Behavioral phenotype of C57Bl/6 mice that endured bullying during infant age period
Daria M. Kuzmina , Nina A. Eremeeva , Natalia A. Schelchkova , Irina V. Mukhina
Genes & Cells ›› 2023, Vol. 18 ›› Issue (4) : 353 -367.
Behavioral phenotype of C57Bl/6 mice that endured bullying during infant age period
BACKGROUND: According to UNESCO data for 2018, every third student is involved in bullying. To study the impact of social conflicts on the state of the nervous system the K. Michek model of chronic social stress was used, but the study of the effects of chronic social stress on prepubertal animals has not been conducted.
AIM: To analyze the effect of chronic stress in infant age period to the behavioral phenotype of C57Bl/6 mice in early and long-term periods.
MATERIALS AND METHODS: The objects of the study were male C57Bl/6 mice (n=48). For bullying modeling we chose chronic social stress in infant age period from 20 to 29 postnatal day (P20–P29) according to the “resident–intruder” scheme. Mice were divided into two subgroups to study the early (P31–P35, infant age period) and long-term (P57–P74, adulthood) consequences of chronic social stress. For the behavioral phenotyping we used the following tests: “open field” test, three-chamber social test, object recognition test, passive avoidance task and Barnes maze.
RESULTS: Bullying modeling led to the changes in the behavioral phenotype both in infant age and in adulthood. The behavioral phenotype in infant age period was characterized by increased social activity and recognition, high anxiety, decreased locomotor and exploratory activity, impaired recognition of inanimate objects, but good characteristics of learning, working and long-term memory. In adulthood, the behavioral phenotype of mice retained high anxiety, low level of exploratory activity, good learning and memory characteristics, decline in social recognition in three-chamber test, while the recognition of inanimate objects was preserved at the same level.
CONCLUSION: Chronic social stress in infant age in a mouse model of bullying causes disruption of the behavioral phenotype in infant and adult age. Features of the behavioral phenotype of mice after bullying were an increase in anxiety and social isolation against the background of the ability to learn and good memory.
bullying / social defeat / behavior / memory / learning
| [1] |
Alexandre C, Di Lodovico L, Szöke A, Schürhoff F. Défaite sociale et schizophrénie: hypothèses, arguments, mécanismes. Encephale. 2021;47(3):238–245. doi: 10.1016/j.encep.2020.07.005 |
| [2] |
Alexandre C., Di Lodovico L., Szoke A., Schürhoff F. Défaite sociale et schizophrénie: hypothèses, arguments, mécanismes // Encephale. 2021. Vol. 47, N 3. P. 238–245. doi: 10.1016/j.encep.2020.07.005 |
| [3] |
Armitage R. Bullying in children: impact on child health. BMJ Paediatr Open. 2021;5(1):e000939. doi: 10.1136/bmjpo-2020-000939 |
| [4] |
Armitage R. Bullying in children: impact on child health // BMJ Paediatr Open. 2021. Vol. 5, N 1. P. e000939. doi: 10.1136/bmjpo-2020-000939 |
| [5] |
LeMoult J, Humphreys KL, Tracy A, et al. Meta-analysis: exposure to early life stress and risk for depression in childhood and adolescence. J Am Acad Child Adolesc Psychiatry. 2020;59(7):842–855. doi: 10.1016/j.jaac.2019.10.011 |
