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A Social Network Approach Reveals Associations between Mouse Social Dominance and Brain Gene Expression
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Modelling complex social behavior in the laboratory is challenging and requires analyses of dyadic interactions occurring over time in a physically and socially complex environment. In the current study, we approached the analyses of complex social interactions in group-housed male CD1 mice living in a large vivarium. Intensive observations of social interactions during a 3-week period indicated that male mice form a highly linear and steep dominance hierarchy that is maintained by fighting and chasing behaviors. Individual animals were classified as dominant, sub-dominant or subordinate according to their David's Scores and I& SI ranking. Using a novel dynamic temporal Glicko rating method, we ascertained that the dominance hierarchy was stable across time. Using social network analyses, we characterized the behavior of individuals within 66 unique relationships in the social group. We identified two individual network metrics, Kleinberg's Hub Centrality and Bonacich's Power Centrality, as accurate predictors of individual dominance and power. Comparing across behaviors, we establish that agonistic, grooming and sniffing social networks possess their own distinctive characteristics in terms of density, average path length, reciprocity out-degree centralization and out-closeness centralization. Though grooming ties between individuals were largely independent of other social networks, sniffing relationships were highly predictive of the directionality of agonistic relationships. Individual variation in dominance status was associated with brain gene expression, with more dominant individuals having higher levels of corticotropin releasing factor mRNA in the medial and central nuclei of the amygdala and the medial preoptic area of the hypothalamus, as well as higher levels of hippocampal glucocorticoid receptor and brain-derived neurotrophic factor mRNA. This study demonstrates the potential and significance of combining complex social housing and intensive behavioral characterization of group-living animals with the utilization of novel statistical methods to further our understanding of the neurobiological basis of social behavior at the individual, relationship and group levels.
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“In some studies the subordinates form linear hierarchies, 136,138,141 while in others ranking is more despotic.80,97,142”
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ResultHow feedback and feed‐forward mechanisms link determinants of social dominance
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A Multiparadigm Approach to Characterize Dominance Behaviors in CD1 and C57BL6 Male Mice
Cum, M., Pérez, J. A. S., Iwata, R. L., Lopez, N., Higgs, A., Li, A., Ye, C., Wangia, E., Wright, E. S., Restrepo, C. G., et al. (2024) · eNeuro · doi:10.1523/eneuro.0342-24.2024 · Cited by 20
“…inbred male C57BL/6 (C57) mice and outbred male CD1 mice because they are commonly used in social neuroscience studies (Varholick et al., 2021; Cum et al., 2024) and form stable linear hierarchies (Wang et al., 2011; So et al., 2015; Williamson et al., 2016; Zhou et al., 2017; W. Lee et al., 2022).”
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Trade-offs between fighting and breeding: a social network analysis of bison male interactions
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“There is growing use of social network analysis to quantify the dominance relationships in social species, especially when dominance relationships are nonlinear, because the formation of dominance relationships is more nuanced than previously believed (Chase et al. 2002; So et al. 2015).”
Stress Varies Along the Social Density Continuum
Love, J., & Zelikowsky, M. (2020) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2020.582985 · Cited by 15
“Work that incorporates network science approaches to understand the effects of social density and social connectivity on the brain and behavior are likely to significantly advance the field (e.g., So et al., 2015; Williamson et al., 2016).”
BackgroundAlonso, L., Peeva, P., Ramos-Prats, A., Alenina, N. V., Winter, Y., & Rivalan, M. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112188 · Cited by 13
Ferrara, N. C., Trask, S., Ritger, A. C., Padival, M., & Rosenkranz, J. A. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.956102 · Cited by 11
“Further, individual differences in fighting and chase versus investigation-like behaviors contribute to dynamic social hierarchies, highlighting the importance of individual differences and perhaps a balance in these behaviors that may promote shifts in social preference (So et al., 2015).”
BackgroundWritten informed consent in health research is outdated
Broekstra, R., Maeckelberghe, E. L. M., & Stolk, R. P. (2016) · European Journal of Public Health · doi:10.1093/eurpub/ckw198 · Cited by 12
How can ethology inform the neuroscience of fear, aggression and dominance?
