A Nitric Oxide-Independent and β-Adrenergic Receptor-Sensitive Form of Metaplasticity Limits θ-Frequency Stimulation-Induced LTP in the Hippocampal CA1 Region

Learning and Memory - Tập 6 Số 6 - Trang 619-633 - 1999
Teena D. Moody1, Holly J. Carlisle2, Thomas J. O’Dell3
1Interdepartmental Ph.D. Program for Neuroscience, School of Medicine, University of California at Los Angeles, 90095, USA.
2Interdepartmental Ph.D. Program for Neuroscience and
3Department of Physiology School of Medicine University of California at Los Angeles Los Angeles, California 90095 USA

Tóm tắt

The induction of long-term potentiation (LTP) and long-term depression (LTD) at excitatory synapses in the hippocampus can be strongly modulated by patterns of synaptic stimulation that otherwise have no direct effect on synaptic strength. Likewise, patterns of synaptic stimulation that induce LTP or LTD not only modify synaptic strength but can also induce lasting changes that regulate how synapses will respond to subsequent trains of stimulation. Collectively known as metaplasticity, these activity-dependent processes that regulate LTP and LTD induction allow the recent history of synaptic activity to influence the induction of activity-dependent changes in synaptic strength and may thus have an important role in information storage during memory formation. To explore the cellular and molecular mechanisms underlying metaplasticity, we investigated the role of metaplasticity in the induction of LTP by υ-frequency (5-Hz) synaptic stimulation in the hippocampal CA1 region. Our results show that brief trains of υ-frequency stimulation not only induce LTP but also activate a process that inhibits the induction of additional LTP at potentiated synapses. Unlike other forms of metaplasticity, the inhibition of LTP induction at potentiated synapses does not appear to arise from activity-dependent changes in NMDA receptor function, does not require nitric oxide signaling, and is strongly modulated by β-adrenergic receptor activation. Together with previous findings, our results indicate that mechanistically distinct forms of metaplasticity regulate LTP induction and suggest that one way modulatory transmitters may act to regulate synaptic plasticity is by modulating metaplasticity.

Từ khóa


Tài liệu tham khảo

10.1016/S0166-2236(96)80018-X

10.1002/(SICI)1098-1063(1997)7:2<137::AID-HIPO3>3.0.CO;2-K

10.1016/S0301-0082(97)00018-X

10.1111/j.1460-9568.1992.tb00177.x

10.1126/science.276.5321.2042

10.1016/0024-3205(80)90509-3

10.1038/349156a0

10.1126/science.3037696

10.1111/j.1460-9568.1995.tb01160.x

Bienenstock, 1982, Theory for the development of neuron selectivity: Orientation specificity and binocular interaction in visual cortex., J. Neurosci., 2, 32, 10.1523/JNEUROSCI.02-01-00032.1982

10.1016/0896-6273(95)90018-7

10.1126/science.280.5371.1940

10.1016/0014-2999(91)90505-K

Chetkovich, 1993, Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus., NeuroReport, 5, 919, 10.1097/00001756-199307000-00020

10.1002/hipo.450050107

Clark, 1995, Synaptic potentiation of dual-component excitatory postsynaptic currents in the rat hippocampus., J. Physiol. (Lond.), 482, 39, 10.1113/jphysiol.1995.sp020498

10.1016/0304-3940(89)90038-4

10.1002/(SICI)1098-2396(199610)24:2<97::AID-SYN1>3.0.CO;2-9

10.1038/36362

10.1016/S0960-9822(95)00262-4

Dunwiddie, 1992, Long-term increases in excitability in the CA1 region of rat hippocampus induced by β-adrenergic stimulation: Possible mediation by cAMP., J. Neurosci., 2, 506, 10.1523/JNEUROSCI.12-02-00506.1992

10.1074/jbc.272.31.19103

10.1016/0306-4522(95)00117-2

10.1016/0006-8993(91)90867-U

Fujii, 1996, The long-term suppressive effect of prior activation of synaptic inputs by low-frequency stimulation on induction of long-term potentiation in CA1 neurons of guinea pig hippocampal slices., Exp. Brain Res., 111, 305

10.1126/science.279.5352.870

Gribkoff, 1992, Evidence for nitric oxide synthase inhibitor-sensitive and insensitive hippocampal synaptic potentiation., J. Neurophysiol., 68, 639, 10.1152/jn.1992.68.2.639

10.1016/0896-6273(92)90288-O

10.1016/0304-3940(93)90919-C

Heginbotham, 1991, Long-term increases in the evoked population spike in the CA1 region of rat hippocampus induced by β-adrenergic receptor activation., J. Neurosci., 11, 2519, 10.1523/JNEUROSCI.11-08-02519.1991

Hoffman, 1999, Neuromodulation of dendritic action potentials., J. Neurophysiol., 81, 408, 10.1152/jn.1999.81.1.408

