The Neurobiology of Overcrowding
- Авторлар: Grigoryan G.A.1
-
Мекемелер:
- Institute of Higher Nervous Activity and Neurophysiology of RAS
- Шығарылым: Том 56, № 4 (2025)
- Беттер: 105-122
- Бөлім: Articles
- URL: https://ogarev-online.ru/0301-1798/article/view/368086
- DOI: https://doi.org/10.7868/S3034611825040067
- ID: 368086
Дәйексөз келтіру
Аннотация
The present article considers the influence of crowded living of rodents in laboratory conditions on the development of emotional, cognitive and motor changes in behavior. Physiological parameters (body weight gain, state of organs and body systems), locomotor/investigatory activity and manifestations of anxiety and depression-like behavior under crowding are presented. Special attention is paid to the relationship between crowding and stress, changes in learning/memory, and gender-specific behaviors in conditions of crowding. A comparative characterization of isolation stress and crowding is given, highlighting the significant role of “social interaction” as a mitigating influence on the development of stress and other negative consequences. The available biochemical, hormonal, immunological, molecular-cellular and other transformations in the organism under the influence of crowding are also considered in different sections of the article.
Негізгі сөздер
Авторлар туралы
G. Grigoryan
Institute of Higher Nervous Activity and Neurophysiology of RAS
Email: grigorygrigoryan@hotmail.com
ORCID iD: 0000-0003-3769-0570
Doctor of Medical Sciences, Chief Scientist Moscow
Әдебиет тізімі
- Гаврилов В.В., Онуфриев М.В., Моисеева Ю.В., Александров Ю.И., Гуляева Н.В. Хронические социальные стрессы изоляции и скученности у крыс по-разному влияют на научение инструментальному поведению и состояние гипоталамо-гипофизарно-адренокортикальной системы // Журн. высш. нервн. деят. 2021. Т. 71. № 5. С. 710–719.
- Зайченко М.И., Сидорина В.В., Шаркова А.В. и др. Влияние раннего провоспалительного стресса и условий содержания на пространственное обучение и память крыс // XXIV съезд физиологического общества им. И.П. Павлова, г. Санкт-Петербург. 2023. С. 149.
- Лосева Е.В. Психосоциальный стресс перенаселенности (скученности): негативные последствия для организма человека и грызунов // Интегративная физиология. 2021. Т. 2. № 1. С. 33–40. https://doi.org/10.33910/2687-1270-2021-2-1-33-40
- Лосева Е.В., Саркисова К.Ю., Логинова Т.А., Кудрин В.С. Депрессивное поведение и содержание моноаминов в структурах мозга у крыс при хронической скученности // Бюллетень экспериментальной биологии и медицины. 2015. Т. 159. № 3. C. 303–307.
- Павлова И.В., Потехина А.М., Лосева Е.В. Влияние сверхдлительного скученного содержания на обучение крыс в пожилом возрасте // 21-й Международный конгресс «Нейронауки для медицины и физиологии». Судак. Россия. 2025. С. 187–188.
- Adavi H., Kowsar R., Radahmadi M., Alaei H. Comparing various types of chronic psychological stress on cognitive functions and behaviors in rats // Basic Clin. Neurosci. 2024. Vol. 15. P. 301–316. https://doi.org/10.32598/bcn.2023.2346.4
- Ago Y., Tanaka T., Ota Y., Kitamoto M. et al. Social crowding in the night-time reduces an anxiety-like behavior and increases social interaction in adolescent mice // Behav. Brain Res. 2014. Vol. 270. P. 37–46. https://doi.org/10.1016/j.bbr.2014.04.047
- Armario A., Ortiz R., Balasch J. Effect of crowding on some physiological and behavioral variables in adult male rats // Physiology and Behavior. 1984. Vol. 32. P. 35–37. https://doi.org/10.1016/0031-9384(84)90066-0
- Beery A.K., Holmes M.M., Lee W., Curley J.P. Stress in groups: lessons from non-traditional rodent species and housing models // Neurosci. Biobehav. Rev. 2020. Vol. 113. P. 354–372. https://doi.org/10.1016/j.neubiorev.2020.03.033
- Bell R.W., Miller C.E., Ordy J.M., Rolsten C. Effects of population density and living space upon neuroanatomy, neurochemistry, and behavior in the CS7B1/10 mouse // Journal of Comparative and Physiological Psychology. 1971. Vol. 75. P. 258–263.
