Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter April 7, 2017

Hippocampal BDNF in physiological conditions and social isolation

  • Ivan Zaletel ORCID logo , Dragana Filipović and Nela Puškaš EMAIL logo

Abstract

Exposure of an organism to chronic psychosocial stress may affect brain-derived neurotrophic factor (BDNF) expression that has been implicated in the etiology of psychiatric disorders, such as depression. Given that depression in humans has been linked with social stress, the chronic social stress paradigms for modeling psychiatric disorders in animals have thus been developed. Chronic social isolation in animal models generally causes changes in hypothalamic-pituitary-adrenal axis functioning, associated with anxiety- and depressive-like behaviors. Also, this chronic stress causes downregulation of BDNF protein and mRNA in the hippocampus, a stress-sensitive brain region closely related to the pathophysiology of depression. In this review, we discuss the current knowledge regarding the structure, function, intracellular signaling, inter-individual differences and epigenetic regulation of BDNF in both physiological conditions and depression and changes in corticosterone levels, as a marker of stress response. Since BDNF levels are age dependent in humans and rodents, this review will also highlight the effects of adolescent and adult chronic social isolation models of both genders on the BDNF expression.

Acknowledgments

This work was supported by the Ministry of Education, Science and Technological Development (MESTD) of the Republic of Serbia, Contracts Nos. 175061 and 173023.

  1. Conflicts of interest: The authors declare that they have no conflict of interest.

References

Abelaira, H.M., Réus, G.Z., and Quevedo, J. (2013). Animal models as tools to study the pathophysiology of depression. Rev. Bras. Psiquiatr. 35, S112–S120.10.1590/1516-4446-2013-1098Search in Google Scholar PubMed

Arain, M., Haque, M., Johal, L., Mathur, P., Nel, W., Rais, A., Sandhu, R., and Sharma, S. (2013). Maturation of the adolescent brain. Neuropsychiatr. Dis. Treat. 9, 449–461.10.2147/NDT.S39776Search in Google Scholar PubMed PubMed Central

Arthur-Farraj, P.J., Latouche, M., Wilton, D.K., Quintes, S., Chabrol, E., Banerjee, A., Woodhoo, A., Jenkins, B., Rahman, M., Turmaine, M., et al. (2012). c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron 75, 633–647.10.1016/j.neuron.2012.06.021Search in Google Scholar PubMed PubMed Central

Asztely, F., Kokaia, M., Olofsdotter, K., Ortegren, U., and Lindvall, O. (2000). Afferent-specific modulation of short-term synaptic plasticity by neurotrophins in dentate gyrus. Eur. J. Neurosci. 12, 662–669.10.1046/j.1460-9568.2000.00956.xSearch in Google Scholar PubMed

Autry, A.E. and Monteggia, L.M. (2012). Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol. Rev. 64, 238–258.10.1124/pr.111.005108Search in Google Scholar PubMed PubMed Central

Barbacid, M. (1995). Neurotrophic factors and their receptors. Curr. Opin. Cell Biol. 7, 148–155.10.1016/0955-0674(95)80022-0Search in Google Scholar PubMed

Barde, Y.A., Edgar, D., and Thoenen, H. (1982). Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1, 549–553.10.1002/j.1460-2075.1982.tb01207.xSearch in Google Scholar PubMed PubMed Central

Barrientos, R.M., Sprunger, D.B., Campeau, S., Higgins, E.A., Watkins, L.R., Rudy, J.W., and Maier, S.F. (2003). Brain-derived neurotrophic factor mRNA downregulation produced by social isolation is blocked by intrahippocampal interleukin-1 receptor antagonist. Neuroscience 121, 847–853.10.1016/S0306-4522(03)00564-5Search in Google Scholar PubMed

Bath, K.G. and Lee, F.S. (2006). Variant BDNF (Val66Met) impact on brain structure and function. Cogn. Affect. Behav. Neurosci. 6, 79–85.10.3758/CABN.6.1.79Search in Google Scholar PubMed

Becker, C., Zeau, B., Rivat, C., Blugeot, A., Hamon, M., and Benoliel, J.J. (2008). Repeated social defeat-induced depression-like behavioral and biological alterations in rats: involvement of cholecystokinin. Mol. Psychiatry 13, 1079–1092.10.1038/sj.mp.4002097Search in Google Scholar PubMed

Biggio, F., Pisu, M.G., Garau, A., Boero, G., Locci, V., Mostallino, M.C., Olla, P., Utzeri, C., and Serra, M. (2014). Maternal separation attenuates the effect of adolescent social isolation on HPA axis responsiveness in adult rats. Eur. Neuropsychopharmacol. 24, 1152–1161.10.1016/j.euroneuro.2014.03.009Search in Google Scholar PubMed

Binder, E.B. and Nemeroff, C.B. (2010). The CRF system, stress, depression and anxiety-insights from human genetic studies. Mol. Psychiatry 15, 574–588.10.1038/mp.2009.141Search in Google Scholar PubMed PubMed Central

Binder, D.K. and Scharfman, H.E. (2004). Brain-derived neurotrophic factor. Growth Factors 22, 123–131.10.1080/08977190410001723308Search in Google Scholar PubMed PubMed Central

Bjørnebekk, A., Mathé, A.A., Gruber, S.H.M., and Brené, S. (2007). Social isolation increases number of newly proliferated cells in hippocampus in female flinders sensitive line rats. Hippocampus 17, 1193–1200.10.1002/hipo.20352Search in Google Scholar PubMed

Boersma, G.J., Lee, R.S., Cordner, Z.A., Ewald, E.R., Purcell, R.H., Moghadam, A.A., and Tamashiro, K.L. (2014). Prenatal stress decreases Bdnf expression and increases methylation of Bdnf exon IV in rats. Epigenetics 9, 437–447.10.4161/epi.27558Search in Google Scholar PubMed PubMed Central

Boulle, F., van den Hove, D.L.A., Jakob, S.B., Rutten, B.P., Hamon, M., van Os, J., Lesch, K.P., Lanfumey, L., Steinbusch, H.W., and Kenis, G. (2012). Epigenetic regulation of the BDNF gene: implications for psychiatric disorders. Mol. Psychiatry 17, 584–596.10.1038/mp.2011.107Search in Google Scholar PubMed

Bramham, C.R. and Messaoudi, E. (2005). BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog. Neurobiol. 76, 99–125.10.1016/j.pneurobio.2005.06.003Search in Google Scholar PubMed

Caldeira, M.V., Melo, C.V., Pereira, D.B., Carvalho, R.F., Carvalho, A.L., and Duarte, C.B. (2007). BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons. Mol. Cell Neurosci. 35, 208–219.10.1016/j.mcn.2007.02.019Search in Google Scholar PubMed

Carrier, N. and Kabbaj, M. (2012). Testosterone and imipramine have antidepressant effects in socially isolated male but not female rats. Horm. Behav. 61, 678–685.10.1016/j.yhbeh.2012.03.001Search in Google Scholar PubMed PubMed Central

