NR2B-subunit dependent facilitation of long-term potentiation in primary visual cortex following visual discrimination training of adult rats

European Journal of Neuroscience

Volumn 34, Issue 8, 2011, Pages 1222-1229

  Gagolewicz, Peter J ^a   Dringenberg, Hans C ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

In vivo; Long Evans rat; Metaplasticity; NMDA receptor; Ro 25 6981

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 4 BENZYL ALPHA (4 HYDROXYPHENYL) BETA METHYL 1 PIPERIDINEPROPANOL; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; URETHAN;

ANESTHESIA INDUCTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; CONTROLLED STUDY; ENZYME ACTIVATION; FACILITATION; LATERAL GENICULATE NUCLEUS; LONG TERM POTENTIATION; MALE; MAZE TEST; MODIFIED MORRIS WATER MAZE; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; STRIATE CORTEX; SWIMMING; TASK PERFORMANCE; THALAMOCORTICAL TRACT; THETA RHYTHM; VISUAL DISCRIMINATION; VISUAL ORIENTATION; VISUAL SYSTEM;

ANIMALS; BEHAVIOR, ANIMAL; CUES; DISCRIMINATION (PSYCHOLOGY); LONG-TERM POTENTIATION; MALE; MAZE LEARNING; NEUROPSYCHOLOGICAL TESTS; RATS; RATS, LONG-EVANS; RECEPTORS, N-METHYL-D-ASPARTATE; SWIMMING; VISUAL CORTEX;

EID: 80054693637     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07842.x     Document Type: Article

References (53)

