Environmental enrichment as a strategy: Attenuates the anxiety and memory impairment in social isolation stress
Background Social isolation (SI) early in life produces behavioral and cognitive abnormalities. On the contrary, environmental enrichment (EE) offers beneficial effects on brain plasticity and development. This study was designed to examine how EE affects memory functions, anxiety level, and the exp...
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Published in | International journal of developmental neuroscience Vol. 82; no. 6; pp. 499 - 512 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
Published |
01.10.2022
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Subjects | |
Online Access | Get full text |
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Abstract | Background
Social isolation (SI) early in life produces behavioral and cognitive abnormalities. On the contrary, environmental enrichment (EE) offers beneficial effects on brain plasticity and development. This study was designed to examine how EE affects memory functions, anxiety level, and the expression levels of memory/anxiety‐related genes such as NR2A, NR2B, BDNF, and cFos in the hippocampus of socially isolated rats.
Materials and Methods
Wistar albino male rats (n = 40) were separated into the five groups: Standard cage (SC), SI, EE, SI + SC, and SI + EE group. For each group, eight rats were housed, either grouped or isolated, in a standard or 3‐week EE, respectively. Morris water maze test (MWMT) was used for measuring the learning and memory function. Elevated plus maze (EPM) and open field (OF) were used for the evaluation of anxiety behavior. Blood corticosterone level was evaluated by the ELISA method. The expression levels of genes were measured by the RT‐PCR method.
Results
Results showed that EE increased memory performance in the SI group (p < 0.05). SI caused anxiety while EE improved anxiety behavior (p < 0.05). There was no significant difference between the groups in the OF test. Corticosterone levels did not change between groups. BDNF expression level was downregulated in EE and SI + SC compared with the SC group (respectively; p = 0.012; p = 0.011). NR2A, NR2B, and cFos expression levels did not change between groups significantly.
Conclusions
SI impaired memory performance while EE has beneficial effects on memory in socially isolated rats. EE alone was insufficient to cause alterations in the memory performance. The therapeutic effects of EE became strengthened while applied together with stress protocol. Together with improving the effectiveness of memory function, EE has the potential to decrease anxiety behavior. EE seemed to be the reason for decreasing in BDNF.
In this study, we examined the effects of environmental enrichment on memory and anxiety in social isolated male rats. We also focused on hippocampal gene expression related with memory function. Environmental enrichment increased the memory function and decreased anxiety behavior. On the other hand, social isolation decreased memory function and increased anxiety. Together with these findings, environmental enrichment decreased the BDNF gene expression level. |
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AbstractList | Background
Social isolation (SI) early in life produces behavioral and cognitive abnormalities. On the contrary, environmental enrichment (EE) offers beneficial effects on brain plasticity and development. This study was designed to examine how EE affects memory functions, anxiety level, and the expression levels of memory/anxiety‐related genes such as NR2A, NR2B, BDNF, and cFos in the hippocampus of socially isolated rats.
Materials and Methods
Wistar albino male rats (n = 40) were separated into the five groups: Standard cage (SC), SI, EE, SI + SC, and SI + EE group. For each group, eight rats were housed, either grouped or isolated, in a standard or 3‐week EE, respectively. Morris water maze test (MWMT) was used for measuring the learning and memory function. Elevated plus maze (EPM) and open field (OF) were used for the evaluation of anxiety behavior. Blood corticosterone level was evaluated by the ELISA method. The expression levels of genes were measured by the RT‐PCR method.
Results
Results showed that EE increased memory performance in the SI group (p < 0.05). SI caused anxiety while EE improved anxiety behavior (p < 0.05). There was no significant difference between the groups in the OF test. Corticosterone levels did not change between groups. BDNF expression level was downregulated in EE and SI + SC compared with the SC group (respectively; p = 0.012; p = 0.011). NR2A, NR2B, and cFos expression levels did not change between groups significantly.
Conclusions
SI impaired memory performance while EE has beneficial effects on memory in socially isolated rats. EE alone was insufficient to cause alterations in the memory performance. The therapeutic effects of EE became strengthened while applied together with stress protocol. Together with improving the effectiveness of memory function, EE has the potential to decrease anxiety behavior. EE seemed to be the reason for decreasing in BDNF.
