Repeated brief social defeat episodes in mice: Effects on cell proliferation in the dentate gyrus

Yap, Jasmine J.; Takase, Luiz Fernando; Kochman, Linda J.; Fornal, Casimir A.; Miczek, Klaus A.; Jacobs, Barry L.

doi:10.1016/j.bbr.2006.05.027

Cited by 79 publications

(63 citation statements)

References 80 publications

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“…This decrease was restricted to the neurogenic SGZ, suggesting a region-specific mechanism for this regulation. This finding agrees with most of the literature showing fewer BrdU-IR cells immediately after chronic stress paradigms (e.g., 23,24,26,27). The reduction in BrdU-IR cell number immediately after stress does not generalize to an overall decrease in the total number of proliferating cells, as assessed by immunoreactivity of the endogenous cell cycle protein Ki67.…”

Section: Discussionsupporting

confidence: 91%

“…When we analyze all defeated mice in this study, regardless of susceptibility to stress, there is no difference in BrdU-IR cell survival postdefeat. The lack of decrease in neurogenesis poststress between stressed and control mice is consistent with no change in cell survival 1 day after chronic unpredictable stress in rats (21) and the normal granule cell layer volume reported in many stress studies (23)(24)(25). However, by analyzing the susceptibility to stress through behavioral outcomes, we have uncovered a striking significant increase in surviving BrdU-IR cells in mice specifically susceptible to stress.…”

Section: Discussionsupporting

confidence: 88%

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Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance

Lagace

Donovan

DeCarolis

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

287

235

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The long-term response to chronic stress is variable, with some individuals developing maladaptive functioning, although other "resilient" individuals do not. Stress reduces neurogenesis in the dentate gyrus subgranular zone (SGZ), but it is unknown if stress-induced changes in neurogenesis contribute to individual vulnerability. Using a chronic social defeat stress model, we explored whether the susceptibility to stress-induced social avoidance was related to changes in SGZ proliferation and neurogenesis. Immediately after social defeat, stressexposed mice (irrespective of whether they displayed social avoidance) had fewer proliferating SGZ cells labeled with the S-phase marker BrdU. The decrease was transient, because BrdU cell numbers were normalized 24 h later. The survival of BrdU cells labeled before defeat stress was also not altered. However, 4 weeks later, mice that displayed social avoidance had more surviving dentate gyrus neurons. Thus, dentate gyrus neurogenesis is increased after social defeat stress selectively in mice that display persistent social avoidance. Supporting a functional role for adult-generated dentate gyrus neurons, ablation of neurogenesis via cranial ray irradiation robustly inhibited social avoidance. These data show that the time window after cessation of stress is a critical period for the establishment of persistent cellular and behavioral responses to stress and that a compensatory enhancement in neurogenesis is related to the long-term individual differences in maladaptive responses to stress. dentate gyrus | nestin-GFP | posttraumatic stress disorder | social defeat | subgranular zone

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 88%

Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance

Lagace

Donovan

DeCarolis

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

287

235

View full text Add to dashboard Cite

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“…In addition, as behavioural and gonadal hormone profiles are more divergent for breeders and subordinates than male and female naked mole-rats, we hypothesized that DCX expression would vary with social status. In line with prior research demonstrating a neurogenic advantage for dominant versus subordinate individuals (Gould et al, 1997;1998;Czeh et al, 2001;Van der Hart et al, 2002;Kozorovitskiy and Gould, 2004;Mitra et al, 2006;Simon et al, 2005;Yap et al, 2006;Czeh et al, 2007, Thomas et al, 2007van Bokhoven et al, 2011), and reproductively active versus inactive animals , we predicted that breeding naked mole-rats would demonstrate higher DCX expression than subordinates. Finally, we expected that DCX…”

Section: The Present Studysupporting

confidence: 60%

“…Conversely, aversive interactions with dominant and aggressive conspecifics reduce cell proliferation and survival in the DG, suggesting that hippocampal neurogenesis is sensitive to status and social threat cues (Gould et al, 1997;1998;Czeh et al, 2001;Van der Hart et al, 2002;Kozorovitskiy and Gould, 2004;Mitra et al, 2006;Simon et al, 2005;Yap et al, 2006;Czeh et al, 2007, Thomas et al, 2007van Bokhoven et al, 2011).…”

