The Role of BDNF in the Development of Fear Learning

Depression and Anxiety

Volumn 33, Issue 10, 2016, Pages 907-916

  Dincheva, Iva ^a   Lynch, Niccola B ^a   Lee, Francis S ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

adolescence; anxiety; BDNF prodomain; extinction learning; fear conditioning; polymorphism

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; ISOPROTEIN; MESSENGER RNA; METHIONINE; NEUROTROPHIN; NEUROTROPHIN RECEPTOR P75;

ADOLESCENCE; ALLELE; BRAIN DEVELOPMENT; BRAIN MATURATION; CONNECTOME; ENVIRONMENTAL FACTOR; FEAR; GENE TARGETING; HEREDITY; HIPPOCAMPUS; HUMAN; LEARNING; MENTAL DISEASE; NERVE CELL PLASTICITY; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REINFORCEMENT; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 84991079552     PISSN: 10914269     EISSN: 15206394     Source Type: Journal    
DOI: 10.1002/da.22497     Document Type: Review

References (91)

1. Liberman LC, Lipp OV, Spence SH, March S. Evidence for retarded extinction of aversive learning in anxious children. Behav Res Ther 2006;44(10):1491–1502.
2. Kessler RC, Demler O, Frank RG, et al. Prevalence and treatment of mental disorders, 1990 to 2003. N Engl J Med 2005;352(24):2515–2523.
3. Duman RS, Li N. A neurotrophic hypothesis of depression: role of synaptogenesis in the actions of NMDA receptor antagonists. Philos Trans R Soc Lond B Biol Sci 2012;367(1601):2475–2484.
4. Duman RS, Monteggia LM. A neurotrophic model for stress-related mood disorders. Biol Psychiatry 2006;59(12):1116–1127.
5. Boyle LM. A neuroplasticity hypothesis of chronic stress in the basolateral amygdala. Yale J Biol Med 2013;86(2):117–125.
6. Huang ZJ, Kirkwood A, Pizzorusso T, et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999;98(6):739–755.
7. Chao MV. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 2003;4(4):299–309.
8. Greenberg ME, Xu B, Lu B, Hempstead BL. New insights in the biology of BDNF synthesis and release: implications in CNS function. J Neurosci 2009;29(41):12764–12767.
9. Anastasia A, Deinhardt K, Chao MV, et al. Val66Met polymorphism of BDNF alters prodomain structure to induce neuronal growth cone retraction. Nat Commun 2013;4:1–12.
10. Cowley S, Paterson H, Kemp P, Marshall CJ. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 1994;77(6):841–852.
11. Mazzucchelli C, Vantaggiato C, Ciamei A, et al. Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron 2002;34(5):807–820.
12. Rosenblum K, Futter M, Voss K, et al. The role of extracellular regulated kinases I/II in late-phase long-term potentiation. J Neurosci 2002;22(13):5432–5441.
13. Chao MV, Rajagopal R, Lee FS. Neurotrophin signalling in health and disease. Clin Sci (Lond) 2006;110(2):167–173.
14. Minichiello L. TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 2009;10(12):850–860.
15. Yang J, Siao CJ, Nagappan G, et al. Neuronal release of proBDNF. Nat Neurosci 2009;12(2):113–115.
16. Teng HK, Teng KK, Lee R, et al. ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 2005;25(22):5455–5463.
17. Yang J, Harte-Hargrove LC, Siao CJ, et al. proBDNF negatively regulates neuronal remodeling, synaptic transmission, and synaptic plasticity in hippocampus. Cell Rep 2014;7(3):796–806.
18. Deinhardt K, Chao MV. Shaping neurons: long and short range effects of mature and proBDNF signalling upon neuronal structure. Neuropharmacology 2014;76 Pt C:603–609.
19. Teng KK, Felice S, Kim T, Hempstead BL. Understanding proneurotrophin actions: recent advances and challenges. Dev Neurobiol 2010;70(5):350–359.
20. Je HS, Yang F, Ji Y, et al. Role of pro-brain-derived neurotrophic factor (proBDNF) to mature BDNF conversion in activity-dependent competition at developing neuromuscular synapses. Proc Natl Acad Sci USA 2012;109(39):15924–15929.
21. Sun Y, Lim Y, Li F, et al. ProBDNF collapses neurite outgrowth of primary neurons by activating RhoA. PLoS One 2012;7(4):e35883.