In this study, we examined the effects of environmental enrichment on memory and anxiety in social isolated male rats. We also focused on hippocampal gene expression related with memory function. Environmental enrichment increased the memory function and decreased anxiety behavior. On the other hand, social isolation decreased memory function and increased anxiety. Together with these findings, environmental enrichment decreased the BDNF gene expression level. Abstract Background Social isolation (SI) early in life produces behavioral and cognitive abnormalities. On the contrary, environmental enrichment (EE) offers beneficial effects on brain plasticity and development. This study was designed to examine how EE affects memory functions, anxiety level, and the expression levels of memory/anxiety‐related genes such as NR2A, NR2B, BDNF, and cFos in the hippocampus of socially isolated rats. Materials and Methods Wistar albino male rats ( n = 40) were separated into the five groups: Standard cage (SC), SI, EE, SI + SC, and SI + EE group. For each group, eight rats were housed, either grouped or isolated, in a standard or 3‐week EE, respectively. Morris water maze test (MWMT) was used for measuring the learning and memory function. Elevated plus maze (EPM) and open field (OF) were used for the evaluation of anxiety behavior. Blood corticosterone level was evaluated by the ELISA method. The expression levels of genes were measured by the RT‐PCR method. Results Results showed that EE increased memory performance in the SI group ( p < 0.05). SI caused anxiety while EE improved anxiety behavior ( p < 0.05). There was no significant difference between the groups in the OF test. Corticosterone levels did not change between groups. BDNF expression level was downregulated in EE and SI + SC compared with the SC group (respectively; p = 0.012; p = 0.011). NR2A, NR2B, and cFos expression levels did not change between groups significantly. Conclusions SI impaired memory performance while EE has beneficial effects on memory in socially isolated rats. EE alone was insufficient to cause alterations in the memory performance. The therapeutic effects of EE became strengthened while applied together with stress protocol. Together with improving the effectiveness of memory function, EE has the potential to decrease anxiety behavior. EE seemed to be the reason for decreasing in BDNF. BACKGROUNDSocial isolation (SI) early in life produces behavioral and cognitive abnormalities. On the contrary, environmental enrichment (EE) offers beneficial effects on brain plasticity and development. This study was designed to examine how EE affects memory functions, anxiety level, and the expression levels of memory/anxiety-related genes such as NR2A, NR2B, BDNF, and cFos in the hippocampus of socially isolated rats. MATERIALS AND METHODSWistar albino male rats (n = 40) were separated into the five groups: Standard cage (SC), SI, EE, SI + SC, and SI + EE group. For each group, eight rats were housed, either grouped or isolated, in a standard or 3-week EE, respectively. Morris water maze test (MWMT) was used for measuring the learning and memory function. Elevated plus maze (EPM) and open field (OF) were used for the evaluation of anxiety behavior. Blood corticosterone level was evaluated by the ELISA method. The expression levels of genes were measured by the RT-PCR method. RESULTSResults showed that EE increased memory performance in the SI group (p < 0.05). SI caused anxiety while EE improved anxiety behavior (p < 0.05). There was no significant difference between the groups in the OF test. Corticosterone levels did not change between groups. BDNF expression level was downregulated in EE and SI + SC compared with the SC group (respectively; p = 0.012; p = 0.011). NR2A, NR2B, and cFos expression levels did not change between groups significantly. CONCLUSIONSSI impaired memory performance while EE has beneficial effects on memory in socially isolated rats. EE alone was insufficient to cause alterations in the memory performance. The therapeutic effects of EE became strengthened while applied together with stress protocol. Together with improving the effectiveness of memory function, EE has the potential to decrease anxiety behavior. EE seemed to be the reason for decreasing in BDNF. |
