Molecular mechanisms of synaptic plasticity and memory

Current Opinion in Neurobiology

Volumn 9, Issue 2, 1999, Pages 209-213

  Elgersma, Ype ^a   Silva, Alcino J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYGDALOID NUCLEUS; APLYSIA; BEHAVIOR; CONDITIONING; CYTOLOGY; FEAR; LEARNING; MEMORY; MOLECULAR BIOLOGY; NERVE CELL PLASTICITY; PRIORITY JOURNAL; REVIEW;

EID: 0032955409     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)80029-4     Document Type: Article

References (43)

1. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:1993;31-39.
2. Morris R.G., Anderson E., Lynch G.S., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature. 319:1986;774-776.
3. Miserendino M.J., Sananes C.B., Melia K.R., Davis M. Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature. 345:1990;716-718.
4. Gewirtz J.C., Davis M. Second-order fear conditioning prevented by blocking NMDA receptors in amygdala. Nature. 388:1997;471-474.
5. Maren S., Aharonov G., Stote D.L., Fanselow M.S. N-methyl-D-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of conditional fear in rats. Behav Neurosci. 110:1996;1365-1374.
6. Bannerman D.M., Good M.A., Butcher S.P., Ramsay M., Morris R.G. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature. 378:1995;182-186.
7. Saucier D., Cain D.P. Spatial learning without NMDA receptor-dependent long-term potentiation. Nature. 378:1995;186-189.
8. Kiyama Y., Manabe T., Sakimura K., Kawakami F., Mori H., Mishina M. Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor epsilon1 subunit. J Neurosci. 18:1998;6704-6712. This paper shows that mice lacking the NR2A subunit of the NMDA receptor have an increased threshold for CA1 LTP. These mutant mice show normal tone fear conditioning. In contrast, they show an increased threshold for contextual conditioning, which is a hippocampal-dependent task. Thus, an increased threshold for LTP correlates with increased threshold for contextual learning.
9. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34:1971;171-175.
10. Kentros C., Hargreaves E., Hawkins R.D., Kandel E.R., Shapiro M., Muller R.V. Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science. 280:1998;2121-2126. Using a pharmacological blocker of the NMDA receptor, the authors demonstrate that the formation of place cell firing fields does not involve NMDA receptor activation, but that long-term stabilization of newly formed fields requires NMDAR transmission.
11. Tsien J.Z., Huerta P.T., Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell. 87:1996;1327-1338.
12. McHugh T.J., Blum K.I., Tsien J.Z., Tonegawa S., Wilson M.A. Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell. 87:1996;1339-1349.
13. Meyer T., Hanson P.I., Stryer L., Schulman H. Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science. 256:1992;1199-1202.
14. 2+ trapping model. The frequency response of CaMKII was modulated by factors such as amplitude, frequency of the spikes, subunit composition and previous activation.
15. 2+/calmodulin-dependent protein kinase molecules of the postsynaptic density. Proc Natl Acad Sci USA. 85:1988;5320-5324.
16. Giese K.P., Fedorov N.B., Filipkowski R.K., Silva A.J. Autophosphorylation at Thr286 of the a calcium-calmodulin kinase II in LTP and learning. Science. 279:1998;870-873. Using a novel gene targeting approach, Thr286 of αCaMKII was mutated to abolish CaM-independent activity of the enzyme. This paper clearly demonstrates that autophosphorylation at Thr286 is essential for NMDAR-dependent LTP in the hippocampal CA1 area, as well as for spatial learning.
17. Barria A., Muller D., Derkach V., Griffith L.C., Soderling T.R. Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science. 276:1997;2042-2045.
18. Muller W., Petrozzino J.J., Griffith L.C., Danho W., Connor J.A. Specific involvement of Ca(2+)-calmodulin kinase II in cholinergic modulation of neuronal responsiveness. J Neurophysiol. 68:1992;2264-2269.
19. αΔ), the authors demonstrate that the autophosphorylation of CaMKII and CREB function are not essential for the generation of hippocampal place fields, but are critical for their stability. Interestingly, the severity of the place cell deficits in the two mutants correlates with the severity of their LTP abnormalities.
20. Matthies H. In search of cellular mechanisms of memory. Prog Neurobiol. 32:1989;277-349.
21. Bailey C.H., Bartsch D., Kandel E.R. Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci USA. 93:1996;13445-13452.
22. Silva A.J., Kogan J.H., Frankland P.W., Kida S. CREB and memory. Annu Rev Neurosci. 21:1998;127-148.
23. Blitzer R.D., Wong T., Nouranifar R., Iyengar R., Landau E.M. Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron. 15:1995;1403-1414.
24. +-independent CaMKII activity in a cAMP-dependent manner. Thiophosphorylated I-1 can overcome the blockade of LTP by a specific PKA inhibitor, but not by a CaMKII inhibitor, demonstrating that the cAMP pathway uses the phosphatase PP1 to modulate CaMKII activity and to gate LTP.
25. Abel T., Nguyen P.V., Barad M., Deuel T.A., Kandel E.R., Bourtchouladze R. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell. 88:1997;615-626.
26. Mansuy I.M., Mayford M., Jacob B., Kandel E.R., Bach M.E. Restricted and regulated overexpression reveals calcineurin as a key component in the transition from short-term to long-term memory. Cell. 92:1998;39-49. Mice with increased calcineurin activity have normal short-term but impaired long-term memory. The impairments in long-term memory can be rescued by increasing the number of training trials. These findings suggest that calcineurin has a role in the transition from short- to long-term memory, which correlates with calcineurin's role in gating late-phase LTP.
