Role of Neurotrophic Factors in Behavioral Processes: Implications for the Treatment of Psychiatric and Neurodegenerative Disorders

Vitamins and Hormones

Volumn 82, Issue , 2010, Pages 185-200

  Pardon, Marie Christine ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Addiction; Anxiety; BDNF; Cognition; Neurodegenerative disorders; Neurotrophins; NGF; Vulnerability to stress

Indexed keywords

NARCOTIC ANALGESIC AGENT; NERVE GROWTH FACTOR;

ADDICTION; ANIMAL; DEGENERATIVE DISEASE; HUMAN; MENTAL DISEASE; METABOLISM; MOUSE; REVIEW;

ANALGESICS, OPIOID; ANIMALS; HUMANS; MENTAL DISORDERS; MICE; NERVE GROWTH FACTORS; NEURODEGENERATIVE DISEASES; SUBSTANCE-RELATED DISORDERS;

EID: 77955887038     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0083-6729(10)82010-2     Document Type: Chapter

References (91)

1. Allaman, I., Papp, M., Kraftsik, R., Fiumelli, H., Magistretti, P.J., Martin, J.L., Expression of brain-derived neurotrophic factor is not modulated by chronic mild stress in the rat hippocampus and amygdala. Pharmacol. Rep. 60 (2008), 1001–1007.
2. Alleva, E., Francia, N., Psychiatric vulnerability: Suggestions from animal models and role of neurotrophins. Neurosci. Biobehav. Rev. 33 (2009), 525–536.
3. Alleva, L., Aloe, F., Cirulli, D., Seta, Della, Tirassa, P., Serum NGF levels increase during lactation and following maternal aggression in mice. Physiol. Behav. 59 (1996), 461–466.
4. Aloe, L., Alleva, E., De Simone, R., Changes of NGF level in mouse hypothalamus following intermale aggressive behaviour: Biological and immunohistochemical evidence. Behav. Brain Res. 39 (1990), 53–61.
5. Alonso, M., Bekinschtein, P., Cammarota, M., Vianna, M.R., Izquierdo, I., Medina, J.H., Endogenous BDNF is required for long-term memory formation in the rat parietal cortex. Learn Mem. 12 (2005), 504–510.
6. Ang, E.T., Gomez-Pinilla, F., Potential therapeutic effects of exercise to the brain. Curr. Med. Chem. 14 (2007), 2564–2571.
7. Angelucci, F., Ricci, V., Pomponi, M., Conte, G., Mathe, A.A., Attilio Tonali, P., Bria, P., Chronic heroin and cocaine abuse is associated with decreased serum concentrations of the nerve growth factor and brain-derived neurotrophic factor. J. Psychopharmacol. 21 (2007), 820–825.
8. Angelucci, F., Ricci, V., Spalletta, G., Pomponi, M., Tonioni, F., Caltagirone, C., Bria, P., Reduced serum concentrations of nerve growth factor, but not brain-derived neurotrophic factor, in chronic cannabis abusers. Eur. Neuropsychopharmacol. 18 (2008), 882–887.
9. Bahi, A., Boyer, F., Chandrasekar, V., Dreyer, J.L., Role of accumbens BDNF and TrkB in cocaine-induced psychomotor sensitization, conditioned-place preference, and reinstatement in rats. Psychopharmacology (Berl.) 199 (2008), 169–182.
10. Bergami, M., Berninger, B., Canossa, M., Conditional deletion of TrkB alters adult hippocampal neurogenesis and anxiety-related behavior. Commun. Integr. Biol. 2 (2009), 14–16.
11. Berglind, W.J., See, R.E., Fuchs, R.A., Ghee, S.M., Whitfield, T.W. Jr., Miller, S.W., McGinty, J.F., A BDNF infusion into the medial prefrontal cortex suppresses cocaine seeking in rats. Eur. J. Neurosci. 26 (2007), 757–766.
12. Bergstrom, A., Jayatissa, M.N., Mork, A., Wiborg, O., Stress sensitivity and resilience in the chronic mild stress rat model of depression; an in situ hybridization study. Brain Res. 1196 (2008), 41–52.
13. Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., Graham, D., Tsankova, N.M., Bolanos, C.A., Rios, M., Monteggia, L.M., Self, D.W., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 (2006), 864–868.
14. Blurton-Jones, M., Kitazawa, M., Martinez-Coria, H., Castello, N.A., Muller, F.J., Loring, J.F., Yamasaki, T.R., Poon, W.W., Green, K.N., LaFerla, F.M., Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc. Natl. Acad. Sci. USA 106 (2009), 13594–13599.
15. Bondar, N.P., Boyarskikh, U.A., Kovalenko, I.L., Filipenko, M.L., Kudryavtseva, N.N., Molecular implications of repeated aggression: Th, Dat1 Snca and Bdnf gene expression in the VTA of victorious male mice. PLoS ONE, 4, 2009, e4190.
16. Broad, K.D., Mimmack, M.L., Keverne, E.B., Kendrick, K.M., Increased BDNF and trk-B mRNA expression in cortical and limbic regions following formation of a social recognition memory. Eur. J. Neurosci. 16 (2002), 2166–2174.
17. Castillo, D.V., Figueroa-Guzman, Y., Escobar, M.L., Brain-derived neurotrophic factor enhances conditioned taste aversion retention. Brain Res. 1067 (2006), 250–255.
18. Chan, J.P., Unger, T.J., Byrnes, J., Rios, M., Examination of behavioral deficits triggered by targeting Bdnf in fetal or postnatal brains of mice. Neuroscience 142 (2006), 49–58.
19. Chourbaji, S., Hellweg, R., Brandis, D., Zorner, B., Zacher, C., Lang, U.E., Henn, F.A., Hortnagl, H., Gass, P., Mice with reduced brain-derived neurotrophic factor expression show decreased choline acetyltransferase activity, but regular brain monoamine levels and unaltered emotional behavior. Brain Res. Mol. Brain Res. 121 (2004), 28–36.
20. Cirulli, F., Alleva, E., The NGF saga: From animal models of psychosocial stress to stress-related psychopathology. Front. Neuroendocrinol. 30 (2009), 379–395.
21. Cirulli, F., Berry, A., Chiarotti, F., Alleva, E., Intrahippocampal administration of BDNF in adult rats affects short-term behavioral plasticity in the Morris water maze and performance in the elevated plus-maze. Hippocampus 14 (2004), 802–807.
22. Cohen, S., Greenberg, M.E., Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu. Rev. Cell Dev. Biol. 24 (2008), 183–209.
23. Conner, J.M., Franks, K.M., Titterness, A.K., Russell, K., Merrill, D.A., Christie, B.R., Sejnowski, T.J., Tuszynski, M.H., NGF is essential for hippocampal plasticity and learning. J. Neurosci. 29 (2009), 10883–10889.
24. Costa, M.S., Botton, P.H., Mioranzza, S., Ardais, A.P., Moreira, J.D., Souza, D.O., Porciuncula, L.O., Caffeine improves adult mice performance in the object recognition task and increases BDNF and TrkB independent on phospho-CREB immunocontent in the hippocampus. Neurochem. Int. 53 (2008), 89–94.
25. Deltheil, T., Tanaka, K., Reperant, C., Hen, R., David, D.J., Gardier, A.M., Synergistic neurochemical and behavioural effects of acute intrahippocampal injection of brain-derived neurotrophic factor and antidepressants in adult mice. Int. J. Neuropsychopharmacol., 2009, 1–11.
26. Fiore, M., Amendola, T., Triaca, V., Tirassa, P., Alleva, E., Aloe, L., Agonistic encounters in aged male mouse potentiate the expression of endogenous brain NGF and BDNF: Possible implication for brain progenitor cells’ activation. Eur. J. Neurosci. 17 (2003), 1455–1464.
27. Fiore, M., Amendola, T., Triaca, V., Alleva, E., Aloe, L., Fighting in the aged male mouse increases the expression of TrkA and TrkB in the subventricular zone and in the hippocampus. Behav. Brain Res. 157 (2005), 351–362.
28. Freeman, A.Y., Pierce, R.C., Neutralization of neutrophin-3 in the ventral tegmental area or nucleus accumbens differentially modulates cocaine-induced behavioral plasticity in rats. Synapse 46 (2002), 57–65.