Castrén, E. and Kojima, M. (2017). Brain-derived neurotrophic factor in mood disorders and antidepressant treatments. Neurobiol. Dis. 97, 119–126.10.1016/j.nbd.2016.07.010Search in Google Scholar PubMed

Chao, M.V. (2003). Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 4, 299–309.10.1038/nrn1078Search in Google Scholar PubMed

Chen, Z.Y., Jing, D., Bath, K.G., Ieraci, A., Khan, T., Siao, C.J., Herrera, D.G., Toth, M., Yang, C., McEwen, B.S., et al. (2006). Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314, 140–143.10.1126/science.1129663Search in Google Scholar PubMed PubMed Central

Chida, Y., Sudo, N., and Kubo, C. (2005). Social isolation stress exacerbates autoimmune disease in MRL/lpr mice. J. Neuroimmunol. 158, 138–144.10.1016/j.jneuroim.2004.09.002Search in Google Scholar PubMed

Christoffel, D.J., Golden, S.A., and Russo, S.J. (2011). Structural and synaptic plasticity in stress-related disorders. Rev. Neurosci. 22, 535–549.10.1515/RNS.2011.044Search in Google Scholar PubMed PubMed Central

Cirulli, F. and Alleva, E. (2016). Early environmental manipulations and long-term effects on brain neurotrophin levels. Environmental Experience and Plasticity of the Developing Brain. A. Sale, ed. (Hoboken, NJ: John Wiley & Sons), pp. 139–160.10.1002/9781118931684.ch7Search in Google Scholar

Cirulli, F., Berry, A., Chiarotti, F., and Alleva, E. (2004). 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, 802–807.10.1002/hipo.10220Search in Google Scholar PubMed

Cowansage, K.K., LeDoux, J.E., and Monfils, M.H. (2010). Brain-derived neurotrophic factor: a dynamic gatekeeper of neural plasticity. Curr. Mol. Pharmacol. 3, 12–29.10.2174/1874467211003010012Search in Google Scholar PubMed

Dellu, F., Piazza, P.V., Mayo, W., Le Moal, M., and Simon, H. (1996). Novelty-seeking in rats – biobehavioral characteristics and possible relationship with the sensation-seeking trait in man. Neuropsychobiology 34, 136–145.10.1159/000119305Search in Google Scholar PubMed

De Foubert, G., Carney, S.L., Robinson, C.S., Destexhe, E.J., Tomlinson, R., Hicks, C.A., Murray, T.K., Gaillard, J.P., Deville, C., Xhenseval, V., et al. (2004). Fluoxetine-induced change in rat brain expression of brain-derived neurotrophic factor varies depending on length of treatment. Neuroscience 128, 597–604.10.1016/j.neuroscience.2004.06.054Search in Google Scholar PubMed

Djordjevic, A., Adzic, M., Djordjevic, J., and Radojcic, M.B. (2010). Chronic social isolation suppresses proplastic response and promotes proapoptotic signalling in prefrontal cortex of Wistar rats. J. Neurosci. Res. 88, 2524–2533.10.1002/jnr.22403Search in Google Scholar PubMed

Djordjevic, J., Djordjevic, A., Adzic, M., and Radojcic, M.B. (2012). Effects of chronic social isolation on Wistar rat behavior and brain plasticity markers. Neuropsychobiology 66, 112–119.10.1159/000338605Search in Google Scholar PubMed

Djordjevic, J., Djordjevic, A., Adzic, M., Mitic, M., Lukic, I., and Radojcic, M.B. (2015). Alterations in the Nrf2-Keap1 signaling pathway and its downstream target genes in rat brain under stress. Brain Res. 1602, 20–31.10.1016/j.brainres.2015.01.010Search in Google Scholar PubMed

Djouma, E., Card, K., Lodge, D.J., and Lawrence, A.J. (2006). The CRF1 receptor antagonist, antalarmin, reverses isolation-induced up-regulation of dopamine D2 receptors in the amygdala and nucleus accumbens of fawn-hooded rats. Eur. J. Neurosci. 23, 3319–3327.10.1111/j.1460-9568.2006.04864.xSearch in Google Scholar PubMed

Dong, E., Dzitoyeva, S.G., Matrisciano, F., Tueting, P., Grayson, D.R., and Guidotti, A. (2015). Brain-derived neurotrophic factor epigenetic modifications associated with schizophrenia-like phenotype induced by prenatal stress in mice. Biol. Psychiatry 77, 589–596.10.1016/j.biopsych.2014.08.012Search in Google Scholar PubMed PubMed Central

Duclot, F. and Kabbaj, M. (2013). Individual differences in novelty seeking predict subsequent vulnerability to social defeat through a differential epigenetic regulation of brain-derived neurotrophic factor expression. J. Neurosci. 33, 11048–11060.10.1523/JNEUROSCI.0199-13.2013Search in Google Scholar PubMed PubMed Central

Duclot, F. and Kabbaj, M. (2015). Epigenetic mechanisms underlying the role of brain-derived neurotrophic factor in depression and response to antidepressants. J. Exp. Biol. 218, 21–31.10.1242/jeb.107086Search in Google Scholar PubMed PubMed Central

Duclot, F., Hollis, F., Darcy, M.J., and Kabbaj, M. (2011). Individual differences in novelty-seeking behavior in rats as a model for psychosocial stress-related mood disorders. Physiol. Behav. 104, 296–305.10.1016/j.physbeh.2010.12.014Search in Google Scholar PubMed PubMed Central

Duman, R.S. (2014). Pathophysiology of depression and innovative treatments: remodeling glutamatergic synaptic connections. Dialogues Clin. Neurosci. 16, 11–27.10.31887/DCNS.2014.16.1/rdumanSearch in Google Scholar PubMed PubMed Central

Duman, R.S. and Monteggia, L.M. (2006). A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 59, 1116–1127.10.1016/j.biopsych.2006.02.013Search in Google Scholar PubMed

Eker, C., Kitis, O., Taneli, F., Eker, O.D., Ozan, E., Yucel, K., Coburn, K., and Gonul, A.S. (2010). Correlation of serum BDNF levels with hippocampal volumes in first episode, medication-free depressed patients. Eur. Arch. Psychiatry Clin. Neurosci. 260, 527–533.10.1007/s00406-010-0110-5Search in Google Scholar PubMed

Ernfors, P., Wetmore, C., Olson, L., and Persson, H. (1990). Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5, 511–526.10.1016/0896-6273(90)90090-3Search in Google Scholar PubMed

Ernst, C., Deleva, V., Deng, X., Sequeira, A., Pomarenski, A., Klempan, T, Ernst, N., Quirion, R., Gratton, A., Szyf, M., et al. (2009). Alternative splicing, methylation state, and expression profile of tropomyosin-related kinase B in the frontal cortex of suicide completers. Arch. Gen. Psychiatry 66, 22–32.10.1001/archpsyc.66.1.22Search in Google Scholar PubMed