Author | Keloglan Musuroglu, Seval Cevik, Kenan Cevik, Ozge Selin Ozturk, Duygu Murat Sahin, Leyla |
Author_xml | – sequence: 1 givenname: Seval orcidid: 0000-0003-3533-7941 surname: Keloglan Musuroglu fullname: Keloglan Musuroglu, Seval email: sevallkeloglan@hotmail.com organization: Adiyaman University – sequence: 2 givenname: Duygu Murat orcidid: 0000-0001-7917-3606 surname: Ozturk fullname: Ozturk, Duygu Murat organization: Amasya University – sequence: 3 givenname: Leyla surname: Sahin fullname: Sahin, Leyla organization: Mersin University – sequence: 4 givenname: Ozge Selin surname: Cevik fullname: Cevik, Ozge Selin organization: Mersin University – sequence: 5 givenname: Kenan surname: Cevik fullname: Cevik, Kenan organization: Mersin University |
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CitedBy_id | crossref_primary_10_20900_jpbs_20220011 crossref_primary_10_1016_j_bbr_2023_114687 crossref_primary_10_1371_journal_pone_0294354 crossref_primary_10_3389_fphar_2024_1367469 crossref_primary_10_1002_brb3_3604 crossref_primary_10_1248_bpb_b24_00118 |
Cites_doi | 10.1016/j.neuroscience.2019.12.028 10.1016/j.expneurol.2018.09.009 10.1515/revneuro-2016-0072 10.1016/j.brainresbull.2021.05.021 10.1371/journal.pone.0240439 10.33549/physiolres.932678 10.1007/s11064-020-03102-2 10.1016/j.bbi.2017.04.009 10.1016/j.bbr.2013.01.015 10.1016/j.bbr.2005.11.024 10.1016/j.neuropharm.2019.03.030 10.1016/j.bbr.2020.112814 10.1111/ejn.15520 10.1111/j.1365-2826.2004.01173.x 10.1016/j.neulet.2021.135834 10.1353/pbm.2003.0049 10.1016/j.bbr.2014.02.022 10.1007/s12035-014-8917-0 10.1016/j.brainresbull.2011.07.008 10.1016/j.neulet.2021.136016 10.1371/journal.pone.0226377 10.1016/j.brainres.2019.146326 10.1016/j.physbeh.2011.08.036 10.1155/2016/6212983 10.1007/s00221-021-06149-x 10.1016/j.lfs.2018.03.029 10.1016/s0165-0173(01)00067-4 10.1016/s0166-4328(05)80324-9 10.1371/journal.pone.0086237 10.1097/PSY.0000000000000052 10.1007/s00441-017-2782-x 10.1111/jnc.15017 10.1016/j.pbb.2020.172993 10.1016/j.physbeh.2003.07.008 10.1002/jdn.10038 10.1016/j.neuroscience.2020.09.058 10.1002/brb3.767 10.3389/fnbeh.2017.00101 10.3389/fnbeh.2018.00177 10.1016/j.bbr.2011.07.007 10.1016/j.physbeh.2021.113440 10.1016/j.neubiorev.2008.03.003 10.1186/1471-2199-10-57 10.1007/7854_2011_134 10.1016/s0091-3057(00)00360-9 10.1002/hipo.20775 10.1016/j.physbeh.2020.113133 10.1016/j.ejphar.2010.09.061 10.1002/hipo.22342 10.1016/0166-4328(95)00216-2 10.1016/j.ijdevneu.2015.07.008 10.1038/nrn1970 10.1016/j.ynstr.2020.100289 10.1016/j.neulet.2020.135133 10.1016/j.bbr.2013.10.046 10.1007/s00213-007-0895-8 10.5603/FM.a2019.0018 10.1016/s0301-0082(96)00021-4 10.2334/josnusd.18-0409 10.1016/j.coesh.2020.09.004 10.1016/s0306-4522(02)00104-5 10.3791/2920 10.1016/j.semcdb.2021.05.017 10.1016/j.expneurol.2006.02.006 10.1111/j.1460-9568.2006.05079.x 10.1016/j.neulet.2012.12.048 10.1002/1098-1063(2000)10:5<605::AID-HIPO11>3.0.CO;2-3 10.1016/j.brainres.2008.05.030 10.1016/j.bbi.2017.11.016 10.1016/s0166-4328(01)00315-1 |
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References | 2019; 1721 2017; 7 2014; 259 2018; 200 2019; 14 2002; 112 2011; 53 2013; 243 2020; 15 2020; 14 2008; 32 2016; 2016 2021; 760 2014; 63 2012; 10 1996; 78 1992; 52 2015; 46 2018; 373 2009; 10 2019; 61 2006; 24 2021; 752 2000; 10 2021; 237 2021; 118 2021; 239 2003; 46 2020; 732 2019; 311 2011; 21 2020; 45 2019; 151 2014; 9 2006; 200 2006; 169 2017; 64 2003; 80 2000; 67 2017; 28 2019; 78 2015; 52 2020; 80 2020; 226 1996; 50 2006; 7 2012; 105 2016; 15 2011; 650 2018; 69 2020; 429 2011; 225 2015; 25 2021; 54 2008; 1222 2020; 394 2021; 453 2007; 195 2004; 16 2020; 197 2020; 154 2017; 11 2013; 536 2021; 19 2002; 128 2011; 86 2021; 173 2018; 12 2014; 265 2001; 36 2014; 76 2005; 14 e_1_2_10_23_1 e_1_2_10_46_1 e_1_2_10_69_1 e_1_2_10_21_1 e_1_2_10_44_1 e_1_2_10_42_1 e_1_2_10_40_1 e_1_2_10_70_1 e_1_2_10_2_1 e_1_2_10_72_1 Durmus L. (e_1_2_10_14_1) 2005; 14 e_1_2_10_4_1 e_1_2_10_18_1 e_1_2_10_53_1 e_1_2_10_6_1 e_1_2_10_16_1 e_1_2_10_39_1 e_1_2_10_55_1 e_1_2_10_8_1 e_1_2_10_37_1 e_1_2_10_57_1 e_1_2_10_58_1 e_1_2_10_13_1 e_1_2_10_34_1 e_1_2_10_11_1 e_1_2_10_32_1 e_1_2_10_30_1 e_1_2_10_51_1 e_1_2_10_61_1 e_1_2_10_29_1 e_1_2_10_63_1 e_1_2_10_27_1 e_1_2_10_65_1 e_1_2_10_25_1 e_1_2_10_48_1 e_1_2_10_67_1 e_1_2_10_24_1 e_1_2_10_45_1 e_1_2_10_22_1 e_1_2_10_43_1 e_1_2_10_20_1 e_1_2_10_41_1 e_1_2_10_71_1 e_1_2_10_73_1 e_1_2_10_52_1 e_1_2_10_3_1 e_1_2_10_19_1 e_1_2_10_54_1 e_1_2_10_5_1 e_1_2_10_17_1 e_1_2_10_38_1 e_1_2_10_56_1 e_1_2_10_7_1 e_1_2_10_36_1 e_1_2_10_12_1 e_1_2_10_35_1 e_1_2_10_9_1 e_1_2_10_59_1 e_1_2_10_10_1 e_1_2_10_33_1 e_1_2_10_31_1 e_1_2_10_50_1 Flinn J. M. (e_1_2_10_15_1) 2016; 15 e_1_2_10_60_1 e_1_2_10_62_1 e_1_2_10_64_1 e_1_2_10_28_1 e_1_2_10_49_1 e_1_2_10_66_1 e_1_2_10_26_1 e_1_2_10_47_1 e_1_2_10_68_1 |
