Contextual learning increases dendrite complexity and EphrinB2 levels in hippocampal mouse neurons

Behavioural Brain Research

Volumn 227, Issue 1, 2012, Pages 175-183

  Trabalza, Antonio ^a   Colazingari, Sandra ^a   Sgobio, Carmelo ^b   Bevilacqua, Arturo ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Amygdala; Contextual fear conditioning; Cued fear conditioning; Dendritic nodes; Dendritic spines; EphrinB2; Hippocampus; Mouse; Pyramidal neurons

Indexed keywords

EPHRIN B2; EPHRIN RECEPTOR A4;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; CONDITIONING; CONTEXTUAL LEARNING; CONTROLLED STUDY; DENDRITE; FEAR; HIPPOCAMPAL CA1 REGION; LATERAL AMYGDALA; LEARNING; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; CELL COUNT; CONDITIONING (PSYCHOLOGY); CUES; DENDRITES; EPHRIN-B2; EXPLORATORY BEHAVIOR; FEAR; GENE EXPRESSION REGULATION; HIPPOCAMPUS; IMMOBILITY RESPONSE, TONIC; MALE; MENTAL RECALL; MICE; MICE, INBRED C57BL; NEURONS; SILVER STAINING; TIME FACTORS;

EID: 82355161279     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.11.008     Document Type: Article

References (60)

