. 2001. Electrical stimuli patterned after theta-rhythm induce multiple forms of LTP. J. Neurophysiol. 86: 1289-1296.
Nguyen, P.V. and Kandel, E.R. 1997. Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn. Mem. 4: 230-243.
Nishiyama, M., Hong, K., Mikoshiba, K., Poo, M., and Kato, K. 2000. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 408: 584-588.
Norris, C.M., Halpain, S., and Foster, T.C. 1998. Reversal of age-related alterations in synaptic plasticity by blockade of L-type Ca2+ channels. J. Neurosci. 18: 3171-3179.
Rosenzweig, E.S. and Barnes, C.A. 2003. Impact of aging on hippocampal function: Plasticity, network dynamics, and cognition. Prog. Neurobiol. 69: 143-179.
Sabatini, B.L., Oertner, T.G., and Svoboda, K. 2002. The life cycle of Ca2+ ions in dendritic spines. Neuron 33: 439-452.
Scheibel, A.B. 1979. The hippocampus: Organizational patterns in health and senescence. Mech. Ageing Dev. 9: 89-102.
Scheibel, M.E., Lindsay, R.D., Tomiyasu, U., and Scheibel, A.B. 1976. Progressive dendritic changes in the aging human limbic system. Exp. Neurol. 53: 420-430.
Shankar, S., Teyler, T.J., and Robbins, N. 1998. Aging differentially alters forms of long-term potentiation in rat hippocampal area CA1. J. Neurophysiol. 79: 334-341.
Thibault, O. and Landfield, P.W. 1996. Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272: 1017-1020.
Thibault, O., Hadley, R., and Landfield, P.W. 2001. Elevated postsynaptic [Ca2+]i and L-type calcium channel activity in aged hippocampal neurons: Relationship to impaired synaptic plasticity. J. Neurosci. 21: 9744-9756.
Veng, L.M., Mesches, M.H., and Browning, M.D. 2003. Age-related working memory impairment is correlated with increases in the L-type calcium channel protein α1D (Cav1.3) in area CA1 of the hippocampus and both are ameliorated by chronic nimodipine treatment. Brain Res. Mol. Brain Res. 110: 193-202.
Zipser, D. and Andersen, R.A. 1988. A back-propagation programmed network that stimulates response properties of a subset of posterior parietal neurons. Nature 331: 679-684.