Ferland, C.L. and Schrader, L.A. (2011). Cage mate separation in pair-housed male rats evokes an acute stress corticosterone response. Neurosci. Lett. 489, 154–158.10.1016/j.neulet.2010.12.006Search in Google Scholar PubMed PubMed Central

Filipović, D. and Pajović, S.B. (2009). Differential regulation of CuZnSOD expression in rat brain by acute and/or chronic stress. Cell Mol. Neurobiol. 29, 673–681.10.1007/s10571-009-9375-5Search in Google Scholar PubMed

Filipović, D., Gavrilović, L., Dronjak, S., and Radojcić, M.B. (2005). Brain glucocorticoid receptor and heat shock protein 70 levels in rats exposed to acute, chronic or combined stress. Neuropsychobiology 51, 107–114.10.1159/000084168Search in Google Scholar PubMed

First, M., Gil-Ad, I., Taler, M., Tarasenko, I., Novak, N., and Weizman, A. (2011). The effects of fluoxetine treatment in a chronic mild stress rat model on depression-related behavior, brain neurotrophins and ERK expression. J. Mol. Neurosci. 45, 246–255.10.1007/s12031-011-9515-5Search in Google Scholar PubMed

Frank, E., Salchner, P., Aldag, J.M., Salomé, N., Singewald, N., Landgraf, R., and Wigger, A. (2006). Genetic predisposition to anxiety-related behavior determines coping style, neuroendocrine responses, and neuronal activation during social defeat. Behav. Neurosci. 120, 60–71.10.1037/0735-7044.120.1.60Search in Google Scholar PubMed

Fuchs, E. (2005). Social stress in tree shrews as an animal model of depression: an example of a behavioral model of a CNS disorder. CNS Spectr. 10, 182–190.10.1017/S1092852900010038Search in Google Scholar

Fuchs, E., Czéh, B., Kole, M.H.P., Michaelis, T., and Lucassen, P.J. (2004). Alterations of neuroplasticity in depression: the hippocampus and beyond. Eur. Neuropsychopharmacol. 14, S481–S490.10.1016/j.euroneuro.2004.09.002Search in Google Scholar PubMed

Gamallo, A., Villanua, A., Trancho, G., and Fraile, A. (1986). Stress adaptation and adrenal activity in isolated and crowded rats. Physiol. Behav. 36, 217–221.10.1016/0031-9384(86)90006-5Search in Google Scholar PubMed

Gambardella, P., Greco, A.M., Sticchi, R., Bellotti, R., and Di Renzo, G. (1994). Individual housing modulates daily rhythms of hypothalamic catecholaminergic system and circulating hormones in adult male rats. Chronobiol. Int. 11, 213–221.10.3109/07420529409067790Search in Google Scholar PubMed

Gentry, J.J., Barker, P.A., and Carter, B.D. (2004). The p75 neurotrophin receptor: multiple interactors and numerous functions. Prog. Brain Res. 146, 25–39.10.1016/S0079-6123(03)46002-0Search in Google Scholar PubMed

Giachino, C., Canalia, N., Capone, F., Fasolo, A., Alleva, E., Riva, M.A., Cirulli, F., and Peretto, P. (2007). Maternal deprivation and early handling affect density of calcium binding protein-containing neurons in selected brain regions and emotional behavior in periadolescent rats. Neuroscience 145, 568–578.10.1016/j.neuroscience.2006.12.042Search in Google Scholar PubMed

Godavarthi, S.K., Sharma, A., and Jana, N.R. (2014). Reversal of reduced parvalbumin neurons in hippocampus and amygdala of Angelman syndrome model mice by chronic treatment of fluoxetine. J. Neurochem. 130, 444–454.10.1111/jnc.12726Search in Google Scholar PubMed

Goodman, L.J., Valverde, J., Lim, F., Geschwind, M.D., Federoff, H.J., Geller, A.I., and Hefti, F. (1996). Regulated release and polarized localization of brain-derived neurotrophic factor in hippocampal neurons. Mol. Cell Neurosci. 7, 222–238.10.1006/mcne.1996.0017Search in Google Scholar PubMed

Götz, R., Köster, R., Winkler, C., Raulf, F., Lottspeich, F., Schartl, M., and Thoenen, H. (1994). Neurotrophin-6 is a new member of the nerve growth factor family. Nature 372, 266–269.10.1038/372266a0Search in Google Scholar PubMed

Greenberg, P.E., Fournier, A.A., Sisitsky, T., Pike, C.T., and Kessler, R.C. (2015). The economic burden of adults with major depressive disorder in the United States (2005 and 2010). J. Clin. Psychiatry 76, 155–162.10.4088/JCP.14m09298Search in Google Scholar PubMed

Hall, J., Thomas, K.L., and Everitt, B.J. (2000). Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat. Neurosci. 3, 533–535.10.1038/75698Search in Google Scholar PubMed

Han, X., Wang, W., Xue, X., Shao, F., and Li, N. (2011). Brief social isolation in early adolescence affects reversal learning and forebrain BDNF expression in adult rats. Brain Res. Bull. 86, 173–178.10.1016/j.brainresbull.2011.07.008Search in Google Scholar PubMed

Harris, N.G., Nogueira, M.S.M., Verley, D.R., and Sutton, R.L. (2013). Chondroitinase enhances cortical map plasticity and increases functionally active sprouting axons after brain injury. J. Neurotrauma 30, 1257–1269.10.1089/neu.2012.2737Search in Google Scholar PubMed PubMed Central

Hasler, G., Drevets, W.C., Manji, H.K., and Charney, D.S. (2004). Discovering endophenotypes for major depression. Neuropsychopharmacology 29, 1765–1781.10.1038/sj.npp.1300506Search in Google Scholar PubMed

Hawkley, L.C., Cole, S.W., Capitanio, J.P., Norman, G.J., and Cacioppo, J.T. (2012). Effects of social isolation on glucocorticoid regulation in social mammals. Horm. Behav. 62, 314–323.10.1016/j.yhbeh.2012.05.011Search in Google Scholar PubMed PubMed Central

Heim, C. and Nemeroff, C.B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 49, 1023–1039.10.1016/S0006-3223(01)01157-XSearch in Google Scholar PubMed

Heinrich, L.M. and Gullone, E. (2006). The clinical significance of loneliness: a literature review. Clin. Psychol. Rev. 26, 695–718.10.1016/j.cpr.2006.04.002Search in Google Scholar PubMed

Hermes, G.L., Rosenthal, L., Montag, A., and McClintock, M.K. (2006). Social isolation and the inflammatory response: sex differences in the enduring effects of a prior stressor. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R273–R282.10.1152/ajpregu.00368.2005Search in Google Scholar PubMed

Hodes, G.E., Walker, D.M., Labonté, B., Nestler, E.J., and Russo, S.J. (2017). Understanding the epigenetic basis of sex differences in depression. J. Neurosci. Res. 95, 692–702.10.1002/jnr.23876Search in Google Scholar PubMed PubMed Central