1. Frankland P.W., Bontempi B. The organization of recent and remote memories. Nat Rev Neurosci 2005, 6:119-130.
2. Leuner B., Falduto J., Shors T.J. Associative memory formation increases the observation of dendritic spines in the hippocampus?. J Neurosci 2003, 23(2):659-665.
3. Knafo S., Ariav G., Barkai E., Libersat F. Olfactory learning-induced increases in spine density along the spine density along the apical dendrites in CA1 hippocampal neuron?. Hippocampus 2004, 14(7):819-825.
4. Restivo L., Roman F.S., Ammassari-Teule M., Marchetti E. Simultaneous olfactory discrimination elicits a strain-specific increase in dendritic spines in the hippocampus of inbred mice?. Hippocampus 2006, 16(5):472-479.
5. Restivo L., Vetere G., Bontempi B., Ammassari-Teule M. The formation of recent and remote memory is associated with time-dependent formation of dendritic spines in the hippocampus and anterior cingulate cortex?. J Neurosci 2009, 29(25):8206-8214.
6. Kullander K., Klein R. Mechanisms and functions of Eph and Ephrin signalling?. Nat Rev Mol Cell Biol 2002, 3(7):475-486.
7. Yoshihara Y., De Roo M., Muller D. Dendritic spine formation and stabilization. Curr Opin Neurobiol 2009, (2):146-153.
8. Klein R. Bidirectional modulation of synaptic functions by Eph/Ephrin signalling?. Nat Neurosci 2009, 12(1):15-20.
9. Pasquale E.B. Eph-Ephrin bidirectional signaling in physiology and disease. Cell 2008, 133:38-52.
10. Rao A., Kim E., Sheng M., Craig A.M. Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture?. J Neurosci 1998, 18(4):1217-1229.
11. Dalva M.B., Takasu M.A., Lin M.Z., Shamah S.M., Hu L., Gale N.W., Greenberg M.E. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation?. Cell 2000, 103(6):945-956.
12. Takasu M.A., Dalva M.B., Zigmond R.E., Greenberg M.E. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 2002, 295:491-495.
13. Grunwald I.C., Korte M., Wolfer D., Wilkinson G.A., Unsicker K., Lipp H.P., Bonhoeffer T., Klein R. Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity. Neuron 2001, 32:1027-1040.
14. Grunwald I.C., Korte M., Adelmann G., Plueck A., Kullander K., Adams R.H., Frotscher M., Bonhoeffer T., Klein R. Hippocampal plasticity requires postsynaptic EphrinBs. Nat Neurosci 2004, 7:33-40.
15. Migani P., Bartlett C., Dunlop S., Beazley L., Roger J. Ephrin-B2 immunoreactivity distribution in adult mouse brain. Brain Res 2007, 1182:60-72.
16. Tremblay M.E., Riad M., Bouvier D., Murai K.K., Pasquale E.B., Descarries L., Doucet G. Localization of EphA4 in axon terminals and dendritic spines of adult rat hippocampus. J Comp Neurol 2007, 501:691-702.
17. Glaser E.M., Van Der Loos G. Analysis of thick brain sections by observe-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J Neurosci Methods 1981, 4:117-125.
18. Gibb R., Kolb B. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J Neurosci Methods 1998, 79:1-4.
19. Franklin K.B.J., Paxinos G. The mouse brain in stereotaxic coordinates 2001, Academic, San Diego. 2nd ed.
20. Vyas A., Mitra R., Shankaranarayana Rao B.S., Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 2002, 22(15):6810-6818.
21. Antibodies: a laboratory manual 1988, 449. Cold Spring Harbor Laboratory, N.Y. E. Harlow, D. Lane (Eds.).
22. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
23. Isoda K., Morimoto M., Matsui F., Hasegawa T., Tozawa T., Morioka S., et al. Postnatal changes in serotonergic innervation to the hippocampus of methyl-CpG-binding protein 2-null mice. Neuroscience 2010, 165:1254-1260.
24. Holland S.J., Gale N.W., Mbamalu G., Yancopoulos G.D., Henkemeyer M., Pawson D. Bidirectional signalling through the EPH-family receptor Nuk and its transmembrane ligands. Nature 1996, 383:722-725.
25. Zola-Morgan S.M., Squire L.R. The primate hippocampal formation: evidence for a time-limited role in memory storage. Science 1990, 250:288-290.
26. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 1992, 256:675-677.
27. Martin S.J., Clark R.E. The rodent hippocampus and spatial memory: from synapses to systems. Cell Mol Life Sci 2007, 64:401-431.
28. Bailey C.H., Kandel E.R., Si K. The persistence of long-term memory: a molecular approach to self-sustaining changes in learning-induced synaptic growth. Neuron 2004, 44:49-57.
29. Sanders M.J., Wiltgen B.J., Fanselow M.S. The place of the hippocampus in fear conditioning?. Eur J Pharmacol 2003, 463(1-3):217-223.
30. Koo J.W., Han J.S., Kim J.J. Selective neurotoxic lesions of basolateral and central nuclei of the amygdala produce differential effects on fear conditioning. J Neurosci 2004, 24:7654-7662.
31. Rodrigues S.M., Schafe G.E., LeDoux J.E. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 2004, 44:75-91.
32. Huff N.C., Frank M., Wright-Hardesty K., Sprunger D., Matus-Amat P., Higgins E., Rudy J.W. Amygdala regulation of immediate-early gene expression in the hippocampus induced by contextual fear conditioning. J Neurosci 2006, 26(5):1616-1623.