References_xml | – volume: 259 start-page: 247 year: 2014 end-page: 252 article-title: Memory, learning, and participation of the cholinergic system in young rats exposed to environmental enrichment publication-title: Behavioural Brain Research – volume: 45 start-page: 2417 issue: 10 year: 2020 end-page: 2432 article-title: Enriched environment and social isolation affect cognition ability via altering excitatory and inhibitory synaptic density in mice hippocampus publication-title: Neurochemical Research – volume: 46 start-page: S39 issue: 3 Suppl year: 2003 end-page: 52 article-title: Social isolation and health, with an emphasis on underlying mechanisms publication-title: Perspectives in Biology and Medicine – volume: 67 start-page: 225 year: 2000 end-page: 232 article-title: Does the increase in locomotion induced by ethanol indicate its stimulant or anxiolytic properties? publication-title: Pharmacology, Biochemistry, and Behavior – volume: 21 start-page: 127 issue: 2 year: 2011 end-page: 132 article-title: Hippocampal epigenetic modification at the brain‐derived neurotrophic factor gene induced by an enriched environment publication-title: Hippocampus – volume: 128 start-page: 153 issue: 2 year: 2002 end-page: 160 article-title: Social isolation stress during the third week of life has age‐dependent effects on spatial learning in rats publication-title: Behavioural Brain Research – volume: 76 start-page: 277 issue: 4 year: 2014 end-page: 84 article-title: The effects of environmental enrichment on depressive and anxiety‐relevant behaviors in socially isolated prairie voles publication-title: Psychosomatic Medicine – volume: 1721 year: 2019 article-title: Effect of enriched environment and predictable chronic stress on spatial memory in adolescent rats: Predominant expression of BDNF, nNOS, and interestingly malondialdehyde in the right hippocampus publication-title: Brain Research – volume: 536 start-page: 47 year: 2013 end-page: 51 article-title: Behavioral effects of repeated handling differ in rats reared in social isolation and environmental enrichment publication-title: Neuroscience Letters – volume: 53 year: 2011 article-title: Morris water maze test for learning and memory deficits in Alzheimer's disease model mice publication-title: Journal of Visualized Experiments – volume: 64 start-page: 232 year: 2017 end-page: 243 article-title: Early enriched physical environment reverses impairments of the hippocampus, but not medial prefrontal cortex, of socially‐isolated mice publication-title: Brain Behavior and Immunity – volume: 225 start-page: 85 issue: 1 year: 2011 end-page: 90 article-title: Effects of social isolation and enriched environment on behavior of adult Swiss mice do not require hippocampal neurogenesis publication-title: Behavioural Brain Research – volume: 19 year: 2021 article-title: Neuroplasticity and environment: A pharmacotherapeutic approach toward preclinical and clinical understanding publication-title: Current Opinion in Environmental Science & Health – volume: 52 start-page: 1421 issue: 3 year: 2015 end-page: 1429 article-title: Social isolation during adolescence strengthens retention of fear memories and facilitates induction of late‐phase long‐term potentiation publication-title: Molecular Neurobiology – volume: 14 year: 2020 article-title: “Live together, die alone”: The effect of re‐socialization on behavioural performance and social‐affective brain‐related proteins after a long‐term chronic social isolation stress publication-title: Neurobiology of Stress – volume: 80 start-page: 259 issue: 2–3 year: 2003 end-page: 266 article-title: Environmental enrichment: Effects on stereotyped behavior and neurotrophin levels publication-title: Physiology & Behavior – volume: 195 start-page: 175 issue: 2 year: 2007 end-page: 182 article-title: Acute and constitutive increases in central serotonin levels reduce social play behaviour in