Hofer, M., Pagliusi, S.R., Hohn, A., Leibrock, J., and Barde, Y.A. (1990). Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J. 9, 2459–2464.10.1002/j.1460-2075.1990.tb07423.xSearch in Google Scholar PubMed PubMed Central

Hollis, F., Duclot, F., Gunjan, A., and Kabbaj, M. (2011). Individual differences in the effect of social defeat on anhedonia and histone acetylation in the rat hippocampus. Horm. Behav. 59, 331–337.10.1016/j.yhbeh.2010.09.005Search in Google Scholar PubMed PubMed Central

Hollis, F., Isgor, C., and Kabbaj, M. (2013). The consequences of adolescent chronic unpredictable stress exposure on brain and behavior. Neuroscience 249, 232–241.10.1016/j.neuroscience.2012.09.018Search in Google Scholar PubMed

Hong, Y.P., Lee, H.C., and Kim, H.T. (2015). Treadmill exercise after social isolation increases the levels of NGF, BDNF, and synapsin I to induce survival of neurons in the hippocampus, and improves depression-like behavior. J. Exerc. Nutrition Biochem. 19, 11–18.10.5717/jenb.2015.19.1.11Search in Google Scholar PubMed PubMed Central

House, J.S. (2001). Social isolation kills, but how and why? Psychosom. Med. 63, 273–274.10.1097/00006842-200103000-00011Search in Google Scholar PubMed

Hu, X., Ballo, L., Pietila, L., Viesselmann, C., Ballweg, J., Lumbard, D., Stevenson, M., Merriam, E., and Dent, E.W. (2011). BDNF-induced increase of PSD-95 in dendritic spines requires dynamic microtubule invasions. J. Neurosci. 31, 15597–15603.10.1523/JNEUROSCI.2445-11.2011Search in Google Scholar PubMed PubMed Central

Huang, E.J. and Reichardt, L.F. (2003). Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72, 609–642.10.1146/annurev.biochem.72.121801.161629Search in Google Scholar PubMed

Huang, T.L., Lee, C.T., and Liu, Y.L. (2008). Serum brain-derived neurotrophic factor levels in patients with major depression: effects of antidepressants. J. Psychiatr. Res. 42, 521–525.10.1016/j.jpsychires.2007.05.007Search in Google Scholar PubMed

Ibi, D., Takuma, K., Koike, H., Mizoguchi, H., Tsuritani, K., Kuwahara, Y., Kamei, H., Nagai, T., Yoneda, Y., Nabeshima, T., et al. (2008). Social isolation rearing-induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion-related behaviors in juvenile mice. J. Neurochem. 105, 921–932.10.1111/j.1471-4159.2007.05207.xSearch in Google Scholar PubMed

Ieraci, A., Mallei, A., and Popoli, M. (2016). Social isolation stress induces anxious-depressive-like behavior and alterations of neuroplasticity-related genes in adult male mice. Neural Plast. 2016, 6212983.10.1155/2016/6212983Search in Google Scholar PubMed PubMed Central

Ikegaya, Y., Ishizaka, Y., and Matsuki, N. (2002). BDNF attenuates hippocampal LTD via activation of phospholipase C: implications for a vertical shift in the frequency-response curve of synaptic plasticity. Eur. J. Neurosci. 16, 145–148.10.1046/j.1460-9568.2002.02051.xSearch in Google Scholar PubMed

Isgor, C., Kabbaj, M., Akil, H., and Watson, S.J. (2004). Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus 14, 636–648.10.1002/hipo.10207Search in Google Scholar PubMed

Jabeen Haleem, D. (2011). Raphe-hippocampal serotonin neurotransmission in the sex related differences of adaptation to stress: focus on serotonin-1A receptor. Curr. Neuropharmacol. 9, 512–521.10.2174/157015911796558019Search in Google Scholar PubMed PubMed Central

Jaworska, N., Dwyer, S.M., and Rusak, B. (2008). Repeated neonatal separation results in different neurochemical and behavioral changes in adult male and female Mongolian gerbils. Pharmacol. Biochem. Behav. 88, 533–541.10.1016/j.pbb.2007.10.012Search in Google Scholar PubMed

Johnston, M.V. (2009). Plasticity in the developing brain: implications for rehabilitation. Dev. Disabil. Res. Rev. 15, 94–101.10.1002/ddrr.64Search in Google Scholar PubMed

Kabbaj, M., Devine, D.P., Savage, V.R., and Akil, H. (2000). Neurobiological correlates of individual differences in novelty-seeking behavior in the rat: differential expression of stress-related molecules. J. Neurosci. 20, 6983–6988.10.1523/JNEUROSCI.20-18-06983.2000Search in Google Scholar PubMed PubMed Central

Kaplan, D.R. and Miller, F.D. (2000). Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381–391.10.1016/S0959-4388(00)00092-1Search in Google Scholar PubMed

Kim, H.K., Nunes, P.V., Oliveira, K.C., Young, L.T., and Lafer, B. (2016). Neuropathological relationship between major depression and dementia: a hypothetical model and review. Prog. Neuropsychopharmacol. Biol. Psychiatry 67, 51–57.10.1016/j.pnpbp.2016.01.008Search in Google Scholar PubMed

Kolb, B. and Gibb, R. (2011). Brain plasticity and behaviour in the developing brain. J. Can. Acad. Child. Adolesc. Psychiatry 20, 265–276.Search in Google Scholar

Korsching, S. (1993). The neurotrophic factor concept: a reexamination. J. Neurosci. 13, 2739–2748.10.1523/JNEUROSCI.13-07-02739.1993Search in Google Scholar PubMed PubMed Central

Krishnan, V. and Nestler, E.J. (2008). The molecular neurobiology of depression. Nature 455, 894–902.10.1038/nature07455Search in Google Scholar PubMed PubMed Central

Lapiz, M.D.S., Fulford, A., Muchimapura, S., Mason, R., Parker, T., and Marsden, C.A. (2003). Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neurosci. Behav. Physiol. 33, 13–29.10.1023/A:1021171129766Search in Google Scholar

Larsen, M.H., Mikkelsen, J.D., Hay-Schmidt, A., and Sandi, C. (2010). Regulation of brain-derived neurotrophic factor (BDNF) in the chronic unpredictable stress rat model and the effects of chronic antidepressant treatment. J. Psychiatr. Res. 44, 808–816.10.1016/j.jpsychires.2010.01.005Search in Google Scholar PubMed

Lee, T., Saruta, J., Sasaguri, K., Sato, S., and Tsukinoki, K. (2008). Allowing animals to bite reverses the effects of immobilization stress on hippocampal neurotrophin expression. Brain Res. 1195, 43–49.10.1016/j.brainres.2007.12.013Search in Google Scholar PubMed

