Linking Hebb's coincidence-detection to memory formation

Current Opinion in Neurobiology

Volumn 10, Issue 2, 2000, Pages 266-273

  Tsien, Joe Z ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

BRAIN DEVELOPMENT; GENETICS; LEARNING; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NEUROCHEMISTRY; PRIORITY JOURNAL; REVIEW; SPATIAL MEMORY;

EID: 0034106451     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(00)00070-2     Document Type: Review

References (51)

1. Hebb D.O. The organization of behavior. 1949;John Wiley, New York.
2. Sejnowski T.J. Storing covariance with nonlinearly interacting neurons. Math Biol. 20:1977;303-321.
3. Bienenstock E., Cooper L., Munro P. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 2:1982;32-48.
4. Stevens C.F., Sullivan J. Synaptic plasticity. Curr Opin Neurobiol. 8:1998;151-153.
5. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:1993;31-39.
6. Bear M.F., Malenka R.C. Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol. 4:1994;389-399.
7. Malenka R.C., Nicoll R.A. Long-term potentiation-a decade of progress? Science. 285:1999;1870-1874.
8. Sweatt J.D. Toward a molecular explanation for long-term potentiation. Learn Memory. 6:1999;399-416.
9. Morris R.G.M., Anderson E., Lynch G., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, APV. Nature. 319:1986;774-776.
10. Saucer D., Cain D.P. Spatial learning without NMDA receptor-dependent long-term potentiation. Nature. 378:1995;186-189.
11. Cain D.P., Saucier D., Hall J., Hargreaves E.L., Boon F. Detailed behavioral analysis of water maze acquisition under APV or CNQX: contribution of sensorimotor disturbances to drug-induced acquisition deficits. Behav Neurosci. 110:1996;86-102.
12. Mohn AR, Gainetdinov RR, Caron MG, Koller BH: Mice with reduced NMDA receptor expression display behavior related schizophrenia. Cell 98:427-436.
13. Elgersma Y., Silva A.J. Molecular mechanisms of synaptic plasticity and memory. Curr Opin Neurobiol. 9:1999;209-213.
14. Lipp H.P., Wolfer D.P. Genetically modified mice and cognition. Curr Opin Neurobiol. 8:1998;272-280.
15. Migaud M., Charlesworth P., Dempster M., Webster L.C., Watabe A.M., Makhinson M., He Y., Ramsay M., Morris R.G.M., Morrison J.H.et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature. 396:1998;433-439. An exciting demonstration that enhanced LTP in all frequency ranges - including at low frequency which usually induced LTD - could be deleterious to spatial learning. It suggests that normal LTD process is also critical for memory formation. The conventional gene knockout approach clearly suggests that PSD-95 is important in coupling the NMDA receptor to intracellular pathways, and may control the threshold of synaptic plasticity.
16. Zamanillo D., Sprengel R., Hvalby O., Jensen V., Burnashev N., Rozov A., Kaiser K.M., Koster H.J., Borchardt T., Worley P.et al. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science. 284:1999;1805-1811. This paper demonstrates that mice lacking the GluRA receptor were viable and healthy. There is reduced AMPA current in the soma but apparent normal synaptic AMPA currents. The typical 100 Hz, 1 second protocol failed to induce LTP in the CA1 region. It would be interesting to see whether other protocols can induce any LTPs. These alterations in the mutant appear to have no significant effect on their performance in the Morris water maze. Intriguingly, these mice had 13 days of pretraining in the water tank before the spatial training began. Other studies have shown that pretraining can somehow change the requirement for NMDA receptors following the water maze learning.
17. Bannerman D., Good M., Butcher S., Ramsey M., Morris R.G.M. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature. 378:1995;182-186.
18. Saucier D., Hargreave E.L., Boon F., Vanderwolf C.H., Cain D.P. Detailed behavioral analysis of water maze acquisition under systematic NMDA or M antagonism: nonspatial pretraining eliminates spatial learning deficits. Behav Neurosci. 110:1996;103-116.
19. Malleret G., Hen R., Guillou J.L., Segu L., Buhot M.C. 5-HT1B receptor knockout mice exhibit increased exploratory activity and enhanced spatial memory performance in the Morris water maze. J Neurosci. 19:1999;6157-6168. This interesting paper shows nicely that mice lacking 5-HT1B exhibited lower thigmotaxis (an index of anxiety) associated with a higher level of object exploratory activity but with normal elevated plus maze behavior. Behavioral performance in the Morris water maze is enhanced, but not in contextual fear conditioning and visible platform water maze. It would be very helpful to measure the LTP in these animals. In addition, it appears that the study used the inbred 129 strain wild-type mice, which are known to float during water maze tests.