| [6] |
LeMoult J., Humphreys K. L., Tracy A., et al. Meta-analysis: exposure to early life stress and risk for depression in childhood and adolescence // J Am Acad Child Adolesc Psychiatry. 2020. Vol. 59. N 7. P. 842–855. doi: 10.1016/j.jaac.2019.10.011 |
| [7] |
Dashuk CV, Dashuk IN. Principles of social and pedagogical organization of support groups of victims of school bullying. Science and School. 2019(2):190–197. (In Russ). |
| [8] |
Дашук К.В., Дашук И.Н. Принципы социально-педагогической организации групп поддержки жертв школьного буллинга // Наука и школа. 2019. Т. 2. С. 190–197. |
| [9] |
Shetgiri R. Bullying and victimization among children. Adv Pediatr. 2013;60(1):33–51. doi: 10.1016/j.yapd.2013.04.004 |
| [10] |
Shetgiri R. Bullying and victimization among children // Adv Pediatr. 2013. Vol. 60, N 1. P. 33–51. doi: 10.1016/j.yapd.2013.04.004 |
| [11] |
Arhuis-Inca W, Ipanaqué-Zapata M, Bazalar-Palacios J, et al. Violence at school and bullying in school environments in Peru: analysis of a virtual platform. Front Psychol. 2021;11:543991. doi: 10.3389/fpsyg.2020.543991 |
| [12] |
Arhuis-Inca W., Ipanaqué-Zapata M., Bazalar-Palacios J., et al. Violence at school and bullying in school environments in Peru: analysis of a virtual platform // Front Psychol. 2021. Vol. 11, N 543991. doi: 10.3389/fpsyg.2020.543991 |
| [13] |
Fisher K, Cassidy B, Mitchell AM. Bullying: effects on school-aged children, screening tools, and referral sources. J Community Health Nurs. 2017;34(4):171–179. doi: 10.1080/07370016.2017.1369801 |
| [14] |
Fisher K., Cassidy B., Mitchell A.M. Bullying: effects on school-aged children, screening tools, and referral sources // J Community Health Nurs. 2017. Vol. 34, N 4. P. 171–179. doi: 10.1080/07370016.2017.1369801 |
| [15] |
Wolke D, Lereya ST. Long-term effects of bullying. Arch Dis Child. 2015;100(9):879–885. doi: 10.1136/archdischild-2014-306667 |
| [16] |
Wolke D., Lereya S.T. Long-term effects of bullying // Arch Dis Child. 2015. Vol. 100, N 9. P. 879–885. doi: 10.1136/archdischild-2014-306667 |
| [17] |
Carnevali L, Montano N, Tobaldini E, et al. The contagion of social defeat stress: Insights from rodent studies. Neurosci Biobehav Rev. 2020;111:12–18. doi: 10.1016/j.neubiorev.2020.01.011 |
| [18] |
Carnevali L., Montano N., Tobaldini E., et al. The contagion of social defeat stress: Insights from rodent studies // Neurosci Biobehav Rev. 2020. Vol. 111. P. 12–18. doi: 10.1016/j.neubiorev.2020.01.011 |
| [19] |
Ferle V, Repouskou A, Aspiotis G, et al. Synergistic effects of early life mild adversity and chronic social defeat on rat brain microglia and cytokines. Physiol Behav. 2020;215:112791. doi: 10.1016/j.physbeh.2019.112791 |
| [20] |
Ferle V., Repouskou A., Aspiotis G., et al. Synergistic effects of early life mild adversity and chronic social defeat on rat brain microglia and cytokines // Physiol Behav. 2020. Vol. 215. P. 112791. doi: 10.1016/j.physbeh.2019.112791 |
| [21] |
Iñiguez SD, Riggs LM, Nieto SJ, et al. Social defeat stress induces a depression-like phenotype in adolescent male c57BL/6 mice. Stress. 2014;17(3):247–255. doi: 10.3109/10253890.2014.910650 |
| [22] |