Lépine, J.P. and Briley, M. (2011). The increasing burden of depression. Neuropsychiatr. Dis. Treat. 7, 3–7.10.2147/NDT.S19617Search in Google Scholar PubMed PubMed Central

Levi-Montalcini, R. and Hamburger, V. (1951). Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo. J. Exp. Zool. 116, 321–361.10.1002/jez.1401160206Search in Google Scholar PubMed

Li, W., He, Q., Wu, C., Pan, X., Wang, J., Tan, Y., Shan, X.Y., and Zeng, H.C. (2015). PFOS disturbs BDNF-ERK-CREB signalling in association with increased microRNA-22 in SH-SY5Y cells. Biomed. Res. Int. 2015, e302653.10.1155/2015/302653Search in Google Scholar PubMed PubMed Central

Li, M., Du, W., Shao, F., and Wang, W. (2016). Cognitive dysfunction and epigenetic alterations of the BDNF gene are induced by social isolation during early adolescence. Behav. Brain Res. 313, 177–183.10.1016/j.bbr.2016.07.025Search in Google Scholar PubMed

Lu, B. (2003). BDNF and activity-dependent synaptic modulation. Learn. Mem. 10, 86–98.10.1101/lm.54603Search in Google Scholar PubMed PubMed Central

Lu, B., Pang, P.T., and Woo, N.H. (2005). The yin and yang of neurotrophin action. Nat. Rev. Neurosci. 6, 603–614.10.1038/nrn1726Search in Google Scholar PubMed

Lucassen, P.J., Meerlo, P., Naylor, A.S., van Dam, A.M., Dayer, A.G., Fuchs, E., Oomen, C.A., and Czéh, B. (2010). Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: implications for depression and antidepressant action. Eur. Neuropsychopharmacol. 20, 1–17.10.1016/j.euroneuro.2009.08.003Search in Google Scholar PubMed

Lukkes, J.L., Mokin, M.V., Scholl, J.L., and Forster, G.L. (2009). Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm. Behav. 55, 248–256.10.1016/j.yhbeh.2008.10.014Search in Google Scholar PubMed

Maier, E.H. and Lachman, M.E. (2000). Consequences of early parental loss and separation for health and well-being in midlife. Int. J. Behav. Dev. 24, 183–189.10.1080/016502500383304Search in Google Scholar

Martinowich, K. and Lu, B. (2007). Interaction between BDNF and serotonin: role in mood disorders. Neuropsychopharmacology 33, 73–83.10.1038/sj.npp.1301571Search in Google Scholar PubMed

Martinowich, K., Manji, H., and Lu, B. (2007). New insights into BDNF function in depression and anxiety. Nat. Neurosci. 10, 1089–1093.10.1038/nn1971Search in Google Scholar PubMed

Massey, K.A., Zago, W.M., and Berg, D.K. (2006). BDNF up-regulates α7 nicotinic acetylcholine receptor levels on subpopulations of hippocampal interneurons. Mol. Cell Neurosci. 33, 381–388.10.1016/j.mcn.2006.08.011Search in Google Scholar PubMed PubMed Central

Mattson, M.P., Maudsley, S., and Martin, B. (2004). BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 27, 589–594.10.1016/j.tins.2004.08.001Search in Google Scholar PubMed

Matsumoto, K., Pinna, G., Puia, G., Guidotti, A., and Costa, E. (2005). Social isolation stress-induced aggression in mice: a model to study the pharmacology of neurosteroidogenesis. Stress 8, 85–93.10.1080/10253890500159022Search in Google Scholar PubMed

McCormick, C.M. and Mathews, I.Z. (2007). HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol. Biochem. Behav. 86, 220–233.10.1016/j.pbb.2006.07.012Search in Google Scholar PubMed

McCormick, C.M. and Mathews, I.Z. (2010). Adolescent development, hypothalamic-pituitary-adrenal function, and programming of adult learning and memory. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 756–765.10.1016/j.pnpbp.2009.09.019Search in Google Scholar PubMed

McCormick, C.M., Robarts, D., Kopeikina, K., and Kelsey, J.E. (2005). Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats. Horm. Behav. 48, 64–74.10.1016/j.yhbeh.2005.01.008Search in Google Scholar PubMed

Meerlo, P., Overkamp, G.J., Daan, S., Van Den Hoofdakker, R.H., and Koolhaas, J.M. (1996). Changes in behaviour and body weight following a single or double social defeat in rats. Stress 1, 21–32.10.3109/10253899609001093Search in Google Scholar PubMed

Meng, Q., Li, N., Han, X., Shao, F., and Wang, W. (2011). Effects of adolescent social isolation on the expression of brain-derived neurotrophic factors in the forebrain. Eur. J. Pharmacol. 650, 229–232.10.1016/j.ejphar.2010.09.061Search in Google Scholar PubMed

Miachon, S., Rochet, T., Mathian, B., Barbagli, B., and Claustrat, B. (1993). Long-term isolation of Wistar rats alters brain monoamine turnover, blood corticosterone, and ACTH. Brain Res. Bull. 32, 611–614.10.1016/0361-9230(93)90162-5Search in Google Scholar PubMed

Miller, F.D. and Kaplan, D.R. (2003). Signaling mechanisms underlying dendrite formation. Curr. Opin. Neurobiol. 13, 391–398.10.1016/S0959-4388(03)00072-2Search in Google Scholar PubMed

Minichiello, L., Korte, M., Wolfer, D., Kühn, R., Unsicker, K., Cestari, V., Rossi-Arnaud, C., Lipp, H.P., Bonhoeffer, T., and Klein, R. (1999). Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24, 401–414.10.1016/S0896-6273(00)80853-3Search in Google Scholar

Mitic, M., Simic, I., Djordjevic, J., Radojcic, M.B., and Adzic, M. (2013). Gender-specific effects of fluoxetine on hippocampal glucocorticoid receptor phosphorylation and behavior in chronically stressed rats. Neuropharmacology 70, 100–111.10.1016/j.neuropharm.2012.12.012Search in Google Scholar PubMed

Mizoguchi, K., Ishige, A., Aburada, M., and Tabira, T. (2003). Chronic stress attenuates glucocorticoid negative feedback: involvement of the prefrontal cortex and hippocampus. Neuroscience 119, 887–897.10.1016/S0306-4522(03)00105-2Search in Google Scholar PubMed

Mizuno, M., Yamada, K., He, J., Nakajima, A., and Nabeshima, T. (2003). Involvement of BDNF receptor TrkB in spatial memory formation. Learn. Mem. 10, 108–115.10.1101/lm.56003Search in Google Scholar PubMed PubMed Central

Molteni, R., Cattaneo, A., Calabrese, F., Macchi, F., Olivier, J.D.A., Racagni, G., Ellenbroek, B.A., Gennarelli, M., and Riva, M.A. (2010). Reduced function of the serotonin transporter is associated with decreased expression of BDNF in rodents as well as in humans. Neurobiol. Dis. 37, 747–755.10.1016/j.nbd.2009.12.014Search in Google Scholar PubMed

