Individual behavioral trajectories shape whole-brain connectivity in mice

Elife. 2023 Jan 16:12:e80379. doi: 10.7554/eLife.80379.

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 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 subnetworks 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.

Keywords: adult neurogenesis; behavioral tracking; hippocampus; individuality; mouse; neuroscience; structural covariance.

Plain language summary

An individual's experiences and behavior shape their brain, thereby building and refining a network of connections between neurons. This unique network may affect an individual's brain resilience in the face of aging, injury or disease. Understanding how individual experiences shape brain connections could help scientists develop personalized treatments. It may also have important implications for preventing brain disease. Studying mice can provide a window into some of these brain processes. By using inbred mice, scientists can rule out the role of genetics in brain differences. Scientists can also control the animals’ environments and track the activity of individuals to study their behavior. Bogado Lopes et al. show that more active mice living in enriched environments have signs of more complex networks of brain connections. In the experiments, the researchers placed genetically identical mice in either standard laboratory mouse housing or in enriched environments. Mice in the enriched housing had access to multi-level enclosures connected with tubes and supplied with a rotating array of toys. A tiny tracking device was inserted under the skin of the mice to follow their movements. Finally, all mice underwent structural magnetic resonance imaging to assess their brain anatomy and connections. This revealed that the most active and adventurous mice in the enriched enclosures had the most robust signs of increased brain connectivity. However, mice with declining activity levels in the enriched enclosures had fewer brain connections. Brain connection patterns in these creatures of habit were nearly identical to the ones in mice housed in small unenriched enclosures. The results show that how individual mice respond to their environments affects their brain structure. More active behavior patterns lead to more robust networks of brain connections. Larger studies in mice could provide more about lifestyle-dependent brain resilience. It may also help scientists to develop individualized approaches to optimizing brain health.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Mapping* / methods
  • Brain* / anatomy & histology
  • Hippocampus
  • Mice

Associated data

  • Dryad/10.5061/dryad.bzkh189ds