- Bernatova I., Puzserova A., Balis P. et al. Chronic stress produces persistent increases in plasma corticosterone, reductions in brain and cardiac nitric oxide production, and delayed alterations in endothelial function in young prehypertensive rats // Front. Physiol. 2018. Vol. 9. P. 1179. https://doi.org/10.3389/fphys.2018.01179
- Botelho S., Estanislau C., Morato S. Effects of under- and overcrowding on exploratory behavior in the elevated plus-maze // Behav. Processes. 2007. Vol. 74. P. 357–362. https://doi.org/10.1016/j.beproc.2006.12.006
- Brown K.J., Grunberg N.E. Effects of housing on male and female rats: crowding stresses male but calm females // Physiol. Behav. 1995. Vol. 58. № 6. P. 1085–1089. https://doi.org/10.1016/0031-9384(95)02043-8
- Bubna-Littitz H., Hofecker G., Kment A., Niedermüller H. Gerontological pilot study on learning ability and memory in the stressed rat // Aktuelle Gerontol. 1981. Vol. 11. P. 28–31.
- Bugajski A.J., Gadek-Michalska A., Bugajski J. The involvement of nitric oxide and prostaglandins in the cholinergic stimulation of hypothalamic-pituitary-adrenal response during crowding stress // J. Physiol. Pharmacol. 2006. V. 57. № 3. P. 63–77.
- Bugajski J., Gadek-Michalska A. Effect of cyclooxygenase inhibitors on the vasopressin induced ACTH and corticosterone response during crowding stress // J. Physiol. Pharmacol. 2003. Vol. 54. № 2. P. 247–256.
- Calhoun J.B. Space and the strategy of life // In: Esser AH, ed. Behavior and environment. New York. NY: Plenum Press. 1971.
- Calhoun J.B. Population density and social pathology // Sci. Am. 1962. Vol. 306. P. 139–148.
- Conner H.S., Gregor G.L. Crowding and isolation: determinants of agonistic and food-seeking behavior in Norway rats // J. Comp. Physiol. Psychol. 1973. Vol. 84. № 3. P. 593–597. https://doi.org/10.1037/h0034894
- Daniels W.M., Pietersen C.Y., Carstens M.E., Daya S., Stein D. Overcrowding induces anxiety and causes loss of serotonin 5HT-1a receptors in rats // Metab. Brain Dis. 2000. Vol. 15. № 4. P. 287–295. https://doi.org/10.1023/a:1011123208674
- Deep S.N., Baitharu I., Sharma A. et al. Neuroprotective role of L-NG-nitroarginine methyl ester (L-NAME) against chronic hypobaric hypoxia with crowding stress (CHC) induced depression-like behaviour // PLoS One. 2016. Vol. 11. № 4:e0153371. https://doi.org/10.1371/journal.pone.0153371
- Delaroque C., Chervy M., Gewirtz A.T., Chassaing B. Social overcrowding impacts gut microbiota, promoting stress, inflammation, and dysglycemia // Gut Microbes. 2021. Vol. 13. № 1. P. 2000275. https://doi.org/10.1080/19490976.2021.2000275
- Djordjevic J., Cvijic G., Davidovic V. Different activation of ACTH and corticosterone release in response to various stressors in rats // Physiol. Res. 2003. Vol. 52. P. 67–72.
- Dronjak S., Gavrilović L., Filipović D., Radojcić M.B. Immobilization and cold stress affect sympatho-adrenomedullary system and pituitary-adrenocortical axis of rats exposed to long-term isolation and crowding // Physiol. Behav. 2004. Vol. 81. № 3. P. 409–415. https://doi.org/10.1016/j.physbeh.2004.01.011
- Dugatkin L.A., Dr. Calhoun's Mousery. The strange tale of a celebrated scientist, a rodent dystopia, and the future of humanity. 2024. Chicago Press. https://doi.org/10.7208/chicago/9780226827865
- Freedman J.L. Crowding and behavior // San Francisco. CA: WH Freeman; 1975.
- Gadek-Michalska A., Tadeusz J., Bugajski A., Bugajski J. Chronic isolation stress affects subsequent crowding stress-induced brain nitric oxides synthase (NOS) isoforms and hypothalamic-pituitary-adrenal (HPA) axis responses // Neurotox. Res. 2019. Vol. 36. № 3. P. 523–539. https://doi.org/10.1007/s12640-019-00067-1
- Gadek-Michalska A., Bugajski J. Repeated handling, restraint, or chronic crowding impair the hypothalamic-pituitary-adrenocortical response to acute restraint stress // J. Physiol. Pharmacol. 2003. Vol. 54(3). P. 449–459.
