Temporal Memory and Its Enhancement by Estradiol Requires Surface Dynamics of Hippocampal CA1 N-Methyl-D-Aspartate Receptors

Biological Psychiatry

Volumn 79, Issue 9, 2016, Pages 735-745

  Potier, Mylène ^a,c   Georges, François ^b,c   Brayda Bruno, Laurent ^a,c   Ladépêche, Laurent ^b,c   Lamothe, Valérie ^a,c   Al Abed, Alice Shaam ^a,c   Groc, Laurent ^b,c   Marighetto, Aline ^a,b  

^a INSTITUT FRANÇOIS MAGENDIE   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Episodic memory; Estrogen; Hippocampus; Lateral diffusion; Long term potentiation; Temporal associations

Indexed keywords

CHLORPHENIRAMINE MALEATE PLUS PHENYLEPHRINE; ESTRADIOL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SEX HORMONE; SEX HORMONE E2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATIVE MEMORY; CELL DENSITY; DENDRITIC SPINE; ELECTROPHYSIOLOGY; EMBRYO; EPISODIC MEMORY; HIPPOCAMPAL CA1 REGION; IN VITRO STUDY; IN VIVO STUDY; MALE; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SURFACE PROPERTY; TEMPORAL CORTEX; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; LONG TERM POTENTIATION; MEMORY; NERVE CELL; PHYSIOLOGY; PROTEIN TRANSPORT; SYNAPSE;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CELLS, CULTURED; ESTRADIOL; LONG-TERM POTENTIATION; MALE; MEMORY; MICE, INBRED C57BL; NEURONS; PROTEIN TRANSPORT; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 84940099447     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2015.07.017     Document Type: Article

References (64)

