Concurrent environmental enrichment and chronic restraint stress: Effects on innate anxiety and depressive-like behavior in male adolescent mice.
adolescent
anxiety
depressive
environmental enrichment
restraint stress
Journal
International journal of developmental neuroscience : the official journal of the International Society for Developmental Neuroscience
ISSN: 1873-474X
Titre abrégé: Int J Dev Neurosci
Pays: United States
ID NLM: 8401784
Informations de publication
Date de publication:
Dec 2020
Dec 2020
Historique:
received:
25
04
2020
revised:
21
08
2020
accepted:
22
08
2020
pubmed:
6
9
2020
medline:
6
10
2021
entrez:
5
9
2020
Statut:
ppublish
Résumé
Adolescence is a period that exhibits both vulnerability and adaptation to environmental stimulus. This study explored the co-existence effect of environmental enrichment (EE) and restraint stress (RS) on innate anxiety and depressive-like behavior in adolescent mice. Male ICR mice were treated with daily EE and RS (4 h/d or 8 h/d) for 2 or 4 weeks from early adolescence (postnatal day 30) and emotional behaviors were evaluated 24 h after the end of treatment. 4 weeks of 8 h RS treatment decreased immobility time in forced swimming test, demonstrating an antidepressant-like effect. For 2 weeks of treatment, 8 h RS significantly reduced the time spent in the lighted compartment of the light-dark box, indicating an increased anxiety level. These results show that under the present experimental design, RS treatment with different duration could have different effect on mice emotion-related behavior, but there was no interaction between EE and RS.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
730-736Subventions
Organisme : National Science Foundation of China
ID : 81703497
Organisme : National Science Foundation of China
ID : 31771194
Organisme : National Key R&D Program of China
ID : 2018YFC1313803
Organisme : Yunnan Provincial Department of Education
ID : 2019J1069
Organisme : Doctor Foundation of Binzhou University
ID : 2016Y18
Informations de copyright
© 2020 International Society for Developmental Neuroscience.
Références
Adriani, W., Macri, S., Pacifici, R., & Laviola, G. (2002). Peculiar vulnerability to nicotine oral self-administration in mice during early adolescence. Neuropsychopharmacology, 27(2), 212-224. https://doi.org/10.1016/S0893-133X(02)00295-6
Andersen, S., & Teicher, M. (2008). Stress, sensitive periods and maturational events in adolescent depression. Trends in Neurosciences, 31, 183-191. https://doi.org/10.1016/j.tins.2008.01.004
Ashokan, A., Hegde, A., Balasingham, A., & Mitra, R. (2018). Housing environment influences stress-related hippocampal substrates and depression-like behavior. Brain Research, 1683, 78-85. https://doi.org/10.1016/j.brainres.2018.01.021
Aspesi, D., & Pinna, G. (2019). Animal models of post-traumatic stress disorder and novel treatment targets. Behavioural Pharmacology, 30, 130-150. https://doi.org/10.1097/FBP.0000000000000467
Benaroya-Milshtein, N., Hollander, N., Apter, A., Kukulansky, T., Raz, N., Wilf, A., … Pick, C. G. (2004). Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. European Journal of Neuroscience, 20(5), 1341-1347. https://doi.org/10.1111/j.1460-9568.2004.03587.x
Brenes, J. C., Rodriguez, O., & Fornaguera, J. (2008). Differential effect of environment enrichment and social isolation on depressive-like behavior, spontaneous activity and serotonin and norepinephrine concentration in prefrontal cortex and ventral striatum. Pharmacology, Biochemistry and Behavior, 89(1), 85-93. https://doi.org/10.1016/j.pbb.2007.11.004
Chen, Y. M., Mao, Y., Zhou, D. M., Hu, X. T., Wang, J. H., & Ma, Y. Y. (2010). Environmental enrichment and chronic restraint stress in ICR mice: Effects on prepulse inhibition of startle and Y-maze spatial recognition memory. Behavioural Brain Research, 212(1), 49-55. https://doi.org/10.1016/j.bbr.2010.03.033