- Gamallo A., Villanua A., Beato M.J. Body weight gain and food intake alterations in crowd-reared rats // Physiol. Behav. 1986. Vol. 36 (5). P. 835–837. https://doi.org/10.1016/0031-9384(86)90439-7
- Gamallo A., Villanua A., Trancho G., Fraile A. Stress adaptation and adrenal activity in isolated and crowded rats // Physiol. Behav. 1986. Vol. 36(2). P. 217–221. https://doi.org/10.1016/0031-9384(86)90006-5
- Geller E., Yuwiller A., Zolman J.F. Effects of environmental complexity on constituents of brain and liver // J. of Neurochemistry. 1965. Vol. 12. P. 949–955.
- Girden E.R. Effect of crowding and litter size on retention and reversal learning by rats // Psychol. Rep. 1982. V. 51(3 Pt 1). P. 935–940. https://doi.org/10.2466/pr0.1982.51.3.935
- Goeckner D.J., Greenough W.T., Mead W.R. Deficits in learning tasks following chronic overcrowding in rats // J. Pers. Soc. Psychol. 1973. Vol. 28(2). P. 256–261. https://doi.org/10.1037/h0035783
- Grigoryan G.A. The systemic effects of the enriched environment on the conditioned fear reaction // Frontiers in Behavioral Neuroscience. 2023. Review article. Front. Behav. Neurosci. 2023. Sec. Learning and Memory. Vol. 17. https://doi.org/10.3389/fnbeh.2023.1227575
- Grigoryan G.A., Pavlova I.V., Zaichenko M.I. Effects of social isolation on the development of anxiety and depression-like behavior in model experiments in animals // Neuroscience and Behavioral Physiology. 2022. Vol. 52 (5). P. 722–738. https://doi.org/10.1007/s11055-022-01297-1
- Grigoryan G.A. Molecular-cellular mechanisms of plastic restructuring produced by an enriched environment. Effects on learning and memory // Neurochemical Journal. 2021. Vol. 15. P. 226–239. © Pleiades Publishing Ltd., 2021. https://doi.org/10.1134/S1819712421030041
- Grippo A.J., Sgoifo A., Mastorci F., McNeal N., Trahanas D.M. Cardiac dysfunction and hypothalamic activation during a social crowding stressor in prairie voles // Auton. Neurosci. 2010. Vol. 156. P. 44–50. https://doi.org/10.1016/j.autneu.2010.03.003
- Hayashi A., Nagaoka M., Yamada K., Ichitani Y., Miake Y., Okado N. Maternal stress induces synaptic loss and developmental disabilities of offspring // Int. J. Dev. Neurosci. 1998. Vol. 16 (3–4). P. 209–216. https://doi.org/10.1016/s0736-5748(98)00028-8
- Jean-Faucher Ch., Berger M., De Turckheim M., Veyssiere G., Jean C. Effects of dense housing on the growth of reproductive organs, plasma testosterone levels and fertility of male mice // J. Endocrinol. 1981. Vol. 90. P. 397–402. https://doi.org/10.1677/joe.0.0900397
- Keely K. Prenatal influence on behavior of offspring of crowded mice // Science. 1962. Vol. 135(3497). P. 44–45. https://doi.org/10.1126/science.135.3497.44.
- Knyazeva S.I., Loginova N.A., Loseva E.V. Anxiety level and body weight changes in rats living in overpopulated cages // Bull. Exp. Biol. Med. 2012. Vol. 154(1). P. 3–6. https://doi.org/10.1007/s10517-012-1860-z
- Kotrschal A., Ilmonen P., Penn D.J. Stress impacts telomere dynamics. Biol. Lett. 2007. Vol. 3 (2). P. 128–130. https://doi.org/10.1098/rsbl.2006.0594
- Lee Y.A., Obora T., Bondonny L. et al. The effects of housing density on social interactions and their correlations with serotonin in rodents and primates // Sci. Rep. 2018. Vol. 8(1). P. 3497. https://doi.org/10.1038/s41598-018-21353-6
- Levitt L., Bennet T.L. Effects of population density on emotionality and transfer of perceptual learning in rats // Psychonomic Science. 1972. Vol. 29. P. 52–54.