Section: Social Control Of Adult Neurogenesismentioning

confidence: 99%

“…In fish, birds, tree shrews, primates, and traditional laboratory rodents, subordinate individuals have reduced cell proliferation and/or neurogenesis in the hippocampus (Gould et al, 1997;1998;Yap et al, 2006Czeh et al, 20012002;van der Hart et al, 2002;Kozorovitskiy and Gould, 2004;Pravosudov et al, 2005;Simon et al, 2005;Czeh et al, 2007;Thomas et al, 2007;Van Bokhoven et al, 2011;Maruska et al, 2012). Though extrahippocampal neurogenesis has received considerably less attention, what few studies have been done report that status-associated differences are not observed in the BLA (Mitra et al, 2006) or SVZ (Czeh et al, 2007).…”

Section: Adult Neurogenesis and Social Factorsmentioning

confidence: 99%

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Social regulation of adult neurogenesis in a eusocial mammal

et al. 2014

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The present study examined social status and adult neurogenesis in the naked mole rat. These animals live in large colonies with a strict reproductive dominance hierarchy; one female and 1-3 males breed, while other members are subordinate and reproductively suppressed. We examined whether social status affects doublecortin (DCX; a marker for immature neurons) immunoreactivity in the dentate gyrus, piriform cortex (PCx), and basolateral amygdala (BLA) by comparing breeders to subordinates. We also examined subordinates removed from their colony and paired with opposite-or same-sex conspecifics for 6 months. Breeders had reduced DCX immunoreactivity in all areas, with BLA effects confined to females. Effects of housing condition were region-specific, with higher PCx DCX immunoreactivity observed in oppositethan same-sex paired subordinates regardless of gonadal status. The opposite pattern was observed in the BLA. Future work will clarify whether findings are attributable to status differences in stress, behavioural plasticity, or life stage.iii

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Characterization of cell proliferation throughout the brain of the African cichlid fish Astatotilapia burtoni and its regulation by social status

Maruska

Carpenter

Fernald

2012

J of Comparative Neurology

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New cells are added in the brains of all adult vertebrates, but fishes have some of the greatest potential for neurogenesis and gliogenesis among all taxa, partly due to their indeterminate growth. Little is known, however, about how social interactions influence cell proliferation in the brain of these fishes that comprise the largest group of vertebrates. We used 5-bromo-2′-deoxy-uridine (BrdU) to identify and localize proliferation zones in the telencephalon, diencephalon, mesencephalon, and rhombencephalon that were primarily associated with ventricular surfaces in the brain of the African cichlid fish Astatotilapia burtoni. Cell migration was evident in some regions by 1 day post injection, and many newborn cells coexpressed the neuronal marker HuC/D at 30 days, suggesting they had differentiated into neurons. To test the hypothesis that social status and perception of an opportunity to rise in rank influenced cell proliferation, we compared numbers of BrdU-labeled cells in multiple brain nuclei among fish of different social status. Socially suppressed subordinate males had the lowest numbers of proliferating cells in all brain regions examined, but males that were given an opportunity to rise in status had higher cell proliferation rates within 1 day, suggesting rapid upregulation of brain mitotic activity associated with this social transition. Furthermore, socially isolated dominant males had similar numbers of BrdU-labeled cells compared with dominant males that were housed in a socially rich environment, suggesting that isolation has little effect on proliferation and that reduced proliferation in subordinates is a result of the social subordination. These results suggest that A. burtoni will be a useful model to analyze the mechanisms of socially induced neurogenesis in vertebrates.

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Repeated brief social defeat episodes in mice: Effects on cell proliferation in the dentate gyrus

Cited by 79 publications

References 80 publications

Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance

Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance

Social regulation of adult neurogenesis in a eusocial mammal

Characterization of cell proliferation throughout the brain of the African cichlid fish Astatotilapia burtoni and its regulation by social status

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