1. Abraham, W.C. (2008) Metaplasticity: tuning synapses and networks for plasticity. Nat. Rev. Neurosci., 9, 387-399.
2. Abraham, W.C. & Bear, M.F. (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci., 19, 126-130.
3. Bayer, K.U., De Koninck, P., Leonard, A.S., Hell, J.W. & Schulman, H. (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature, 411, 801-805.
4. Bear, M.F. (2003) Bidirectional synaptic plasticity: from theory to reality. Phil. Trans R. Soc. Lond. B. Biol. Sci., 358, 649-655.
5. Clapp, W.C., Eckert, M.J., Teyler, T.J. & Abraham, W.C. (2006) Rapid visual stimulation induces N-methyl-D-aspartate receptor-dependent sensory long-term potentiation in the rat cortex. Neuroreport, 17, 511-515.
6. Cooke, S.F. & Bear, M.F. (2010) Visual experience induces long-term potentiation in the primary visual cortex. J. Neurosci., 30, 16304-16313.
7. Coutrap, S.J., Bickford, P.C. & Browning, M.D. (2008) Blueberry-enriched diet ameliorates age-related declines in NMDA receptor-dependent LTP. Age, 30, 263-272.
8. de Marchena, J., Roberts, A.C., Middlebrooks, P.G., Valakh, V., Yashiro, K., Wilfley, L.R. & Philpot, B.D. (2008) NMDA receptor antagonists reveal age-dependent differences in the properties of visual cortical plasticity. J. Neurophysiol., 100, 1936-1948.
9. Dringenberg, H.C., Hamze, B., Wilson, A., Speechly, W. & Kuo, M.C. (2007) Heterosynaptic facilitation of in vivo thalamocortical long-term potentiation in the adult rat visual cortex by acetylcholine. Cereb. Cortex, 17, 839-848.
10. Dringenberg, H.C., Kuo, M.-C. & Tomaszek, S. (2004) Stabilization of thalamo-cortical long-term potentiation by the amygdala: cholinergic and transcription-dependent mechanisms. Eur. J. Neurosci., 20, 557-565.
11. Duffy, S.N., Craddock, K.J., Abel, T. & Nguyen, P.V. (2001) Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus-dependent memory. Learn. Mem., 8, 26-34.
12. Dumas, T.C. (2005) Developmental regulation of cognitive abilities: modified composition of a molecular switch turns on associative learning. Prog. Neurobiol., 76, 189-211.
13. Epp, J., Keith, J.R., Spanswick, S.C., Stone, J.C., Prusky, G.T. & Sutherland, R.J. (2008) Retrograde amnesia for visual memories after hippocampal damage in rats. Learn. Mem., 15, 214-221.
14. Fischer, G., Mutel, V., Trube, G., Malherbe, P., Kew, J.N.C., Mohacsi, E., Heitz, M.P. & Kemp, J.A. (1997) Ro 25-6981, a highly potent and selective blocker of N-methyl-D-aspartate receptors containing the NR2B subunit. Characterization in vitro. J. Pharmacol. Exp. Ther., 283, 1285-1292.
15. Fitzjohn, S.M., Bortolotto, Z.A., Palmer, M.J., Doherty, A.J., Ornstein, P.L., Schoepp, D.D., Kingston, A.E., Lodge, D. & Collingridge, G.L. (1998) The potent mGlu receptor antagonist LY341495 identifies roles for both cloned and novel mGlu receptors in hippocampal synaptic plasticity. Neuropharmacology, 12, 1445-1458.
16. Fontan-Lozano, A., Saez-Cassanelli, J.L., Inda, M.C., los Santos-Arteaga, M., Sierra-Dominguez, S.A., Lopez-Lluch, G., Delgado-Garcia, J.M. & Carrion, A.M. (2007) Caloric restriction increases learning consolidation and facilitates synaptic plasticity through mechanisms dependent on NR2B subunits of the NMDA receptor. J. Neurosci., 27, 10185-10195.
17. Frenkel, M.Y., Sawtell, N.B., Diogo, A.C.M., Yoon, B., Neve, R.L. & Bear, M.R. (2006) Instructive effect of visual experience in mouse visual cortex. Neuron, 51, 339-349.
18. Hager, M. & Dringenberg, H.C. (2010) Training-induced plasticity in the visual cortex of adult rats following visual discrimination learning. Learn. Mem., 17, 394-401.
19. He, H.Y., Hodos, W. & Quinlan, E.M. (2006) Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex. J. Neurosci., 26, 1951-1955.
20. Heynen, A.J. & Bear, M.F. (2001) Long-term potentiation of thalamocortical transmission in the adult visual cortex in vivo. J. Neurosci., 21, 9801-9813.
21. Hogsden, J.L. & Dringenberg, H.C. (2009) NR2B subunit-dependent long-term potentiation enhancement in the rat cortical auditory system in vivo following masking of patterned auditory input by white noise exposure during early postnatal life. Eur. J. Neurosci., 30, 376-384.
22. Kingston, A.E., Ornstein, P.L., Wright, R.A., Johnson, B.G., Mayne, N.G., Burnett, J.P., Belagaje, R., Wu, S. & Schoepp, D.D. (1998) LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology, 37, 1-12.
23. Kopp, C., Longordo, F. & Lüthi, A. (2007) Experience-dependent changes in NMDA receptor composition at mature central synapses. Neuropharmacology, 53, 1-9.
24. Kuo, M.C. & Dringenberg, H.C. (2009) Short-term (2 to 5h) dark exposure lowers long-term potentiation (LTP) induction threshold in rat primary visual cortex. Brain Res., 1276, 58-66.
25. Kuo, M.C. & Dringenberg, H.C. (2008) Histamine facilitates in vivo thalamocortical long-term potentiation in the mature visual cortex of anesthetized rats. Eur. J. Neurosci., 27, 1731-1738.