1. Eichenbaum, H., Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron 44 (2004), 109–120.
2. 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.
3. Collingridge, G.L., Isaac, J.T., Wang, Y.T., Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 5 (2004), 952–962.
4. Huerta, P.T., Sun, L.D., Wilson, M.A., Tonegawa, S., Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 25 (2000), 473–480.
5. Taylor, A.M., Bus, T., Sprengel, R., Seeburg, P.H., Rawlins, J.N., Bannerman, D.M., Hippocampal NMDA receptors are important for behavioural inhibition but not for encoding associative spatial memories. Philos Trans R Soc Lond B Biol Sci, 369, 2014, 20130149.
6. Tovar, K.R., Westbrook, G.L., Mobile NMDA receptors at hippocampal synapses. Neuron 34 (2002), 255–264.
7. Bard, L., Groc, L., Glutamate receptor dynamics and protein interaction: Lessons from the NMDA receptor. Mol Cell Neurosci 48 (2011), 298–307.
8. Dupuis, J.P., Ladepeche, L., Seth, H., Bard, L., Varela, J., Mikasova, L., et al. Surface dynamics of GluN2B-NMDA receptors controls plasticity of maturing glutamate synapses. EMBO J 33 (2014), 842–861.
9. McEwen, B.S., Stress, sex, and neural adaptation to a changing environment: Mechanisms of neuronal remodeling. Ann N Y Acad Sci 1204:suppl (2010), E38–E59.
10. Shors, T.J., Lewczyk, C., Pacynski, M., Mathew, P.R., Pickett, J., Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. Neuroreport 9 (1998), 419–423.
11. Sandstrom, N.J., Williams, C.L., Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 115 (2001), 384–393.
12. Luine, V.N., Jacome, L.F., Maclusky, N.J., Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144 (2003), 2836–2844.
13. Leuner, B., Mendolia-Loffredo, S., Shors, T.J., High levels of estrogen enhance associative memory formation in ovariectomized females. Psychoneuroendocrinology 29 (2004), 883–890.
14. Hojo, Y., Murakami, G., Mukai, H., Higo, S., Hatanaka, Y., Ogiue-Ikeda, M., et al. Estrogen synthesis in the brain-role in synaptic plasticity and memory. Mol Cell Endocrinol 290 (2008), 31–43.
15. Mitra, S.W., Hoskin, E., Yudkovitz, J., Pear, L., Wilkinson, H.A., Hayashi, S., et al. Immunolocalization of estrogen receptor beta in the mouse brain: Comparison with estrogen receptor alpha. Endocrinology 144 (2003), 2055–2067.
16. Mitterling, K.L., Spencer, J.L., Dziedzic, N., Shenoy, S., McCarthy, K., Waters, E.M., et al. Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J Comp Neurol 518 (2010), 2729–2743.
17. Good, M., Day, M., Muir, J.L., Cyclical changes in endogenous levels of oestrogen modulate the induction of LTD and LTP in the hippocampal CA1 region. Eur J Neurosci 11 (1999), 4476–4480.
18. Gould, E., Woolley, C.S., Frankfurt, M., McEwen, B.S., Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10 (1990), 1286–1291.
19. Mukai, H., Tsurugizawa, T., Murakami, G., Kominami, S., Ishii, H., Ogiue-Ikeda, M., et al. Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. J Neurochem 100 (2007), 950–967.
20. Woolley, C.S., McEwen, B.S., Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12 (1992), 2549–2554.
21. Zamani, M.R., Desmond, N.L., Levy, W.B., Estradiol modulates long-term synaptic depression in female rat hippocampus. J Neurophysiol 84 (2000), 1800–1808.
22. Woolley, C.S., Gould, E., Frankfurt, M., McEwen, B.S., Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10 (1990), 4035–4039.
23. Gazzaley, A.H., Weiland, N.G., McEwen, B.S., Morrison, J.H., Differential regulation of NMDAR1 mRNA and protein by estradiol in the rat hippocampus. J Neurosci 16 (1996), 6830–6838.
24. Woolley, C.S., Weiland, N.G., McEwen, B.S., Schwartzkroin, P.A., Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: Correlation with dendritic spine density. J Neurosci 17 (1997), 1848–1859.
25. Smith, C.C., McMahon, L.L., Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J Neurosci 26 (2006), 8517–8522.
26. Snyder, M.A., Cooke, B.M., Woolley, C.S., Estradiol potentiation of NR2B-dependent EPSCs is not due to changes in NR2B protein expression or phosphorylation. Hippocampus 21 (2011), 398–408.
27. Adams, M.M., Fink, S.E., Janssen, W.G., Shah, R.A., Morrison, J.H., Estrogen modulates synaptic N-methyl-D-aspartate receptor subunit distribution in the aged hippocampus. J Comp Neurol 474 (2004), 419–426.
28. Groc, L., Choquet, D., Chaouloff, F., The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci 11 (2008), 868–870.
29. Heine, M., Groc, L., Frischknecht, R., Beique, J.C., Lounis, B., Rumbaugh, G., et al. Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320 (2008), 201–205.
30. Mingaud, F., Le Moine, C., Etchamendy, N., Mormede, C., Jaffard, R., Marighetto, A., The hippocampus plays a critical role at encoding discontiguous events for subsequent declarative memory expression in mice. Hippocampus 17 (2007), 264–270.
31. Kaouane, N., Porte, Y., Vallee, M., Brayda-Bruno, L., Mons, N., Calandreau, L., et al. Glucocorticoids can induce PTSD-like memory impairments in mice. Science 335 (2012), 1510–1513.
32. Misane, I., Tovote, P., Meyer, M., Spiess, J., Ogren, S.O., Stiedl, O., Time-dependent involvement of the dorsal hippocampus in trace fear conditioning in mice. Hippocampus 15 (2005), 418–426.
33. Fanselow, M.S., Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 15 (1980), 177–182.