22. Roux PP, Barker PA. Neurotrophin signaling through the p75 neurotrophin receptor. Prog Neurobiol 2002;67(3):203–233.
23. Woo NH, Teng HK, Siao CJ, et al. Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat Neurosci 2005;8(8):1069–1077.
24. Cowansage KK, LeDoux JE, Monfils MH. Brain-derived neurotrophic factor: a dynamic gatekeeper of neural plasticity. Curr Mol Pharmacol 2010;3(1):12–29.
25. Katoh-Semba R, Takeuchi IK, Semba R, Kato K. Distribution of brain-derived neurotrophic factor in rats and its changes with development in the brain. J Neurochem 1997;69(1):34–42.
26. Kolbeck R, Bartke I, Eberle W, Barde YA. Brain-derived neurotrophic factor levels in the nervous system of wild-type and neurotrophin gene mutant mice. J Neurochem 1999;72(5):1930-1938.
27. Ivanova T, Beyer C. Pre- and postnatal expression of brain-derived neurotrophic factor mRNA/protein and tyrosine protein kinase receptor B mRNA in the mouse hippocampus. Neurosci Lett 2001;307(1):21–24.
28. Kim J, Yang M, Song L, et al. Developmental and degenerative modulation of brain-derived neurotrophic factor transcript variants in the mouse hippocampus. Int J Dev Neurosci 2014;38:68–73.
29. Galvin C, Lee FS, Ninan I. Alteration of the centromedial amygdala glutamatergic synapses by the BDNF Val66Met polymorphism. Neuropsychopharmacology 2015;40(9):2269–2277.
30. Rauskolb S, Zagrebelsky M, Dreznjak A, et al. Global deprivation of brain-derived neurotrophic factor in the CNS reveals an area-specific requirement for dendritic growth. J Neurosci 2010;30(5):1739–1749.
31. Mizui T, Ishikawa Y, Kumanogoh H, et al. BDNF pro-peptide actions facilitate hippocampal LTD and are altered by the common BDNF polymorphism Val66Met. Proc Natl Acad Sci USA 2015;112(23):E3067–E3074.
32. Egan MF, Kojima M, Callicott JH, et al. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 2003;112(2):257–269.
33. Petryshen TL, Sabeti PC, Aldinger KA, et al. Population genetic study of the brain-derived neurotrophic factor (BDNF) gene. Mol Psychiatry 2010;15(8):810–815.
34. Dincheva I, Glatt CE, Lee FS. Impact of the BDNF Val66Met polymorphism on cognition: implications for behavioral genetics. Neuroscientist 2012;18(5):439–451.
35. Hariri AR, Goldberg TE, Mattay VS, et al. Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J Neurosci 2003;23(17):6690–6694.
36. Pezawas L, Verchinski BA, Mattay VS, et al. The brain-derived neurotrophic factor val66met polymorphism and variation in human cortical morphology. J Neurosci 2004;24(45):10099–10102.
37. Verhagen M, van der Meij A, van Deurzen PA, et al. Meta-analysis of the BDNF Val66Met polymorphism in major depressive disorder: effects of gender and ethnicity. Mol Psychiatry 2010;15(3):260–271.
38. Montag C, Basten U, Stelzel C, et al. The BDNF Val66Met polymorphism and anxiety: support for animal knock-in studies from a genetic association study in humans. Psychiatry Res 2010;179(1):86–90.
39. Felmingham KL, Dobson-Stone C, Schofield PR, et al. The brain-derived neurotrophic factor Val66Met polymorphism predicts response to exposure therapy in posttraumatic stress disorder. Biol Psychiatry 2013;73(11):1059–1063.
40. Chen ZY, Jing D, Bath KG, et al. Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 2006;314(5796):140–143.
41. Chen ZY, Patel PD, Sant G, et al. Variant brain-derived neurotrophic factor (BDNF) (Met66) alters the intracellular trafficking and activity-dependent secretion of wild-type BDNF in neurosecretory cells and cortical neurons. J Neurosci 2004;24(18):4401–4411.
42. Chen ZY, Ieraci A, Teng H, et al. Sortilin controls intracellular sorting of brain-derived neurotrophic factor to the regulated secretory pathway. J Neurosci 2005;25(26):6156–6166.
