BDNF contributes to the facilitation of hippocampal synaptic plasticity and learning enabled by environmental enrichment

Hippocampus

Volumn 25, Issue 1, 2015, Pages 1-15

  Novkovic, Tanja ^a,b   Mittmann, Thomas ^c   Manahan Vaughan, Denise ^a,b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b International Graduate School of Neuroscience   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

CA1; Enrichment; LTD; LTP; Object recognition

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; ENVIRONMENT; FEMALE; HIPPOCAMPUS; LEARNING; MALE; METABOLISM; MOUSE; NERVE CELL PLASTICITY; PHYSIOLOGY; RECOGNITION; TRANSGENIC MOUSE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; ENVIRONMENT; FEMALE; HIPPOCAMPUS; LEARNING; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONAL PLASTICITY; RECOGNITION (PSYCHOLOGY);

EID: 84916897532     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22342     Document Type: Article

References (133)

1. Alonso M, Vianna MRM, Depino AM, Mello e Souza T, Pereira P, Szapiro G, Viola H, Pitossi F, Izquierdo I, Medina JH. 2002. BDNF-triggered events in the rat hippocampus are required for both short-and long-term memory formation. Hippocampus 12:551-560.
2. Artola A, Von Frijtag JC, Fermont PCJ, Gispen WH, Schrama LH, Kamal A, Spruijt BM. 2006. Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur J Neurosci 23:261-272.
3. Auvergne R, Leré C, El Bahh B, Arthaud S, Lespinet V, Rougier A, Le Gal La Salle G. 2002. Delayed kindling epileptogenesis and increased neurogenesis in adult rats housed in an enriched environment. Brain Res 954:277-285.
4. Balkowiec A, Katz DM. 2002. Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J Neurosci 22:10399-407.
5. Barnes P, Thomas KL. 2008. Proteolysis of proBDNF is a key regulator in the formation of memory. PLoS One 3:e3248.
6. Bashir ZI, Collingridge GL. 1994. An investigation of depotentiation of long-term potentiation in the CA1 region of the hippocampus. Exp Brain Res 100:437-443.
7. Bekinschtein P, Cammarota M, Igaz LM, Bevilaqua LRM, Izquierdo I, Medina JH. 2007. Persistence of long-term memory storage requires a late protein synthesis-and BDNF-dependent phase in the hippocampus. Neuron 53:261-277.
8. Ben M'Barek K, Pla P, Orvoen S, Benstaali C, Godin JD, Gardier AM, Saudou F, David DJ, Humbert S. 2013. Huntingtin mediates anxiety/depression related behaviors and hippocampal neurogenesis. J Neurosci 33:8608-8620.
9. Bergami M, Rimondini R, Santi S, Blum R, Götz M, Canossa M. 2008. Deletion of TrkB in adult progenitors alters newborn neuron integration intohippocampal circuits and increases anxiety-like behavior. Proc Natl Acad Sci USA 105:15570-15575.
10. Bernstein L. 1973. A study of some enriching variables in a free-environment for rats. J Psychosom Res 17:85-88.
11. Bevins RA, Besheer J. 2006. Object recognition in rats and mice: A one-trial non-matching-to-sample learning task to study 'recognition memory'. Nat Protoc 1:1306-1311.
12. Binder DK, Scharfman HE. 2004. Brain-derived neurotrophic factor. Growth Factors 22:123-131.
13. Birch AM, McGarry NB, Kelly AM. 2013. Short-term environmental enrichment in the absence of exercise, improves memory, and increases NGF concentration, early neuronal survival, and synaptogenesis in the dentate gyrus in a time-dependent manner. Hippocampus 23:437-450.
14. Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT. 1990. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA 87:5568-5572.
15. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. 1994. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59-68.
16. Bruel-Jungerman E, Laroche S, Rampon C. 2005. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 21:513-521.
17. Bruel-Jungerman E, Rampon C, Laroche S. 2007. Adult hippocampal neurogenesis, synaptic plasticity and memory: Facts and hypotheses. Rev Neurosci 18:93-114.
