Essential Role of Mesolimbic Brain-Derived Neurotrophic Factor in Chronic Social Stress–Induced Depressive Behaviors

Biological Psychiatry

Volumn 80, Issue 6, 2016, Pages 469-478

  Wook Koo, Ja ^a,b   Labonté, Benoit ^a   Engmann, Olivia ^a   Calipari, Erin S ^a   Juarez, Barbara ^a   Lorsch, Zachary ^a   Walsh, Jessica J ^a   Friedman, Allyson K ^a   Yorgason, Jordan T ^c   Han, Ming Hu ^a   Nestler, Eric J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Korea Brain Research Institute (KBRI)   (South Korea)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

BDNF; Chronic defeat stress; Dopamine; Nucleus accumbens; Social avoidance; Ventral tegmental area

Indexed keywords

8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; ANA 12; BRAIN DERIVED NEUROTROPHIC FACTOR; DOPAMINE; DOPAMINE 1 RECEPTOR; ETICLOPRIDE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE KINASE INHIBITOR; UNCLASSIFIED DRUG; ANA 12 COMPOUND; AZEPINE DERIVATIVE; BENZAMIDE DERIVATIVE; BENZAZEPINE DERIVATIVE; COCAINE; PROTEIN TYROSINE KINASE; SALICYLAMIDE DERIVATIVE; TRKB PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; CHRONIC STRESS; CONTROLLED STUDY; DEPRESSION; DOPAMINE RELEASE; ENZYME PHOSPHORYLATION; GENE SILENCING; MALE; MESOLIMBIC DOPAMINERGIC SYSTEM; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOCIAL AVOIDANCE BEHAVIOR; SOCIAL INTERACTION TEST; SOCIAL STRESS; VENTRAL TEGMENTUM; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CONDITIONING; DRUG EFFECTS; GENETICS; MENTAL STRESS; METABOLISM; MICROINJECTION; MOUSE; NERVE TRACT; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; SOCIAL BEHAVIOR; TRANSGENIC MOUSE;

ANIMALS; AZEPINES; BENZAMIDES; BENZAZEPINES; BRAIN-DERIVED NEUROTROPHIC FACTOR; COCAINE; CONDITIONING (PSYCHOLOGY); DEPRESSION; DOPAMINE; GENE KNOCKDOWN TECHNIQUES; MALE; MICE; MICE, TRANSGENIC; MICROINJECTIONS; NEURAL PATHWAYS; NUCLEUS ACCUMBENS; PROTEIN-TYROSINE KINASES; SALICYLAMIDES; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL; VENTRAL TEGMENTAL AREA;

EID: 84990303161     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2015.12.009     Document Type: Article

References (41)

