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Mesolimbic Dopamine Neurons in the Brain Reward Circuit Mediate Susceptibility to Social Defeat and Antidepressant Action

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Mesolimbic Dopamine Neurons in the Brain Reward Circuit Mediate Susceptibility to Social Defeat and Antidepressant Action The Journal of Neuroscience, December 8, 2010 • 30(49):16453–16458 • 16453 Brief Communications Mesolimbic Dopamine Neurons in the Brain Reward Circuit Mediate Susceptibility to Social Defeat and Antidepressant Action Jun-Li Cao,1,2 Herbert E. Covington III,3 Allyson K. Friedman,4 Matthew B. Wilkinson,3 Jessica J. Walsh,4 Donald C. Cooper,1 Eric J. Nestler,3,4 and Ming-Hu Han1,3,4 1Department of Psychiatry, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9070, 2Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical College, Xuzhou 221002, China, and 3Fishberg Department of Neuroscience, and 4Department of Pharmacology and Systems Therapeutics, Mount Sinai School of Medicine, New York, New York, 10029-6574 We previously reported that the activity of mesolimbic dopamine neurons of the ventral tegmental area (VTA) is a key determinant of behavioral susceptibility vs resilience to chronic social defeat stress. However, this was based solely on ex vivo measurements, and the in vivo firing properties of VTA dopamine neurons in susceptible and resilient mice, as well as the effects of antidepressant treatments, remain completely unknown. Here, we show that chronic (10 d) social defeat stress significantly increased the in vivo spontaneous firing rates and bursting events in susceptible mice but not in the resilient subgroup. Both the firing rates and bursting events were significantly negatively correlated with social avoidance behavior, a key behavioral abnormality induced by chronic social defeat stress. Moreover, the increased firing rates, bursting events, and avoidance behavior in susceptible mice were completely reversed by chronic (2 week), but not acute (single dose), treatments with the antidepressant medication fluoxetine (20 mg/kg). Chronic social defeat stress increased hyperpolarization-activated cation current (Ih ) in VTA dopamine neurons, an effect that was also normalized by chronic treatment with ␮ ␮ fluoxetine. As well, local infusion of Ih inhibitors ZD7288 (0.1 g) or DK-AH 269 (0.6 g) into the VTA exerted antidepressant-like behavioral effects. Together, these data suggest that the firing patterns of mesolimbic dopamine neurons in vivo mediate an individual’s responses to chronic stress and antidepressant action. Introduction defeat-induced behavioral abnormalities (Berton et al., 2006), Antidepressants acutely induce a rapid increase in monoamine and we inferred that the activity of VTA DA neurons, measured in neurotransmission in the brain, but the mood-elevating effects of brain slices ex vivo, is a key determinant of behavioral suscepti- these medications in depressed patients, effects that are absent in bility vs resilience to social defeat (Krishnan et al., 2007; Feder et healthy humans, take several weeks to months to manifest (Os- al., 2009). These earlier results were surprising, since they showed wald et al., 1972; Nestler et al., 2002; Berton and Nestler, 2006). increased VTA firing ex vivo, a proreward effect, in susceptible These clinical observations suggest that antidepressants induce but not resilient mice, raising the question of whether such an gradually developing changes in brain uniquely in affected indi- increase is relevant to the in vivo situation. viduals. In previous studies, we characterized a chronic social It is well known that VTA DA neurons exhibit two patterns of defeat stress model of depression, one of the few in which chronic spontaneous firing activity: a slow-frequency, single-spike firing stress-induced molecular and behavioral changes are responsive and a burst firing. The burst-firing mode generates a substantially to chronic, but not acute, antidepressant administration (Berton larger increase of dopamine release than single spiking, and more et al., 2006). Using this model, we demonstrated that the me- effectively regulates the activity of neurons in DA target areas, by solimbic dopamine system, a depression-related neural pathway which VTA DA neurons encode reward-related signals (Grace et (Fibiger and Phillips, 1981) composed of dopaminergic (DA) al., 2007). However, while burst-firing activity is functionally neurons of the ventral tegmental area (VTA) and their projec- very important, it is absent in VTA slice preparations (Kitai et al., tions to the nucleus accumbens, plays an essential role in social 1999). In the present study, we used this established depression model to investigate the effects of social defeat on the in vivo firing properties of VTA DA neurons. Furthermore, we studied the Received June 20, 2010; revised Sept. 23, 2010; accepted Oct. 6, 2010. ThisworkwassupportedbygrantsfromtheNationalInstituteofMentalHealth(E.J.N.)andNationalAlliancefor effects of acute and chronic fluoxetine, a widely prescribed anti- Research on Schizophrenia and Depression (M.H.H.). depressant, in this model to test whether these