18. Buschler A, Manahan-Vaughan D. 2012. Brief environmental enrichment elicits metaplasticity of hippocampal synaptic long-term potentiation in vivo. Front Behav Neurosci 6:85.
19. Chen G, Kolbeck R, Barde YA, Bonhoeffer T, Kossel A. 1999. Relative contribution of endogenous neurotrophins in hippocampal long-term potentiation. J Neurosci 19:7983-7990.
20. Chen ZY, Patel PD, Sant G, Meng CX, Teng KK, Hempstead BL, Lee FS. 2004. 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 24:4401-4411.
21. Clarke JR, Cammarota M, Gruart A, Izquierdo I, Delgado-Garcia JM. 2010. Plastic modifications induced by object recognition memory processing. Proc Natl Acad Sci USA 107:2652-2657.
22. Croll SD, Suri C, Compton DL, Simmons MV, Yancopoulos GD, Lindsay RM, Wiegand SJ, Rudge JS, Scharfman HE. 1999. Brain-derived neurotrophic factor transgenic mice exhibit passive avoidance deficits, increased seizure severity and in vitro hyperexcitability in the hippocampus and entorhinal cortex. Neuroscience 93:1491-1506.
23. Dahlqvist P, Zhao L, Johansson IM, Mattsson B, Johansson BB, Seckl JR, Olsson T. 1999. Environmental enrichment alters nerve growth factor-induced gene A and glucocorticoid receptor messenger RNA expression after middle cerebral artery occlusion in rats. Neuroscience 93:527-535.
24. Dash PK, Hochner B, Kandel ER. 1990. Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345:718-721.
25. Dieni S, Matsumoto T, Dekkers M, Rauskolb S, Ionescu MS, Deogracias R, Gundelfinger ED, Kojima M, Nestel S, Frotscher M, Barde YA. 2012. BDNF and its pro-peptide are stored in presynaptic dense core vesicles in brain neurons. J Cell Biol 196:775-788.
26. Ding Q, Vaynman S, Akhavan M, Ying Z, Gomez-Pinilla F. 2006. Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 140:823-833.
27. Ding Q, Ying Z, Gómez-Pinilla F. 2011. Exercise influences hippocampal plasticity by modulating brain-derived neurotrophic factor processing. Neuroscience 192:773-780.
28. Dudek SM, Bear MF. 1993. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 13:2910-2918.
29. Duffy SN, Craddock KJ, Abel T, Nguyen PV. 2001. Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus-dependent memory. Learn Mem 8:26-34.
30. Dunwiddie T, Madison D, Lynch G. 1978. Synaptic transmission is required for initiation of long-term potentiation. Brain Res 150:413.
31. Eichenbaum H, Dudchenko P, Wood E, Shapiro M, Tanila H. 1999. The hippocampus, memory, and place cells: Is it spatial memory or a memory space? Neuron 23:209-226.
32. Fahnestock M, Michalski B, Xu B, Coughlin MD. 2001. The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol Cell Neurosci 18:210-220.
33. Falkenberg T, Mohammed AK, Henriksson B, Persson H, Winblad B, Lindefors N. 1992. Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neursosci Lett 138:153-156.
34. Figurov A, Pozzo-Miller LD, Olafsson P, Wang T, Lu B. 1996. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381:706-709.
35. Foster TC, Dumas TC. 2001. Mechanism for increased hippocampal synaptic strength following differential experience. J Neurophysiol 85:1377-1383.
36. Frade JM, Rodríguez-Tébar A, Barde YA. 1996. Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 383:166-168.
37. Frey U, Krug M, Reymann KG, Matthies H. 1988. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57.
38. Globus A, Rosenzweig MR, Bennett EL, Diamond MC. 1973. Effects of differential experience on dendritic spine counts in rat cerebral cortex. J Comp Physiol Psychol 82:175.