29. Frick, K.M., Price, D.L., Koliatsos, V.E., Markowska, A.L., The effects of nerve growth factor on spatial recent memory in aged rats persist after discontinuation of treatment. J. Neurosci. 17 (1997), 2543–2550.
30. Frielingsdorf, H., Thal, L.J., Pizzo, D.P., The septohippocampal cholinergic system and spatial working memory in the Morris water maze. Behav. Brain Res. 168 (2006), 37–46.
31. Fumagalli, F., Di Pasquale, L., Caffino, L., Racagni, G., Riva, M.A., Repeated exposure to cocaine differently modulates BDNF mRNA and protein levels in rat striatum and prefrontal cortex. Eur. J. Neurosci. 26 (2007), 2756–2763.
32. Furini, C.R., Rossato, J.I., Bitencourt, L.L., Medina, J.H., Izquierdo, I., Cammarota, M., beta-Adrenergic receptors link NO/sGC/PKG signaling to BDNF expression during the consolidation of object recognition long-term memory. Hippocampus, 2009.
33. Gorski, J.A., Balogh, S.A., Wehner, J.M., Jones, K.R., Learning deficits in forebrain-restricted brain-derived neurotrophic factor mutant mice. Neuroscience 121 (2003), 341–354.
34. Graham, D.L., Edwards, S., Bachtell, R.K., DiLeone, R.J., Rios, M., Self, D.W., Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nat. Neurosci. 10 (2007), 1029–1037.
35. Griesbach, G.S., Hovda, D.A., Gomez-Pinilla, F., Exercise-induced improvement in cognitive performance after traumatic brain injury in rats is dependent on BDNF activation. Brain Res. 1288 (2009), 105–115.
36. Grimm, J.W., Lu, L., Hayashi, T., Hope, B.T., Su, T.P., Shaham, Y., Time-dependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: Implications for incubation of cocaine craving. J. Neurosci. 23 (2003), 742–747.
37. Gronli, J., Bramham, C., Murison, R., Kanhema, T., Fiske, E., Bjorvatn, B., Ursin, R., Portas, C.M., Chronic mild stress inhibits BDNF protein expression and CREB activation in the dentate gyrus but not in the hippocampus proper. Pharmacol. Biochem. Behav. 85 (2006), 842–849.
38. Haenisch, B., Bilkei-Gorzo, A., Caron, M.G., Bonisch, H., Knockout of the norepinephrine transporter and pharmacologically diverse antidepressants prevent behavioral and brain neurotrophin alterations in two chronic stress models of depression. J. Neurochem. 111 (2009), 403–416.
39. Heberlein, A., Bleich, S., Bayerlein, K., Frieling, H., Groschl, M., Kornhuber, J., Hillemacher, T., NGF plasma levels increase due to alcohol intoxication and decrease during withdrawal. Psychoneuroendocrinology 33 (2008), 999–1003.
40. Heldt, S.A., Stanek, L., Chhatwal, J.P., Ressler, K.J., Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol. Psychiatry 12 (2007), 656–670.
41. Huang, E.J., Reichardt, L.F., Trk receptors: Roles in neuronal signal transduction. Annu. Rev. Biochem. 72 (2003), 609–642.
42. Ibarguen-Vargas, Y., Surget, A., Vourc'h, P., Leman, S., Andres, C.R., Gardier, A.M., Belzung, C., Deficit in BDNF does not increase vulnerability to stress but dampens antidepressant-like effects in the unpredictable chronic mild stress. Behav. Brain Res. 202 (2009), 245–251.
43. Jockers-Scherubl, M.C., Bauer, A., Kuhn, S., Reischies, F., Danker-Hopfe, H., Schmidt, L.G., Rentzsch, J., Hellweg, R., Nerve growth factor in serum is a marker of the stage of alcohol disease. Neurosci. Lett. 419 (2007), 78–82.
44. Jockers-Scherubl, M.C., Zubraegel, D., Baer, T., Linden, M., Danker-Hopfe, H., Schulte-Herbruggen, O., Neu, P., Hellweg, R., Nerve growth factor serum concentrations rise after successful cognitive-behavioural therapy of generalized anxiety disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 31 (2007), 200–204.
