Individual behavioral trajectories shape whole-brain connectivity in mice
- TU Dresden, Germany
- King's College London, United Kingdom
Abstract
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.
Data availability
The structural MR images used in this manuscript are publicly available on the OSF platform (https://osf.io/m7gpd/). The volumetric MRI data are found in Supplementary Files 1 (absolute values) and 2 (relative values). The behavioral data from the cage (animal IDs with time-stamped raw antenna contacts) are assessible at Dryad: https://doi.org/10.5061/dryad.bzkh189ds
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Individual behavioral trajectories shape whole-brain connectivity in miceDryad Digital Repository, doi:10.5061/dryad.bzkh189ds.
Article and author information
Author details
Funding
Helmholtz Association (Basic Funding)
- Anna N Senko
- Gerd Kempermann
Medizinische Fakultät Carl Gustav Carus, Technische Universität Dresden (Basic Funding)
- Anna N Senko
- Gerd Kempermann
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (88881.129646/2016-01)
- Jadna Bogado Lopes
Joachim Herz Stiftung
- Jadna Bogado Lopes
Medical Research Council (New Investigator Research Grant MR/N025377/1 (AV); Centre Grant MR/N026063/1)
- Anthony C Vernon
TransCampus (TransCampus Research Award)
- Anthony C Vernon
- Gerd Kempermann
Deutsche Forschungsgemeinschaft (EH 367/7-1)
- Stefan Ehrlich
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: The experiment was conducted in accordance with the applicable European and national regulations and approved by the local authority (Landesdirektion Sachsen, file number 7/2016 TVT DD24 5131-365-8-SAC). All analyses were performed in a blinded manner.
Copyright
© 2023, Bogado Lopes et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Individual behavioral trajectories shape whole-brain connectivity in mice
eLife 12:e80379.
https://doi.org/10.7554/eLife.80379
Further reading
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The central amygdala (CeA) has emerged as an important brain region for regulating both negative (fear and anxiety) and positive (reward) affective behaviors. The CeA has been proposed to encode affective information in the form of valence (whether the stimulus is good or bad) or salience (how significant is the stimulus), but the extent to which these two types of stimulus representation occur in the CeA is not known. Here, we used single cell calcium imaging in mice during appetitive and aversive conditioning and found that majority of CeA neurons (~65%) encode the valence of the unconditioned stimulus (US) with a smaller subset of cells (~15%) encoding the salience of the US. Valence and salience encoding of the conditioned stimulus (CS) was also observed, albeit to a lesser extent. These findings show that the CeA is a site of convergence for encoding oppositely valenced US information.
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Movie-watching is a central aspect of our lives and an important paradigm for understanding the brain mechanisms behind cognition as it occurs in daily life. Contemporary views of ongoing thought argue that the ability to make sense of events in the ‘here and now’ depend on the neural processing of incoming sensory information by auditory and visual cortex, which are kept in check by systems in association cortex. However, we currently lack an understanding of how patterns of ongoing thoughts map onto the different brain systems when we watch a film, partly because methods of sampling experience disrupt the dynamics of brain activity and the experience of movie-watching. Our study established a novel method for mapping thought patterns onto the brain activity that occurs at different moments of a film, which does not disrupt the time course of brain activity or the movie-watching experience. We found moments when experience sampling highlighted engagement with multi-sensory features of the film or highlighted thoughts with episodic features, regions of sensory cortex were more active and subsequent memory for events in the movie was better—on the other hand, periods of intrusive distraction emerged when activity in regions of association cortex within the frontoparietal system was reduced. These results highlight the critical role sensory systems play in the multi-modal experience of movie-watching and provide evidence for the role of association cortex in reducing distraction when we watch films.