Battivelli, D., Fan, Z., Hu, H., & Gross, C. T. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00858-2 · Cited by 11
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The impact of cage dividers on mouse aggression, dominance and hormone levels
Streiff, C., Herrera, A., Voelkl, B., Palme, R., Würbel, H., & Novak, J. (2024) · PLoS ONE · doi:10.1371/journal.pone.0297358 · Cited by 10
“To cope with enforced proximity with conspecifics and to avoid escalated aggression [2], both male and female mice form dominance hierarchies [3, 4].”
BackgroundHonorio, R., Châline, N., & Chameron, S. (2019) · Animal Behaviour · doi:10.1016/j.anbehav.2019.09.007 · Cited by 10
“In our study, following the guidelines of 209 Glickman (1999; and see So et al., 2015), we used a value of 1 for ‘c’.”
MethodThönnes, M., Prause, R., Levavi‐Sivan, B., & Pfennig, F. (2022) · PLoS ONE · doi:10.1371/journal.pone.0268140 · Cited by 9
“Most studies focusing on gene expression in social phenomena like dominance have looked at the brain as a whole [55, 56, 75, 80].”
BackgroundThe genomic case against genetic determinism
Robinson, G. E., Bliss, R., & Hudson, M. E. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002510 · Cited by 9
Krüppel-homologue 1 Mediates Hormonally Regulated Dominance Rank in a Social Bee
Pandey, A., & Bloch, G. (2021) · Biology · doi:10.3390/biology10111188 · Cited by 9
Tsuda, M. C., Nagata, K., Sagoshi, S., & Ogawa, S. (2018) · Integrative Zoology · doi:10.1111/1749-4877.12343 · Cited by 9
Shaping the development of complex social behavior
Curley, J. P., & Champagne, F. A. (2023) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15076 · Cited by 7
Self-citationCollective Housing of Mice of Different Age Groups before Maturity Affects Mouse Behavior
Ueno, H., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Takahashi, Y., Matsumoto, Y., Okamoto, M., & Ishihara, T. (2020) · Behavioural Neurology · doi:10.1155/2020/6856935 · Cited by 8
“An advantage hierarchy based on combat and tracking has been identified in this context, and the hostile relationships of these mice were organized [39].”
BackgroundMarkov-Modulated Hawkes Processes for Sporadic and Bursty Event OccurrencesPreprint
Wu, J., Ward, O. G., Curley, J. P., & Zheng, T. (2019) · arXiv (Cornell University) · doi:10.48550/arxiv.1903.03223 · Cited by 8
“Given a set of fights among a group of mice, one can calculate the win/loss matrix, which is a frequency sociomatrix of wins and losses (So et al., 2015).”
BackgroundSelf-citationMilewski, T. M., Lee, W., Young, R. L., Hofmann, H. A., & Curley, J. P. (2025) · PLoS Genetics · doi:10.1371/journal.pgen.1011548 · Cited by 7
Self-citationInduction of territorial dominance and subordination behaviors in laboratory mice
Battivelli, D., Boldrini, L., Jaiswal, M., Patil, P., Torchia, S., Engelen, E., Spagnoletti, L., Kaspar, S., & Gross, C. T. (2024) · Scientific Reports · doi:10.1038/s41598-024-75545-4 · Cited by 9
A social switch: daylength drives meadow vole group dynamics in automatically tracked habitats
Power, K. C., Lee, N. S., Rendon-Torres, K., Soergel, D. A. W., & Beery, A. K. (2025) · Animal Behaviour · doi:10.1016/j.anbehav.2025.123084 · Cited by 6
Wu, J., Ward, O. G., Curley, J. P., & Zheng, T. (2022) · The Annals of Applied Statistics · doi:10.1214/21-aoas1539 · Cited by 6
“Given a set of fights among a group of mice, one can calculate the win/loss matrix, which is a frequency sociomatrix of wins and losses (So et al., 2015).”