Iñiguez S.D., Riggs L.M., Nieto S.J., et al. L. Social defeat stress induces a depression-like phenotype in adolescent male c57BL/6 mice // Stress. 2014. Vol. 17, N 3. P. 247–255. doi: 10.3109/10253890.2014.910650 |
| [23] |
Warren BL, Mazei-Robison MS, Robison AJ, Iñiguez SD. Can I get a witness? Using vicarious defeat stress to study mood-related illnesses in traditionally understudied populations. Biol Psychiatry. 2020;88(5):381–391. doi: 10.1016/j.biopsych.2020.02.004 |
| [24] |
Warren B.L., Mazei-Robison M.S., Robison A.J., Iñiguez S.D. Can I get a witness? Using vicarious defeat stress to study mood-related illnesses in traditionally understudied populations // Biol Psychiatry. 2020. Vol. 88, N 5. P. 381–391. doi: 10.1016/j.biopsych.2020.02.004 |
| [25] |
Patel D, Anilkumar S, Chattarji S, Buwalda B. Repeated social stress leads to contrasting patterns of structural plasticity in the amygdala and hippocampus. Behav Brain Res. 2018;347:314–324. doi: 10.1016/j.bbr.2018.03.034 |
| [26] |
Patel D., Anilkumar S., Chattarji S., Buwalda B. Repeated social stress leads to contrasting patterns of structural plasticity in the amygdala and hippocampus // Behav Brain Res. 2018. Vol. 347. P. 314–324. doi: 10.1016/j.bbr.2018.03.034 |
| [27] |
Kinsey SG, Bailey MT, Sheridan JF, et al. Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice. Brain Behav Immun. 2007;21(4):458–466. doi: 10.1016/j.bbi.2006.11.001 |
| [28] |
Kinsey S.G., Bailey M.T., Sheridan J.F., et al. Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice // Brain Behav Immun. 2007. Vol. 21, N 4. P. 458–466. doi: 10.1016/j.bbi.2006.11.001 |
| [29] |
Matsumoto K, Takata K, Yamada D, et al. Juvenile social defeat stress exposure favors in later onset of irritable bowel syndrome-like symptoms in male mice. Sci Rep. 2021;11(1):16276. doi: 10.1038/s41598-021-95916-5 |
| [30] |
Matsumoto K., Takata K., Yamada D., et al. Juvenile social defeat stress exposure favors in later onset of irritable bowel syndrome-like symptoms in male mice // Sci Rep. 2021. Vol. 11, N 1. P. 16276. doi: 10.1038/s41598-021-95916-5 |
| [31] |
Mancini GF, Marchetta E, Pignani I, et al. Social defeat stress during early adolescence confers resilience against a single episode of prolonged stress in adult rats. Cells. 2021;10(2):360. doi: 10.3390/cells10020360 |
| [32] |
Mancini G.F., Marchetta E., Pignani I., et al. Social defeat stress during early adolescence confers resilience against a single episode of prolonged stress in adult rats // Cells. 2021. Vol. 10, N 2. P. 360. doi: 10.3390/cells10020360 |
| [33] |
Zhao T, Gao XL, Huang GB. Effects of chronic social defeat stress on behavior and dopamine receptors in adolescent mice with 6-hydroxydopamine lesions of the medial prefrontal cortex. Front Behav Neurosci. 2021;12:731373. doi: 10.3389/fnbeh.2021.731373 |
| [34] |
Zhao T., Gao X.L., Huang G.B. Effects of chronic social defeat stress on behavior and dopamine receptors in adolescent mice with 6-hydroxydopamine lesions of the medial prefrontal cortex // Front Behav Neurosci. 2021. Vol. 15. P. 731373. doi: 10.3389/fnbeh.2021.731373 |
| [35] |
Hanson JL, Williams AV, Bangasser DA, Peña CJ. Impact of early life stress on reward circuit function and regulation. Front Psychiatry. 2021;15:744690. doi: 10.3389/fpsyt.2021.744690 |
| [36] |