- Lin E.J., Sun M., Choi E.Y. et al. Social overcrowding as a chronic stress model that increases adiposity in mice // Psychoneuroendocrinology. 2015. Vol. 51. P. 318–330. https://doi.org/10.1016/j.psyneuen.2014.10.007
- Loseva E.V., Loginova N.A., Potekhina A.A. et al. Effects of imipramine on anxiety, depressive-like behavior and body weight gain in rats housed in overcrowded conditions // Journal of Evolutionary Biochemistry and Physiology. 2024. Vol. 60. Suppl. 1. P. S183–S195. © Pleiades Publishing, Ltd., 2024.
- Myers R.D., Fox J. Differences in maze performance of group vs isolation-reared rats // Psychological Reports. 1963. Vol. 12. P. 199–202.
- Normann M.C., Cox M., Akinbo O.I., Watanasriyakul W.T. et al. Differential paraventricular nucleus activation and behavioral responses to social isolation in prairie voles following environmental enrichment with and without physical exercise // Soc. Neurosci. 2021. Vol. 16 (4). P. 375–390. https://doi.org/10.1080/17470919.2021.1926320
- Ouagazzal A.M., Moreau J.L., Pauly-Evers M., Jenck F. Impact of environmental housing conditions on the emotional responses of mice deficient for nociceptin/orphanin FQ peptide precursor gene // Behav. Brain Res. 2003. Vol. 144. P. 111–117. https://doi.org/10.1016/s0166-4328(03)00066-4
- Oztan O., Aydin C., Isgor C. Stressful environmental and social stimulation in adolescence causes antidepressant-like effects associated with epigenetic induction of the hippocampal BDNF and mossy fibre sprouting in the novelty-seeking phenotype // Neurosci. Lett. 2011. Vol. 501(2). P. 107–111. https://doi.org/10.1016/j.neulet.2011.06.058
- Parker H.B., Smith R.F., Erickson R.E., Cromer C.C. Clumping: a cue to limitation of rodent density studies and their interpretation // Behavioral and Neural Biology. 1980. Vol. 28. P. 335–342.
- Pavlova I.V., Broshevitskaya N.D., Potekhina A.A., Shvadchenko A.M. The effect of chronic overcrowding on social behavior and expression of neuroinflammation-associated genes in rats // Biochemistry (Mosc). 2024. Vol. 89 (9). P. 1582–1594. https://doi.org/10.1134/S0006297924090050
- Pavlova I.V., Broshevitskaya N.D. Effect of keeping rats in conditions of increased crowding on anxiety and conditioned reflex fear // Neuroscience and Behavioral Physiology. 2024. Vol. 54. № 9. P. 1399–1411. https://doi.org/10.1007/s11055-024-01739-y
- Pavlova I.V., Broshevitskaya N.D., Grigoryan G.A. A single reminder trial updates fear memory and affect extinction in rats housed under different living conditions // Learning and Motivation. 2025. Vol. 89. https://doi.org/10.1016/j.lmot.2025.102098
- Peng X., Lang C.M., Drozdowicz C.K., Ohlsson-Wilhelm B.M. Effect of cage population density on plasma corticosterone and peripheral lymphocyte populations of laboratory mice // Lab. Anim. 1989. Vol. 23 (4). P. 302–306. https://doi.org/10.1258/002367789780746042
- Pilcher C.W., Jones S.M. Social crowding enhances aversiveness naloxone in rats // Pharmacol. Biochem. Behav. 1981. Vol. 14(3). P. 299–303. https://doi.org/10.1016/0091-3057(81)90394-4
- Płaźnik A., Pałejko W., Stefański R., Kostowski W. Open field behavior of rats reared in different social conditions: the effects of stress and imipramine // Pol. J. Pharmacol. 1993. Vol. 45 (3). P. 243–252.
- Poole T.B., Morgan H.D.R. Differences in aggressive behaviour between male mice (Mus musculus L.) in colonies of different sizes // Anim. Behav. 1973. Vol. 21. P. 788–795.