45. Kerns, R.T., Ravindranathan, A., Hassan, S., Cage, M.P., York, T., Sikela, J.M., Williams, R.W., Miles, M.F., Ethanol-responsive brain region expression networks: Implications for behavioral responses to acute ethanol in DBA/2J versus C57BL/6J mice. J. Neurosci. 25 (2005), 2255–2266.
46. Khabour, O.F., Alzoubi, K.H., Alomari, M.A., Alzubi, M.A., Changes in spatial memory and BDNF expression to concurrent dietary restriction and voluntary exercise. Hippocampus, 2009.
47. Koizumi, H., Hashimoto, K., Iyo, M., Dietary restriction changes behaviours in brain-derived neurotrophic factor heterozygous mice: Role of serotonergic system. Eur. J. Neurosci. 24 (2006), 2335–2344.
48. Koponen, E., Voikar, V., Riekki, R., Saarelainen, T., Rauramaa, T., Rauvala, H., Taira, T., Castren, E., 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. 26 (2004), 166–181.
49. Krishnan, V., Han, M.H., Graham, D.L., Berton, O., Renthal, W., Russo, S.J., Laplant, Q., Graham, A., Lutter, M., Lagace, D.C., Ghose, S., Reister, R., et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131 (2007), 391–404.
50. Lang, U.E., Gunther, L., Scheuch, K., Klein, J., Eckhart, S., Hellweg, R., Danker-Hopfe, H., Oehler, J., Higher BDNF concentrations in the hippocampus and cortex of an aggressive mouse strain. Behav. Brain Res. 197 (2009), 246–249.
51. Le Foll, B., Diaz, J., Sokoloff, P., A single cocaine exposure increases BDNF and D3 receptor expression: Implications for drug-conditioning. Neuroreport 16 (2005), 175–178.
52. Li, S., Wang, C., Wang, M., Li, W., Matsumoto, K., Tang, Y., Antidepressant like effects of piperine in chronic mild stress treated mice and its possible mechanisms. Life Sci. 80 (2007), 1373–1381.
53. Li, X.H., Liu, N.B., Zhang, M.H., Zhou, Y.L., Liao, J.W., Liu, X.Q., Chen, H.W., Effects of chronic multiple stress on learning and memory and the expression of Fyn, BDNF, TrkB in the hippocampus of rats. Chin. Med. J. (Engl.) 120 (2007), 669–674.
54. Linnarsson, S., Bjorklund, A., Ernfors, P., Learning deficit in BDNF mutant mice. Eur. J. Neurosci. 9 (1997), 2581–2587.
55. Liu, I.Y., Lyons, W.E., Mamounas, L.A., Thompson, R.F., Brain-derived neurotrophic factor plays a critical role in contextual fear conditioning. J. Neurosci. 24 (2004), 7958–7963.
56. Logrip, M.L., Janak, P.H., Ron, D., Escalating ethanol intake is associated with altered corticostriatal BDNF expression. J. Neurochem. 109 (2009), 1459–1468.
57. Lu, L., Dempsey, J., Liu, S.Y., Bossert, J.M., Shaham, Y., A single infusion of brain-derived neurotrophic factor into the ventral tegmental area induces long-lasting potentiation of cocaine seeking after withdrawal. J. Neurosci. 24 (2004), 1604–1611.
58. Lucca, G., Comim, C.M., Valvassori, S.S., Pereira, J.G., Stertz, L., Gavioli, E.C., Kapczinski, F., Quevedo, J., Chronic mild stress paradigm reduces sweet food intake in rats without affecting brain derived neurotrophic factor protein levels. Curr. Neurovasc. Res. 5 (2008), 207–213.
59. Lukoyanov, N.V., Pereira, P.A., Paula-Barbosa, M.M., Cadete-Leite, A., Nerve growth factor improves spatial learning and restores hippocampal cholinergic fibers in rats withdrawn from chronic treatment with ethanol. Exp. Brain Res. 148 (2003), 88–94.
60. Lyons, W.E., Mamounas, L.A., Ricaurte, G.A., Coppola, V., Reid, S.W., Bora, S.H., Wihler, C., Koliatsos, V.E., Tessarollo, L., Brain-derived neurotrophic factor-deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc. Natl. Acad. Sci. USA 96 (1999), 15239–15244.