Murakami, S., Imbe, H., Morikawa, Y., Kubo, C., and Senba, E. (2005). Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci. Res. 53, 129–139.10.1016/j.neures.2005.06.008Search in Google Scholar PubMed

Nair, A., Vadodaria, K.C., Banerjee, S.B., Benekareddy, M., Dias, B.G., Duman, R.S., and Vaidya, V.A. (2007). Stressor-specific regulation of distinct brain-derived neurotrophic factor transcripts and cyclic AMP response element-binding protein expression in the postnatal and adult rat hippocampus. Neuropsychopharmacology 32, 1504–1519.10.1038/sj.npp.1301276Search in Google Scholar PubMed

Nederhof, E. and Schmidt, M.V. (2012). Mismatch or cumulative stress: toward an integrated hypothesis of programming effects. Physiol. Behav. 106, 691–700.10.1016/j.physbeh.2011.12.008Search in Google Scholar PubMed

Neeper, S.A., Gómez-Pinilla, F., Choi, J., and Cotman, C.W. (1996). Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res. 726, 49–56.10.1016/0006-8993(96)00273-9Search in Google Scholar

Nibuya, M., Morinobu, S., and Duman, R.S. (1995). Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J. Neurosci. 15, 7539–7547.10.1523/JNEUROSCI.15-11-07539.1995Search in Google Scholar PubMed PubMed Central

Niknazar, S., Nahavandi, A, Peyvandi, A.A., Peyvandi, H., Akhtari, A.S., and Karimi, M. (2016). Comparison of the adulthood chronic stress effect on hippocampal BDNF signaling in male and female rats. Mol. Neurobiol. 53, 4026–4033.10.1007/s12035-015-9345-5Search in Google Scholar PubMed

Nilsson, A.S., Fainzilber, M., Falck, P., and Ibáñez, C.F. (1998). Neurotrophin-7: a novel member of the neurotrophin family from the zebrafish. FEBS Lett. 424, 285–290.10.1016/S0014-5793(98)00192-6Search in Google Scholar

Nin, M.S., Martinez, L.A., Pibiri, F., Nelson, M., and Pinna, G. (2011). Neurosteroids reduce social isolation-induced behavioral deficits: a proposed link with neurosteroid-mediated upregulation of BDNF expression. Front. Endocrinol. (Lausanne) 2, 73.10.3389/fendo.2011.00073Search in Google Scholar PubMed PubMed Central

Nowacka, M. and Obuchowicz, E. (2013). BDNF and VEGF in the pathogenesis of stress-induced affective diseases: an insight from experimental studies. Pharmacol. Rep. 65, 535–546.10.1016/S1734-1140(13)71031-4Search in Google Scholar

Numakawa, T., Yokomaku, D., Richards, M., Hori, H., Adachi, N., and Kunugi, H. (2010). Functional interactions between steroid hormones and neurotrophin BDNF. World J. Biol. Chem. 1, 133–143.10.4331/wjbc.v1.i5.133Search in Google Scholar PubMed PubMed Central

Ohba, S., Ikeda, T., Ikegaya, Y., Nishiyama, N., Matsuki, N., and Yamada, M.K. (2005). BDNF locally potentiates GABAergic presynaptic machineries: target-selective circuit inhibition. Cereb. Cortex 15, 291–298.10.1093/cercor/bhh130Search in Google Scholar PubMed

Ohta, K., Kuno, S., Inoue, S., Ikeda, E., Fujinami, A., and Ohta, M. (2010). The effect of dopamine agonists: the expression of GDNF, NGF, and BDNF in cultured mouse astrocytes. J. Neurol. Sci. 291, 12–16.10.1016/j.jns.2010.01.013Search in Google Scholar PubMed

Orefice, L.L., Waterhouse, E.G., Partridge, J.G., Lalchandani, R.R., Vicini, S., and Xu, B. (2013). Distinct roles for somatically and dendritically synthesized brain-derived neurotrophic factor in morphogenesis of dendritic spines. J. Neurosci. 33, 11618–11632.10.1523/JNEUROSCI.0012-13.2013Search in Google Scholar PubMed PubMed Central

Oztan, O., Aydin, C., and Isgor, C. (2011a). Chronic variable physical stress during the peripubertal-juvenile period causes differential depressive and anxiogenic effects in the novelty-seeking phenotype: functional implications for hippocampal and amygdalar brain-derived neurotrophic factor and the mossy fibre plasticity. Neuroscience 192, 334–344.10.1016/j.neuroscience.2011.06.077Search in Google Scholar PubMed PubMed Central

Oztan, O., Aydin, C., and Isgor, C. (2011b). Stressful environmental and social stimulation in adolescence causes antidepressant-like effects associated with epigenetic induction of the hippocampal BDNF and mossy fibre sprouting in the novelty-seeking phenotype. Neurosci. Lett. 501, 107–111.10.1016/j.neulet.2011.06.058Search in Google Scholar PubMed PubMed Central

Palazidou, E. (2012). The neurobiology of depression. Br. Med. Bull. 101, 127–145.10.1093/bmb/lds004Search in Google Scholar PubMed

Paré, W.P., Blair, G.R., Kluczynski, J., and Tejani-Butt, S. (1999). Gender differences in acute and chronic stress in Wistar Kyoto (WKY) rats. Integr. Physiol. Behav. Sci. 34, 227–241.10.1007/BF02688691Search in Google Scholar PubMed

Park, H. and Poo, M. (2013). Neurotrophin regulation of neural circuit development and function. Nat. Rev. Neurosci. 14, 7–23.10.1038/nrn3379Search in Google Scholar PubMed

Perelló, M., Chacon, F., Cardinali, D.P., Esquifino, A.I., and Spinedi, E. (2006). Effect of social isolation on 24-h pattern of stress hormones and leptin in rats. Life Sci. 78, 1857–1862.10.1016/j.lfs.2005.08.029Search in Google Scholar PubMed

Piccinelli, M. and Wilkinson, G. (2000). Gender differences in depression. Br. J. Psychiatry 177, 486–492.10.1192/bjp.177.6.486Search in Google Scholar PubMed

Pisu, M.G., Dore, R., Mostallino, M.C., Loi, M., Pibiri, F., Mameli, R., Cadeddu, R., Secci, P.P., and Serra, M. (2011). Down-regulation of hippocampal BDNF and Arc associated with improvement in aversive spatial memory performance in socially isolated rats. Behav. Brain Res. 222, 73–80.10.1016/j.bbr.2011.03.021Search in Google Scholar PubMed

Pisu, M.G., Garau, A., Boero, G., Biggio, F., Pibiri, V., Dore, R., Locci, V., Paci, E., Porcu, P., and Serra, M. (2016). Sex differences in the outcome of juvenile social isolation on HPA axis function in rats. Neuroscience 320, 172–182.10.1016/j.neuroscience.2016.02.009Search in Google Scholar PubMed