39. Gobbo OL, O'mara S. 2004. Impact of enriched-environment housing on brain-derived neurotrophic factor and on cognitive performance after a transient global ischemia. Behav Brain Res 152:231-241.
40. Goh J, Manahan-Vaughan D. 2013a. Spatial object recognition enables endogenous LTD that curtails LTP in the mouse hippocampus. Cerebral Cortex 23:1118-1125.
41. Goh J, Manahan-Vaughan D. 2013b. Endogenous hippocampal LTD that is enabled by spatial object recognition requires activation of NMDA receptors and the metabotropic glutamate receptor, mGlu5. Hippocampus 23:129-138.
42. Goh J, Manahan-Vaughan D. Hippocampal long-term depression in LTD in freely behaving mice requires activation of beta-adrenergic receptors. Hippocampus 23:1299-1308.
43. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
44. Griffin EW, Bechara RG, Birch AM, Kelly AM. 2009. Exercise enhances hippocampal-dependent learning in the rat: Evidence for a BDNF-related mechanism. Hippocampus 19:973-980.
45. Hall J, Thomas KL, Everitt BJ. 2000. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 3:533-534.
46. 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 12:656-670.
47. Hofer MM, Barde YA. 1988. Brain-derived neurotrophic factor prevents neuronal death in vivo. Nature 331:261-262.
48. Huang EJ, Reichardt LF. 2003. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72:609-642.
49. Huang FL, Huang KP, Wu J, Boucheron C. 2006. Environmental enrichment enhances neurogranin expression and hippocampal learning and memory but fails to rescue the impairments of neurogranin null mutant mice. J Neurosci 26:6230-6237.
50. Janz R, Südhof TC, Hammer RE, Unni V, Siegelbaum SA, Bolshakov VY. 1999. Essential roles in synaptic plasticity for synaptogyrin I and synaptophysin I. Neuron 24:687-700.
51. Ibáñez CF. 2002. Jekyll-Hyde neurotrophins: the story of proNGF. Trends Neurosci 25:284-286.
52. Ickes BR, Pham TM, Sanders LA, Albeck DS, Mohammed AH, Granholm AC. 2000. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp Neurol 164:45-52.
53. Kalcheim C, Gendreau M. 1988. Brain-derived neurotrophic factor stimulates survival and neuronal differentiation in cultured avian neural crest. Brain Res 469:79.
54. Kang H, Schuman EM. 1995. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267:1658-1662.
55. Kang H, Welcher AA, Shelton D, Schuman EM. 1997. Neurotrophins and time: Different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19:653-664.
56. Kaplan DR, Miller F. 2000. Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10:381-391.
57. Kelly A, Laroche S, Davis S. 2003. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J Neurosci 23:5354-5360.
58. Kemp N, McQueen J, Faulkes S, Bashir ZI. 2000. Different forms of LTD in the CA1 region of the hippocampus: role of age and stimulus protocol. Eur J Neurosci 12:360-366.
59. Kempermann G, Kuhn HG, Gage FH. 1997. More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
60. Kesler SR, Adams HF, Blasey CM, Bigler ED. 2003. Premorbid intellectual functioning, education, and brain size in traumatic brain injury: An investigation of the cognitive reserve hypothesis. Appl Neuropsychol 10:153-162.
61. Klein R, Nanduri V, Jing S, Lamballe F, Tapley P, Bryant S, Cordon-Cardo C, Jones KR, Reichardt LF, Barbacid M. 1991. The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 66:395.
62. Knipper M, Leung LS, Zhao D, Rylett RJ. 1994. Short-term modulation of glutamatergic synapses in adult rat hippocampus by NGF. Neuroreport 20:2433-246.
63. Kondo M, Takei Y, Hirokawa N. 2012. Motor protein KIF1A is essential for hippocampal synaptogenesis and learning enhancement in an enriched environment. Neuron 73:743-757.
64. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T. 1995. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 92:8856-8860.