27. Winder D.G., Mansuy I.M., Osman M., Moallem T.M., Kandel E.R. Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell. 92:1998;25-37. The author report that mice overexpressing a truncated form of calcineurin possess diminished LTP induced by multiple high-frequency trains, but not by a single train. Together with pharmacological analysis of wild-type mice, this paper indicates a role for calcineurin in gating late LTP.
28. Mansuy I.M., Winder D.G., Moallem T.M., Osman M., Mayford M., Hawkins R.D., Kandel E.R. Inducible and reversible gene expression with the rtTA system for the study of memory. Neuron. 21:1998;257-265.
29. Bourtchouladze R., Abel T., Berman N., Gordon R., Lapidus K., Kandel E. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem. 5:1998;365-374. The authors used genetics and pharmacology to reveal when PKA activity and protein synthesis is required in long-term memory for contextual conditioning in mice. Interestingly, the authors found that depending on the training conditions, there are either one or two brief consolidation periods that require both synthesis of new proteins and PKA activity.
30. Glanzman D.L. The cellular basis of classical conditioning in Aplysia californica - it's less simple than you think. Trends Neurosci. 18:1995;30-36.
31. Byrne J.H., Kandel E.R. Presynaptic facilitation revisited: state and time dependence. J Neurosci. 16:1996;425-435.
32. Murphy G.G., Glanzman D.L. Mediation of classical conditioning in Aplysia californica by long-term potentiation of sensorimotor synapses. Science. 278:1997;467-471. The authors provide evidence that NMDA-mediated LTP could be involved in associative invertebrate learning. Using a cellular analog of classical conditioning in Aplysia, the authors found that a NMDAR blocker disrupted synaptic enhancement after associative training but not after nonassociative training.
33. Rogan M.T., LeDoux J.E. LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit. Neuron. 15:1995;127-136.
34. McKernan M.G., Shinnick-Gallagher P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature. 390:1997;607-611. The authors provide a compelling demonstration that associative learning (fear-conditioning) results in increased synaptic strength, as measured in brain slices isolated from conditioned animals.
35. Rogan M.T., Staubli U.V., LeDoux J.E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature. 390:1997;604-607. In this unique study, field potentials were measured in freely behaving rats before and after fear conditioning. It provides one of the most compelling demonstrations that associative learning (i.e. pairing of shock and tone) recruits changes in synaptic strength that resemble LTP induction.
36. Romanski L.M., Clugnet M.C., Bordi F., LeDoux J.E. Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behav Neurosci. 107:1993;444-450.
37. Doyere V., Laroche S. Linear relationship between the maintenance of hippocampal long-term potentiation and retention of an associative memory. Hippocampus. 2:1992;39-48.
38. Xu L., Anwyl R., Rowan M.J. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature. 394:1998;891-894. Increases in synaptic strength induced by high-frequency stimulation of CA3-CA1 synapses in vivo are reversed by exploration of a new environment. A number of carefully designed control experiments show that this erasure of synaptic enhancement is not attributable to handling stress or to simply changing environments, but that it requires novelty. Reversal was not observed if the rats were exposed to a novel environment 24 h after the artificial induction of synaptic strength, suggesting that the protein-synthesis phase of long-lasting changes in synaptic function protects synapses from this erasure process.
39. McNaughton B.L., Barnes C.A., Rao G., Baldwin J., Rasmussen M. Long-term enhancement of hippocampal synaptic transmission and the acquisition of spatial information. J Neurosci. 6:1986;563-571.
40. Barnes C.A., Jung M.W., McNaughton B.L., Korol D.L., Andreasson K., Worley P.F. LTP saturation and spatial learning disruption: effects of task variables and saturation levels. J Neurosci. 14:1994;5793-5806.
41. Moser E.I., Krobert K.A., Moser M.B., Morris R.G.M. Impaired spatial learning after saturation of long-term potentiation. Science. 281:1998;2038-2042. If learning depends on changes in synaptic weight, then driving synapses to their maximum efficacy should impair learning. Using a clever saturation protocol, the authors demonstrate that saturation of hippocampal LTP does indeed impair spatial learning.
42. Manabe T., Noda Y., Mamiya T., Katagiri H., Houtani T., Nishi M., Noda T., Takahashi T., Sugimoto T., Nabeshima T., Takeshima H. Facilitation of long-term potentiation and memory in mice lacking nociceptin receptors. Nature. 394:1998;577-581. An interesting demonstration that increased LTP can result in improved learning and memory. Mice lacking the nociceptin receptor show enhanced LTP in the hippocampal CA1 region, and better learning and memory than controls.
43. Gerlai R., Henderson J.T., Roder J.C., Jia Z. Multiple behavioral anomalies in GluR2 mutant mice exhibiting enhanced LTP. Behav Brain Res. 95:1998;37-45.