Social regulation of adult neurogenesis in a eusocial mammal

Peragine, D.E.; Simpson, J.A.; Mooney, S.J.; Lovern, M.B.; Holmes, M.M.

doi:10.1016/j.neuroscience.2014.02.044

Cited by 37Neurogenesis and neuroplasticity mechanismsStress Responses and CortisolNeuroendocrine regulation and behavior

Social regulation of adult neurogenesis in a eusocial mammal

Peragine, D.E., Simpson, J.A., Mooney, S.J., Lovern, M.B., Holmes, M.M.·2014·Neuroscience

DOI 10.1016/j.neuroscience.2014.02.044

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Abstract

The present study examined the effects of social status on adult neurogenesis in an extreme cooperative breeder: the naked mole rat. These animals live in large colonies of up to 300 individuals, with a strict reproductive dominance hierarchy; one female and one to three males breed, and all other members are socially subordinate and reproductively suppressed. We examined the effects of social and gonadal cues on doublecortin (DCX; a marker for immature neurons) immunoreactivity in the dentate gyrus (DG), piriform cortex (PCx) and basolateral amygdala (BLA) by comparing dominant breeding animals to non-breeding subordinates from intact colonies. We also examined DCX expression in subordinate animals that had been removed from their colony and paired with an opposite- or same-sex conspecific for 6months. Compared to subordinates, dominant breeders had significantly reduced DCX immunoreactivity in all brain areas, with BLA effects confined to females. By contrast, the effects of same- versus opposite-sex housing were region-specific. In the DG and PCx, more DCX immunoreactivity was observed for opposite- than same-sex-paired subordinates. Conversely, same-sex-paired females had more DCX immunoreactivity than opposite-sex-paired females in the BLA. Gonadectomy did not affect DCX expression in opposite-sex-paired animals, and no significant relationships between gonadal steroids and DCX immunoreactivity were detected, suggesting that group differences in neurogenesis are independ…

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Dominant rats show enhanced adult neurogenesis in the ventral dentate gyrus; effect also shown in baboons.
“Specifically, dominant rats show enhanced adult neurogenesis in the ventral dentate gyrus of the hippocampal formation, an effect that also has been shown in baboons (Kozorovitskiy and Gould, 2004, Peragine et al., 2014, Wu et al., 2014).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Peragine et al., 2014