Hanson J.L., Williams A.V., Bangasser D.A., Peña C.J. Impact of early life stress on reward circuit function and regulation // Front Psychiatry. 2021. Vol. 12. P. 744690. doi: 10.3389/fpsyt.2021.744690 |
| [37] |
Moore SE, Norman RE, Suetani S, et al. Consequences of bullying victimization in childhood and adolescence: a systematic review and meta-analysis. World J Psychiatry. 2017;7(1):60–76. doi: 10.5498/wjp.v7.i1.60 |
| [38] |
Moore S.E., Norman R.E., Suetani S., et al. Consequences of bullying victimization in childhood and adolescence: a systematic review and meta-analysis // World J Psychiatry. 2017. Vol. 7, N 1. P. 60–76. doi: 10.5498/wjp.v7.i1.60 |
| [39] |
Liu Y, Deng SL, Li LX, et al. A circuit from dorsal hippocampal CA3 to parvafox nucleus mediates chronic social defeat stress-induced deficits in preference for social novelty. Sci Adv. 2022;8(8):eabe8828. doi: 10.1126/sciadv.abe8828 |
| [40] |
Liu Y., Deng S.L., Li L.X., et al. A circuit from dorsal hippocampal CA3 to parvafox nucleus mediates chronic social defeat stress-induced deficits in preference for social novelty // Sci Adv. 2022. Vol. 8, N 8. P. eabe8828. doi: 10.1126/sciadv.abe8828 |
| [41] |
Dere E, Ronnenberg A, Tampe B, et al. Cognitive, emotional and social phenotyping of mice in an observer-independent setting. Neurobiol Learn Mem. 2018;150:136–150. doi: 10.1016/j.nlm.2018.02.023 |
| [42] |
Dere E., Ronnenberg A., Tampe B., et al. Cognitive, emotional and social phenotyping of mice in an observer-independent setting // Neurobiol Learn Mem. 2018. Vol. 150. P. 136–150. doi: 10.1016/j.nlm.2018.02.023 |
| [43] |
Franzen M, de Jong PJ, Veling W. Victims of bullying: emotion recognition and understanding. Front Psychol. 2021;12:729835. doi: 10.3389/fpsyg.2021.729835 |
| [44] |
Franzen M., de Jong P.J., Veling W. Victims of bullying: emotion recognition and understanding // Front Psychol. 2021. Vol. 12. P. 729835. doi: 10.3389/fpsyg.2021.729835 |
| [45] |
Poon K. Understanding risk-taking behavior in bullies, victims, and bully victims using cognitive-and emotion-focused approaches. Front Psychol. 2016;7:1838. doi: 10.3389/fpsyg.2016.01838 |
| [46] |
Poon K. Understanding risk-taking behavior in bullies, victims, and bully victims using cognitive-and emotion-focused approaches // Front Psychol. 2016. Vol. 7. P. 1838. doi: 10.3389/fpsyg.2016.01838 |
| [47] |
Hollis F, Kabbaj M. Social defeat as an animal model for depression. ILAR J. 2014;55(2):221–232. doi: 10.1093/ilar/ilu002 |
| [48] |
Hollis F., Kabbaj M. Social defeat as an animal model for depression // ILAR J. 2014. Vol. 55, N 2. P. 221–232. doi: 10.1093/ilar/ilu002 |
| [49] |
Guy A, Lee K, Wolke D. Comparisons between adolescent bullies, victims, and bully-victims on perceived popularity, social impact, and social preference. Front Psychiatry. 2019:10:868. doi: 10.3389/fpsyt.2019.00868 |
| [50] |
Guy A., Lee K., Wolke D. Comparisons between adolescent bullies, victims, and bully-victims on perceived popularity, social impact, and social preference // Front Psychiatry. 2019. Vol. 10. P. 868. doi: 10.3389/fpsyt.2019.00868 |
| [51] |
Jonides J, Lewis RL, Nee DE, et al. The mind and brain of short-term memory. Annu Rev Psychol. 2008;59:193–224. doi: 10.1146/annurev.psych.59.103006.093615 |
| [52] |
Jonides J., Lewis R.L., Nee D.E., et al. The mind and brain of short-term memory // Annu Rev Psychol. 2008. Vol. 59. P. 193–224. doi: 10.1146/annurev.psych.59.103006.093615 |