61. MacQueen, G.M., Ramakrishnan, K., Croll, S.D., Siuciak, J.A., Yu, G., Young, L.T., Fahnestock, M., Performance of heterozygous brain-derived neurotrophic factor knockout mice on behavioral analogues of anxiety, nociception, and depression. Behav. Neurosci. 115 (2001), 1145–1153.
62. Markowska, A.L., Koliatsos, V.E., Breckler, S.J., Price, D.L., Olton, D.S., Human nerve growth factor improves spatial memory in aged but not in young rats. J. Neurosci. 14 (1994), 4815–4824.
63. Markowska, A.L., Price, D., Koliatsos, V.E., Selective effects of nerve growth factor on spatial recent memory as assessed by a delayed nonmatching-to-position task in the water maze. J. Neurosci. 16 (1996), 3541–3548.
64. Marmigere, F., Givalois, L., Rage, F., Arancibia, S., Tapia-Arancibia, L., Rapid induction of BDNF expression in the hippocampus during immobilization stress challenge in adult rats. Hippocampus 13 (2003), 646–655.
65. Martinowich, K., Manji, H., Lu, B., New insights into BDNF function in depression and anxiety. Nat. Neurosci. 10 (2007), 1089–1093.
66. Meredith, G.E., Callen, S., Scheuer, D.A., Brain-derived neurotrophic factor expression is increased in the rat amygdala, piriform cortex and hypothalamus following repeated amphetamine administration. Brain Res. 949 (2002), 218–227.
67. Moguel-Gonzalez, M., Gomez-Palacio-Schjetnan, A., Escobar, M.L., BDNF reverses the CTA memory deficits produced by inhibition of protein synthesis. Neurobiol. Learn. Mem. 90 (2008), 584–587.
68. Mufson, E.J., Kroin, J.S., Sendera, T.J., Sobreviela, T., Distribution and retrograde transport of trophic factors in the central nervous system: Functional implications for the treatment of neurodegenerative diseases. Prog. Neurobiol. 57 (1999), 451–484.
69. Murakami, S., Imbe, H., Morikawa, Y., Kubo, C., Senba, E., Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci. Res. 53 (2005), 129–139.
70. Naimark, A., Barkai, E., Matar, M.A., Kaplan, Z., Kozlovsky, N., Cohen, H., Upregulation of neurotrophic factors selectively in frontal cortex in response to olfactory discrimination learning. Neural. Plast., 2007, 2007, 13427.
71. Nakajo, Y., Miyamoto, S., Nakano, Y., Xue, J.H., Hori, T., Yanamoto, H., Genetic increase in brain-derived neurotrophic factor levels enhances learning and memory. Brain Res. 1241 (2008), 103–109.
72. Pardon, M.C., Kendall, D.A., Perez-Diaz, F., Duxon, M.S., Marsden, C.A., Repeated sensory contact with aggressive mice rapidly leads to an anticipatory increase in core body temperature and physical activity that precedes the onset of aversive responding. Eur. J. Neurosci. 20 (2004), 1033–1050.
73. Pardon, M.C., Roberts, R.E., Marsden, C.A., Bianchi, M., Latif, M.L., Duxon, M.S., Kendall, D.A., Social threat and novel cage stress-induced sustained extracellular-regulated kinase1/2 (ERK1/2) phosphorylation but differential modulation of brain-derived neurotrophic factor (BDNF) expression in the hippocampus of NMRI mice. Neuroscience 132 (2005), 561–574.
74. Pierce, R.C., Pierce-Bancroft, A.F., Prasad, B.M., Neurotrophin-3 contributes to the initiation of behavioral sensitization to cocaine by activating the Ras/Mitogen-activated protein kinase signal transduction cascade. J. Neurosci. 19 (1999), 8685–8695.
75. Pietropaolo, S., Paterna, J.C., Bueler, H., Feldon, J., Yee, B.K., Bidirectional changes in water-maze learning following recombinant adenovirus-associated viral vector (rAAV)-mediated brain-derived neurotrophic factor expression in the rat hippocampus. Behav. Pharmacol. 18 (2007), 533–547.