BackgroundSelf-citationMigliaro, M., Sánchez‐Zavaleta, R., Soto‐Tinoco, E., Ruiz‐Contreras, A. E., Méndez‐Díaz, M., Herrera-Solís, A., de la Mora, M. P., & Prospero-Garcia, O. E. (2022) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2022.173483 · Cited by 6
Meloni, E. G., Carlezon, W. A., & Bolshakov, V. Y. (2024) · Scientific Reports · doi:10.1038/s41598-024-59459-9 · Cited by 7
Ghahramani, Z. N., Perelmuter, J. T., Varughese, J., Kyaw, P., Palmer, W. C., Sisneros, J. A., & Forlano, P. M. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.113745 · Cited by 4
“The null hypothesis under QAP entails no association between the two matrices being compared, hence an insignificant p-value indicates that they are different [42,57 – 60].”
BackgroundMethodHiadlovská, Z., Hamplová, P., Berchová‐Bímová, K., Macholán, M., & Bímová, B. V. (2021) · Behavioural Processes · doi:10.1016/j.beproc.2021.104316 · Cited by 5
Guilherme, M. D. S., Tsoutsouli, T., Todorov, H., Teifel, S., Nguyen, V. T. T., Gerber, S., & Endres, K. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.705986 · Cited by 5
“Another example is the higher mRNA expression of CRF in the medial amygdala and hypothalamus of more dominant outbred CD1 male mice (So et al., 2015).”
BackgroundHou, W., Ma, H., Huang, C., Yin, L., Li, L., Zhang, L., Qu, Y., Xun, Y., Yang, Q., He, Z., et al. (2024) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105536 · Cited by 4
Differential expression of Hdac2 in male and female mice of differing social status
Douglas, R. S., Hartley, M. R., Yang, J., & Franklin, T. B. (2023) · Physiology & Behavior · doi:10.1016/j.physbeh.2023.114406 · Cited by 5
Conspecific interactions predict social transmission of fear in female rats
Seese, S., Tinsley, C. E., Wulffraat, G. C., Hixon, J. G., & Monfils, M. (2024) · Scientific Reports · doi:10.1038/s41598-024-58258-6 · Cited by 5
Han, M., Luo, H., Bai, Y., Zheng, S., Li, F., Fu, J., Jiang, S., Liu, Z., & Zheng, X. (2019) · Stress · doi:10.1080/10253890.2019.1702642 · Cited by 4
“…could not discriminate the specific “nature” of the “active social interactions”, e.g. the affiliative social behaviors (such as sniffing, crawling and following) and agonistic behaviors (such as fighting), the time engaged in these two kinds of behaviors was calculated manually (So et al., 2015).”
BackgroundGrossel, L. A., Javorouski, M. L., Moreira, N., & Monteiro‐Filho, E. L. A. (2021) · acta ethologica · doi:10.1007/s10211-021-00386-7 · Cited by 4
BlueBerry: Closed-loop wireless optogenetic manipulation in freely moving animalsPreprint
Nourizonoz, A., Girard, B. J. T., Guyoton, M., Galiñanes, G. L., Thurnherr, R., Pellat, S., Bellone, C., & Huber, D. (2025) · eLife · doi:10.1101/2025.01.30.635697 · Cited by 5
“Characterized by dominance and submission relationships, they influence social interactions, often presented as asymmetric agonistic behaviors such as chasing and aggression (Wang et al. 2011; So et al. 2015).”
Metadata
- Authors
- So, N., Franks, B., Lim, S., & Curley, J. P.
- Affiliations
- Columbia University (US)
- University of British Columbia (CA)
- Corresponding author
- Curley, James P.
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-07-30
- Volume
- 10
- Issue
- 7
- Pages
- e0134509
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4520683
- OpenAlex
- W1852628838
- Cited by
- 135
- References
- 114
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 15 · 2023: 10 · 2022: 17 · 2021: 17 · 2020: 14 · 2019: 15 · 2018: 16 · 2017: 6 · 2016: 9
- FWCI
- 16.91
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Columbia Academic Commons (Columbia University)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- social dominance, dominance hierarchy, social network analysis, mouse social behavior, ICR mice, grooming, sniffing, agonistic behavior, corticotropin-releasing factor, amygdala, medial preoptic area, hippocampus, glucocorticoid receptor, brain-derived neurotrophic factor, gene expression
- MeSH terms
- Animals, Brain, Gene Expression Regulation, Male, Social Behavior, Social Dominance, Mice, Real-Time Polymerase Chain Reaction
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