Abstract
Microinfusion of BDNF or its neutralizing antibody into the basolateral amygdala (BLA), infralimbic cortex (IL) or hippocampus (HPC) points to synapses in the IL as requiring this neurotrophin for the relatively long-duration long-term potentiation (lLTP) supporting fear extinction. During fear extinction the increase of BDNF in the IL follows the increase of BDNF in ventral HPC (Chhatwal et al. 2006; Peters et al. 2010). The excitability of IL neurons is enhanced by microinfusion of BDNF into the ventral HPC following fear conditioning, (Rosas-Vidal et al. 2014) suggesting that BDNF has been transported from the latter to the former (Burgos-Robles et al. 2007; Chang et al. 2010; Knapska and Maren 2009; Peters et al. 2010; Rosas-Vidal et al. 2014). This is supported by the observation that co-microinfusion of BDNF into the hippocampus together with BDNF antibody into IL blocks the BDNF-generated extinction (Peters et al. 2010). Rats that are opaque to extinction training show poor BDNF projections from the middle HPC to the IL (Peters et al. 2010).
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References
Amaral MD, Pozzo-Miller L (2007) TRPC3 channels are necessary for brain-derived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J Neurosci 27(19):5179–5189. https://doi.org/10.1523/JNEUROSCI.5499-06.2007
Bambah-Mukku D, Travaglia A, Chen DY, Pollonini G, Alberini CM (2014) A positive autoregulatory BDNF feedback loop via C/EBPβ mediates hippocampal memory consolidation. J Neurosci 34(37):12547–12559. https://doi.org/10.1523/JNEUROSCI.0324-14.2014
Bekinschtein P, Cammarota M, Katche C, Slipczuk L, Rossato JI, Goldin A et al (2008) BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci 105(7):2711–2716. https://doi.org/10.1073/pnas.0711863105
Bracaglia G, Conca B, Bergo A, Rusconi L, Zhou Z, Greenberg ME et al (2009) Methyl-CpG-binding protein 2 is phosphorylated by homeodomain-interacting protein kinase 2 and contributes to apoptosis. EMBO Rep 10(12):1327–1333. https://doi.org/10.1038/embor.2009.217
Burgos-Robles A, Vidal-Gonzalez I, Santini E, Quirk GJ (2007) Consolidation of fear extinction requires NMDA receptor-dependent bursting in the ventromedial prefrontal cortex. Neuron 53(6):871–880. https://doi.org/10.1016/j.neuron.2007.02.021
Cardinaux JR, Notis JC, Zhang Q, Vo N, Craig JC, Fass DM et al (2000) Recruitment of CREB binding protein is sufficient for CREB-mediated gene activation. Mol Cell Biol 20(5):1546–1552
Chang CH, Berke JD, Maren S (2010) Single-unit activity in the medial prefrontal cortex during immediate and delayed extinction of fear in rats. PLoS One 5(8):e11971. https://doi.org/10.1371/journal.pone.0011971
Chen WG, Chang Q, Lin Y, Meissner A, West AE, Griffith EC et al (2003) Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302(5646):885–889. https://doi.org/10.1126/science.1086446
Chhatwal JP, Stanek-Rattiner L, Davis M, Ressler KJ (2006) Amygdala BDNF signaling is required for consolidation but not encoding of extinction. Nat Neurosci 9(7):870–872. https://doi.org/10.1038/nn1718
Cohen S, Greenberg ME (2010) A bird’s-eye view of MeCP2 binding. Mol Cell 37(4):451–452. https://doi.org/10.1016/j.molcel.2010.02.006
Cohen S, Gabel HW, Hemberg M, Hutchinson AN, Sadacca LA, Ebert DH et al (2011) Genome-wide activity-dependent MeCP2 phosphorylation regulates nervous system development and function. Neuron 72(1):72–85. https://doi.org/10.1016/j.neuron.2011.08.022
Gonzales ML, Adams S, Dunaway KW, LaSalle JM (2012) Phosphorylation of distinct sites in MeCP2 modifies cofactor associations and the dynamics of transcriptional regulation. Mol Cell Biol 32(14):2894–2903. https://doi.org/10.1128/mcb.06728-11
Hartmann M, Heumann R, Lessmann V (2001) Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J 20(21):5887–5897. https://doi.org/10.1093/emboj/20.21.5887
Heldt SA, Stanek L, Chhatwal JP, Ressler KJ (2007) Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 12(7):656–670. https://doi.org/10.1038/sj.mp.4001957
Heldt SA, Zimmermann K, Parker K, Gaval M, Ressler KJ (2014) Bdnf deletion or TrkB impairment in amygdala inhibits both appetitive and aversive learning. J Neurosci 34(7):2444–2450. https://doi.org/10.1523/JNEUROSCI.4085-12.2014
Hsu C-C, Lu C-W, Huang B-M, Wu M-H, Tsai S-J (2008) Cyclic adenosine 3′,5′-monophosphate response element-binding protein and CCAAT/enhancer-binding protein mediate prostaglandin E(2)-induced steroidogenic acute regulatory protein expression in endometriotic stromal cells. Am J Pathol 173(2):433–441. https://doi.org/10.2353/ajpath.2008.080199
Hutchinson AN, Deng JV, Cohen S, West AE (2012) Phosphorylation of MeCP2 at Ser421 contributes to chronic antidepressant action. J Neurosci 32(41):14355–14363. https://doi.org/10.1523/jneurosci.2156-12.2012
Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R, Beausoleil SA et al (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143(7):1174–1189. https://doi.org/10.1016/j.cell.2010.12.001
Katche C, Cammarota M, Medina JH (2013) Molecular signatures and mechanisms of long-lasting memory consolidation and storage. Neurobiol Learn Mem 106:40–47. https://doi.org/10.1016/j.nlm.2013.06.018
Knapska E, Maren S (2009) Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learn Mem 16(8):486–493. https://doi.org/10.1101/lm.1463909
Kohara K, Kitamura A, Morishima M, Tsumoto T (2001) Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 291(5512):2419–2423. https://doi.org/10.1126/science.1057415
Kojima M, Takei N, Numakawa T, Ishikawa Y, Suzuki S, Matsumoto T et al (2001) Biological characterization and optical imaging of brain-derived neurotrophic factor-green fluorescent protein suggest an activity-dependent local release of brain-derived neurotrophic factor in neurites of cultured hippocampal neurons. J Neurosci Res 64(1):1–10. https://doi.org/10.1002/jnr.1080
Kruttgen A, Moller JC, Heymach JV Jr, Shooter EM (1998) Neurotrophins induce release of neurotrophins by the regulated secretory pathway. Proc Natl Acad Sci USA 95(16):9614–9619
Lessmann V, Brigadski T (2009) Mechanisms, locations, and kinetics of synaptic BDNF secretion: an update. Neurosci Res 65(1):11–22. https://doi.org/10.1016/j.neures.2009.06.004
Lessmann V, Gottmann K, Malcangio M (2003) Neurotrophin secretion: current facts and future prospects. Prog Neurobiol 69(5):341–374
Li H, Chang Q (2014) Regulation and function of stimulus-induced phosphorylation of MeCP2. Front Biol (Beijing) 9(5):367–375. https://doi.org/10.1007/s11515-014-1330-2
Li H, Zhong X, Chau KF, Williams EC, Chang Q (2011) Loss of activity-induced phosphorylation of MeCP2 enhances synaptogenesis, LTP and spatial memory. Nat Neurosci 14(8):1001–1008. https://doi.org/10.1038/nn.2866
Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y et al (2003) DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302(5646):890–893. https://doi.org/10.1126/science.1090842
Peters J, Dieppa-Perea LM, Melendez LM, Quirk GJ (2010) Induction of fear extinction with hippocampal-infralimbic BDNF. Science 328(5983):1288–1290. https://doi.org/10.1126/science.1186909
Plendl W, Wotjak CT (2010) Dissociation of within- and between-session extinction of conditioned fear. J Neurosci 30(14):4990–4998. https://doi.org/10.1523/JNEUROSCI.6038-09.2010
Rosas-Vidal LE, Do-Monte FH, Sotres-Bayon F, Quirk GJ (2014) Hippocampal—prefrontal BDNF and memory for fear extinction. Neuropsychopharmacology 39(9):2161–2169. https://doi.org/10.1038/npp.2014.64
Rousseaud A, Delepine C, Nectoux J, Billuart P, Bienvenu T (2015) Differential expression and regulation of brain-derived neurotrophic factor (BDNF) mRNA isoforms in brain cells from Mecp2(308/y) mouse model. J Mol Neurosci 56(4):758–767. https://doi.org/10.1007/s12031-014-0487-0
Sakata K, Martinowich K, Woo NH, Schloesser RJ, Jimenez DV, Ji Y et al (2013) Role of activity-dependent BDNF expression in hippocampal-prefrontal cortical regulation of behavioral perseverance. Proc Natl Acad Sci USA 110(37):15103–15108. https://doi.org/10.1073/pnas.1222872110
Tao J, Hu K, Chang Q, Wu H, Sherman NE, Martinowich K et al (2009) Phosphorylation of MeCP2 at Serine 80 regulates its chromatin association and neurological function. Proc Natl Acad Sci USA 106(12):4882–4887. https://doi.org/10.1073/pnas.0811648106
Taubenfeld SM, Milekic MH, Monti B, Alberini CM (2001a) The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat Neurosci 4(8):813–818. https://doi.org/10.1038/90520
Taubenfeld SM, Wiig KA, Monti B, Dolan B, Pollonini G, Alberini CM (2001b) Fornix-dependent induction of hippocampal CCAAT enhancer-binding protein [beta] and [delta] Co-localizes with phosphorylated cAMP response element-binding protein and accompanies long-term memory consolidation. J Neurosci 21(1):84–91
Young JI, Hong EP, Castle JC, Crespo-Barreto J, Bowman AB, Rose MF et al (2005) Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2. Proc Natl Acad Sci USA 102(49):17551–17558. https://doi.org/10.1073/pnas.0507856102
Zhou Z, Hong EJ, Cohen S, Zhao WN, Ho HY, Schmidt L et al (2006) Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52(2):255–269. https://doi.org/10.1016/j.neuron.2006.09.037
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Bennett, M., Lagopoulos, J. (2018). Modulation of the Core Synaptic Network in Extinction: The Role of Brain-Derived Neurotrophic Factor. In: Stress, Trauma and Synaptic Plasticity. Springer, Cham. https://doi.org/10.1007/978-3-319-91116-8_7
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