65. Kuzumaki N, Ikegami D, Tamura R, Hareyama N, Imai S, Narita M, Torigoe K, Niikura K, Takeshima H, Ando T, Igarashi K, Kanno J, Ushijima T, Suzuki T, Narita M. 2011. Hippocampal epigenetic modification at the brain-derived neurotrophic factor gene induced by an enriched environment. Hippocampus 21:127-132.
66. Lambert TJ, Fernandez SM, Frick KM. 2005. Different types of environmental enrichment have discrepant effects on spatial memory and synaptophysin levels in female mice. Neurobiol Learn Mem 83:206-216.
67. Lee R, Kermani P, Teng KK, Hempstead BL. 2001. Regulation of cell survival by secreted proneurotrophins. Science 294:1945-1948.
68. Lee EH, Hsu WL, Ma YL, Lee PJ, Chao CC. 2003. Enrichment enhances the expression of sgk, a glucocorticoid-induced gene, and facilitates spatial learning through glutamate AMPA receptor mediation. Eur J Neurosci 18:2842-2852.
69. Lee JLC, Everitt BJ, Thomas KL. 2004. Independent cellular processes for hippocampal memory consolidation and reconsolidation. Sci Signal 304:839.
70. Lessmann V, Gottmann K, Heumann R. 1994. BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. Neuroreport 6:21-25.
71. Li S, Tian X, Hartley DM, Feig LA. 2006. The environment versus genetics in controlling the contribution of MAP kinases to synaptic plasticity. Curr Biol 16:2303-13.
72. Li R, Huang FS, Abbas AK, Wigström H. 2007. Role of NMDA receptor subtypes in different forms of NMDA-dependent synaptic plasticity. BMC Neurosci 8:55.
73. Linnarsson S, Björklund A, Ernfors P. 2006. Learning deficit in BDNF mutant mice. Eur J Neurosci 9:2581-2587.
74. Liu L, Moesner P, Kovach NL, Bailey R, Hamilton AD, Sebti SM, Harlan JM. 1999. Integrin-dependent leukocyte adhesion involves geranylgeranylated protein (s). J Biol Chem 274:33334-33340.
75. Lu B. 2003. Pro-region of neurotrophins: role in synaptic modulation. Neuron 39:735-738.
76. Lu B, Pang PT, Woo NH. 2005. The yin and yang of neurotrophin action. Nat Rev Neurosci 6:603-614.
77. Ma YL, Wang HL, Wu HC, Wei CL, Lee EHY. 1997. Brain-derived neurotrophic factor antisense oligonucleotide impairs memory retention and inhibits long-term potentiation in rats. Neuroscience 82:957-967.
78. Manahan-Vaughan D, Kulla A, Frey JU. 2000. Requirement of translation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats. J Neurosci 20:8572-8576.
79. Matsumoto T, Rauskolb S, Polack M, Klose J, Kolbeck R, Korte M, Barde YA. 2008. Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat Neurosci 11:131-133.
80. Meng X, D'Arcy C. 2012. Education and dementia in the context of the cognitive reserve hypothesis: A systematic review with meta-analyses and qualitative analyses. PloS one 7:e38268.
81. McNair K, Broad J, Riedel G, Davies CH, Cobb SR. 2007. Global changes in the hippocampal proteome following exposure to an enriched environment. Neuroscience 145:413-422.
82. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RG, Morrison JH, O'Dell TJ, Grant SG. 1998. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396:433-439.
83. 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.
84. Mowla SJ, Farhadi HF, Pareek S, Atwal JK, Morris SJ, Seidah NG, Murphy RA. 2001. Biosynthesis and post-translational processing of the precursor to brain-derived neurotrophic factor. J Biol Chem 276:12660-12666.
85. Mullany PM, Lynch MA. 1998. Evidence for a role for synaptophysin in expression of long-term potentiation in rat dentate gyrus. Neuroreport 9:2489-2494.
86. Naka F, Narita N, Okado N, Narita M. 2005. Modification of AMPA receptor properties following environmental enrichment. Brain Dev 27:275-278.