43. Lou H, Kim SK, Zaitsev E, et al. Sorting and activity-dependent secretion of BDNF require interaction of a specific motif with the sorting receptor carboxypeptidase e. Neuron 2005;45(2):245–255.
44. Dincheva I, Pattwell SS, Tessarollo L, et al. BDNF modulates contextual fear learning during adolescence. Dev Neurosci 2014;36(3–4):269–276.
45. Fryer RH, Kaplan DR, Feinstein SC, et al. Developmental and mature expression of full-length and truncated TrkB receptors in the rat forebrain. J Comp Neurol 1996;374(1):21–40.
46. Silhol M, Bonnichon V, Rage F, Tapia-Arancibia L. Age-related changes in brain-derived neurotrophic factor and tyrosine kinase receptor isoforms in the hippocampus and hypothalamus in male rats. Neuroscience 2005;132(3):613–624.
47. Petralia RS, Sans N, Wang YX, Wenthold RJ. Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol Cell Neurosci 2005;29(3):436–452.
48. Escandon E, Soppet D, Rosenthal A, et al. Regulation of neurotrophin receptor expression during embryonic and postnatal development. J Neurosci 1994;14(4):2054–2068.
49. Bracken BK, Turrigiano GG. Experience-dependent regulation of TrkB isoforms in rodent visual cortex. Dev Neurobiol 2009;69(5):267–278.
50. Andero R, Choi DC, Ressler KJ. BDNF-TrkB receptor regulation of distributed adult neural plasticity, memory formation, and psychiatric disorders. Prog Mol Biol Transl Sci 2014;122:169–192.
51. Collins DR, Pare D. Differential fear conditioning induces reciprocal changes in the sensory responses of lateral amygdala neurons to the CS(+) and CS(-). Learn Mem 2000;7(2):97–103.
52. Quirk GJ, Repa C, LeDoux JE. Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 1995;15(5):1029–1039.
53. Sotres-Bayon F, Sierra-Mercado D, Pardilla-Delgado E, Quirk GJ. Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron 2012;76(4):804–812.
54. Maren S. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 2001;24:897–931.
55. Corcoran KA, Quirk GJ. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J Neurosci 2007;27(4):840–844.
56. Burgos-Robles A, Vidal-Gonzalez I, Quirk GJ. Sustained conditioned responses in prelimbic prefrontal neurons are correlated with fear expression and extinction failure. J Neurosci 2009;29(26):8474–8482.
57. Hefner K, Whittle N, Juhasz J, et al. Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J Neurosci 2008;28(32):8074–8085.
58. Knapska E, Maren S. Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learn Mem 2009;16(8):486–493.
59. Berretta S, Pantazopoulos H, Caldera M, et al. Infralimbic cortex activation increases c-Fos expression in intercalated neurons of the amygdala. Neuroscience 2005;132(4):943–953.
60. Likhtik E, Popa D, Apergis-Schoute J, et al. Amygdala intercalated neurons are required for expression of fear extinction. Nature 2008;454(7204):642–645.
61. Peters J, Dieppa-Perea LM, Melendez LM, Quirk GJ. Induction of fear extinction with hippocampal-infralimbic BDNF. Science 2010;328(5983):1288–1290.
62. Rosas-Vidal LE, Do-Monte FH, Sotres-Bayon F, Quirk GJ. Hippocampal—prefrontal BDNF and memory for fear extinction. Neuropsychopharmacology 2014;39(9):2161–2169.
63. Chhatwal JP, Stanek-Rattiner L, Davis M, Ressler KJ. Amygdala BDNF signaling is required for consolidation but not encoding of extinction. Nat Neurosci 2006;9(7):870–872.
64. Liu IY, Lyons WE, Mamounas LA, Thompson RF. Brain-derived neurotrophic factor plays a critical role in contextual fear conditioning. J Neurosci 2004;24(36):7958–7963.
65. Koponen E, Voikar V, Riekki R, et al. Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLCgamma pathway, reduced anxiety, and facilitated learning. Mol Cell Neurosci 2004;26(1):166–181.
66. Woolley SM, Fremouw TE, Hsu A, Theunissen FE. Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds. Nat Neurosci 2005;8(10):1371–1379.
67. Boskovic Z, Alfonsi F, Rumballe BA, et al. The role of p75NTR in cholinergic basal forebrain structure and function. J Neurosci 2014;34(39):13033–13038.
