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Environmental enrichment effects after early stress on behavior and functional brain networks in adult rats.

ABSTRACT: 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.

SUBMITTER: Gonzalez-Pardo H

PROVIDER: S-EPMC6907785 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe hypothalamus plays a key role in the stress response. While early life stress (ELS) increases susceptibility to psychiatric disorders including major depressive disorder (MDD), acute stress during adulthood can also precipitate MDD after ELS.AimHere, we tested the expression of miRNAs following ELS and susceptibility to depression-like behavior and whether sex or acute stress exacerbates this response. We also tested whether environmental enrichment (Enr) promotes early life and adult behavioral stress resilience and its effect on hypothalamic miRNA and gene expression. Following rat maternal separation (MS) as an ELS model, Enr from weaning through adulthood, and restraint (RS) as acute adult stress, we tested both animal behavior and miRNA expression in the hypothalamus. Target genes and their enrichment and ontology were analyzed using bioinformatic tools. Target gene expression changes were tested using qPCR, and miRNA promoter methylation was studied using methylated-DNA immunoprecipitation qPCR.ResultsMS, Enr, RS, and sex altered hypothalamic miRNAs, including several previously reported in MS literature: miRs-29, - 124, - 132, - 144, - 504. Sex had a significant effect on the greatest number of miRNAs. Also, Enr reversed downregulation of miR-29b-1-5p and -301b-3p in MS. qPCR showed that MAPK6 and MMP19, targets of miR-301b-3p, were upregulated in MS and reversed by Enr. Additionally, miR-219a was hypermethylated in MS coinciding with decreased miR-219a expression.ConclusionsThis study found that sex plays a critical role in the hypothalamic miRNA response to both ELS and acute stress, with males expressing greater changes following postnatal stress. Moreover, enrichment significantly altered behavior as well as hypothalamic miRNA expression and their gene targets. Because of its role as the initiator of the autonomic stress response and connection to hedonic and motivational behavior, the hypothalamic miRNA landscape may significantly alter both the short and long-term behavioral response to stress.

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.

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Environmental enrichment effects after early stress on behavior and functional brain networks in adult rats.

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