Chiba, S., Numakawa, T., Ninomiya, M., Richards, M., Wakabayashi, C., & Kunugi, H. (2012). Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Progress in neuro-psychopharmacology & Biological Psychiatry, 39, 112-119. https://doi.org/10.1016/j.pnpbp.2012.05.018
Costall, B., Jones, B. J., Kelly, M. E., Naylor, R. J., & Tomkins, D. M. (1989). Exploration of mice in a black and white test box-Validation as a model of anxiety. Pharmacology Biochemistry and Behavior, 32(3), 777-785. https://doi.org/10.1016/0091-3057(89)90033-6
Cryan, J. F., & Holmes, A. (2005). The ascent of mouse: Advances in modelling human depression and anxiety. Nature Reviews Drug Discovery, 4(9), 775-790. https://doi.org/10.1038/nrd1825
Cui, M., Yang, Y. A., Yang, J., Zhang, J., Han, H., Ma, W., … Cao, J. (2006). Enriched environment experience overcomes the memory deficits and depressive-like behavior induced by early life stress. Neuroscience Letters, 404(1-2), 208-212. https://doi.org/10.1016/j.neulet.2006.05.048
Dutta, S., & Sengupta, P. (2016). Men and mice: Relating their ages. Life Sciences, 152, 244-248. https://doi.org/10.1016/j.lfs.2015.10.025
Gregus, A., Wintink, A. J., Davis, A. C., & Kalynchuk, L. E. (2005). Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behavioural Brain Research, 156(1), 105-114. https://doi.org/10.1016/j.bbr.2004.05.013
Hendershott, T. R., Cronin, M. E., Langella, S., McGuinness, P. S., & Basu, A. C. (2016). Effects of environmental enrichment on anxiety-like behavior, sociability, sensory gating, and spatial learning in male and female C57BL/6J mice. Behavioural Brain Research, 314, 215-225. https://doi.org/10.1016/j.bbr.2016.08.004
Hibicke, M., Graham, M. A., & Hayslett, R. L. (2017). Adolescent Chronic Restraint Stress (aCRS) elicits robust depressive-like behavior in freely cycling, adult female rats without increasing anxiety-like behaviors. Experimental and Clinical Psychopharmacology, 25(2), 74-83. https://doi.org/10.1037/pha0000119
Kaviani, H., Gray, J. A., Checkley, S. A., Raven, P. W., Wilson, G. D., & Kumari, V. (2004). Affective modulation of the startle response in depression: Influence of the severity of depression, anhedonia, and anxiety. Journal of Affective Disorders, 83(1), 21-31. https://doi.org/10.1016/j.jad.2004.04.007
Koss, W., Belden, C., Hristov, A., & Juraska, J. (2014). Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats. Synapse, 68(2), 61-72. https://doi.org/10.1002/syn.21716
Leger, M., Paizanis, E., Dzahini, K., Quiedeville, A., Bouet, V., Cassel, J.-C., … Boulouard, M. (2015). Environmental enrichment duration differentially affects behavior and neuroplasticity in adult mice. Cerebral Cortex, 25(11), 4048-4061. https://doi.org/10.1093/cercor/bhu119
Locci, A., Geoffroy, P., Miesch, M., Mensah-Nyagan, A.-G., & Pinna, G. (2017). Social isolation in early versus late adolescent mice is associated with persistent behavioral deficits that can be improved by neurosteroid-based treatment. Frontiers in Cellular Neuroscience, 11(208). https://doi.org/10.3389/fncel.2017.00208
Manzano-Nieves, G., Bravo, M., Baskoylu, S., & Bath, K. G. (2020). Early life adversity decreases pre-adolescent fear expression by accelerating amygdala PV cell development. eLife, 9, e55263. https://doi.org/10.7554/eLife.55263
Miller, C. N., Caruso, M. J., & Kamens, H. M. (2019). Early-adolescent male C57BL/6J and DBA/2J mice display reduced sensitivity to acute nicotine administration. Neuroscience Letters, 690, 151-157. https://doi.org/10.1016/j.neulet.2018.10.014
Morley-Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003). Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. European Journal of Neuroscience, 18(12), 3367-3374. https://doi.org/10.1046/j.1460-9568.2003.03070.x
O'Mahony, C., Sweeney, F., Daly, E., Dinan, T., & Cryan, J. (2010). Restraint stress-induced brain activation patterns in two strains of mice differing in their anxiety behaviour. Behavioural Brain Research, 213, 148-154. https://doi.org/10.1016/j.bbr.2010.04.038
Porsolt, R. D., Pichon, M. L., & Jalfre, M. (1977). Depression: A new animal model sensitive to antidepressant treatments. Nature, 266(5604), 730-732.
