The seasonal changes in brain size of some shrews represent the most drastic reversible transformation in the mammalian central nervous system known to date. Brain mass decreases 10–26% from summer to winter and regrows 9–16% in spring, but the underlying structural changes at the cellular level are not yet understood. Here, we describe the volumetric differences in brain structures between seasons and sexes of the common shrew (Sorex araneus) in detail, confirming that changes in different brain regions vary in the magnitude of change. Notably, shrews show a decrease in hypothalamus, thalamus, and hippocampal volume and later regrowth in spring, whereas neocortex and striatum volumes decrease in winter and do not recover in size. For some regions, males and females showed different patterns of seasonal change from each other. We also analyzed the underlying changes in neuron morphology. We observed a general decrease in soma size and total dendrite volume in the caudoputamen and anterior cingulate cortex. This neuronal retraction may partially explain the overall tissue shrinkage in winter. While not sufficient to explain the entire seasonal process, it represents a first step toward understanding the mechanisms beneath this remarkable phenomenon.Electronic supplementary materialThe online version of this article (10.1007/s00429-018-1666-5) contains supplementary material, which is available to authorized users.
Postnatal size changes in most vertebrates are unidirectional and finite once the individual reaches full size [1]. In rare cases, changes of body length may occur in response to harsh environmental conditions. Such reactionary changes are distinct from seasonal, often anticipatory morphological changes, such as the reversible size change of some adult bird brains [2]. A unique pattern of profound anatomical change known as Dehnel's phenomenon has been described for the body, skull and brain size of red-toothed shrews and some mustelids [3-5]. The seasonal 20% decrease and 15% re-growth of the most common proxy, braincase height, were documented at population level from extracted skulls post-mortem. Quantifying intra-individual change had so far been methodologically prohibitive. Here, we followed the intra-individual change in skull size and body mass throughout the full cycle in wild recaptured shrews (Sorex araneus). Using X-ray images we showed that individuals decreased the size of their braincases in anticipation of winter by an average of 15.3%. Braincases then partially regrew in spring by 9.3%. Body mass decreased by 17.6% and then dramatically increased by 83.4% in spring. Thus, we demonstrate that the dramatic changes incurred by Dehnel's phenomenon occur in the individual's bone and other tissues.
In a rare phenomenon, shrews and a few other species cope with seasonal environments by reducing and regrowing brain size, potentially at the cost of changes in cognitive abilities. Here, we confirm an extensive seasonal shrinkage (21.4%) and regrowth (17.0%) of brain mass in winter and spring, respectively, in the common shrew ( L.) in Southern Germany. In a spatial learning task experiment, individuals with reduced winter brain size covered larger distances to find food, compared with the relatively large-brained summer juveniles and regrown spring adults. By reducing their brain mass, these shrews may reduce their energetic demands, but at the cost of cognitive performance, implying a complex trade-off for coping with seasonally fluctuating resources. These results are relevant for our understanding of evolution and the dynamics of mammalian nervous systems in response to environmental changes.
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