The individuality paradigm: Automated longitudinal activity tracking of large cohorts of genetically identical mice in an enriched environment

Kempermann, Gerd; Lopes, Jadna Bogado; Zocher, Sara; Schilling, Susan; Ehret, Fanny; Garthe, Alexander; Karasinsky, Anne; Brandmaier, Andreas M.; Lindenberger, Ulman; Winter, York; Overall, Rupert W.

doi:10.1016/j.nbd.2022.105916

Cited by 19 publications

(23 citation statements)

References 42 publications

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“…The shared enriched environment took place in a cage system custom-built to our specifications (PhenoSys GmbH, now marketed as ‘PhenoSys ColonyRack Individuality 3.0’), consisting of 70 polycarbonate cages (1264C Type II, Tecniplast) that are connected via transparent tunnels and distributed on seven levels. With this cage system, longitudinal tracking of mice is obtained by RFID antennae, located on connecting tunnels ( Kempermann et al, 2022 ). For this specific experiment, ENR mice only had access to 35 polycarbonate cages in four levels (total area of 1.37 m 2 ), equipped with toys and hideouts, that were replaced and rearranged once a week.…”

Section: Methodsmentioning

confidence: 99%

“…Antenna contacts, resulting from mice activity, were recorded with the software PhenoSoft Control (PhenoSys GmbH), which identifies the specific antenna and mouse, as well as the time stamp of the antenna contact. As previously described ( Kempermann et al, 2022 ), Shannon entropy of the roaming distribution was calculated as

…”

Section: Methodsmentioning

confidence: 99%

“…The ENR mice also showed greater variability in measures linked to brain plasticity, such as adult hippocampal neurogenesis ( Körholz et al, 2018 ) accompanied by distinguishing epigenetic patterns in the hippocampal dentate gyrus ( Zocher et al, 2021 ; Zocher et al, 2020 ). From these results we have developed the Individuality paradigm that exposes the influence of the non-shared environment on phenotypic variation ( Kempermann, 2019 ; Kempermann et al, 2022 ). Its key feature is that both genes and environment are kept constant, while behavior is continuously measured to assess the emergence of differential behavioral trajectories.…”

Section: Introductionmentioning

confidence: 99%

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Individual behavioral trajectories shape whole-brain connectivity in mice

Lopes

Senko

Bahnsen

et al. 2023

eLife

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It is widely assumed that our actions shape our brains and that the resulting connections determine who we are. To test this idea in a reductionist setting, in which genes and environment are controlled, we investigated differences in neuroanatomy and structural covariance by ex vivo structural magnetic resonance imaging (MRI) in mice whose behavioral activity was continuously tracked for 3 months in a large, enriched environment. We confirmed that environmental enrichment increases mouse hippocampal volumes. Stratifying the enriched group according to individual longitudinal behavioral trajectories, however, revealed striking differences in mouse brain structural covariance in continuously highly active mice compared to those whose trajectories showed signs of habituating activity. Network-based statistics identified distinct sub-networks of murine structural covariance underlying these differences in behavioral activity. Together, these results reveal that differentiated behavioral trajectories of mice in an enriched environment are associated with differences in brain connectivity.

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Section: Methodsmentioning

confidence: 99%

…”

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Individual behavioral trajectories shape whole-brain connectivity in mice

Lopes

Senko

Bahnsen

et al. 2023

eLife

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“…Some of these automated home-cage testing systems are modular, allowing the connection of multiple cages to create a more complex envinronment. For instance, IntelliCage can be connected to two social boxes containing different social stimuli (Mitjans et al, 2017 ), while in ColonyRack mice can freely roam across 70 cages, arranged in a two-sided rack with fivs columns and seven rows, in which the cages are connected both horizontally and vertically (Zocher et al, 2020 ; Kempermann et al, 2022 ). The most recent innovation within this automated behavioral testing approach is connecting home-cages to mazes (Mei et al, 2020 ; Kohler et al, 2022 ), granting the experimental subjects free access to the novel test environment.…”

Section: How To Design An Animal-friendly Behavioral Testmentioning

confidence: 99%

Designing animal-friendly behavioral tests for neuroscience research: The importance of an ethological approach

d’Isa

2023

Front. Behav. Neurosci.

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“…At an age of 4 weeks, 50% of the mice of either genotype were randomly assigned to the two different housing conditions either living in custom-built Individuality enrichment enclosure (marketed as "PhenoSys ColonyRack Individuality 3.0" by PhenoSys GmbH, Berlin, Germany) and referred to here as enriched housing (ENR), or standard laboratory housing in type-II cages and four animals per cage (STD). The cage system has been described in detail elsewhere (Kempermann et al, 2022). Briefly, it consists of 70 regular type II cages that are mounted on a standard, double-sided stainless steel rack (Tecniplast 1246C) and connected by connector tubes.…”

Section: Animals and Housing Conditionsmentioning

confidence: 99%

Loss of individualized behavioral trajectories in adult neurogenesis‐deficient cyclin D2 knockout mice

et al. 2023

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There is still limited mechanistic insight into how the interaction of individuals with their environment results in the emergence of individuality in behavior and brain structure. Nevertheless, the idea that personal activity shapes the brain is implicit in strategies for healthy cognitive aging as well as in the idea that individuality is reflected in the brain's connectome. We have shown that even isogenic mice kept in a shared enriched environment (ENR) developed divergent and stable social and exploratory trajectories. As these trajectories—measured as roaming entropy (RE)—positively correlated with adult hippocampal neurogenesis, we hypothesized that a feedback between behavioral activity and adult hippocampal neurogenesis might be a causal factor in brain individualization. We used cyclin D2 knockout mice with constitutively extremely low levels of adult hippocampal neurogenesis and their wild‐type littermates. We housed them for 3 months in a novel ENR paradigm, consisting of 70 connected cages equipped with radio frequency identification antennae for longitudinal tracking. Cognitive performance was evaluated in the Morris Water Maze task (MWM). With immunohistochemistry we confirmed that adult neurogenesis correlated with RE in both genotypes and that D2 knockout mice had the expected impaired performance in the reversal phase of the MWM. But whereas the wild‐type animals developed stable exploratory trajectories with increasing variance, correlating with adult neurogenesis, this individualizing phenotype was absent in D2 knockout mice. Here the behaviors started out more random and revealed less habituation and low variance. Together, these findings suggest that adult neurogenesis contributes to experience‐dependent brain individualization.

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The individuality paradigm: Automated longitudinal activity tracking of large cohorts of genetically identical mice in an enriched environment

Cited by 19 publications

References 42 publications

Individual behavioral trajectories shape whole-brain connectivity in mice

Individual behavioral trajectories shape whole-brain connectivity in mice

Designing animal-friendly behavioral tests for neuroscience research: The importance of an ethological approach

Loss of individualized behavioral trajectories in adult neurogenesis‐deficient cyclin D2 knockout mice

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