neurons might Correspondence should be addressed to Ming-Hu Han, Department of Pharmacology and Systems Therapeutics, contribute to antidepressant action. Mount Sinai School of Medicine, New York, NY 10029-6574. E-mail: [email protected]. D. C. Cooper’s present address: Department of Psychology and Neuroscience, Institute for Behavioral Genetics, University of Colorado, Boulder, CO 80303. Materials and Methods DOI:10.1523/JNEUROSCI.3177-10.2010 Animals. Seven-week-old C57BL/6 male mice (Jackson Laboratories) Copyright © 2010 the authors 0270-6474/10/3016453-06$15.00/0 and CD1 retired breeders (Charles River) were used for these studies. All 16454 • J. Neurosci., December 8, 2010 • 30(49):16453–16458 Cao et al. • Burst Mediates Stress and Antidepressant Responses experiments were conducted in accordance with guidelines of the Insti- directly above the VTA (AP, Ϫ3.2; ML, 0.4; DV, Ϫ3.6 mm) (supplemen- tutional Animal Care and Use Committees at University of Texas South- tal Fig. S1, available at www.jneurosci.org as supplemental material). western Medical Center and Mount Sinai School of Medicine. After 6–8 d of postoperative recovery, simultaneous bilateral microin- Chronic social defeat stress. This paradigm was performed exactly as jections of ZD7288 (0.1 ␮g), DK-AH 269 (0.6 ␮g), or PBS were delivered reported (Krishnan et al., 2007). C57BL/6 mice were exposed to a differ- through an injector cannula in a total volume 0.4 ␮l/side at a continuous ent CD1 aggressor mouse each day for 10 min over a total of 10 d. On day rate of 0.1 ␮l/min under the control of a micro-infusion pump (Harvard 11, a social interaction test (Ethovision 3.0 software) identified sub- Apparatus). Concentrations of ZD7288 and DK-AH 269 were selected groups of susceptible and resilient mice. This was accomplished by plac- based on earlier in vivo studies (Chevaleyre and Castillo, 2002; Kocsis and ing mice in an interaction test box, with their movement tracked for 2.5 Li, 2004). Injector cannulae were removed 2 min after the stopping of min in the absence and presence of a caged, unfamiliar target CD1 each infusion, and mice remained undisturbed in their home cages for an mouse, respectively. The interaction ratio was calculated as 100 ϫ (inter- additional 3 min (ZD7288) or 60 min (DK-AH 269) before testing for action time, target present)/(interaction time, target absent). Based on social interaction behavior. our previous work, an interaction ratio of 100 was set as a cutoff: mice Statistics. Data are expressed as mean Ϯ SEM. One-way ANOVAs with scores Ͻ100 were defined as “susceptible” and those with scores followed by a Newman–Keuls post hoc test were used to compare three or Ն100 were defined as “unsusceptible” or resilient. more groups in behavioral and in vivo recording data. ␹ 2 tests were used Fluoxetine treatment. Fluoxetine (20 mg/kg; Eli Lily and Company) in to analyze the change of percentage of bursting cells. Two-way ANOVA PBS was administered through intraperitoneal injection daily at 4:00– was performed when analyzing Ih currents and behavioral data for infu- 5:00 P.M. for 14–27 d in susceptible and control mice. sion of ZD7288 or DK-AH 269. p Ͻ 0.05 was considered statistically In vivo recordings. In vivo extracellular single-cell recordings were per- significant. GraphPad Prism 5 was used for all statistical analyses. formed using published methods (McClung et al., 2005; Mameli-Engvall et al., 2006). Mice were anesthetized with 8% chloral hydrate (400 mg/kg, Results i.p.). Microelectrodes (15–20 M⍀) were filled with 2 M NaCl with 1% fast Mice subjected to chronic social defeat were segregated into green (to mark location of the electrode tip). Coordinates for the VTA susceptible and resilient subpopulations based on their social were as follows (in mm): anteroposterior (AP), 2.92–3.88; midline (ML), avoidance, which correlates with several other behavioral ab- 0.24–0.96; and dorsoventral (DV), 3.5–4.5. normalities (Krishnan et al., 2007). Sixty to 70 percent of mice DA cells were identified by anatomical location in the VTA (fast green subjected to this paradigm fell into the susceptible subgroup in check) and according to standard physiological criteria (Marinelli and this study. Susceptible mice spent significantly less time interact- White, 2000; McClung et al., 2005). These neurons exhibited the follow- ing with other mice compared with controls, a phenomenon ab- ing: (1) a typical triphasic action potential with a marked negative deflec- sent in resilient mice (Fig. 1A,B)(F ϭ 22.03, p Ͻ 0.0001) tion; (2) a characteristic long duration (Ͼ2.0 ms); (3) an action potential (2,38) width from start to negative trough Ն1.1 ms; and (4) a slow firing rate (supplemental Fig. S2, available at www.jneurosci.org as supple- (Ͻ10 Hz) with an irregular single spiking pattern and occasional short, mental material). We then obtained extracellular single-unit re- slow bursting activity. Two criteria were used to confirm burst firing: (1) cordings from 195 putative VTA DA neurons in anesthetized onset was defined by two consecutive spikes within an interval Ͻ80 ms; control, susceptible, and resilient mice.
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