Information de reference pour ce titreAccession Number: | 00006056-201301240-00046.
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Author: | Chaudhury, Dipesh 1,6; Walsh, Jessica J. 1,2,6; Friedman, Allyson K. 1; Juarez, Barbara 1,2; Ku, Stacy M. 1,2; Koo, Ja Wook 2; Ferguson, Deveroux 2; Tsai, Hsing-Chen 3; Pomeranz, Lisa 4; Christoffel, Daniel J. 2; Nectow, Alexander R. 4; Ekstrand, Mats 4; Domingos, Ana 4; Mazei-Robison, Michelle S. 2; Mouzon, Ezekiell 2; Lobo, Mary Kay 2; Neve, Rachael L. 5; Friedman, Jeffrey M. 4; Russo, Scott J. 2; Deisseroth, Karl 3; Nestler, Eric J. 1,2; Han, Ming-Hu 1,2,*
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Institution: | (1)Department of Pharmacology and Systems Therapeutics, Friedman Brain Institute, Mount Sinai School of Medicine, New York, New York 10029, USA (2)Fishberg Department of Neuroscience, Friedman Brain Institute, Mount Sinai School of Medicine, New York, New York 10029, USA (3)Departments of Bioengineering and Psychiatry and Behavioural Sciences, Stanford University, Stanford, California 94305, USA (4)Laboratory of Molecular Genetics, Howard Hughes Medical Institute, Rockefeller University, New York, New York 10056, USA (5)McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA (6)These authors contributed equally to this work.
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Title: | Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons.[Letter]
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Source: | Nature. 493(7433):532-536, January 24, 2013.
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Abstract: | : Ventral tegmental area (VTA) dopamine neurons in the brain's reward circuit have a crucial role in mediating stress responses 1-4, including determining susceptibility versus resilience to social-stress-induced behavioural abnormalities 5. VTA dopamine neurons show two in vivo patterns of firing: low frequency tonic firing and high frequency phasic firing 6-8. Phasic firing of the neurons, which is well known to encode reward signals 6,7,9, is upregulated by repeated social-defeat stress, a highly validated mouse model of depression 5,8,10-13. Surprisingly, this pathophysiological effect is seen in susceptible mice only, with no apparent change in firing rate in resilient individuals 5,8. However, direct evidence-in real time-linking dopamine neuron phasic firing in promoting the susceptible (depression-like) phenotype is lacking. Here we took advantage of the temporal precision and cell-type and projection-pathway specificity of optogenetics to show that enhanced phasic firing of these neurons mediates susceptibility to social-defeat stress in freely behaving mice. We show that optogenetic induction of phasic, but not tonic, firing in VTA dopamine neurons of mice undergoing a subthreshold social-defeat paradigm rapidly induced a susceptible phenotype as measured by social avoidance and decreased sucrose preference. Optogenetic phasic stimulation of these neurons also quickly induced a susceptible phenotype in previously resilient mice that had been subjected to repeated social-defeat stress. Furthermore, we show differences in projection-pathway specificity in promoting stress susceptibility: phasic activation of VTA neurons projecting to the nucleus accumbens (NAc), but not to the medial prefrontal cortex (mPFC), induced susceptibility to social-defeat stress. Conversely, optogenetic inhibition of the VTA-NAc projection induced resilience, whereas inhibition of the VTA-mPFC projection promoted susceptibility. Overall, these studies reveal novel firing-pattern- and neural-circuit-specific mechanisms of depression.