1. 1 Kumpulainen, K., Psychiatric conditions associated with bullying. Int J Adolesc Med Health 20 (2008), 121–132.
2. 2 Huhman, K.L., Social conflict models: Can they inform us about human psychopathology?. Horm Behav 50 (2006), 640–646.
3. 3 Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 (2006), 864–868.
4. 4 Krishnan, V., Han, M.H., Graham, D.L., Berton, O., Renthal, W., Russo, S.J., et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131 (2007), 391–404.
5. 5 Hollis, F., Kabbaj, M., Social defeat as an animal model for depression. ILAR J 55 (2014), 221–232.
6. 6 Cao, J.L., Covington, H.E. 3rd, Friedman, A.K., Wilkinson, M.B., Walsh, J.J., Cooper, D.C., et al. Mesolimbic dopamine neurons in the brain reward circuit mediate susceptibility to social defeat and antidepressant action. J Neurosci 30 (2010), 16453–16458.
7. 7 Chaudhury, D., Walsh, J.J., Friedman, A.K., Juarez, B., Ku, S.M., Koo, J.W., et al. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 493 (2013), 532–536.
8. 8 Walsh, J.J., Friedman, A.K., Sun, H., Heller, E.A., Ku, S.M., Juarez, B., et al. Stress and CRF gate neural activation of BDNF in the mesolimbic reward pathway. Nat Neurosci 17 (2014), 27–29.
9. 9 Bass, C.E., Grinevich, V.P., Gioia, D., Day-Brown, J.D., Bonin, K.D., Stuber, G.D., et al. Optogenetic stimulation of VTA dopamine neurons reveals that tonic but not phasic patterns of dopamine transmission reduce ethanol self-administration. Front Behav Neurosci, 7, 2013, 173.
10. 10 Tsai, H.C., Zhang, F., Adamantidis, A., Stuber, G.D., Bonci, A., de Lecea, L., et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324 (2009), 1080–1084.
11. 11 Narita, M., Aoki, K., Takagi, M., Yajima, Y., Suzuki, T., Implication of brain-derived neurotrophic factor in the release of dopamine and dopamine-related behaviors induced by methamphetamine. Neuroscience 119 (2003), 767–775.
12. 12 Trainor, B.C., Stress responses and the mesolimbic dopamine system: Social contexts and sex differences. Horm Behav 60 (2011), 457–469.
13. 13 Lammel, S., Lim, B.K., Malenka, R.C., Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology 76:pt B (2014), 351–359.
14. 14 Wise, R.A., Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotox Res 14 (2008), 169–183.
15. 15 Pani, L., Gessa, G.L., Evolution of the dopaminergic system and its relationships with the psychopathology of pleasure. Int J Clin Pharmacol Res 17 (1997), 55–58.
16. 16 Dunlop, B.W., Nemeroff, C.B., The role of dopamine in the pathophysiology of depression. Arch Gen Psychiatry 64 (2007), 327–337.
17. 17 Roy, A., Recent biologic studies on suicide. Suicide Life Threat Behav 24 (1994), 10–14.
18. 18 Lambert, G., Johansson, M., Agren, H., Friberg, P., Reduced brain norepinephrine and dopamine release in treatment-refractory depressive illness: Evidence in support of the catecholamine hypothesis of mood disorders. Arch Gen Psychiatry 57 (2000), 787–793.
19. 19 Tye, K.M., Mirzabekov, J.J., Warden, M.R., Ferenczi, E.A., Tsai, H.C., Finkelstein, J., et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493 (2013), 537–541.
20. 20 Di Matteo, V., Di Mascio, M., Di Giovanni, G., Esposito, E., Acute administration of amitriptyline and mianserin increases dopamine release in the rat nucleus accumbens: Possible involvement of serotonin2C receptors. Psychopharmacology (Berl) 150 (2000), 45–51.
21. 21 Willner, P., The mesolimbic dopamine system as a target for rapid antidepressant action. Int Clin Psychopharmacol 12:suppl 3 (1997), S7–14.
22. 22 D'Aquila, P.S., Collu, M., Gessa, G.L., Serra, G., The role of dopamine in the mechanism of action of antidepressant drugs. Eur J Pharmacol 405 (2000), 365–373.
23. 23 Gong, S., Zheng, C., Doughty, M.L., Losos, K., Didkovsky, N., Schambra, U.B., et al. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425 (2003), 917–925.
24. 24 Koo, J.W., Mazei-Robison, M.S., Chaudhury, D., Juarez, B., LaPlant, Q., Ferguson, D., et al. BDNF is a negative modulator of morphine action. Science 338 (2012), 124–128.
25. 25 Boye, S.M., Grant, R.J., Clarke, P.B., Disruption of dopaminergic neurotransmission in nucleus accumbens core inhibits the locomotor stimulant effects of nicotine and D-amphetamine in rats. Neuropharmacology 40 (2001), 792–805.
26. 26 Calipari, E.S., Sun, H., Eldeeb, K., Luessen, D.J., Feng, X., Howlett, A.C., et al. Amphetamine self-administration attenuates dopamine D2 autoreceptor function. Neuropsychopharmacology 39 (2014), 1833–1842.
27. 27 Lobo, M.K., Covington, H.E. 3rd, Chaudhury, D., Friedman, A.K., Sun, H., Damez-Werno, D., et al. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330 (2010), 385–390.
28. 28 Yorgason, J.T., Espana, R.A., Jones, S.R., Demon voltammetry and analysis software: analysis of cocaine-induced alterations in dopamine signaling using multiple kinetic measures. J Neurosci Methods 202 (2011), 158–164.
29. 29 Golden, S.A., Covington, H.E. 3rd, Berton, O., Russo, S.J., A standardized protocol for repeated social defeat stress in mice. Nat Protoc 6 (2011), 1183–1191.
30. 30 Valjent, E., Bertran-Gonzalez, J., Herve, D., Fisone, G., Girault, J.A., Looking BAC at striatal signaling: cell-specific analysis in new transgenic mice. Trends Neurosci 32 (2009), 538–547.
31. 31 Abercrombie, E.D., Keefe, K.A., DiFrischia, D.S., Zigmond, M.J., Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J Neurochem 52 (1989), 1655–1658.
32. 32 Tidey, J.W., Miczek, K.A., Social defeat stress selectively alters mesocorticolimbic dopamine release: An in vivo microdialysis study. Brain Res 721 (1996), 140–149.
33. 33 Louilot, A., Le Moal, M., Simon, H., Differential reactivity of dopaminergic neurons in the nucleus accumbens in response to different behavioral situations. An in vivo voltammetric study in free moving rats. Brain Res 397 (1986), 395–400.
34. 34 Russo, S.J., Nestler, E.J., The brain reward circuitry in mood disorders. Nat Rev Neurosci 14 (2013), 609–625.
35. 35 Lobo, M.K., Zaman, S., Damez-Werno, D.M., Koo, J.W., Bagot, R.C., Dinieri, J.A., et al. DeltaFosB induction in striatal medium spiny neuron subtypes in response to chronic pharmacological, emotional, and optogenetic stimuli. J Neurosci 33 (2013), 18381–18395.
36. 36 Gertler, T.S., Chan, C.S., Surmeier, D.J., Dichotomous anatomical properties of adult striatal medium spiny neurons. J Neurosci 28 (2008), 10814–10824.
37. 37 Francis, T.C., Chandra, R., Friend, D.M., Finkel, E., Dayrit, G., Miranda, J., et al. Nucleus accumbens medium spiny neuron subtypes mediate depression-related outcomes to social defeat stress. Biol Psychiatry 77 (2015), 212–222.
38. 38 Lim, B.K., Huang, K.W., Grueter, B.A., Rothwell, P.E., Malenka, R.C., Anhedonia requires MC4R-mediated synaptic adaptations in nucleus accumbens. Nature 487 (2012), 183–189.
39. 39 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.
40. 40 Nestler, E.J., Carlezon, W.A. Jr, The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59 (2006), 1151–1159.
41. 41 Gangarossa, G., Espallergues, J., de Kerchove, d'Exaerde A, El Mestikawy, S., Gerfen, C.R., Herve, D., et al. Distribution and compartmental organization of GABAergic medium-sized spiny neurons in the mouse nucleus accumbens. Front Neural Circuits, 7, 2013, 22.