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Properties of Doublecortin-(DCX)-Expressing Cells in the Piriform Cortex Compared to the Neurogenic Dentate Gyrus of Adult Mice
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Both pre- and posttraining excitotoxic lesions of the basolateral amygdala abolish the expression of olfactory and contextual fear conditioning.
Cousens, G. A., & Otto, T. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.5.1092 · Cited by 136 · see citing works
Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle
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Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late antidepressant treatment
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19‐Nortestosterone influences neural stem cell proliferation and neurogenesis in the rat brain
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Estradiol enhances neurogenesis in the dentate gyri of adult male meadow voles by increasing the survival of young granule neurons
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Increased Number of BrdU-Labeled Neurons in the Rostral Migratory Stream of the Estrous Prairie Vole
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Male pheromones initiate prolactin-induced neurogenesis and advance maternal behavior in female mice
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Androgens Increase Survival of Adult-Born Neurons in the Dentate Gyrus by an Androgen Receptor-Dependent Mechanism in Male Rats
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Disruption of Adult Neurogenesis in the Olfactory Bulb Affects Social Interaction but not Maternal Behavior
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Chemical characterization of newly generated neurons in the striatum of adult primates
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Stress coping stimulates hippocampal neurogenesis in adult monkeys
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Intracolony aggression in the eusocial naked mole-rat, Heterocephalus glaber
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Age-dependent susceptibility of adult hippocampal cell proliferation to chronic psychosocial stress
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Estrogen regulation of cell proliferation and distribution of estrogen receptor‐α in the brains of adult female prairie and meadow voles
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Social control of reproduction in breeding and non-breeding male naked mole-rats ( Heterocephalus glaber )
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Social stress-related behavior affects hippocampal cell proliferation in mice
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Repeated brief social defeat episodes in mice: Effects on cell proliferation in the dentate gyrus
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Investigation of numbers and motility of spermatozoa in reproductively active and socially suppressed males of two eusocial African mole-rats, the naked mole-rat ( Heterocephalus glaber ) and the Damaraland mole-rat ( Cryptomys damarensis )
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LH responses of female naked mole-rats, Heterocephalus glaber , to single and multiple doses of exogenous GnRH
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Basolateral amygdala regulation of adult hippocampal neurogenesis and fear-related activation of newborn neurons
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Progesterone promotes the survival of newborn neurons in the dentate gyrus of adult male mice
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Evidence that primer pheromones do not cause social suppression of reproduction in male and female naked mole-rats (Heterocephalus glaber).
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Characterization of cell proliferation throughout the brain of the African cichlid fish Astatotilapia burtoni and its regulation by social status
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Origin, migration and fate of newly generated neurons in the adult rodent piriform cortex
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Extinction of a conditioned response in rainbow trout selected for high or low responsiveness to stress
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Neurogenesis in the rat primary olfactory cortex
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Neuroendocrinology and sexual differentiation in eusocial mammals
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Anatomical evidence for transsynaptic influences of estrogen on brain‐derived neurotrophic factor expression
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Reproductive status influences the survival of new cells in the dentate gyrus of adult male meadow voles
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Integration and sensory experience‐dependent survival of newly‐generated neurons in the accessory olfactory bulb of female mice
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Newborn Interneurons in the Accessory Olfactory Bulb Promote Mate Recognition in Female Mice
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Behavioral and Hormonal Changes in Female Naked Mole-Rats (Heterocephalus glaber) Following Removal of the Breeding Female from a Colony
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The Social Environment and Neurogenesis in the Adult Mammalian Brain
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Neural plasticity is affected by stress and heritable variation in stress coping style
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Where's my dinner? Adult neurogenesis in free‐living food‐storing rodents
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Role of adult neurogenesis in hippocampus-dependent memory, contextual fear extinction and remote contextual memory: New insights from ERK5 MAP kinase
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The dynamics of growth in naked mole‐rats: the effects of litter order and changes in social structure
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Dominance‐related changes in spatial memory are associated with changes in hippocampal cell proliferation rates in mountain chickadees
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Estrogen Receptor Immunoreactivity in Specific Brain Areas of the Prairie Vole (Microtus ochrogaster) is Altered by Sexual Receptivity and Genetic Sex
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Sexually dimorphic neurogenesis is topographically matched with the anterior accessory olfactory bulb of the adult rat
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Social status and sex independently influence androgen receptor expression in the eusocial naked mole-rat brain
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Olfactory Bulb Cells Generated in Adult Male Golden Hamsters Are Specifically Activated by Exposure to Estrous Females
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Growing out of a caste - reproduction and the making of the queen mole-rat
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Olfactory enrichment enhances the survival of newly born cortical neurons in adult mice
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Male-female associations and female olfactory neurogenesis with pair bonding in Mus spicilegus
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Paced-Mating Increases the Number of Adult New Born Cells in the Internal Cellular (Granular) Layer of the Accessory Olfactory Bulb
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Socially regulated reproductive development: Analysis of GnRH‐1 and kisspeptin neuronal systems in cooperatively breeding naked mole‐rats (Heterocephalus glaber)
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Repeated clomipramine treatment reversed the inhibition of cell proliferation in adult hippocampus induced by chronic unpredictable stress
Liu, Q., Yu, J. M., Mao-Ying, Q.-L., Mi, W.-L., Li, B., Yq, W., Wang, J., & Wu, G. (2008) · The Pharmacogenomics Journal · doi:10.1038/sj.tpj.6500485 · Cited by 35 · see citing works
Sexual Behaviour Induces the Expression of Activity‐Regulated Cytoskeletal Protein and Modifies Neuronal Morphology in the Female Rat Ventromedial Hypothalamus
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Breeding status affects motoneuron number and muscle size in naked mole‐rats: Recruitment of perineal motoneurons?
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Repeated paced mating promotes the arrival of more newborn neurons in the main and accessory olfactory bulbs of adult female rats
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Social condition and oxytocin neuron number in the hypothalamus of naked mole-rats (Heterocephalus glaber)
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Social and hormonal triggers of neural plasticity in naked mole-rats
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Androgen Biosynthesis And Degradation
Chung, B., & Meng-Chun, H. (2002) · Springer eBooks · doi:10.1007/978-1-4615-1161-8_1 · Cited by 10 · see citing works