(C) 2013 Nature Publishing Group
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References: | 1. Willner, P., Hale, A. S. & Argyropoulos, S. Dopaminergic mechanism of antidepressant action in depressed patients. J. Affect. Disord. 86, 37-45 (2005)
2. Nestler, E. J. & Carlezon, W. A., Jr The mesolimbic dopamine reward circuit in depression. Biol. Psychiatry 59, 1151-1159 (2006)
3. Berton, O. & Nestler, E. J. New approaches to antidepressant drug discovery: beyond monoamines. Nature Rev. Neurosci. 7, 137-151 (2006)
4. Yadid, G. & Friedman, A. Dynamics of the dopaminergic system as a key component to the understanding of depression. Prog. Brain Res. 172, 265-286 (2008)
5. Krishnan, V. et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391-404 (2007)
6. Grace, A. A., Floresco, S. B., Goto, Y. & Lodge, D. J. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci. 30, 220-227 (2007)
7. Tsai, H. C. et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080-1084 (2009)
8. Cao, J. L. et al. Mesolimbic dopamine neurons in the brain reward circuit mediate susceptibility to social defeat and antidepressant action. J. Neurosci. 30, 16453-16458 (2010)
9. Schultz, W. Dopamine signals for reward value and risk: basic and recent data. Behav. Brain Funct. 6, 24 (2010)
10. Berton, O. et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868 (2006)
11. Anstrom, K. K., Miczek, K. A. & Budygin, E. A. Increased phasic dopamine signaling in the mesolimbic pathway during social defeat in rats. Neuroscience 161, 3-12 (2009)
12. Razzoli, M., Andreoli, M., Michielin, F., Quarta, D. & Sokal, D. M. Increased phasic activity of VTA dopamine neurons in mice 3 weeks after repeated social defeat. Behav. Brain Res. 218, 253-257 (2011)
13. Krishnan, V., Berton, O. & Nestler, E. The use of animal models in psychiatric research and treatment. Am. J. Psychiatry 165, 1109 (2008)
14. Lobo, M. K. et al. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330, 385-390 (2010)
15. Iniguez, S. D. et al. Extracellular signal-regulated kinase-2 within the ventral tegmental area regulates responses to stress. J. Neurosci. 30, 7652-7663 (2010)
16. Valenti, O., Gill, K. M. & Grace, A. A. Different stressors produce excitation or inhibition of mesolimbic dopamine neuron activity: response alteration by stress pre-exposure. Eur. J. Neurosci. 35, 1312-1321 (2012)
17. Ungless, M. A., Magill, P. J. & Bolam, J. P. Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303, 2040-2042 (2004)
18. Venzala, E., Garcia-Garcia, A. L., Elizalde, N. & Tordera, R. M. Social vs. environmental stress models of depression from a behavioural and neurochemical approach. Eur. Neuropsychopharmacol. advance online publication, http://dx.doi.org/10.1016/j.euro...- ouverture dans une nouvelle fenêtre (June 27, 2012)
19. Lammel, S., Ion, D. I., Roeper, J. & Malenka, R. C. Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 70, 855-862 (2011)
20. Willner, P. The mesolimbic dopamine system as a target for rapid antidepressant action. Int. Clin. Psychopharmacol. 12 (Suppl. 3). S7-S14 (1997)
21. Radulescu, A. R. Mechanisms explaining transitions between tonic and phasic firing in neuronal populations as predicted by a low dimensional firing rate model. PLoS ONE 5, e12695 (2010)
22. Inyushin, M. U., Arencibia-Albite, F., Vazquez-Torres, R., Velez-Hernandez, M. E. & Jimenez-Rivera, C. A. Alpha-2 noradrenergic receptor activation inhibits the hyperpolarization-activated cation current (Ih) in neurons of the ventral tegmental area. Neuroscience 167, 287-297 (2010)
23. Han, H. M. et al. Essential role of ventral tegmental area dopamine neurons in mediating the induction and rapid reversal of depression-like behaviours. Abstract, http://www.acnp.org/annualmeetin...- ouverture dans une nouvelle fenêtre (The 50th Anniversary Meeting of ACNP, 2011)
24. Berman, R. M. et al. Antidepressant effects of ketamine in depressed patients. Biol. Psychiatry 47, 351-354 (2000)
25. Li, N. et al. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329, 959-964 (2010)
26. Autry, A. E. et al. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475, 91-95 (2011)
27. Hemmeter, U. M., Hemmeter-Spernal, J. & Krieg, J. C. Sleep deprivation in depression. Expert Rev. Neurother. 10, 1101-1115 (2010)
28. Giacobbe, P., Mayberg, H. S. & Lozano, A. M. Treatment resistant depression as a failure of brain homeostatic mechanisms: implications for deep brain stimulation. Exp. Neurol. 219, 44-52 (2009)
29. Sartorius, A. et al. Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol. Psychiatry 67, e9-e11 (2010)
30. Li, B. et al. Synaptic potentiation onto habenula neurons in the learned helplessness model of depression. Nature 470, 535-539 (2011)
31. Lindeberg, J. et al. Transgenic expression of Cre recombinase from the tyrosine hydroxylase locus. Genesis 40, 67-73 (2004)
32. Cardin, J. A. et al. Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nature Protocols 5, 247-254 (2010)
33. Hommel, J. D., Sears, R. M., Georgescu, D., Simmons, D. L. & DiLeone, R. J. Local gene knockdown in the brain using viral-mediated RNA interference. Nature Med. 9, 1539-1544 (2003)
34. Sparta, D. R. et al. Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nature Protocols 7, 12-23 (2011)
35. Gradinaru, V. et al. Targeting and readout strategies for fast optical neural control in vitro and in vivo. J. Neurosci. 27, 14231-14238 (2007)
36. Golden, S. A., Covington, H. E., III, Berton, O. & Russo, S. J. A standardized protocol for repeated social defeat stress in mice. Nature Protocols 6, 1183-1191 (2011)
37. Stuber, G. D. et al. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475, 377-380 (2011)
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Language: | English.
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Document Type: | LETTER.
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Journal Subset: | Life & Biomedical Sciences. Science.
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ISSN: | 0028-0836
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NLM Journal Code: | 0410462, nsc
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DOI Number: | https://dx.doi.org/10.1038/natur...- ouverture dans une nouvelle fenêtre
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