Roy, V., Belzung, C., Delarue, C., & Chapillon, P. (2001). Environmental enrichment in BALB/c mice: Effects in classical tests of anxiety and exposure to a predatory odor. Physiology & Behavior, 74(3), 313-320. https://doi.org/10.1016/S0031-9384(01)00561-3
Sadler, A. M., & Bailey, S. J. (2016). Repeated daily restraint stress induces adaptive behavioural changes in both adult and juvenile mice. Physiology & Behavior, 167, 313-323. https://doi.org/10.1016/j.physbeh.2016.09.014
Shilpa, B. M., Bhagya, V., Harish, G., Srinivas Bharath, M. M., & Shankaranarayana Rao, B. S. (2017). Environmental enrichment ameliorates chronic immobilisation stress-induced spatial learning deficits and restores the expression of BDNF, VEGF, GFAP and glucocorticoid receptors. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 76, 88-100. https://doi.org/10.1016/j.pnpbp.2017.02.025
Shoji, H., & Miyakawa, T. (2019). Differential effects of stress exposure via two types of restraint apparatuses on behavior and plasma corticosterone level in inbred male BALB/cAJcl mice. Neuropsychopharmacology Reports, 40, 73-84. https://doi.org/10.1002/npr2.12093
Smith, B. L., Morano, R. L., Ulrich-Lai, Y. M., Myers, B., Solomon, M. B., & Herman, J. P. (2017). Adolescent environmental enrichment prevents behavioral and physiological sequelae of adolescent chronic stress in female (but not male) rats. Stress, 21(5), 464-473. https://doi.org/10.1080/10253890.2017.1402883
Suo, L., Zhao, L., Si, J., Liu, J., Zhu, W., Chai, B., … Lu, L. (2013). Predictable chronic mild stress in adolescence increases resilience in adulthood. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 38(8), 1387-1400. https://doi.org/10.1038/npp.2013.67
van Loo, H. M., Schoevers, R. A., Kendler, K. S., de Jonge, P., & Romeijn, J. W. (2016). psychiatric comorbidity does not only depend on diagnostic thresholds: An illustration with major depressive disorder and generalized anxiety disorder. Depression and Anxiety, 33(2), 143-152. https://doi.org/10.1002/da.22453
van Praag, H., Kempermann, G., & Gage, F. H. (2000). Neural consequences of environmental enrichment. Nature Reviews Neuroscience, 1(3), 191-198. https://doi.org/10.1038/35044558
Vyas, A., Pillai, A. G., & Chattarji, S. (2004). Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience, 128(4), 667-673. https://doi.org/10.1016/j.neuroscience.2004.07.013
Willner, P. (1997). Validity, reliability and utility of the chronic mild stress model of depression: A 10-year review and evaluation. Psychopharmacology, 134(4), 319-329. https://doi.org/10.1007/s002130050456
Xu, Z. W., Hou, B., Zhang, Y. Z., Gao, Y., Wu, Y. H., Zhao, S. F., & Zhang, C. G. (2009). Antidepressive behaviors induced by enriched environment might be modulated by glucocorticoid levels. European Neuropsychopharmacology, 19(12), 868-875. https://doi.org/10.1016/j.euroneuro.2009.07.004
Zimmermann, K., Richardson, R., & Baker, K. (2019). Maturational changes in prefrontal and amygdala circuits in adolescence: Implications for understanding fear inhibition during a vulnerable period of development. Brain Sciences, 9, 65. https://doi.org/10.3390/brainsci9030065