peri‐adolescent rats publication-title: Psychopharmacology – volume: 237 year: 2021 article-title: Effect of chronic handling and social isolation on emotion and cognition in adolescent rats publication-title: Physiology & Behavior – volume: 80 start-page: 396 issue: 5 year: 2020 end-page: 408 article-title: Sex‐dependent effects of postweaning exposure to an enriched environment on novel objective recognition memory and anxiety‐like behaviors: The role of hippocampal BDNF level publication-title: International Journal of Developmental Neuroscience – volume: 24 start-page: 1867 issue: 7 year: 2006 end-page: 1873 article-title: Locomotor activity correlates with modifications of hippocampal mossy fibre synaptic transmission publication-title: The European Journal of Neuroscience – volume: 78 start-page: 57 issue: 1 year: 1996 end-page: 65 article-title: Psychobiology of plasticity: Effects of training and experience on brain and behavior publication-title: Behavioural Brain Research – volume: 32 start-page: 1087 issue: 6 year: 2008 end-page: 1102 article-title: Behavioural and neurochemical effects of post‐weaning social isolation in rodents‐relevance to developmental neuropsychiatric disorders publication-title: Neuroscience and Biobehavioral Reviews – volume: 373 start-page: 729 issue: 3 year: 2018 end-page: 741 article-title: BDNF effects on dendritic spine morphology and hippocampal function publication-title: Cell and Tissue Research – volume: 10 year: 2009 article-title: Validation of housekeeping genes for quantitative real‐time PCR in in‐vivo and in‐vitro models of cerebral ischaemia publication-title: BMC Molecular Biology – volume: 78 start-page: 668 issue: 4 year: 2019 end-page: 675 article-title: Long‐term treadmill exercise upregulated hippocampal learning‐related genes without improving cognitive behaviour in socially isolated rats publication-title: Folia Morphologica – volume: 169 start-page: 10 issue: 1 year: 2006 end-page: 20 article-title: Influence of differential housing on emotional behaviour and neurotrophin levels in mice publication-title: Behavioural Brain Research – volume: 226 year: 2020 article-title: Impact of enriched environment during adolescence on adult social behavior, hippocampal synaptic density and dopamine D2 receptor expression in rats publication-title: Physiology & Behavior – volume: 9 issue: 1 year: 2014 article-title: Untangling the influences of voluntary running, environmental complexity, social housing and stress on adult hippocampal neurogenesis publication-title: PLoS ONE – volume: 25 start-page: 1 issue: 1 year: 2015 end-page: 15 article-title: BDNF contributes to the facilitation of hippocampal synaptic plasticity and learning enabled by environmental enrichment publication-title: Hippocampus – volume: 14 issue: 12 year: 2019 article-title: Environmental enrichment effects after early stress on behavior and functional brain networks in adult rats publication-title: PLoS ONE – volume: 2016 year: 2016 article-title: Social isolation stress induces anxious‐depressive‐like behavior and alterations of neuroplasticity‐related genes in adult male mice publication-title: Neural Plasticity – volume: 63 start-page: S191 issue: Suppl 1 year: 2014 end-page: S203 article-title: Structure, function, and pharmacology of NMDA receptor channels publication-title: Physiological Research – volume: 197 year: 2020 article-title: Differential impact of stress and environmental enrichment on corticolimbic circuits publication-title: Pharmacology, Biochemistry, and Behavior – volume: 394 year: 2020 article-title: Enriched environment effect on lipopolysaccharide‐induced spatial learning, memory impairment and hippocampal inflammatory cytokine levels in male rats publication-title: Behavioural Brain Research – volume: 239 start-page: 2537 issue: 8 year: 2021 end-page: 2550 article-title: Paradoxical changes in mood‐related behaviors on continuous social isolation after weaning publication-title: Experimental Brain Research – volume: 105 start-page: 269 issue: 2 year: 2012 end-page: 275 article-title: Social isolation in adolescence alters behaviors in the forced swim and sucrose preference tests in female but not in male rats publication-title: Physiology & Behavior – volume: 173 start-page: 174 year: 2021 end-page: 183 article-title: Fluoxetine exerts