76. Pizarro, J.M., Lumley, L.A., Medina, W., Robison, C.L., Chang, W.E., Alagappan, A., Bah, M.J., Dawood, M.Y., Shah, J.D., Mark, B., Kendall, N., Smith, M.A., et al. Acute social defeat reduces neurotrophin expression in brain cortical and subcortical areas in mice. Brain Res. 1025 (2004), 10–20.
77. Pizzo, D.P., Thal, L.J., Intraparenchymal nerve growth factor improves behavioral deficits while minimizing the adverse effects of intracerebroventricular delivery. Neuroscience 124 (2004), 743–755.
78. Price, R.D., Milne, S.A., Sharkey, J., Matsuoka, N., Advances in small molecules promoting neurotrophic function. Pharmacol. Ther. 115 (2007), 292–306.
79. Rage, F., Givalois, L., Marmigere, F., Tapia Arancibia, L., Arancibia, S., Immobilization stress rapidly modulates BDNF mRNA expression in the hypothalamus of adult male rats. Neuroscience 112 (2002), 309–318.
80. Reichardt, L.F., Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361 (2006), 1545–1564.
81. Schmidt, H.D., Duman, R.S., The role of neurotrophic factors in adult hippocampal neurogenesis, antidepressant treatments and animal models of depressive-like behavior. Behav. Pharmacol. 18 (2007), 391–418.
82. Skaper, S.D., The biology of neurotrophins, signalling pathways, and functional peptide mimetics of neurotrophins and their receptors. CNS Neurol. Disord. Drug. Targets 7 (2008), 46–62.
83. Spillantini, M.G., Aloe, L., Alleva, E., De Simone, R., Goedert, M., Levi-Montalcini, R., Nerve growth factor mRNA and protein increase in hypothalamus in a mouse model of aggression. Proc. Natl. Acad. Sci. USA 86 (1989), 8555–8559.
84. Strohle, A., Physical activity, exercise, depression and anxiety disorders. J. Neural. Transm. 116 (2009), 777–784.
85. Vargas-Perez, H., Kee, R.T., Walton, C.H., Hansen, D.M., Razavi, R., Clarke, L., Bufalino, M.R., Allison, D.W., Steffensen, S.C., van der Kooy, D., Ventral tegmental area BDNF induces an opiate-dependent-like reward state in naive rats. Science 324 (2009), 1732–1734.
86. Webster, N.J., Pirrung, M.C., Small molecule activators of the Trk receptors for neuroprotection. BMC Neurosci., 9(Suppl. 2), 2008, S1.
87. Woolley, M.L., Waters, K.A., Gartlon, J.E., Lacroix, L.P., Jennings, C., Shaughnessy, F., Ong, A., Pemberton, D.J., Harries, M.H., Southam, E., Jones, D.N., Dawson, L.A., Evaluation of the pro-cognitive effects of the AMPA receptor positive modulator, 5-(1-piperidinylcarbonyl)-2,1,3-benzoxadiazole (CX691), in the rat. Psychopharmacology (Berl.) 202 (2009), 343–354.
88. Xie, C.W., Sayah, D., Chen, Q.S., Wei, W.Z., Smith, D., Liu, X., Deficient long-term memory and long-lasting long-term potentiation in mice with a targeted deletion of neurotrophin-4 gene. Proc. Natl. Acad. Sci. USA 97 (2000), 8116–8121.
89. Yamada, K., Nabeshima, T., Brain-derived neurotrophic factor/TrkB signaling in memory processes. J. Pharmacol. Sci. 91 (2003), 267–270.
90. Yee, B.K., Zhu, S.W., Mohammed, A.H., Feldon, J., Levels of neurotrophic factors in the hippocampus and amygdala correlate with anxiety- and fear-related behaviour in C57BL6 mice. J. Neural. Transm. 114 (2007), 431–444.
91. Yoon, S.J., Roh, S., Lee, H., Lee, J.Y., Lee, B.H., Kim, Y.K., Kim, D.J., Possible role of nerve growth factor in the pathogenesis of alcohol dependence. Alcohol Clin. Exp. Res. 30 (2006), 1060–1065.