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Early-life environmental enrichment generates persistent individualized behavior in mice.

ABSTRACT: Individuals differ in their response to environmental stimuli, but the stability of individualized behaviors and their associated changes in brain plasticity are poorly understood. We developed a novel model of enriched environment to longitudinally monitor 40 inbred mice exploring 35 connected cages over periods of 3 to 6 months. We show that behavioral individuality that emerged during the first 3 months of environmental enrichment persisted when mice were withdrawn from the enriched environment for 3 additional months. Behavioral trajectories were associated with stable interindividual differences in adult hippocampal neurogenesis and persistent epigenetic effects on neuronal plasticity genes in the hippocampus. Using genome-wide DNA methylation sequencing, we show that one-third of the DNA methylation changes were maintained after withdrawal from the enriched environment. Our results suggest that, even under conditions that control genetic background and shared environment, early-life experiences result in lasting individualized changes in behavior, brain plasticity, and epigenetics.

SUBMITTER: Zocher S

PROVIDER: S-EPMC7449688 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Early-life environmental enrichment generates persistent individualized behavior in mice.

Zocher Sara S Schilling Susan S Grzyb Anna N AN Adusumilli Vijay S VS Bogado Lopes Jadna J Günther Sandra S Overall Rupert W RW Winter York Y Kempermann Gerd G

Science advances 20200826 35

Individuals differ in their response to environmental stimuli, but the stability of individualized behaviors and their associated changes in brain plasticity are poorly understood. We developed a novel model of enriched environment to longitudinally monitor 40 inbred mice exploring 35 connected cages over periods of 3 to 6 months. We show that behavioral individuality that emerged during the first 3 months of environmental enrichment persisted when mice were withdrawn from the enriched environme ...[more]

PMID: 32923634

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Project description:Enriched environments are known to beneficially affect the behavior of pigs, as compared with barren pens. The influence of enrichment may, however, depend on pigs' early life housing experiences. The aim of this study was to investigate the long-term effects of early and later life environmental enrichment on behavior and growth in pigs with different coping styles. Pigs were housed in either barren pens or in larger pens enriched with rooting substrates from birth, and half of them experienced a housing switch, i.e., a loss or gain of enrichment, at 7 weeks of age, creating four treatment groups. Home pen behavior and body weight were recorded until 19 weeks of age. Pigs were classified as reactive or proactive based on a backtest at 2 weeks of age. Enrichment increased time spent exploring, chewing, and play and decreased oral manipulation of penmates and pen-directed exploring and chewing. Behavior of pigs that switched from barren to enriched pens or vice versa reflected not only their actual environment, but also their early life housing. As early and later life enrichment affected most behaviors in opposite directions, effects of enrichment, or lack thereof, after the switch were more pronounced in pigs that had experienced a different early life condition. For instance, pigs experiencing an upgrade from barren to enriched pens seemed to "catch-up" by showing more exploration and play. Conversely, pigs exposed to a downgrade displayed more oral manipulation of penmates than ones kept barren throughout, which particularly held for pigs with a reactive coping style. Effects of early life and current housing on several other behaviors depended on coping style too. Pigs housed in enriched conditions appeared better able to cope with weaning than barren housed pigs, as they gained more weight and had higher feed intake post-weaning. Barren housed pigs had a lower body weight than enriched pigs just before the switch, after which growth was mainly determined by actual housing, with enriched kept pigs having a higher feed intake and body weight. Thus, not only current housing conditions, but also a (mis)match with the early life environment may affect behavior and growth of pigs.

Project description:Early life stress is associated with long-term and pervasive adverse effects on neuroendocrine development, affecting normal cognitive and emotional development. Experimental manipulations like environmental enrichment (EE) may potentially reverse the effects of early life stress induced by maternal separation (MS) paradigm in rodents. However, the functional brain networks involved in the effects of EE after prolonged exposure to MS have not yet been investigated. In order to evaluate possible changes in brain functional connectivity induced by EE after MS, quantitative cytochrome c oxidase (CCO) histochemistry was applied to determine regional brain oxidative metabolism in adult male rats. Unexpectedly, results show that prolonged MS during the entire weaning period did not cause any detrimental effects on spatial learning and memory, including depressive-like behavior evaluated in the forced-swim test, and decreased anxiety-like behavior. However, EE seemed to alter anxiety- and depression-like behaviors in both control and MS groups, but improved spatial memory in the latter groups. Analysis of brain CCO activity showed significantly lower metabolic capacity in most brain regions selected in EE groups probably associated with chronic stress, but no effects of MS on brain metabolic capacity. In addition, principal component analysis of CCO activity revealed increased large-scale functional brain connectivity comprising at least three main networks affected by EE in both MS and control groups. Moreover, EE induced a pattern of functional brain connectivity associated with stress and anxiety-like behavior as compared with non-enriched groups. In conclusion, EE had differential effects on cognition and emotional behavior irrespective of exposure to MS. In view of the remarkable effects of EE on brain function and behavior, implementation of rodent housing conditions should be optimized by evaluating the balance between scientific validity and animal welfare.

Project description:The gut microbiome is a pivotal player in toxicological responses. We investigated the effects of maternal exposure to 3 human health-relevant toxicants (BDE-47, tetrabromobisphenol [TBBPA], and bisphenol S [BPS]) on the composition and metabolite levels (bile acids [BAs] and short-chain fatty acids [SCFAs]) of the gut microbiome in adult pups. CD-1 mouse dams were orally exposed to vehicle (corn oil, 10 ml/kg), BDE-47 (0.2 mg/kg), TBBPA (0.2 mg/kg), or BPS (0.2 mg/kg) once daily from gestational day 8 to the end of lactation (postnatal day 21). 16S rRNA sequencing and targeted metabolomics were performed in feces of 20-week-old adult male pups (n = 14 - 23/group). Host gene expression and BA levels were quantified in liver. BPS had the most prominent effect on the beta-diversity of the fecal microbiome compared with TBPPA and BDE-47 (QIIME). Seventy-three taxa were persistently altered by at least 1 chemical, and 12 taxa were commonly regulated by all chemicals (most of which were from the Clostridia class and were decreased). The most distinct microbial biomarkers were S24-7 for BDE-47, Rikenellaceae for TBBPA, and Lactobacillus for BPS (LefSe). The community-wide contributions to the shift in microbial pathways were predicted using FishTaco. Consistent with FishTaco predictions, BDE-47 persistently increased fecal and hepatic BAs within the 12α hydroxylation pathway, corresponding to an up-regulation with the hepatic BA-synthetic enzyme Cyp7a1. Fecal BAs were also persistently up-regulated by TBBPA and BPS (liquid chromatography-mass spectrometry). TBBPA increased propionic acid and succinate, whereas BPS decreased acetic acid (gas chromatography-mass spectrometry). There was a general trend in the hepatic down-regulation of proinflammatory cytokines and the oxidative stress sensor target gene (Nqo1), and a decrease in G6Pdx (the deficiency of which leads to dyslipidemia). In conclusion, maternal exposure to these toxicants persistently modified the gut-liver axis, which may produce an immune-suppressive and dyslipidemia-prone signature later in life.

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Early-life environmental enrichment generates persistent individualized behavior in mice.

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Early-life environmental enrichment generates persistent individualized behavior in mice.

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