33. Isiegas C., Park A., Kandel E.R., Abel T., Lattal K.M. Transgenic inhibition of neuronal protein kinase A activity facilitates fear extinction. J Neurosci 2006, 26:12700-12707.
34. Tronson N.C., Schrick C., Fischer A., Sananbenesi F., Pages G., Pouyssegur J., Radulovic J. Regulatory mechanisms of fear extinction and depression-like behavior. Neuropsychopharmacology 2008, 33:1570-1583.
35. Sananbenesi F., Fischer A., Wang X., Schrick C., Neve R., Radulovic J., Tsai L.H. A hippocampal Cdk5 pathway regulates extinction of contextual fear. Nat Neurosci 2007, 10:1012-1019.
36. Radulovic J., Kammermeier J., Spiess J. Relationship between fos production and classical fear conditioning: effects of novelty, latent inhibition, and unconditioned stimulus preexposure. J Neurosci 1998, 18:7452-7461.
37. Matsuo N., Reijmers L., Mayford M. Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 2008, 319:1104-1107.
38. Goosens K.A., Holt W., Maren S. A role for amygdaloid PKA and PKC in the acquisition of long-term conditional fear memories in rats. Behav Brain Res 2000, 114:145-152.
39. Weeber E.J., Atkins C.M., Selcher J.C., Varga A.W., Mirnikjoo B., Paylor R., Leitges M., Sweatt J.D. A role for the beta isoform of protein kinase C in fear conditioning. J Neurosci 2000, 20:5906-5914.
40. Schafe G.E., Atkins C.M., Swank M.W., Bauer E.P., Sweatt J.D., LeDoux J.E. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning. J Neurosci 2000, 20:8177-8187.
41. 2+/calmodulin-dependent protein kinase II at lateral amygdala synapses. J Neurosci 2004, 24:3281-3288.
42. Scicli A.P., Petrovich G.D., Swanson L.W., Thompson R.F. Contextual fear conditioning is associated with lateralized expression of the immediate early gene c-fos in the central and basolateral amygdalar nuclei. Behav Neurosci 2004, 118:5-14.
43. Liebl D.J., Morris C.J., Henkemeyer M., Parada L.F. mRNA expression of Ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system. J Neurosci Res 2003, 71:7-22.
44. Friedman G.C., O'Leary D.D.M. Eph receptor tyrosine kinases and their ligands in neural development. Curr Opin Neurobiol 1996, 6:127-133.
45. Winslow J.M., Moral O., Valverde J., Shih A., Yuan J.Q., Wong S.C., Tsai S.P., Goddard A., Henzel W.J., Hefti F., Beck K.D., Caras I.W. Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. Neuron 1995, 14:973-981.
46. Donoghue M.J., Merlie J.P., Sanes J.R. The Eph Kinase Ligand AL-1 is expressed by rostral muscles and inhibits outgrowth from caudal neurons. Mol Cell Neurosci 1996, 8(2/3):185-198.
47. Flanagan J.G., Vanderhaeghen P. The Ephrins and Eph receptors in neural development. Annu Rev Neurosci 1998, 21:390-445.
48. Gao W.Q., Shinsky N., Armanini M.P., Moran P., Zheng J.L., Mendoza-Ramirez J.L., Phillips H.S., Winslow J.W., Caras I.W. Regulation of hippocampal synaptic plasticity by the tyrosine kinase receptor, REK7/EphA5, and its ligand, AL-1/Ephrin-A5. Mol Cell Neurosci 1998, (5-6):247-259.
49. Murai K.K., Pasquale E.B. Eph receptor, Ephrins, and synaptic function. Neuroscientist 2004, 10(4):304-314.
50. Contractor A., Rogers C., Maron C., Henkemeyer M., Swanson G.T., Heinemann S.F. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 2002, 296(5574):1864-1869.
51. Henderson J.T., Georgiou J., Jia Z., Robertson J., Elowe S., Roder J.C., Pawson T. The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron 2001, 32:1041-1056.
52. Suárez J., Llorente R., Romero-Zerbo S.Y., Mateos B., Bermúdez-Silva F.J., de Fonseca F.R., Viveros M.P. Early maternal deprivation induces gender-dependent changes on the expression of hippocampal CB(1) and CB(2) cannabinoid receptors of neonatal rats. Hippocampus 2009, 19(7):623-632.
53. Ferri P., Cecchini T., Ambrogini P., Betti M., Cuppini R., Del Grande P., Ciaroni S. Alpha-tocopherol affects neuronal plasticity in adult rat dentate gyrus: the possible role of PKCdelta. J Neurobiol 2006, 66(8):793-810.
54. Tang S.J., Reis G., Kang H., Gingras A.C., Sonenberg N., Schuman E.M. A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci USA 2002, 99:467-472.
55. Kang H., Schuman E.M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 1996, 273:1402-1406.
56. Huber K.M., Kayser M.S., Bear M.F. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent LTD. Science 2000, 288:1254-1257.
57. Cracco J.B., Serrano P., Moskowitz S.I., Bergold P.J., Sacktor T.C. Protein synthesis-dependent LTP in isolated dendrites of CA1 pyramidal cells. Hippocampus 2005, 15:551-556.
58. Pfeiffer B.E., Huber M. Current advances in local protein synthesis and synaptic plasticity. J Neurosci 2006, 26(27):7147-7150.
59. Silva A.J. Molecular and cellular cognitive studies of the role of synaptic plasticity in memory. J Neurobiol 2003, 54:224-237.
60. Squire L.R., Bayley P.J. The neuroscience of remote memory. Curr Opin Neurobiol 2007, 17:185-196.