Holland, 1998, Primed facilitation of homosynaptic long-term depression and depotentiation in rat hippocampus., J. Neurosci., 18, 887, 10.1523/JNEUROSCI.18-03-00887.1998

10.1126/science.1346729

10.1126/science.1519065

10.1016/0304-3940(92)90364-D

Kato, 1993, Nitric oxide inhibitors facilitate the induction of hippocampal long-term potentiation by modulating NMDA responses., J. Neurophysiol., 70, 1260, 10.1152/jn.1993.70.3.1260

Katsuki, 1997, Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region., J. Neurophysiol., 77, 3013, 10.1152/jn.1997.77.6.3013

10.1016/0896-6273(88)90148-1

Ko, 1999, Nitric oxide acts as a postsynaptic signaling molecule in calcium/calmodulin-induced synaptic potentiation in hippocampal CA1 pyramidal neurons., J. Neurosci., 19, 6784, 10.1523/JNEUROSCI.19-16-06784.1999

10.1016/0166-2236(94)90014-0

Lou, 1989, Distinct autophosphorylation sites sequentially produce autonomy and inhibition of the multifunctional Ca2+/calmodulin-dependent protein kinase., J. Neurosci., 9, 2020, 10.1523/JNEUROSCI.09-06-02020.1989

Makhinson, 1999, Adenylyl cyclase activation modulates activity-dependent changes in synaptic strength and Ca2+/calmodulin-dependent kinase II autophosphorylation., J. Neurosci., 19, 2500, 10.1523/JNEUROSCI.19-07-02500.1999

Malen, 1997, Nitric oxide facilitates long-term potentiation, but not long-term depression., J. Neurosci., 17, 2645, 10.1523/JNEUROSCI.17-07-02645.1997

10.1016/0092-8674(94)90517-7

10.1016/0166-2236(93)90197-T

10.1016/0092-8674(95)90009-8

10.1126/science.256.5060.1199

10.1016/0092-8674(86)90008-5

10.1016/0896-6273(88)90109-2

10.1016/S0006-8993(98)00217-0

10.1002/syn.890050203

10.1126/science.2904701

10.1111/j.1469-7793.1999.453ac.x

O'Conner, 1995, Tetanically induced LTP involves a similar increase in the AMPA and NMDA receptor components of the excitatory postsynaptic current: Investigations of the involvement of mGlu receptors., J. Neurosci., 15, 2013, 10.1523/JNEUROSCI.15-03-02013.1995

10.1101/lm.1.2.129

10.1126/science.7518615

Otmakhov, 1997, Postsynaptic inhibitors of calcium/calmodulin-dependent protein kinase type II block induction but not maintenance of pairing-induced long-term potentiation., J. Neurosci., 17, 5357, 10.1523/JNEUROSCI.17-14-05357.1997

10.1113/jphysiol.1993.sp019911

10.1016/S0896-6273(00)80059-8

10.1101/lm.3.1.1

Roberson, 1999, The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus., J. Neurosci., 19, 4337, 10.1523/JNEUROSCI.19-11-04337.1999

Sah, 1996, Apical dendritic location of slow afterhyperpolarization current in hippocampal pyramidal neurons: Implications for the integration of long-term potentiation., J. Neurosci., 16, 4537, 10.1523/JNEUROSCI.16-15-04537.1996

10.1016/0896-6273(95)90045-4

Schworer, 1988, Ca2+/calmodulin-dependent protein kinase II: Identification of a regulatory autophosphorylation site adjacent to the inhibitory and calmodulin-binding domains., J. Biol. Chem., 263, 13486, 10.1016/S0021-9258(18)68264-X

10.1073/pnas.92.5.1724

10.1002/(SICI)1098-1063(1996)6:1<35::AID-HIPO7>3.0.CO;2-6

10.1016/0006-8993(90)91096-Y

10.1073/pnas.85.17.6337

10.1016/S0896-6273(00)80179-8

Thomas, 1998, Postsynaptic complex spike bursting enables the induction of LTP by theta frequency synaptic stimulation., J. Neurosci., 18, 7118, 10.1523/JNEUROSCI.18-18-07118.1998

Wagner, 1995, GABAergic and developmental influences on homosynaptic LTD and depotentiation in rat hippocampus., J. Neurosci., 15, 1577, 10.1523/JNEUROSCI.15-02-01577.1995

10.1016/0896-6273(95)90048-9

10.1101/lm.3.2-3.170

Wang, 1997, Cellular and molecular bases of memory: Synaptic and neuronal plasticity., J. Clin. Neurophysiol., 14, 264, 10.1097/00004691-199707000-00002

10.1097/00001756-199305000-00034

10.1016/S0092-8674(00)80896-X

Zorumski, 1998, Modulation of LTP induction by NMDA receptor activation and nitric oxide release., Prog. Brain Res., 118, 173, 10.1016/S0079-6123(08)63207-0