34. Assini, F.L., Duzzioni, M., Takahashi, R.N., Object location memory in mice: Pharmacological validation and further evidence of hippocampal CA1 participation. Behav Brain Res 204 (2009), 206–211.
35. Waters, E.M., Mitterling, K., Spencer, J.L., Mazid, S., McEwen, B.S., Milner, T.A., Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus. Brain Res 1290 (2009), 1–11.
36. Jelks, K.B., Wylie, R., Floyd, C.L., McAllister, A.K., Wise, P., Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: Critical role of estrogen receptor-alpha. J Neurosci 27 (2007), 6903–6913.
37. Murphy, D.D., Segal, M., Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 16 (1996), 4059–4068.
38. Srivastava, D.P., Woolfrey, K.M., Jones, K.A., Shum, C.Y., Lash, L.L., Swanson, G.T., Penzes, P., Rapid enhancement of two-step wiring plasticity by estrogen and NMDA receptor activity. Proc Natl Acad Sci U S A 105 (2008), 14650–14655.
39. Woolley, C.S., McEwen, B.S., Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 14 (1994), 7680–7687.
40. Barker, G.R., Warburton, E.C., When is the hippocampus involved in recognition memory?. J Neurosci 31 (2011), 10721–10731.
41. Nabavi, S., Kessels, H.W., Alfonso, S., Aow, J., Fox, R., Malinow, R., Metabotropic NMDA receptor function is required for NMDA receptor-dependent long-term depression. Proc Natl Acad Sci U S A 110 (2013), 4027–4032.
42. Eichenbaum, H., Memory on time. Trends Cogn Sci 17 (2013), 81–88.
43. Woolley, C.S., Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 47 (2007), 657–680.
44. Smith, C.C., Vedder, L.C., McMahon, L.L., Estradiol and the relationship between dendritic spines, NR2B containing NMDA receptors, and the magnitude of long-term potentiation at hippocampal CA3-CA1 synapses. Psychoneuroendocrinology 34:suppl 1 (2009), S130–S142.
45. Lau, C.G., Zukin, R.S., NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat Rev Neurosci 8 (2007), 413–426.
46. Yashiro, K., Philpot, B.D., Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 55 (2008), 1081–1094.
47. Frick, K.M., Molecular mechanisms underlying the memory-enhancing effects of estradiol. Horm Behav 74 (2015), 4–18.
48. Tuscher, J.J., Fortress, A.M., Kim, J., Frick, K.M., Regulation of object recognition and object placement by ovarian sex steroid hormones. Behav Brain Res 285 (2015), 140–157.
49. Kesner, R.P., Lee, I., Gilbert, P., A behavioral assessment of hippocampal function based on a subregional analysis. Rev Neurosci 15 (2004), 333–351.
50. Hunsaker, M.R., Tran, G.T., Kesner, R.P., A behavioral analysis of the role of CA3 and CA1 subcortical efferents during classical fear conditioning. Behav Neurosci 123 (2009), 624–630.
51. McHugh, T.J., Tonegawa, S., CA3 NMDA receptors are required for the rapid formation of a salient contextual representation. Hippocampus 19 (2009), 1153–1158.
52. Place, R., Lykken, C., Beer, Z., Suh, J., McHugh, T.J., Tonegawa, S., et al. NMDA signaling in CA1 mediates selectively the spatial component of episodic memory. Learn Mem 19 (2012), 164–169.
53. Rogers, J.L., Hunsaker, M.R., Kesner, R.P., Effects of ventral and dorsal CA1 subregional lesions on trace fear conditioning. Neurobiol Learn Mem 86 (2006), 72–81.
54. Bast, T., Zhang, W.N., Feldon, J., Dorsal hippocampus and classical fear conditioning to tone and context in rats: Effects of local NMDA-receptor blockade and stimulation. Hippocampus 13 (2003), 657–675.
55. Czerniawski, J., Ree, F., Chia, C., Otto, T., Dorsal versus ventral hippocampal contributions to trace and contextual conditioning: Differential effects of regionally selective NMDA receptor antagonism on acquisition and expression. Hippocampus 22 (2012), 1528–1539.
56. Gao, C., Gill, M.B., Tronson, N.C., Guedea, A.L., Guzman, Y.F., Huh, K.H., et al. Hippocampal NMDA receptor subunits differentially regulate fear memory formation and neuronal signal propagation. Hippocampus 20 (2010), 1072–1082.
57. Quinn, J.J., Loya, F., Ma, Q.D., Fanselow, M.S., Dorsal hippocampus NMDA receptors differentially mediate trace and contextual fear conditioning. Hippocampus 15 (2005), 665–674.
58. Schenberg, E.E., Oliveira, M.G., Effects of pre or posttraining dorsal hippocampus D-AP5 injection on fear conditioning to tone, background, and foreground context. Hippocampus 18 (2008), 1089–1093.
59. Stiedl, O., Birkenfeld, K., Palve, M., Spiess, J., Impairment of conditioned contextual fear of C57BL/6J mice by intracerebral injections of the NMDA receptor antagonist APV. Behav Brain Res 116 (2000), 157–168.
60. Wanisch, K., Tang, J., Mederer, A., Wotjak, C.T., Trace fear conditioning depends on NMDA receptor activation and protein synthesis within the dorsal hippocampus of mice. Behav Brain Res 157 (2005), 63–69.
61. Vedder, L.C., Smith, C.C., Flannigan, A.E., McMahon, L.L., Estradiol-induced increase in novel object recognition requires hippocampal NR2B-containing NMDA receptors. Hippocampus 23 (2013), 108–115.
62. Dalla, C., Shors, T.J., Sex differences in learning processes of classical and operant conditioning. Physiol Behav 97 (2009), 229–238.
63. Eadie, B.D., Cushman, J., Kannangara, T.S., Fanselow, M.S., Christie, B.R., NMDA receptor hypofunction in the dentate gyrus and impaired context discrimination in adult Fmr1 knockout mice. Hippocampus 22 (2012), 241–254.
64. Kheirbek, M.A., Tannenholz, L., Hen, R., NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J Neurosci 32 (2012), 8696–8702.