From summer growth to winter decline :‬ ‭brain‬‭size‬‭, captive effect, and cognitive outcomes‬ ‭in the common shrew during Dehnel's phenomenon‬

Abstract

The vertebrate brain is a marvel of biological complexity and sophistication, responsible for coordinating sensory experiences, motor functions, and cognitive processes. Evolutionary studies have demonstrated that while brain size generally correlates with body size, there is significant variation among species. Larger brains relative to body size are often linked to enhanced cognitive abilities, as seen in both birds and mammals, suggesting that such adaptations are responses to complex environmental challenges. However, the size of the brain is constrained by its high metabolic costs, necessitating efficient neural mechanisms to optimize cognitive functions. Brain plasticity, or neuroplasticity, enables the brain to adapt to new situations and challenges by reorganizing neural connections. This adaptability is particularly crucial for species living in temperate climates, where seasonal variations impact physiology and behavior. The common shrew, Sorex araneus, exemplifies this adaptability through Dehnel's phenomenon, a seasonal cycle in which brain and body size decrease during winter, with regrowth occurring in warmer months—an adaptation likely aimed at reducing metabolic demands when food resources are scarce. Studying these cyclical changes in the common shrew can reveal the relationship between brain structure and cognitive function, showing how brain plasticity enables organisms to cope with environmental fluctuations. In my PhD research, I explored the dynamics of brain plasticity in the common shrew through advanced imaging techniques and behavioral analysis. In the first chapter, I present the development of the first high-resolution brain atlases for the common shrew, representing an advancement in our ability to study neurological structures across different developmental stages and environmental conditions. These atlases, derived from both histological sections and Magnetic Resonance Imaging (MRI), serve as essential tools for both fundamental and applied neuroscience research. Creating these atlases will facilitate identifying changes in brain structures as they undergo significant seasonal size fluctuations, providing a framework to correlate these structural changes with functional outcomes. In the second chapter, I used diffusion-weighted MRI (DW-MRI) imaging to investigate the microstructural changes in the shrew's brain during seasonal size changes. I found that brain size reduction in common shrews is marked by significant microstructural changes from summer to winter. These results reveal a notable decrease in intracellular water volume fraction from summer to winter and an increase in extracellular water volume across most brain regions. Importantly, our cell population analyses indicate no reduction in the number of cells, suggesting that the observed changes result from a decrease in cell size. This adaptation likely leads to reduced energy requirements for cellular processes: smaller cells typically exhibit lower metabolic demands, which becomes essential in winter, when resources are limited and efficient metabolism is necessary for survival. In the third chapter, I examined the impact of captivity on brain morphology, cognitive functions, and activity patterns of shrews from summer to winter, comparing wild-caught shrews with those kept in semi-natural captivity. In tasks involving associative learning with visual and olfactory cues, performance was better in summer shrews, especially in early trials. The slowdown of cognitive processes in winter suggests a potential trade-off: maintaining broader cognitive functions might come at the cost of reduced processing speed under resource-limited conditions. In the fourth chapter, I assessed the associative and spatial learning abilities of shrews in relation to their seasonal brain size changes. Despite an overall reduction in brain volume during winter, cognitive testing indicates that common shrews maintain a certain level of functionality, particularly in tasks involving spatial navigation. However, the operational speed of these cognitive functions is compromised. This chapter connects structural brain changes with cognitive functions, demonstrating the importance of cognitive flexibility in adapting to environmental fluctuations. The differential prioritization of cognitive abilities could stem from their varied ecological functions. Spatial learning may be prioritized during winter despite reductions in hippocampal volume, possibly because navigating the environment remains important when resources are scarce. Overall, my dissertation advances the understanding of brain plasticity, environmental adaptability, and cognitive functionality, emphasizing the seasonal impact on brain structure and behavior in the common shrew.