87. Ngezahayo A, Schachner M, Artola A. 2000. Synaptic activity modulates the induction of bidirectional synaptic changes in adult mouse hippocampus. J Neurosci 20:2451-2458.
88. Nithianantharajah J, Hannan AJ. 2006. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697-709.
89. O'Callaghan RM, Ohle R, Kelly AM. 2007. The effects of forced exercise on hippocampal plasticity in the rat: A comparison of LTP, spatial-and non-spatial learning. Behav Brain Res 176:362-366.
90. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map. Vol. 3. Oxford: Clarendon Press.
91. Olson AK, Eadie BD, Ernst C, Christie BR. 2006. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16:250-260.
92. Pang PT, Lu B. 2004. Regulation of late-phase LTP and long-term memory in normal and aging hippocampus: Role of secreted proteins tPA and BDNF. Ageing Res Rev 3:407.
93. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B. 2004. Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Sci Signal 306:487.
94. Patapoutian A, Reichardt LF. 2001. Trk receptors: Mediators of neurotrophin action. Curr Opin Neurobiol 11:272-280.
95. Patterson SL, Pittenger C, Morozov A, Martin KC, Scanlin H, Drake C, Kandel ER. 2001. Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32:123-140.
96. Poo M. 2001. Neurotrophins as synaptic modulators. Nat Rev Neurosci 2:24-32.
97. Rampon C, Jiang CH, Dong H, Tang YP, Lockhart DJ, Schultz PG, Tsien JZ, Hu Y. 2000a. Effects of environmental enrichment on gene expression in the brain. Proc Natl Acad Sci USA 97:12880-12884.
98. Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ. 2000b. Supplement to: Enrichment induces structural changes and recovery from nonspatial-memory deficits in CA1-NMDAR1-knockout mice. Nat Neurosci 3:238-244.
99. Reid T, Bathoorn A, Ahmadian MR, Collard JG. 1999. Identification and characterization of hPEM-2, a guanine nucleotide exchange factor specific for Cdc42. J Biol Chem 274:33587-33593.
100. Rosenzweig MR, Bennett EL. 1969. Effects of differential environments on brain weights and enzyme activities in gerbils, rats, and mice. Dev Psychobiol 2:87-95.
101. 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.
102. Rösch H, Schweigreiter R, Bonhoeffer T, Barde YA, Korte M. 2005. The neurotrophin receptor p75NTR modulates long-term depression and regulates the expression of AMPA receptor subunits in the hippocampus. Proc Natl Acad Sci USA 102:7362-7367.
103. Sato K, Morimoto K, Suemaru S, Sato T, Yamada N. 2000. Increased synapsin I immunoreactivity during long-term potentiation in rat hippocampus. Brain Res 872:219-222.
104. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R. 1999. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811-1816.
105. Sisti HM, Glass AL, Shors TJ. 2007. Neurogenesis and the spacing effect: Learning over time enhances memory and the survival of new neurons. Learn Mem 14:368-375.
106. Snyder JS, Kee N, Wojtowicz JM. 2001. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol 85:2423-2431.
107. Spires TL, Grote HE, Varshney NK, Cordery PM, van Dellen A, Blakemore C, Hannan AJ. 2004. Environmental enrichment rescues protein deficits in a mouse model of Huntington's disease, indicating a possible disease mechanism. J Neurosci 24:2270-2276.
108. Staubli UV, Ji ZX. 1996. The induction of homo- vs. heterosynaptic LTD in area CA1 of hippocampal slices from adult rats. Brain Res 714:169-176.
109. Steffener J, Stern Y. 2012. Exploring the neural basis of cognitive reserve in aging. Biochim Biophys Acta 1822:467-473.
110. Stern Y. 2002. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 8:448-460.
111. Sweatt JD. 2001. The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1-10.
112. Tang YP, Wang H, Feng R, Kyin M, Tsien JZ. 2001. Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacol 41:779-790.
113. Tashiro A, Makino H, Gage FH. 2007. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: A critical period during an immature stage. J Neurosci 27:3252-3259.