26. Linden, A.-M., Johnson, B.G., Trokovic, N., Korpi, E.R. & Schoepp, D.D. (2009) Use of MGLUR2 and MGLUR3 knockout mice to explore in vivo receptor specificity of the MGLUR2/3 selective antagonist LY341495. Neuropharmacology, 57, 172-182.
27. Lu, H.C., Gonzalez, E. & Crair, M.C. (2001) Barrel cortex critical period plasticity is independent of changes in NMDA receptor subunit composition. Neuron, 32, 619-634.
28. Mainardi, M., Landi, S., Gianfranceschi, L., Baldini, S., De Pasquale, R., Berardi, N., Maffei, L. & Caleo, M. (2010) Environmental enrichment potentiates thalamocortical transmission and plasticity in the adult rat visual cortex. J. Neurosci. Res., 88, 3048-3059.
29. Martin, S.J. & Morris, R.G. (2002) New life in an old idea: the synaptic plasticity and memory hypothesis revisited. Hippocampus, 12, 609-636.
30. Malenka, R.C. & Bear, M.F. (2004) LTP and LTD: an embarrassment of riches. Neuron, 44, 5-21.
31. Monfils, M.-H. & Teskey, G.C. (2004) Skilled-learning-induced potentiation in rat sensorimotor cortex: a transient form of behavioural long-term potentiation. Neuroscience, 125, 329-336.
32. Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B. & Seeburg, P.H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron, 12, 529-540.
33. 2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials. Neuron, 24, 727-737.
34. Neves, G., Cooke, S.F. & Bilss, T.V.P. (2008) Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat. Rev. Neurosci., 9, 65-75.
35. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press, San Diego, CA.
36. Rao, Y. & Daw, N.W. (2004) Layer variations of long-term depression in rat visual cortex. J. Neurophysiol., 92, 2652-2658.
37. Rioult-Pedotti, M.S., Friedman, D. & Donoghue, J.P. (2000) Learning-induced LTP in neocortex. Science, 290, 533-536.
38. Rogan, M.T., Stäubli, U.V. & LeDoux, J.E. (1997) Fear conditioning induced associative long-term potentiation in the amygdala. Nature, 390, 604-607.
39. Sale, A., De Pasquale, R., Bonaccorsi, J., Pietra, G., Olivieri, D., Berardi, N. & Maffei, L. (2011) Visual perceptual learning induces long-term potentiation in the visual cortex. Neuroscience, 172, 219-225.
40. Sale, A., Maya Vetencourt, J.F., Medini, P., Cenni, M.C., Baroncelli, L., De Pasquale, R. & Maffei, L. (2007) Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat. Neurosci., 10, 679-681.
41. Sawtell, N.B., Huber, K.M., Roder, J.C. & Bear, M.F. (1999) Induction of NMDA receptor-dependent long-term depression in visual cortex does not require metabotropic glutamate receptors. J. Neurophysiol., 82, 3594-3597.
42. Snyder, M.A., Cooke, B.M. & Woolley, C.S. (2011) Estradiol potentiation of NR2B-dependent EPSCs is not due to changes in NR2B protein expression or phosphorylation. Hippocampus, 21, 398-408.
43. 2+] signaling in individual hippocampal dendritic spines. J. Neurosci., 25, 6037-6046.
44. Strack, S. & Colbran, R.J. (1998) Autophosphorylation-dependent targeting of calcium/calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem., 273, 20689-20692.
45. Tang, Y.P., Shimizu, E., Dube, G.R., Rampon, C., Kerchner, G.A., Zhuo, M., Liu, G. & Tsien, J.Z. (1999) Genetic enhancement of learning and memory in mice. Nature, 401, 63-69.
46. Topolnik, L., Azzi, M., Morin, F., Kougioumoutzakis, A. & Lacaille, J.C. (2006) mGluR1/5 subtype-specific calcium signaling and induction of long-term potentiation in rat hippocampal oriens/alveus interneurones. J. Physiol., 575, 115-131.
47. Tsanov, M. & Manahan-Vaughan, D. (2007) The adult visual cortex expresses dynamic synaptic plasticity that is driven by the light/dark cycle. J. Neurosci., 27, 8414-8421.
48. Whitlock, J.R., Heynen, A.J., Shuler, M.G. & Bear, M.F. (2006) Learning induces long-term potentiation in the hippocampus. Science, 313, 1093-1097.
49. Wu, J., Harney, S., Rowan, M.J. & Anwyl, R. (2008) Involvement of group I mGluRs in LTP induced by strong high frequency stimulation in the dentate gyrus in vitro. Neurosci. Lett., 436, 335-238.
50. Xu, X. & Zhang, Z. (2006) Effects of estradiol benzoate on learning-memory behavior and synaptic structure in ovariectomized mice. Life Sci., 79, 1553-1560.
51. Yashiro, K. & Philpot, B.D. (2008) Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology, 55, 1081-1094.
52. Zhao, M.G., Toyoda, H., Lee, Y.S., Wu, L.J., Ko, S.W., Zhang, X.H., Jia, Y., Shum, F., Xu, H., Li, B.M., Kaang, B.K. & Zhuo, M. (2005) Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron, 47, 859-872.
53. Zhou, Y., Takahashi, E., Li, W., Halt, A., Wiltgen, B., Ehninger, D., Li, G.-D., Hell, J.W., Kennedy, M.B. & Silva, A.J. (2007) Interactions between the NR2B receptor and CaMKII modulate synaptic plasticity and spatial learning. J. Neurosci., 27, 13843-13853.