| [53] |
Russo SJ, Murrough JW, Han MH, et al. Neurobiology of resilience. Nat Neurosci. 2012;15(11):1475–1484. doi: 10.1038/nn.3234 |
| [54] |
Russo S.J., Murrough J.W., Han M.H., et al. Neurobiology of resilience // Nat Neurosci. 2012. Vol. 15, N 11. P. 1475–1484. doi: 10.1038/nn.3234 |
| [55] |
Denninger JK, Smith BM, Kirby ED. Novel object recognition and object location behavioral testing in mice on a budget. J Vis Exp. 2018;(141):e58593. doi: 10.3791/58593 |
| [56] |
Denninger J.K., Smith B.M., Kirby E.D. Novel object recognition and object location behavioral testing in mice on a budget // J Vis Exp. 2018. N 141. P. e58593. doi: 10.3791/58593 |
| [57] |
Vaillancourt T, Duku E, Becker S, et al. Peer victimization, depressive symptoms, and high salivary cortisol predict poorer memory in children. Brain Cogn. 2011;77(2):191–199. doi: 10.1016/j.bandc.2011.06.012 |
| [58] |
Vaillancourt T., Duku E., Becker S., et al. Peer victimization, depressive symptoms, and high salivary cortisol predict poorer memory in children // Brain Cogn. 2011. Vol. 77, N 2. P. 191–199. doi: 10.1016/j.bandc.2011.06.012 |
| [59] |
Medeiros W, Torro-Alves N, Malloy-Diniz LF, Minervino CM. Executive functions in children who experience bullying situations. Front Psychol. 2016;7:1197. doi: 10.3389/fpsyg.2016.01197 |
| [60] |
Medeiros W., Torro-Alves N., Malloy-Diniz L.F., Minervino C.M. Executive functions in children who experience bullying situations // Front Psychol. 2016. Vol. 7. P. 1197. doi: 10.3389/fpsyg.2016.01197 |
| [61] |
Lagace DC, Donovan MH, DeCarolis NA, et al. Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance. Proc Natl Acad Sci U S A. 2010;107(9):4436–4441. doi: 10.1073/pnas.0910072107 |
| [62] |
Lagace D.C., Donovan M.H., DeCarolis N.A., et al. J. Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance // Proc Natl Acad Sci U S A. 2010. Vol. 107, N 9. P. 4436–4441. doi: 10.1073/pnas.0910072107 |
| [63] |
Chen Sh, He L, Huang AJY, et al. A hypothalamic novelty signal modulates hippocampal memory. Nature. 2020;586(7828):270–274. doi: 10.1038/s41586-020-2771-1 |
| [64] |
Chen Sh., He L., Huang A.J.Y., et al. A hypothalamic novelty signal modulates hippocampal memory // Nature. 2020. Vol. 586, N 7828. P. 270–274. doi: 10.1038/s41586-020-2771-1 |
| [65] |
Blaser R, Heyser C. Spontaneous object recognition: a promising approach to the comparative study of memory. Front Behav Neurosci. 2015;9:183. doi: 10.3389/fnbeh.2015.00183 |
| [66] |
Blaser R., Heyser C. Spontaneous object recognition: a promising approach to the comparative study of memory // Front Behav Neurosci. 2015. Vol. 9. P. 183. doi: 10.3389/fnbeh.2015.00183 |
| [67] |
Young-Jones A, Fursa S, Byrket JS, Sly JS. Bullying affects more than feelings: the long-term implications of victimization on academic motivation in higher education. Social Psychol Educ. 2015;18(1):185–200. doi: 10.1007/s11218-014-9287-1 |
| [68] |
Young-Jones A., Fursa S., Byrket J.S., Sly J.S. Bullying affects more than feelings: the long-term implications of victimization on academic motivation in higher education // Social Psychol Educ. 2015. Vol. 18, N 1. P. 185–200. doi: 10.1007/s11218-014-9287-1 |
Eco-Vector
/
| 〈 |
|
〉 |