Brain-derived neurotrophic factor interacts with adult-born immature cells in the dentate gyrus during consolidation of overlapping memories

Hippocampus

Volumn 24, Issue 8, 2014, Pages 905-911

  Bekinschtein, Pedro ^a,b   Kent, Brianne A ^a,b   Oomen, Charlotte A ^a,b   Clemenson, Gregory D ^c   Gage, Fred H ^c   Saksida, Lisa M ^a,b   Bussey, Timothy J ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

BDNF; Dentate gyrus; Memory consolidation; Neurogenesis

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; RECOMBINANT PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; BRAIN REGION; CELL MATURATION; CONTROLLED STUDY; DENTATE GYRUS; IMMUNOHISTOCHEMISTRY; MALE; MEMORY CONSOLIDATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; HUMAN; LONG EVANS RAT; MEMORY; METABOLISM; NERVE CELL; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DENTATE GYRUS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MEMORY; NEUROGENESIS; NEURONS; NEUROPSYCHOLOGICAL TESTS; RATS, LONG-EVANS; RECOMBINANT PROTEINS;

EID: 84904246559     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22304     Document Type: Article

References (31)

1. Aimone JB, Wiles J, Gage FH. 2009. Computational influence of adult neurogenesis on memory encoding. Neuron 61:187-202.
2. Aimone JB, Deng W, Gage FH. 2011. Resolving new memories: A critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70:589-596.
3. Bekinschtein P, Oomen CA, Saksida LM, Bussey TJ. 2011. Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable? Semin Cell Dev Biol 22:536-542.
4. Bekinschtein P, Kent BA, Oomen CA, Clemenson GD, Gage FH, Saksida LM, Bussey TJ. 2013. BDNF in the dentate gyrus is required for consolidation of "pattern-separated" memories. Cell Rep 5:759-768.
5. Bergami M, Rimondini R, Santi S, Blum R, Gotz M, Canossa M. 2008. Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc Natl Acad Sci USA 105:15570-15575.
6. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ. 2009. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:210-213.
7. Creer DJ, Romberg C, Saksida LM, van Praag H, Bussey TJ. 2010. Running enhances spatial pattern separation in mice. Proc Natl Acad Sci USA 107:2367-2372.
8. Ennaceur A, Neave N, Aggleton JP. 1997. Spontaneous object recognition and object location memory in rats: The effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 113:509-519.
9. Ge S, Yang CH, Hsu KS, Ming GL, Song H. 2007. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54:559-566.
10. Gilbert PE, Kesner RP, DeCoteau WE. 1998. Memory for spatial location: Role of the hippocampus in mediating spatial pattern separation. J Neurosci 18:804-810.
11. Holm MM, Nieto-Gonzalez JL, Vardya I, Vaegter CB, Nykjaer A, Jensen K. 2009. Mature BDNF, but not proBDNF, reduces excitability of fast-spiking interneurons in mouse dentate gyrus. J Neurosci 29:12412-12418.
12. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, Lie DC, Squire LR, Gage FH. 2009. Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16:147-154.
13. Kheirbek MA, Tannenholz L, Hen R. 2012. NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J Neurosci 32:8696-8702.
14. Kitamura T, Saitoh Y, Takashima N, Murayama A, Niibori Y, Ageta H, Sekiguchi M, Sugiyama H, Inokuchi K. 2009. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 139:814-827.
15. Leutgeb JK, Leutgeb S, Moser MB, Moser EI. 2007. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966.
16. Levine ES, Kolb JE. 2000. Brain-derived neurotrophic factor increases activity of NR2B-containing N-methyl-D-aspartate receptors in excised patches from hippocampal neurons. J Neurosci Res 62:357-362.
17. Lie DC, Colamarino SA, Song HJ, Desire L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH. 2005. Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370-1375.
18. Lu H, Cheng PL, Lim BK, Khoshnevisrad N, Poo MM. 2010. Elevated BDNF after cocaine withdrawal facilitates LTP in medial prefrontal cortex by suppressing GABA inhibition. Neuron 67:821-833.
19. McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S. 2007. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317:94-99.
20. Mizuno M, Yamada K, He J, Nakajima A, Nabeshima T. 2003. Involvement of BDNF receptor TrkB in spatial memory formation. Learn Mem 10:108-115.
21. Mou L, Heldt SA, Ressler KJ. 2011. Rapid brain-derived neurotrophic factor-dependent sequestration of amygdala and hippocampal GABA(A) receptors via different tyrosine receptor kinase B-mediated phosphorylation pathways. Neuroscience 176:72-85.
22. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S. 2012. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188-201.
23. Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, Joels M, Lucassen PJ, Krugers H. 2010. Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J Neurosci 30:6635-6645.
24. Paxinos G, Watson C. 1998. The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press.
25. Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F, Fabbri ME, Tessarollo L, Maffei L, Berardi N, Caleo M. 2006. Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 24:1850-1856.
26. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R. 2011. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466-470.
27. Scharfman H, Goodman J, Macleod A, Phani S, Antonelli C, Croll S. 2005. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol 192:348-356.
28. Schmidt-Hieber C, Jonas P, Bischofberger J. 2004. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184-187.
29. Tronel S, Belnoue L, Grosjean N, Revest JM, Piazza PV, Koehl M, Abrous DN. 2012. Adult-born neurons are necessary for extended contextual discrimination. Hippocampus 22:292-298.
30. Warburton EC, Baird AL, Morgan A, Muir JL, Aggleton JP. 2000. Disconnecting hippocampal projections to the anterior thalamus produces deficits on tests of spatial memory in rats. Eur J Neurosci 12:1714-1726.
31. Xu F, Plummer MR, Len GW, Nakazawa T, Yamamoto T, Black IB, Wu K. 2006. Brain-derived neurotrophic factor rapidly increases NMDA receptor channel activity through Fyn-mediated phosphorylation. Brain Res 1121:22-34.