114. Teather LA, Magnusson JE, Chow CM, Wurtman RJ. 2002. Environmental conditions influence hippocampus-dependent behaviours and brain levels of amyloid precursor protein in rats. Eur J Neurosci 16:2405-2415.
115. Teng HK, Teng KK, Lee R, Wright S, Tevar S, Almeida RD, Kermani P, Torkin R, Chen ZY, Lee FS, Kraemer RT, Nykjaer A, Hempstead BL. 2005. ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 25:5455-5463.
116. Tognoli C, Rossi F, Di Cola F, Baj G, Tongiorgi E, Terova G, Saroglia M, Bernardini G, Gornati R. 2010. Acute stress alters transcript expression pattern and reduces processing of proBDNF to mature BDNF in Dicentrarchus labrax. BMC Neurosci 11:4.
117. Tyler WJ, Alonso M, Bramham CR, Pozzo-Miller LD. 2002. From acquisition to consolidation: On the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn Mem 9:224-237.
118. Van Praag H, Christie BR, Sejnowski TJ, Gage FH. 1999a. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:1342731.
119. Van Praag H, Kempermann G, Gage FH. 1999b. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
120. Van Praag H, Kempermann G, Gage FH. 2000. Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191-198.
121. Vaynman S, Ying Z, Gomez-Pinilla F. 2003. Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience 22:647-57.
122. Volkmar FR, Greenough WT. 1972. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science 176:1445-1447.
123. Wainwright PE, Lévesque S, Krempulec L, Bulman-Fleming B, McCutcheon D. 1993. Effects of environmental enrichment on cortical depth and Morris-maze performance in B6D2F2 mice exposed prenatally to ethanol. Neurotoxicol Teratol 15:11-20.
124. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z. 2002. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420:74-78.
125. Williams BM, Luo Y, Ward C, Redd K, Gibson R, Kuczaj SA, McCoy JG. 2001. Environmental enrichment: effects on spatial memory and hippocampal CREB immunoreactivity. Physiol Behav 73:649-658.
126. Woo NH, Teng HK, Siao CJ, Chiaruttini C, Pang PT, Milner TA, Hempstead BL, Lu B. 2005. Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat Neurosci 8:1069-1077.
127. Wrann CD, White JP, Salogiannnis J, Laznik-Bogoslavski D, Wu J, Ma D, Lin JD, Greenberg ME, Spiegelman BM. 2013. Exercise induces hippocampal BDNF through a PGC-1α/FNDC5 pathway. Cell Metab 18:649-659.
128. Xu B, Gottschalk W, Chow A, Wilson RI, Schnell E, Zang K, Wang D, Nicoll RA, Lu B, Reichardt LF. 2000. The role of brain-derived neurotrophic factor receptors in the mature hippocampus: modulation of long-term potentiation through a presynaptic mechanism involving TrkB. J Neurosci 20:6888-6897.
129. Yang J, Siao CJ, Nagappan G, Marinic T, Jing D, McGrath K, Chen ZY, Mark W, Tessarollo L, Lee FS, Lu B, Hempstead BL. 2009. Neuronal release of proBDNF. Nat Neurosci 12:113-115.
130. Yin X, Takei Y, Kido MA, Hirokawa N. 2011. Molecular motor KIF17 is fundamental for memory and learning via differential support of synaptic NR2A/2B levels. Neuron 70:310-325.
131. Zajac MS, Pang TY, Wong N, Weinrich B, Leang LS, Craig JM, Saffery R, Hannan AJ. 2010. Wheel running and environmental enrichment differentially modify exon-specific BDNF expression in the hippocampus of wild-type and pre-motor symptomatic male and female Huntington's disease mice. Hippocampus 20:621-636.
132. Zakharenko SS, Zablow L, Siegelbaum SA. 2001. Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat Neurosci 4:711-717.
133. Zakharenko SS, Patterson SL, Dragatsis I, Zeitlin SO, Siegelbaum SA, Kandel ER, Morozov A. 2003. Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39:975-990.