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Hippocampal learning, memory, and neurogenesis: Effects of sex and estrogens across the lifespan in adults.
Duarte-Guterman, P., Yagi, S., Chow, C., & Galea, L. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.024 · Cited by 194 · see citing works
Adult hippocampal neurogenesis and its impairment in Alzheimer’s disease
Kim, T. A., Syty, M. D., Wu, K., & Ge, S. (2022) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2021.479 · Cited by 114 · see citing works
Adult Hippocampal Neurogenesis in Natural Populations of MammalsPreprint
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Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior
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Astrocyte Hypertrophy Contributes to Aberrant Neurogenesis after Traumatic Brain Injury
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RFamide-related peptide-3 (RFRP-3) suppresses sexual maturation in a eusocial mammal
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Protracted brain development in a rodent model of extreme longevity
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Extended Postnatal Brain Development in the Longest-Lived Rodent: Prolonged Maintenance of Neotenous Traits in the Naked Mole-Rat Brain
Orr, M. E., Garbarino, V. R., Salinas, A., & Buffenstein, R. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00504 · Cited by 55 · see citing works
Stress in groups: Lessons from non-traditional rodent species and housing models
Beery, A. K., Holmes, M. M., Lee, W., & Curley, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.03.033 · Cited by 51 · see citing works
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Methods to study adult hippocampal neurogenesis in humans and across the phylogeny
Terreros‐Roncal, J., Flor‐García, M., Moreno‐Jiménez, E. P., Rodríguez-Moreno, C. B., Márquez‐Valadez, B., Gallardo‐Caballero, M., Rábano, A., & Llorens-Martı́n, M. (2022) · Hippocampus · doi:10.1002/hipo.23474 · Cited by 51 · see citing works
Social regulation of adult neurogenesis: A comparative approach
Holmes, M. M. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.02.001 · Cited by 47 · see citing works
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Adult neurogenesis and its anatomical context in the hippocampus of three mole-rat species
Amrein, I., Becker, A. S., Engler, S., Huang, S., ller, J. M. ⁄., Slomianka, L., & Oosthuizen, M. K. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00039 · Cited by 46 · see citing works
Social dominance differentially alters gene expression in the medial prefrontal cortex without affecting adult hippocampal neurogenesis or stress and anxiety‐like behavior
Pallé, A., Zorzo, C., Luskey, V. E., McGreevy, K. R., Fernández, S., & Trejo, J. L. (2019) · The FASEB Journal · doi:10.1096/fj.201801600r · Cited by 37 · see citing works
The social network: Neural control of sex differences in reproductive behaviors, motivation, and response to social isolation
Zilkha, N., Sofer, Y., Kashash, Y., & Kimchi, T. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.03.005 · Cited by 37 · see citing works
Postnatal and Adult Neurogenesis in Mammals, Including Marsupials
Bartkowska, K., Tepper, B., Turlejski, K., & Djavadian, R. L. (2022) · Cells · doi:10.3390/cells11172735 · Cited by 30 · see citing works
Oxytocin has sex-specific effects on social behaviour and hypothalamic oxytocin immunoreactive cells but not hippocampal neurogenesis in adult rats
Duarte‐Guterman, P., Lieblich, S. E., Qiu, W., Splinter, J. E. J., Go, K. A., Casanueva-Reimon, L., & Galea, L. A. M. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104734 · Cited by 23 · see citing works
Social runaway: Fisherian elaboration (or reduction) of socially selected traits via indirect genetic effects
Bailey, N. W., & Kölliker, M. (2019) · Evolution · doi:10.1111/evo.13791 · Cited by 19 · see citing works
Solving the Neurogenesis Puzzle: Looking for Pieces Outside the Traditional Box
Faykoo-Martinez, M., Toor, I., & Holmes, M. M. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00505 · Cited by 18 · see citing works
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Sex, social status, and CRF receptor densities in naked mole‐rats
Beery, A. K., Bicks, L. K., Mooney, S. J., Goodwin, N. L., & Holmes, M. M. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23834 · Cited by 18 · see citing works
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Adult mammalian neurogenesis and motivated behaviors
Jorgensen, C. (2018) · Integrative Zoology · doi:10.1111/1749-4877.12335 · Cited by 15 · see citing works
Contrasting effects of opposite- versus same-sex housing on hormones, behavior and neurogenesis in a eusocial mammal
Peragine, D. E., Yousuf, Y., Fu, Y., Swift‐Gallant, A., Ginzberg, K., & Holmes, M. M. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.03.005 · Cited by 14 · see citing works
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Trading new neurons for status: Adult hippocampal neurogenesis in eusocial Damaraland mole-rats
Oosthuizen, M. K., & Amrein, I. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.03.020 · Cited by 13 · see citing works
Isolation and characterization of neural stem/progenitor cells in the subventricular zone of the naked mole-rat brain
Yamamura, Y., Kawamura, Y., Oiwa, Y., Oka, K., Onishi, N., Saya, H., & Miura, K. (2021) · Inflammation and Regeneration · doi:10.1186/s41232-021-00182-7 · Cited by 12 · see citing works
Spatial working memory is disparately interrelated with social status through different developmental stages in rats
suha, A. J., Hosseinmardi, N., & Janahmadi, M. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113547 · Cited by 11 · see citing works
Influencing the Social Group
McNamara, G. I., & Isles, A. R. (2014) · Advances in genetics · doi:10.1016/b978-0-12-800222-3.00006-1 · Cited by 8 · see citing works
Comparative neurobiology and genetics of mammalian social behavior
Beery, A. K., Kamal, Y., Sobrero, R., & Hayes, L. D. (2016) · Wiley eBooks · doi:10.1002/9781118846506.ch3 · Cited by 9 · see citing works
From Mice to Mole-Rats: Species-Specific Modulation of Adult Hippocampal Neurogenesis
Oosthuizen, M. K. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00602 · Cited by 8 · see citing works
Brain atlas of the African mole‐ratFukomys anselli
Dollas, A., Oelschläger, H., Begall, S., Burda, H., & Malkemper, E. P. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24647 · Cited by 8 · see citing works
Adult Neural Plasticity in Naked Mole-Rats: Implications of Fossoriality, Longevity and Sociality on the Brain’s Capacity for Change
Mooney, S. J., Forger, N. G., & Holmes, M. M. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65943-1_4 · Cited by 5 · see citing works
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Natural variations of adolescent neurogenesis and anxiety predict the hierarchical status of adult inbred mice
Grieco, F., Balla, A., Larrieu, T., & Toni, N. (2025) · EMBO Reports · doi:10.1038/s44319-025-00367-y · Cited by 4 · see citing works
Adult Neurogenesis and Social Behavior: A Reciprocal Relationship
Jorgensen, C., & Wang, Z. (2024) · Masterclass in neuroendocrinology · doi:10.1007/978-3-031-51112-7_6 · Cited by 2 · see citing works
Protracted neuronal maturation in a long-lived, highly social rodent
Faykoo-Martinez, M., Collins, T. F., Peragine, D. E., Malik, M., Javed, F., Kolisnyk, M., Ziolkowski, J., Jeewa, I., Cheng, A. H., Lowden, C., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0273098 · Cited by 2 · see citing works
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Additional file 3 of Isolation and characterization of neural stem/progenitor cells in the subventricular zone of the naked mole-rat brain
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Additional file 2 of Isolation and characterization of neural stem/progenitor cells in the subventricular zone of the naked mole-rat brain
Yamamura, Y., Kawamura, Y., Oiwa, Y., Oka, K., Onishi, N., Saya, H., & Miura, K. (2021) · Figshare · doi:10.6084/m9.figshare.16911246
Additional file 4 of Isolation and characterization of neural stem/progenitor cells in the subventricular zone of the naked mole-rat brain
Yamamura, Y., Kawamura, Y., Oiwa, Y., Oka, K., Onishi, N., Saya, H., & Miura, K. (2021) · Figshare · doi:10.6084/m9.figshare.16911252