Pugh, C.R., Nguyen, K.T., Gonyea, J.L., Fleshner, M., Wakins, L.R., Maier, S.F., and Rudy, J.W. (1999). Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation. Behav. Brain Res. 106, 109–118.10.1016/S0166-4328(99)00098-4Search in Google Scholar PubMed

Pyter, L.M., Kelly, S.D., Harrell, C.S., and Neigh, G.N. (2013). Sex differences in the effects of adolescent stress on adult brain inflammatory markers in rats. Brain Behav. Immun. 30, 88–94.10.1016/j.bbi.2013.01.075Search in Google Scholar PubMed PubMed Central

Radley, J.J., Kabbaj, M., Jacobson, L., Heydendael, W., Yehuda, R., and Herman, J.P. (2011). Stress risk factors and stress-related pathology: neuroplasticity, epigenetics and endophenotypes. Stress 14, 481–497.10.3109/10253890.2011.604751Search in Google Scholar PubMed PubMed Central

Rakofsky, J.J., Ressler, K.J., and Dunlop, B.W. (2012). BDNF function as a potential mediator of bipolar disorder and post-traumatic stress disorder comorbidity. Mol. Psychiatry 17, 22–35.10.1038/mp.2011.121Search in Google Scholar PubMed PubMed Central

Razzoli, M., Domenici, E., Carboni, L., Rantamaki, T., Lindholm, J., Castrén, E., and Arban, R. (2011). A role for BDNF/TrkB signaling in behavioral and physiological consequences of social defeat stress. Genes Brain Behav. 10, 424–433.10.1111/j.1601-183X.2011.00681.xSearch in Google Scholar PubMed

Rizzi, S., Bianchi, P., Guidi, S., Ciani, E., and Bartesaghi, R. (2007). Neonatal isolation impairs neurogenesis in the dentate gyrus of the guinea pig. Hippocampus 17, 78–91.10.1002/hipo.20247Search in Google Scholar PubMed

Roceri, M., Cirulli, F., Pessina, C., Peretto, P., Racagni, G., and Riva, M.A. (2004). Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol. Psychiatry 55, 708–714.10.1016/j.biopsych.2003.12.011Search in Google Scholar PubMed

Rossi, C., Angelucci, A., Costantin, L., Braschi, C., Mazzantini, M., Babbini, F., Fabbri, M.E., Tessarollo, L., Maffei, L., Berardi, N., et al. (2006). Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur. J. Neurosci. 24, 1850–1856.10.1111/j.1460-9568.2006.05059.xSearch in Google Scholar PubMed

Rothwell, N.J. and Luheshi, G.N. (2000). Interleukin 1 in the brain: biology, pathology and therapeutic target. Trends Neurosci. 23, 618–625.10.1016/S0166-2236(00)01661-1Search in Google Scholar PubMed

Rygula, R., Abumaria, N., Flügge, G., Fuchs, E., Rüther, E., and Havemann-Reinecke, U. (2005). Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav. Brain Res. 162, 127–134.10.1016/j.bbr.2005.03.009Search in Google Scholar PubMed

Sandi, C. and Richter-Levin, G. (2009). From high anxiety trait to depression: a neurocognitive hypothesis. Trends Neurosci. 32, 312–320.10.1016/j.tins.2009.02.004Search in Google Scholar PubMed

Sánchez, M.M., Aguado, F., Sánchez-Toscano, F., and Saphier, D. (1998). Neuroendocrine and immunocytochemical demonstrations of decreased hypothalamo-pituitary-adrenal axis responsiveness to restraint stress after long-term social isolation. Endocrinology 139, 579–587.10.1210/endo.139.2.5720Search in Google Scholar PubMed

Scaccianoce, S., Del Bianco, P., Paolone, G., Caprioli, D., Modafferi, A.M.E., Nencini, P., and Badiani, A. (2006). Social isolation selectively reduces hippocampal brain-derived neurotrophic factor without altering plasma corticosterone. Behav. Brain Res. 168, 323–325.10.1016/j.bbr.2005.04.024Search in Google Scholar PubMed

Schmidt, H.D., Shelton, R.C., and Duman, R.S. (2011). Functional biomarkers of depression: diagnosis, treatment, and pathophysiology. Neuropsychopharmacology 36, 2375–2394.10.1038/npp.2011.151Search in Google Scholar PubMed PubMed Central

Schroeder, M., Krebs, M.O., Bleich, S., and Frieling, H. (2010). Epigenetics and depression: current challenges and new therapeutic options. Curr. Opin. Psychiatry 23, 588–592.10.1097/YCO.0b013e32833d16c1Search in Google Scholar PubMed

Sen, S., Duman, R., and Sanacora, G. (2008). Serum brain-derived neurotrophic factor, depression, and antidepressant medications: meta-analyses and implications. Biol. Psychiatry 64, 527–532.10.1016/j.biopsych.2008.05.005Search in Google Scholar PubMed PubMed Central

Serra, M., Pisu, M.G., Floris, I., and Biggio, G. (2005). Social isolation-induced changes in the hypothalamic-pituitary-adrenal axis in the rat. Stress 8, 259–264.10.1080/10253890500495244Search in Google Scholar PubMed

Shao, F., Han, X., Shao, S., and Wang, W. (2013). Adolescent social isolation influences cognitive function in adult rats. Neural. Regen. Res. 8, 1025–1030.Search in Google Scholar

Shors, T.J. and Matzel, L.D. (1997). Long-term potentiation: what’s learning got to do with it? Behav. Brain Sci. 20, 597–614, discussion 614–655.10.1017/S0140525X97001593Search in Google Scholar

Slavich, G.M., Monroe, S.M., and Gotlib, I.H. (2011). Early parental loss and depression history: associations with recent life stress in major depressive disorder. J. Psychiatr. Res. 45, 1146–1152.10.1016/j.jpsychires.2011.03.004Search in Google Scholar PubMed PubMed Central

Spasojević, N., Gavrilović, Lj., Varagić, V., and Dronjak, S. (2007). Effects of chronic diazepam treatments on behavior on individually housed rats. Arch. Biol. Sci 59, 113–117.10.2298/ABS0702113SSearch in Google Scholar

Sun, H., Kennedy, P.J., and Nestler, E.J. (2013). Epigenetics of the depressed brain: role of histone acetylation and methylation. Neuropsychopharmacology 38, 124–137.10.1038/npp.2012.73Search in Google Scholar PubMed PubMed Central

Suri, D., Veenit, V., Sarkar, A., Thiagarajan, D., Kumar, A., Nestler, E.J., Galande, S., and Vaidya. V.A. (2013). Early stress evokes age-dependent biphasic changes in hippocampal neurogenesis, BDNF expression, and cognition. Biol. Psychiatry 73, 658–666.10.1016/j.biopsych.2012.10.023Search in Google Scholar PubMed PubMed Central