20. Manabe T., Noda Y., Mamiya T., Katagiri H., Houtani T., Nishi M., Noda T., Takahashi T., Sygimoto T., Nabeshima T., Takeshima H. Facilitation of long-term potentiation and memory in mice lacking nociceptin receptors. Nature. 394:1998;577-581. This exciting study showed that in mice lacking the nociceptin/orphanin FQ receptor, the mild enhancement of LTP in the CA1 region correlates with a measurable improvement in the Morris water maze and passive avoidance test. However, it is not clear to what extent the phenotype is influenced by the possible changes in stress responses mediated by the decreased dopamine levels in the frontal cortex.
21. Mamiya T., Noda Y., Nishi M., Takeshima H., Nabeshima T. Enhancement of spatial attention in nociceptin/orphanin FQ receptor-knockout mice. Brain Res. 783:1998;236-240. This is a continuation of the characterization of the mice lacking the nociceptin/orphanin FQ receptor. These mice appear to have normal nociceptive responses as assayed by hot-plate, electric foot shock, and tail-flick tests. These mice appear to have an enhanced retention of spatial attention compared to wild-type. Biochemical studies revealed that dopamine content in the frontal cortex was lower in the knockout mice, suggesting that the possible role of nociceptin receptor in regulating spatial attention and learning via the dopamine system.
22. Nishi M., Houtani T., Noda Y., Mamiya T., Sato K., Doi T., Kuno J., Takeshima H., Nukada T., Nabeshima T.et al. Unstrained nociceptive response and disregulation of hearing ability in mice lacking the nociceptin/orphanin FQ receptor. EMBO J. 16:1997;1858-1864.
23. Calabresi P., Saiardi A., Pisani A., Baik J.H., Centonze D., Mercuri N., Bernardi G., Borrelli E. Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors. J Neurosci. 17:1997;4536-4544.
24. Jia Z., Agopyan N., Miu P., Xiong Z., Henderson J.T., Gerlai R., Taverna F., Velumian A., MacDonald J., Carlen P.et al. Enhanced LTP in mice deficient in the AMPA receptor, GluR2. Neuron. 17:1996;945-956.
25. 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.
26. Lu Y.F., Kojima N., Tomizawa K., Moriwaki A., Matsushita M., Obata K., Matsui H. Enhanced synaptic transmission and reduced threshold for LTP induction in fyn-transgenic mice. Euro J Neurosci. 11:1999;75-82. Authors produced mice overexpressing wild-type fyn or a transgene encoding constitutively active mutant fyn (m-fyn). They found that in m-fyn transgenic hippocampal slices, the paired-pulse facilitation was reduced and basal synaptic transmission was enhanced. Interestingly, a weak theta burst (subthreshold for the induction of LTP in control slices) also elicited LTP in the mutant slices. These changes appeared to contribute to the enhanced seizure susceptibility in these mice.
27. Kim J.J., Shih J.C., Chen K., Chen L., Bao S., Maren S., Anagnostaras S.G., Fanselow M.S., Maeyer E.D., Seif S., Thompson R.F. Selective enhancement of emotional, but not motor, learning in monoamine oxidase A-deficient mice. Proc Natl Acad Sci USA. 94:1997;5929-5933.
28. Brunner H.G., Nelen M., Breakefield X.O., Ropers H.H., van Oost B.A. Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science. 262:1993;578-580.
29. Futatsugi A., Kato K., Ogura H., Li S.T., Nagata E., Kuwajima G., Tanaka K., Itohara S., Mikoshiba K. Facilitation of NMDAR-independent LTP and spatial learning in mutant mice lacking ryanodine receptor type 3. Neuron. 24:1999;701-713. This very interesting study reported that mice lacking the RyR3 receptor have normal LTP induced by 100 Hz, 1 s stimulation, but with enhanced LTP in response to the 100 Hz, 100 millisecond stimulation protocol (short tetanus). In contrast to the LTP in wild-type slices, this short tetanus-induced LTP is independent of the NMDA receptor. It seems that the typical LTD protocol also failed to induce normal LTD, a nice example of diversity and complexity of LTP under various experimental conditions. Despite the above alterations, these conventional knockout mice learned the Morris water maze normally in comparison to the wild-type controls as indicated by the escape latency but, in the transfer test, they spent an unusually high amount of total time (~56%) in the target quadrant (versus ~40% for typical wild-types) in searching the platform.
30. Madani R., Hulo S., Toni N., Madani H., Steimer T., Muller D., Vassalli J.D. Enhanced hippocampal long-term potentiation and learning by increased neuronal expression of tissue-type plasminogen activator in transgenic mice. EMBO J. 18:1999;3007-3012. This very interesting study suggests that extracellular protease may play an important role in modulating synaptic plasticity. Authors described that mice overexpressing the tissue-plasminogen activator gene have increased and prolonged LTP and improved performance in the water maze.
31. Tsien J.Z., (Qian Z)., Gilbert M.E., Colicos M.A., Kandel E.R., Kuhl D. Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature. 361:1993;453-457.
32. Frey U., Muller M., Kuhl D. A different form of long-lasting potentiation revealed in tissue plasminogen activator mutant mice. J Neurosci. 16:1996;2057-2063.
