Concurrent environmental enrichment and chronic restraint stress: Effects on innate anxiety and depressive-like behavior in male adolescent mice
Yu Mao
Scientific Research Center, Yunnan University of Chinese Medicine, Kunming, P.R. China
Search for more papers by this authorYanmei Chen
Medical Faculty, Kunming University of Science & Technology, Kunming, P.R. China
Search for more papers by this authorXiaomi Yang
Scientific Research Center, Yunnan University of Chinese Medicine, Kunming, P.R. China
Search for more papers by this authorJianhong Wang
Kunming Primates Research Center, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, P.R. China
Search for more papers by this authorLongjiao Ge
Kunming Primates Research Center, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, P.R. China
Search for more papers by this authorJuan Fu
College of Biological and Environmental Engineering, Binzhou University, Binzhou, P.R. China
Search for more papers by this authorCorresponding Author
Huaying Sun
Scientific Research Center, Yunnan University of Chinese Medicine, Kunming, P.R. China
The Key Laboratory of External Drug Delivery System and Preparation Technology in University of Yunnan Province, School of Chinese Materia Medica, Yunnan Univertity of Chinese Medicine, Kunming, P.R. China
Correspondence
Huaying Sun, Yunnan University of Chinese Medicine, Kunming, P.R. China.
Email: [email protected]
Yuanye Ma, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Yuanye Ma
Kunming Primates Research Center, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, P.R. China
Correspondence
Huaying Sun, Yunnan University of Chinese Medicine, Kunming, P.R. China.
Email: [email protected]
Yuanye Ma, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
Email: [email protected]
Search for more papers by this authorYu Mao
Scientific Research Center, Yunnan University of Chinese Medicine, Kunming, P.R. China
Search for more papers by this authorYanmei Chen
Medical Faculty, Kunming University of Science & Technology, Kunming, P.R. China
Search for more papers by this authorXiaomi Yang
Scientific Research Center, Yunnan University of Chinese Medicine, Kunming, P.R. China
Search for more papers by this authorJianhong Wang
Kunming Primates Research Center, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, P.R. China
Search for more papers by this authorLongjiao Ge
Kunming Primates Research Center, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, P.R. China
Search for more papers by this authorJuan Fu
College of Biological and Environmental Engineering, Binzhou University, Binzhou, P.R. China
Search for more papers by this authorCorresponding Author
Huaying Sun
Scientific Research Center, Yunnan University of Chinese Medicine, Kunming, P.R. China
The Key Laboratory of External Drug Delivery System and Preparation Technology in University of Yunnan Province, School of Chinese Materia Medica, Yunnan Univertity of Chinese Medicine, Kunming, P.R. China
Correspondence
Huaying Sun, Yunnan University of Chinese Medicine, Kunming, P.R. China.
Email: [email protected]
Yuanye Ma, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Yuanye Ma
Kunming Primates Research Center, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, P.R. China
Correspondence
Huaying Sun, Yunnan University of Chinese Medicine, Kunming, P.R. China.
Email: [email protected]
Yuanye Ma, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
Email: [email protected]
Search for more papers by this authorFunding information
This study was supported by grant from National Science Foundation of China (81703497, 31771194), National Key R&D Program of China (2018YFC1313803), scientific research fund project of Yunnan Provincial Department of Education (2019J1069) and the Doctor Foundation of Binzhou University (2016Y18)
Abstract
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.
CONFLICT OF INTEREST
The authors declare that they have no competing interests.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
Filename | Description |
---|---|
jdn10061-sup-0001-Supinfo.docxWord document, 14.8 KB | Supplementary Material |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 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
10.1016/j.brainres.2018.01.021 Google Scholar
- 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
10.1097/FBP.0000000000000467 Google Scholar
- 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
10.1016/0091-3057(89)90033-6 Google Scholar
- 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
10.1093/cercor/bhu119 Google Scholar
- 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
10.1016/j.neulet.2018.10.014 Google Scholar
- 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