- Puzserova A., Slezak P., Balis P., Bernatova I. Long-term social stress induces nitric oxide-independent endothelial dysfunction in normotensive rats // Stress Amst. Neth. 2013. Vol. 16. P. 331–339. https://doi.org/10.3109/10253890.2012.725116
- Ramsden E. The urban animal: population density and social pathology in rodents and humans // Bull. World Health Organ. 2009. Vol. 87(2). P. 82. https://doi.org/10.2471/blt.09.062836
- Reiss D., Wolter-Sutter A., Krezel W., Ouagazzal A.M. Effects of social crowding on emotionality and expression of hippocampal nociceptin/orphanin FQ system transcripts in mice // Behav. Brain Res. 2007. Vol. 184(2). P. 167–173. https://doi.org/10.1016/j.bbr.2007.07.010
- Robinson E. The effects of litter size and crowding on position learning by male and female albino rats // Psychological Record. 1976. Vol. 26. P. 61–66.
- Robinson E. Litter and crowding effects on position learning by albino rats under low incentive motivation // Psychological Record. 1977. Vol. 27. P. 479–488.
- Skalicky M., Bubna-Littitz H., Hofecker G. The influence of persistent crowding on the age changes of behavioral parameters and survival characteristics of rats // Mech. Ageing Dev. 1984. Vol. 28(2–3). P. 325–336. https://doi.org/10.1016/0047-6374(84)90033-2
- Stokols D. On the distinction between density and crowding: some implications for future research // Psychol. Rev. 1972. Vol. 79(3). P. 275–277. https://doi.org/10.1037/h003270
- Takatsu-Coleman A.L., Patti C.L., Zanin K.A. et al. Short-term social isolation induces depressive-like behaviour and reinstates the retrieval of an aversive task: mood-congruent memory in male mice? // J. Psychiatry Neurosci. 2013. Vol. 38(4). P. 259–268. https://doi.org/10.1503/jpn.120050
- Toth L.A., Trammell R.A., Ilsley-Woods M. Interactions between housing density and ambient temperature in the cage environment: effects on mouse physiology and behavior // J. Am. Assoc. Lab. Anim. Sci. 2015. Vol. 54(6). P. 708–717.
- Tramullas M., Dinan T.G., Cryan J.F. Chronic psychosocial stress induces visceral hyperalgesia in mice // Stress Amst. Neth. 2012. Vol. 15. P. 281–292. https://doi.org/10.3109/10253890.2011.622816
- Tsukamoto K., Machida K., Ina Y. et al. Effects of crowding on immune functions in mice // Nihon Eiseigaku Zasshi. 1994. Vol. 49(4). P. 827–836. https://doi.org/10.1265/jjh.49.827
- Uarquin D.G., Meyer J.S., Cardenas F.P., Rojas M.J. Effect of overcrowding on hair corticosterone concentrations in juvenile male Wistar rats // J. Am. Assoc. Lab. Anim. Sci. 2016. Vol. 55(6). P. 749–755.
- Van Loo P.L., Mol J.A., Koolhaas J.M., Van Zutphen B.F., Baumans Vol. Modulation of aggression in male mice: influence of group size and cage size // Physiol. Behav. 2001. Vol. 7.2(5). P. 675–683. https://doi.org/10.1016/s0031-9384(01)00425-5
- Vitale G., Arletti R., Ruggieri V., Cifani C., Massi M. Anxiolytic-like effects of nociceptin/orphanin FQ in the elevated plus maze and in the conditioned defensive burying test in rats // Peptides. 2006. Vol. 27. P. 2193–2200.
- Viveros M.P., Hernández R., Martínez I., González P. Effects of social isolation and crowding upon adrenocortical reactivity and behavior in the rat // Rev. Esp. Fisiol. 1988. Vol. 44(3). P. 315–321.
- Yildiz A., Hayirli A., Okumus Z., Kaynar O., Kisa F. Physiological profile of juvenile rats: effects of cage size and cage density // Lab. Anim. (NY). 2007. Vol. 36(2). P. 28–38. https://doi.org/10.1038/laban0207-28
- Zelek-Molik A., Bobula B., Gądek-Michalska A. et al. Psychosocial crowding stress-induced changes in synaptic transmission and glutamate receptor expression in the rat frontal cortex // Biomolecules. 2021. Vol. 11(2). P. 294. https://doi.org/10.3390/biom11020294
- Zhai X., Ai L., Chen D., Zhou D. et al. Multiple integrated social stress induces depressive-like behavioral and neural adaptations in female C57BL/6J mice // Neurobiol. Dis. 2024. Vol. 190: 106374. https://doi.org/10.1016/j.nbd.2023.106374
Қосымша файлдар