subregion/layer specific effects on parvalbumin/GAD67 protein expression in the dorsal hippocampus of male rats showing social isolation‐induced depressive‐like behaviour publication-title: Brain Research Bulletin – volume: 14 start-page: 52 issue: 1 year: 2005 end-page: 59 article-title: The effect of social isolation stress on learning in male juvenile rats publication-title: Journal of Health Science – volume: 12 year: 2018 article-title: Environmental enrichment during adolescence acts as a protective and therapeutic tool for ethanol binge‐drinking, anxiety‐like, novelty seeking and compulsive‐like behaviors in C57BL/6J mice during adulthood publication-title: Frontiers in Behavioral Neuroscience – volume: 52 start-page: 49 issue: 1 year: 1992 end-page: 59 article-title: Brief exposure to an enriched environment improves performance on the Morris water task and increases hippocampal cytosolic protein kinase C activity in young rats publication-title: Behavioural Brain Research – volume: 118 start-page: 73 year: 2021 end-page: 82 article-title: Persistent behavioral and neurobiological consequences of social isolation during adolescence publication-title: Seminars in Cell & Developmental Biology – volume: 200 start-page: 209 issue: 1 year: 2006 end-page: 215 article-title: Experience‐dependent regulation of zif268 gene expression and spatial learning publication-title: Experimental Neurology – volume: 650 start-page: 229 issue: 1 year: 2011 end-page: 232 article-title: Effects of adolescent social isolation on the expression of brain‐derived neurotrophic factors in the forebrain publication-title: European Journal of Pharmacology – volume: 50 start-page: 83 issue: 2–3 year: 1996 end-page: 107 article-title: Activation of c‐fos in the brain publication-title: Progress in Neurobiology – volume: 10 start-page: 605 issue: 5 year: 2000 end-page: 609 article-title: Genetic analysis of learning behavior‐induced structural plasticity publication-title: Hippocampus – volume: 112 start-page: 631 issue: 3 year: 2002 end-page: 637 article-title: Environmental enrichment attenuates cognitive deficits, but does not alter neurotrophin gene expression in the hippocampus following lateral fluid percussion brain injury publication-title: Neuroscience – volume: 200 start-page: 126 year: 2018 end-page: 133 article-title: Long term treadmill exercise performed to chronic social isolated rats regulate anxiety behavior without improving learning publication-title: Life Sciences – volume: 429 start-page: 23 year: 2020 end-page: 32 article-title: Differential effects of short‐term environmental enrichment in juvenile and adult mice publication-title: Neuroscience – volume: 61 start-page: 516 issue: 4 year: 2019 end-page: 520 article-title: Effect of social isolation stress on saliva BDNF in rat publication-title: Journal of Oral Science – volume: 265 start-page: 76 year: 2014 end-page: 83 article-title: Early enriched environment induces an increased conversion of proBDNF to BDNF in the adult rat's hippocampus publication-title: Behavioural Brain Research – volume: 11 year: 2017 article-title: The evidence for altered BDNF expression in the brain of rats reared or housed in social ısolation: A systematic review publication-title: Frontiers in Behavioral Neuroscience – volume: 10 start-page: 293 year: 2012 end-page: 316 article-title: Potential benefits and limitations of enriched environments and cognitive activity on age‐related behavioural decline publication-title: Current Topics in Behavioral Neurosciences – volume: 243 start-page: 191 year: 2013 end-page: 198 article-title: Are you real? Visual simulation of social housing by mirror image stimulation in single housed mice publication-title: Behavioural Brain Research – volume: 7 start-page: 697 issue: 9 year: 2006 end-page: 709 article-title: Enriched environments, experience‐dependent plasticity and disorders of the nervous system publication-title: Nature Reviews. Neuroscience – volume: 752 year: 2021 article-title: The role of pre‐pubertal training history on hippocampal neurotrophic factors and glucocorticoid receptor protein levels in adult male rats publication-title: Neuroscience Letters – volume: 16 start-page: 423 issue: 5 year: 2004 end-page: 431 article-title: Effect of environmental enrichment on stress related systems in rats publication-title: Journal of Neuroendocrinology – volume: 86 start-page: 173 issue: 3–4 year: 2011 end-page: 178 article-title: Brief social isolation in early adolescence affects reversal learning and forebrain BDNF expression in adult rats publication-title: Brain Research Bulletin – volume: 1222 start-page: 31 year: 2008 end-page: 41 article-title: Enviromental enrichment during adolescence regulates gene expression in the striatum of mice publication-title: Brain Research – volume: 28 start-page: 675 issue: 6 year: 2017 end-page: 692 article-title: Hippocampal BDNF in physiological conditions and social isolation publication-title: Reviews in the Neurosciences – volume: 15 start-page: R14 issue: 1 year: 2016 end-page: R16 article-title: Both genetic and environmental changes can enhance learning and memory publication-title: Journal of Undergraduate Neuroscience Education – volume: 311 start-page: 213 year: 2019 end-page: 224 article-title: Long‐term social isolation inhibits autophagy activation, induces postsynaptic dysfunctions and impairs spatial memory publication-title: Experimental Neurology – volume: 7 issue: 8 year: 2017 article-title: Social and environmental enrichment has different effects on ethanol and sucrose consumption in mice publication-title: Brain and Behavior – volume: 69 start-page: 235 year: 2018 end-page: 254 article-title: CD8(+) T cells are essential for the effects of enriched environment on hippocampus‐dependent behavior, hippocampal neurogenesis and synaptic plasticity publication-title: Brain, Behavior, and Immunity – volume: 36 start-page: 60 issue: 1 year: 2001 end-page: 90 article-title: Applications of the Morris water maze in the study of learning and memory publication-title: Brain Research. Brain Research Reviews – volume: 760 year: 2021 article-title: Chronic early‐life social isolation affects NMDA and TrkB receptor expression in a sex‐specific manner publication-title: Neuroscience Letters – volume: 732 year: 2020 article-title: Effects of exposure to enriched environment during adolescence on passive avoidance memory, nociception, and prefrontal BDNF level in adult male and female rats publication-title: Neuroscience Letters – volume: 54 start-page: 7790 issue: 11 year: 2021 end-page: 7804 article-title: Long‐term consequences of periadolescent social isolation on social preference, anxiety‐like behavior, and vasopressin neural circuitry of male and female rats publication-title: The European Journal of Neuroscience – volume: 46 start-page: 108 year: 2015 end-page: 114 article-title: Post‐weaning environmental enrichment improves BDNF response of adult male rats publication-title: International Journal of Developmental Neuroscience – volume: 15 issue: 10 year: 2020 article-title: Social isolation in rats: Effects on animal welfare and molecular markers for neuroplasticity publication-title: PLoS ONE – volume: 453 start-page: 138 year: 2021 end-page: 147 article-title: Postweaning enriched environment enhances cognitive function and brain‐derived neurotrophic factor signaling in the hippocampus in maternally separated rats publication-title: Neuroscience – volume: 154 start-page: 41 issue: 1 year: 2020 end-page: 55 article-title: BDNF deficiency and enriched environment treatment affect neurotransmitter gene expression differently across ages publication-title: Journal of Neurochemistry – volume: 151 start-page: 45 year: 2019 end-page: 54 article-title: Social enrichment reverses the isolation‐induced deficits of neuronal plasticity in the hippocampus of male rats publication-title: Neuropharmacology – ident: e_1_2_10_10_1 doi: 10.1016/j.neuroscience.2019.12.028 – ident: e_1_2_10_69_1 doi: 10.1016/j.expneurol.2018.09.009 – ident: e_1_2_10_71_1 doi: 10.1515/revneuro-2016-0072 – ident: e_1_2_10_51_1 doi: 10.1016/j.brainresbull.2021.05.021 – ident: e_1_2_10_2_1 doi: 10.1371/journal.pone.0240439 – ident: e_1_2_10_68_1 doi: 10.33549/physiolres.932678 – ident: e_1_2_10_70_1 doi: 10.1007/s11064-020-03102-2 – ident: e_1_2_10_7_1 doi: 10.1016/j.bbi.2017.04.009 – ident: e_1_2_10_18_1 doi: 10.1016/j.bbr.2013.01.015 – ident: e_1_2_10_73_1 doi: 10.1016/j.bbr.2005.11.024 – ident: e_1_2_10_3_1 doi: 10.1016/j.neuropharm.2019.03.030 – ident: e_1_2_10_34_1 doi: 10.1016/j.bbr.2020.112814 – ident: e_1_2_10_35_1 doi: 10.1111/ejn.15520 – ident: e_1_2_10_44_1 doi: 