33. Huang Y.Y., Bach M.E., Lipp H.P., Zhuo M., Wolfer D.P., Hawkins R.D., Schoonjans L., Kandel E.R., Godfraind J.M., Mulligan R.et al. Mice lacking the gene encoding tissue-plasminogen activator show a selective interference with late-phase long-term potentiation in both chaffer collateral and mossy fiber pathways. Proc Natl Acad Sci USA. 93:1996;8699-8704.
34. Gerlai R. Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci. 19:1996;177-181.
35. Lipp H.P., Wolfer D.P. Genetically modified mice and cognition. Curr Opin Neurobiol. 8:1998;272-280.
36. Crawley J.N. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res. 835:1999;18-26.
37. Wolfer D.P., Stagliar-Bozicevic M., Lipp H.P. Spatial memory and learning in transgenic mice: fact or artifact? News Physiol Sci. 13:1998;118-123.
38. Tsien J.Z., Chen D.F., Gerber D., Tom C., Mercer E.H., Anderson D.J., Mayford M., Kandel E.R., Tonegawa S. Subregion- and cell type-restricted gene knockout in mouse brain. Cell. 87:1996;1317-1326.
39. 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.
40. Rampon C., Tang Y., Goodhouse J., Shimizu E., Kyin E., Tsien J.Z. Enrichment induces structural changes and recovery from nonspatial-memory deficits in CA1-NMDAR1-knockout mice. Nat Neurosci. 3:2000;238-244. The study is the continuation of the characterization of the CA1-specific NMDA receptor 1 gene knockout mice described in Tsien et al. [39]. Authors found that the conditional mutants have profound impairment in three hippocampal dependent nonspatial memory tasks, namely novel object recognition, social preference of food transmission, and contextual fear conditioning. Surprisingly, these deficits can be rescued if the mutants were pre-exposed to the enriched environment. Furthermore, authors have employed unbiased stereological electronic microscopy, and found that the enriched-experience induced an increase of the synapse density in the CA1 region in knockouts as well as control littermates, indicating that this type of experience-induced structural plasticity does not require the NMDA receptor activity in the adult animals.
41. Mayford M., Mansuy I.M., Muller R.U., Kandel E.R. Memory and behavior: a second generation of genetically modified mice. Curr Biol. 7:1997;R580.
42. Nakanishi S. Molecular diversity of glutamate receptors and implications for brain function. Science. 258:1992;597-603.
43. 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.
44. Laurie D.J., Bartke I., Schoepfer R., Naujoks K., Seeburg P.H. Regional, developmental and interspecies expression of the four NMDAR2 subunits, examined using monoclonal antibodies. Brain Res Mol Brain Res. 51:1997;23-32.
45. Sheng M., Cummings J., Roldan L.A., Yan Y.N., Yan L.Y. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature. 368:1994;144-147.
46. Hestrin S. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature. 357:1992;686-689.
47. Carmignoto G., Vicini S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science. 258:1992;1007-1011.
48. Tang Y., Shimizu E., Dube G., Rampon C., Kerchner G., Zhuo M., Liu G., Tsien J.Z. Genetic enhancement of learning and memory in mice. Nature. 401:1999;63-69. In a crucial test of Hebb's rule in learning and memory, the authors have genetically enhanced the coincidence-detection function of the NMDA receptor in the mouse forebrain. In two independent transgenic lines, overexpression of the gene encoding the NR2B subunit in the forebrain has resulted in the selective enhancement of synaptic plasticity in response to 10-100 Hz frequency stimulation with normal LTD and long-term depotentiation at the 1-5 Hz range. Remarkably, these NR2B transgenic mice outperformed their wild-type littermates in six different learning and memory tests. These results have provided the most convincing evidence for linking NMDA receptor's coincidence-detection function to learning and memory in the brain.
49. 2+ dependency and a longer channel opening duration. Overexpression of the NR2D gene in the forebrain resulted in intriguing changes (downregulation of endogenous NR2B expression, smaller NMDA-mediated EPSP peak amplitudes, longer channel kinetics). In juvenile hippocampal slices, transgenic mice have normal LTP but are impaired in LTD, whereas in the adult slices, these mice displayed a smaller LTP with normal long-term depotentiation. Their performance in the Morris water maze appeared to be similar to that of the wild-type mice; however, large variations in the escape latency during the initial six training sessions made the precise comparison problematic. In addition, these mice have also received three pretraining sessions to learn to escape to the platform from three directions. It is not clear whether such practice changes the dependency on the NMDA receptors.
50. Sprengel R., Suchanek B., Amico C., Brusa R., Burnashev N., Rosov A., Hvalby O., Jensen V., Paulsen D., Andersen P.et al. Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell. 92:1998;279-289.
51. Hopfield J.J., Tank D.W. Computing with neural circuits: a model. Science. 233:1986;625-633.