68. Gogtay N, Giedd JN, Lusk L, et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 2004;101(21):8174–8179.
69. Lenroot RK, Giedd JN. Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neurosci Biobehav Rev 2006;30(6):718–729.
70. Sowell ER, Thompson PM, Holmes CJ, et al. In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 1999;2(10):859–861.
71. Frankland PW, Josselyn SA, Bradwejn J, et al. Activation of amygdala cholecystokininB receptors potentiates the acoustic startle response in the rat. J Neurosci 1997;17(5):1838–1847.
72. Yeo JF, Tang FR, Leong SK. Expression of glutamate receptor subunit 1 and nitric oxide synthase in the hypoglossal nucleus and dorsal vagal nucleus in the rat after neurectomy. Int J Neurosci 1997;90(1–2):9–20.
73. Stamford JA, Isaac D, Hicks CA, et al. Ascorbic acid is neuroprotective against global ischaemia in striatum but not hippocampus: histological and voltammetric data. Brain Res 1999;835(2):229–240.
74. Kim JH, Li S, Richardson R. Immunohistochemical analyses of long-term extinction of conditioned fear in adolescent rats. Cereb Cortex 2011;21(3):530–538.
75. McCallum J, Kim JH, Richardson R. Impaired extinction retention in adolescent rats: effects of D-cycloserine. Neuropsychopharmacology 2010;35(10):2134–2142.
76. Pattwell SS, Duhoux S, Hartley CA, et al. Altered fear learning across development in both mouse and human. Proc Natl Acad Sci USA 2012;109(40):16318–16323.
77. Pattwell SS, Bath KG, Casey BJ, et al. Selective early-acquired fear memories undergo temporary suppression during adolescence. Proc Natl Acad Sci USA 2011;108(3):1182–1187.
78. Casey BJ, Pattwell SS, Glatt CE, Lee FS. Treating the developing brain: implications from human imaging and mouse genetics. Annu Rev Med 2013;64:427–439.
79. Shechner T, Britton JC, Ronkin EG, et al. Fear conditioning and extinction in anxious and nonanxious youth and adults: examining a novel developmentally appropriate fear-conditioning task. Depress Anxiety 2015;32(4):277–288.
80. Gee DG, Gabard-Durnam LJ, Flannery J, et al. Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proc Natl Acad Sci USA 2013;110(39):15638–15643.
81. Gordon JA, Stryker MP. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci 1996;16(10):3274–3286.
82. Cabelli RJ, Hohn A, Shatz CJ. Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 1995;267(5204):1662–1666.
83. Soliman F, Glatt CE, Bath KG, et al. A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science 2010;327(5967):863–866.
84. Middlemas DS, Lindberg RA, Hunter T. trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol Cell Biol 1991;11(1):143–153.
85. Carim-Todd L, Bath KG, Fulgenzi G, et al. Endogenous truncated TrkB.T1 receptor regulates neuronal complexity and TrkB kinase receptor function in vivo. J Neurosci 2009;29(3):678–685.
86. Biffo S, Offenhauser N, Carter BD, Barde YA. Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development. Development 1995;121(8):2461–2470.
87. Eide FF, Vining ER, Eide BL, et al. Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling. J Neurosci 1996;16(10):3123–3129.
88. Pattwell SS, Bath KG, Perez-Castro R, et al. The BDNF Val66Met polymorphism impairs synaptic transmission and plasticity in the infralimbic medial prefrontal cortex. J Neurosci 2012;32(7):2410–2421.
89. Bath KG, Chuang J, Spencer-Segal JL, et al. Variant brain-derived neurotrophic factor (Valine66Methionine) polymorphism contributes to developmental and estrous stage-specific expression of anxiety-like behavior in female mice. Biol Psychiatry 2012;72(6):499–504.
90. Spear LP. Adolescent brain development and animal models. Ann N Y Acad Sci 2004;1021:23–26.
91. Spencer JL, Waters EM, Milner TA, et al. BDNF variant Val66Met interacts with estrous cycle in the control of hippocampal function. Proc Natl Acad Sci USA 2010;107(9):4395–4400.