10.1111/j.1365-2826.2004.01173.x – ident: e_1_2_10_58_1 doi: 10.1016/j.neulet.2021.135834 – ident: e_1_2_10_6_1 doi: 10.1353/pbm.2003.0049 – ident: e_1_2_10_8_1 doi: 10.1016/j.bbr.2014.02.022 – ident: e_1_2_10_40_1 doi: 10.1007/s12035-014-8917-0 – ident: e_1_2_10_25_1 doi: 10.1016/j.brainresbull.2011.07.008 – ident: e_1_2_10_20_1 doi: 10.1016/j.neulet.2021.136016 – ident: e_1_2_10_21_1 doi: 10.1371/journal.pone.0226377 – ident: e_1_2_10_32_1 doi: 10.1016/j.brainres.2019.146326 – ident: e_1_2_10_30_1 doi: 10.1016/j.physbeh.2011.08.036 – ident: e_1_2_10_31_1 doi: 10.1155/2016/6212983 – ident: e_1_2_10_41_1 doi: 10.1007/s00221-021-06149-x – ident: e_1_2_10_9_1 doi: 10.1016/j.lfs.2018.03.029 – ident: e_1_2_10_12_1 doi: 10.1016/s0165-0173(01)00067-4 – ident: e_1_2_10_50_1 doi: 10.1016/s0166-4328(05)80324-9 – ident: e_1_2_10_22_1 doi: 10.1371/journal.pone.0086237 – ident: e_1_2_10_23_1 doi: 10.1097/PSY.0000000000000052 – ident: e_1_2_10_67_1 doi: 10.1007/s00441-017-2782-x – ident: e_1_2_10_13_1 doi: 10.1111/jnc.15017 – ident: e_1_2_10_62_1 doi: 10.1016/j.pbb.2020.172993 – ident: e_1_2_10_66_1 doi: 10.1016/j.physbeh.2003.07.008 – ident: e_1_2_10_60_1 doi: 10.1002/jdn.10038 – ident: e_1_2_10_11_1 doi: 10.1016/j.neuroscience.2020.09.058 – ident: e_1_2_10_28_1 doi: 10.1002/brb3.767 – ident: e_1_2_10_46_1 doi: 10.3389/fnbeh.2017.00101 – ident: e_1_2_10_56_1 doi: 10.3389/fnbeh.2018.00177 – ident: e_1_2_10_61_1 doi: 10.1016/j.bbr.2011.07.007 – ident: e_1_2_10_63_1 doi: 10.1016/j.physbeh.2021.113440 – ident: e_1_2_10_16_1 doi: 10.1016/j.neubiorev.2008.03.003 – ident: e_1_2_10_24_1 doi: 10.1186/1471-2199-10-57 – ident: e_1_2_10_54_1 doi: 10.1007/7854_2011_134 – ident: e_1_2_10_4_1 doi: 10.1016/s0091-3057(00)00360-9 – ident: e_1_2_10_37_1 doi: 10.1002/hipo.20775 – ident: e_1_2_10_19_1 doi: 10.1016/j.physbeh.2020.113133 – ident: e_1_2_10_42_1 doi: 10.1016/j.ejphar.2010.09.061 – ident: e_1_2_10_49_1 doi: 10.1002/hipo.22342 – ident: e_1_2_10_57_1 doi: 10.1016/0166-4328(95)00216-2 – ident: e_1_2_10_45_1 doi: 10.1016/j.ijdevneu.2015.07.008 – volume: 15 start-page: R14 issue: 1 year: 2016 ident: e_1_2_10_15_1 article-title: Both genetic and environmental changes can enhance learning and memory publication-title: Journal of Undergraduate Neuroscience Education contributor: fullname: Flinn J. M. – ident: e_1_2_10_48_1 doi: 10.1038/nrn1970 – ident: e_1_2_10_55_1 doi: 10.1016/j.ynstr.2020.100289 – ident: e_1_2_10_59_1 doi: 10.1016/j.neulet.2020.135133 – ident: e_1_2_10_39_1 doi: 10.1016/j.bbr.2013.10.046 – ident: e_1_2_10_29_1 doi: 10.1007/s00213-007-0895-8 – ident: e_1_2_10_33_1 doi: 10.5603/FM.a2019.0018 – ident: e_1_2_10_26_1 doi: 10.1016/s0301-0082(96)00021-4 – ident: e_1_2_10_47_1 doi: 10.2334/josnusd.18-0409 – ident: e_1_2_10_43_1 doi: 10.1016/j.coesh.2020.09.004 – volume: 14 start-page: 52 issue: 1 year: 2005 ident: e_1_2_10_14_1 article-title: The effect of social isolation stress on learning in male juvenile rats publication-title: Journal of Health Science contributor: fullname: Durmus L. – ident: e_1_2_10_27_1 doi: 10.1016/s0306-4522(02)00104-5 – ident: e_1_2_10_5_1 doi: 10.3791/2920 – ident: e_1_2_10_38_1 doi: 10.1016/j.semcdb.2021.05.017 – ident: e_1_2_10_65_1 doi: 10.1016/j.expneurol.2006.02.006 – ident: e_1_2_10_36_1 doi: 10.1111/j.1460-9568.2006.05079.x – ident: e_1_2_10_52_1 doi: 10.1016/j.neulet.2012.12.048 – ident: e_1_2_10_53_1 doi: 10.1002/1098-1063(2000)10:5<605::AID-HIPO11>3.0.CO;2-3 – ident: e_1_2_10_64_1 doi: 10.1016/j.brainres.2008.05.030 – ident: e_1_2_10_72_1 doi: 10.1016/j.bbi.2017.11.016 – ident: e_1_2_10_17_1 doi: 10.1016/s0166-4328(01)00315-1 |
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Social isolation (SI) early in life produces behavioral and cognitive abnormalities. On the contrary, environmental enrichment (EE) offers... Abstract Background Social isolation (SI) early in life produces behavioral and cognitive abnormalities. On the contrary, environmental enrichment (EE) offers... BACKGROUNDSocial isolation (SI) early in life produces behavioral and cognitive abnormalities. On the contrary, environmental enrichment (EE) offers beneficial... |
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Title | Environmental enrichment as a strategy: Attenuates the anxiety and memory impairment in social isolation stress |
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