Thompson Ray, M., Weickert, C.S., Wyatt, E., and Webster, M.J. (2011). Decreased BDNF, trkB-TK+ and GAD67 mRNA expression in the hippocampus of individuals with schizophrenia and mood disorders. J. Psychiatry Neurosci. 36, 195–203.10.1503/jpn.100048Search in Google Scholar PubMed PubMed Central

Tirelli, E., Laviola, G., and Adriani, W. (2003). Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents. Neurosci. Biobehav. Rev. 27, 163–178.10.1016/S0149-7634(03)00018-6Search in Google Scholar

Tong, L., Prieto, G.A., Kramár, E.A., Smith, E.D., Cribbs, D.H., Lynch, G., and Cotman, C.W. (2012). BDNF-dependent synaptic plasticity is suppressed by IL-1β via p38 MAPK. J. Neurosci. 32, 17714–17724.10.1523/JNEUROSCI.1253-12.2012Search in Google Scholar PubMed PubMed Central

Toth, M., Mikics, E., Tulogdi, A., Aliczki, M., and Haller, J. (2011). Post-weaning social isolation induces abnormal forms of aggression in conjunction with increased glucocorticoid and autonomic stress responses. Horm. Behav. 60, 28–36.10.1016/j.yhbeh.2011.02.003Search in Google Scholar PubMed

Tsankova, N.M., Berton, O., Renthal, W., Kumar, A., Neve, R.L., and Nestler, E.J. (2006). Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 9, 519–525.10.1038/nn1659Search in Google Scholar PubMed

Tyler, W.J. and Pozzo-Miller, L. (2003). Miniature synaptic transmission and BDNF modulate dendritic spine growth and form in rat CA1 neurones. J. Physiol. (London) 553, 497–509.10.1113/jphysiol.2003.052639Search in Google Scholar PubMed PubMed Central

Van Bokhoven, P., Oomen, C.A., Hoogendijk, W.J.G., Smit, A.B., Lucassen, P.J., and Spijker, S. (2011). Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late antidepressant treatment. Eur. J. Neurosci. 33, 1833–1840.10.1111/j.1460-9568.2011.07668.xSearch in Google Scholar PubMed

Vaynman, S., Ying, Z., and Gomez-Pinilla, F. (2004). Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur. J. Neurosci. 20, 2580–2590.10.1111/j.1460-9568.2004.03720.xSearch in Google Scholar PubMed

Venna, V.R., Xu, Y., Doran, S.J., Patrizz, A., and McCullough, L.D. (2014). Social interaction plays a critical role in neurogenesis and recovery after stroke. Transl. Psychiatry 4, e351.10.1038/tp.2013.128Search in Google Scholar PubMed PubMed Central

von Bohlen und Halbach, O., Minichiello, L., and Unsicker, K. (2005). Haploinsufficiency for trkB and trkC receptors induces cell loss and accumulation of α-synuclein in the substantia nigra. FASEB J. 19, 1740–1742.10.1096/fj.05-3845fjeSearch in Google Scholar PubMed

Wahlstrom, D., Collins, P., White, T., and Luciana, M. (2010). Developmental changes in dopamine neurotransmission in adolescence: behavioral implications and issues in assessment. Brain Cogn. 72, 146–159.10.1016/j.bandc.2009.10.013Search in Google Scholar PubMed PubMed Central

Waterhouse, E.G., An, J.J., Orefice, L.L., Baydyuk, M., Liao, G.Y., Zheng, K., Lu, B., and Xu, B. (2012). BDNF promotes differentiation and maturation of adult-born neurons through GABAergic transmission. J. Neurosci. 32, 14318–14330.10.1523/JNEUROSCI.0709-12.2012Search in Google Scholar PubMed PubMed Central

Weintraub, A., Singaravelu, J., and Bhatnagar, S. (2010). Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res. 1343, 83–92.10.1016/j.brainres.2010.04.068Search in Google Scholar PubMed

Weiss, I.C., Pryce, C.R., Jongen-Rêlo, A.L., Nanz-Bahr, N.I., and Feldon, J. (2004). Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav. Brain Res. 152, 279–295.10.1016/j.bbr.2003.10.015Search in Google Scholar PubMed

Westenbroek, C., Den Boer, J.A., Veenhuis, M., and Ter Horst, G.J. (2004). Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res. Bull. 64, 303–308.10.1016/j.brainresbull.2004.08.006Search in Google Scholar PubMed

Williams, J.B., Pang, D., Delgado, B., Kocherginsky, M., Tretiakova, M., Krausz, T., Pan, D., He, J., McClintock, M.K., and Conzen, S.D. (2009). A model of gene-environment interaction reveals altered mammary gland gene expression and increased tumor growth following social isolation. Cancer Prev. Res. (Phila) 2, 850–861.10.1158/1940-6207.CAPR-08-0238Search in Google Scholar PubMed PubMed Central

Wongwitdecha, N. and Marsden, C.A. (1996). Effects of social isolation rearing on learning in the Morris water maze. Brain Res. 715, 119–124.10.1016/0006-8993(95)01578-7Search in Google Scholar PubMed

Woo, N.H., Teng, H.K., Siao, C.J., Chiaruttini, C., Pang, P.T., Milner, T.A., Hempstead, B.L., and Lu, B. (2005). Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat. Neurosci. 8, 1069–1077.10.1038/nn1510Search in Google Scholar PubMed

Xu, B., Gottschalk, W., Chow, A., Wilson, R.I., Schnell, E., Zang, K., Wang, D., Nicoll, R.A., Lu, B., and Reichardt, L.F. (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, 6888–6897.10.1523/JNEUROSCI.20-18-06888.2000Search in Google Scholar PubMed PubMed Central

Yoshii, A. and Constantine-Paton, M. (2010). Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Dev. Neurobiol. 70, 304–322.10.1002/dneu.20765Search in Google Scholar PubMed PubMed Central

Zafra, F., Castrén, E., Thoenen, H., and Lindholm, D. (1991). Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc. Natl. Acad. Sci. USA 88, 10037–10041.10.1073/pnas.88.22.10037Search in Google Scholar PubMed PubMed Central

Zaletel, I., Filipović, D., and Puškaš, N. (2016). Chronic stress, hippocampus and parvalbumin-positive interneurons: what do we know so far? Rev. Neurosci. 27, 397–409.10.1515/revneuro-2015-0042Search in Google Scholar PubMed

Zlatković, J., Todorović, N., Bošković, M., Pajović, S.B., Demajo, M., and Filipović, D. (2014). Different susceptibility of prefrontal cortex and hippocampus to oxidative stress following chronic social isolation stress. Mol. Cell Biochem. 393, 43–57.10.1007/s11010-014-2045-zSearch in Google Scholar PubMed

Received: 2016-10-30
Accepted: 2017-02-16
Published Online: 2017-04-07
Published in Print: 2017-07-26

©2017 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 22.5.2024 from https://www.degruyter.com/document/doi/10.1515/revneuro-2016-0072/html
Scroll to top button