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      The Contribution of Environmental Enrichment to Phenotypic Variation in Mice and Rats

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          Abstract

          The reproducibility and translation of neuroscience research is assumed to be undermined by introducing environmental complexity and heterogeneity. Rearing laboratory animals with minimal (if any) environmental stimulation is thought to control for biological variability but may not adequately test the robustness of our animal models. Standard laboratory housing is associated with reduced demonstrations of species typical behaviors and changes in neurophysiology that may impact the translation of research results. Modest increases in environmental enrichment (EE) mitigate against insults used to induce animal models of disease, directly calling into question the translatability of our work. This may in part underlie the disconnect between preclinical and clinical research findings. Enhancing environmental stimulation for our model organisms promotes ethological natural behaviors but may simultaneously increase phenotypic trait variability. To test this assumption, we conducted a systematic review and evaluated coefficients of variation (CVs) between EE and standard housed mice and rats. Given findings of suboptimal reporting of animal laboratory housing conditions, we also developed a methodological reporting table for enrichment use in neuroscience research. Our data show that animals housed in EE were not more variable than those in standard housing. Therefore, environmental heterogeneity introduced into the laboratory, in the form of enrichment, does not compromise data integrity. Overall, human life is complicated, and by embracing such nuanced complexity into our laboratories, we may paradoxically improve on the rigor and reproducibility of our research.

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          Most cited references42

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          Enriched environments, experience-dependent plasticity and disorders of the nervous system.

          Behavioural, cellular and molecular studies have revealed significant effects of enriched environments on rodents and other species, and provided new insights into mechanisms of experience-dependent plasticity, including adult neurogenesis and synaptic plasticity. The demonstration that the onset and progression of Huntington's disease in transgenic mice is delayed by environmental enrichment has emphasized the importance of understanding both genetic and environmental factors in nervous system disorders, including those with Mendelian inheritance patterns. A range of rodent models of other brain disorders, including Alzheimer's disease and Parkinson's disease, fragile X and Down syndrome, as well as various forms of brain injury, have now been compared under enriched and standard housing conditions. Here, we review these findings on the environmental modulators of pathogenesis and gene-environment interactions in CNS disorders, and discuss their therapeutic implications.
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            Environmental enrichment, new neurons and the neurobiology of individuality

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              Female rats are not more variable than male rats: a meta-analysis of neuroscience studies

              Background Not including female rats or mice in neuroscience research has been justified due to the variable nature of female data caused by hormonal fluctuations associated with the female reproductive cycle. In this study, we investigated whether female rats are more variable than male rats in scientific reports of neuroscience-related traits. Methods PubMed and Web of Science were searched for the period from August 1, 2010, to July 31, 2014, for articles that included both male and female rats and that measured diverse aspects of brain function. Only empirical articles using both male and female gonad-intact adult rats, written in English, and including the number of subjects (or a range) were included. This resulted in 311 articles for analysis. Data were extracted from digital images from article PDFs and from manuscript tables and text. The mean and standard deviation (SD) were determined for each data point and their quotient provided a coefficient of variation (CV) as a measure of trait-specific variability for each sex. Additionally, the results were coded for the type of research being measured (behavior, electrophysiology, histology, neurochemistry, and non-brain measures) and for the strain of rat. Over 6000 data points were extracted for both males and females. Subsets of the data were coded for whether male and female mean values differed significantly and whether animals were grouped or individually housed. Results Across all traits, there were no sex differences in trait variability, as indicated by the CV, and there were no sex differences in any of the four neuroscience categories, even in instances in which mean values for males and females were significantly different. Female rats were not more variable at any stage of the estrous cycle than male rats. There were no sex differences in the effect of housing conditions on CV. On one of four measures of non-brain function, females were more variable than males. Conclusions We conclude that even when female rats are used in neuroscience experiments without regard to the estrous cycle stage, their data are not more variable than those of male rats. This is true for behavioral, electrophysiological, neurochemical, and histological measures. Thus, when designing neuroscience experiments to include both male and female rats, power analyses based on variance in male measures are sufficient to yield accurate numbers for females as well, even when the estrous cycle is not taken into consideration. Electronic supplementary material The online version of this article (doi:10.1186/s13293-016-0087-5) contains supplementary material, which is available to authorized users.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                22 February 2021
                11 March 2021
                Mar-Apr 2021
                : 8
                : 2
                : ENEURO.0539-20.2021
                Affiliations
                [1 ]School of Arts and Sciences, Massachusetts College of Pharmacy and Health Sciences , Boston, MA 02115
                [2 ]Library and Learning Resources, Massachusetts College of Pharmacy and Health Sciences , Boston, MA 02115
                Author notes

                The authors declare no competing financial interests.

                Author contributions: A.C.K. and J.D. designed research; A.C.K., A.V.S., J.D., and R.C.R. performed research; A.C.K., A.V.S., J.D., and R.C.R. analyzed data; A.C.K. and A.V.S. wrote the paper.

                This work was supported by the National Institute of Mental Health Award R15MH114035 (to A.C.K.) and a Massachusetts College of Pharmacy and Health Sciences Summer Undergraduate Research Fellowship (SURF; R.C.R.).

                Correspondence should be addressed to Amanda Kentner at amanda.kentner@ 123456mcphs.edu .
                Author information
                https://orcid.org/0000-0001-7069-486X
                Article
                eN-NWR-0539-20
                10.1523/ENEURO.0539-20.2021
                7986535
                33622702
                9ebf2154-ffad-4ffc-adf1-cce38e7a675a
                Copyright © 2021 Kentner et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 12 December 2020
                : 31 January 2021
                : 8 February 2021
                Page count
                Figures: 4, Tables: 1, Equations: 1, References: 43, Pages: 10, Words: 00
                Funding
                Funded by: http://doi.org/10.13039/100000025HHS | NIH | National Institute of Mental Health (NIMH)
                Award ID: R15MH114035
                Funded by: MCPHS Summer Undergraduate Research Fellowship (SURF)
                Categories
                1
                Research Article: New Research
                Cognition and Behavior
                Custom metadata
                March/April 2021

                animal welfare,coefficient of variation,environmental heterogeneity,phenotypic variability,sex differences,translation

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