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Holmes, M. M., Rosen, G. J., Jordan, C. L., Vries, G. J. D., Goldman, B. D., & Forger, N. G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610344104 · Cited by 91 · see citing works
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Authors: Peragine, D. E., Simpson, J. A., Mooney, S. J., Lovern, M. B., & Holmes, M. M.
Affiliations: University of Toronto (CA)
Oklahoma State University (US)
Corresponding author: Peragine, D.E.
ORCID: Lovern, M.B.
Holmes, M.M.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 2014-05
Volume: 268
Pages: 10-20
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/j.neuroscience.2014.02.044
OpenAlex: W2031374101
Cited by: 37
References: 148
Citations by year: 2025: 1 · 2024: 2 · 2023: 1 · 2022: 4 · 2021: 7 · 2020: 2 · 2019: 3 · 2018: 1 · 2017: 4 · 2016: 6 · 2015: 4 · 2014: 2
FWCI: 1.85
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
Library and Archives Canada (Government of Canada) (submittedVersion)
TSpace (University of Toronto) (submittedVersion)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords: adult neurogenesis, social status, naked mole-rat, social subordination, doublecortin, gonadal hormones, gonadectomy, dentate gyrus, piriform cortex, basolateral amygdala
MeSH terms: Doublecortin Domain Proteins, Doublecortin Protein, Animals, Castration, Cell Count, Female, Hormones, Housing, Animal, Male, Microtubule-Associated Proteins, Neuropeptides, Photomicrography, Radioimmunoassay, Sexual Behavior, Animal, Sex Characteristics, Social Behavior, Social Dominance, Linear Models, Dentate Gyrus, Mole Rats, Neurogenesis, Piriform Cortex, Basolateral Nuclear Complex

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Social regulation of adult neurogenesis in a eusocial mammal

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