Comparing seasonal changes in brain organization in two populations
As previously published for the Radolfzell population, the results from Gugny confirm different patterns of decrease and/or regrowth (or lack of change) in the volume of each brain region (Fig. 5). As each region contributed to the overall decrease/regrowth of brain volume to a different extent, we observed a seasonal change in the organization of the brain. However, the pattern of decrease and regrowth in most brain regions was similar in Radolfzell and Gugny. Olfactory bulbs of females but not males significantly decreased from summer juveniles to winter subadults at both locations (P < 0.05) reflected by a significant interaction of age and sex (F = 4.2, P< 0.05), but we found no difference in seasonal olfactory bulb size between Radolfzell and Gugny at neither factor nor interaction level (P > 0.1). The only other brain region where we found a different pattern between the sexes was the cerebellum but only in Radolfzell (see also Lázaro et al. 2018b). The cerebellum did not vary seasonally at either location (P > 0.5). However, subadult winter females in Radolfzell had larger cerebelli than males, while in Gugny we did not find this sexual dimorphism. Changes for all other brain regions are discussed for males and females together. Volume of the neocortex significantly declined from summer juveniles to winter subadults at both locations (P <0.001). We found that summer juveniles have a larger neocortex in Gugny (P < 0.01), but we found no difference in winter, meaning that there was a more pronounced decrease in Gugny. We did not find a difference in neocortex volumes between winter subadults and adults at either location. The rhinal and piriform cortices decreased their volume from summer to winter (P< 0.01) and did not regrow in adults, again with no difference between locations. Also, overall striatum volume decreased from summer juveniles to winter (P < 0.001), but did not increase in adults (P > 0.5). Again, there was no difference between locations. Within the striatum, this pattern was repeated in the caudoputamen (P (juv-sub) < 0.001; P (sub-ad) > 0.5) and amygdala (P (juv-sub) < 0.05;P (sub-ad) > 0.1), while the nucleus accumbens did not significantly change size at all. The overall volume of the hippocampus decreased from summer to winter (P < 0.05) and did not regrow in adults. There was no difference between locations. Within the hippocampus, volume decrease was only found in CA2 (P (juv-sub) < 0.05). Both the thalamus and hypothalamus decreased and regrew significantly, with no difference between locations (thalamus: P (juv-sub) < 0.001; P (sub-ad) < 0.05); hypothalamus: (P (juv-sub) < 0.001;P (sub-ad) < 0.001).
In summary, although each brain region makes a different contribution to the seasonal changes in brain size, giving rise to a marked re-organization of the brain structure along individuals’ life. The seasonal changes in each brain region in Gugny are remarkably similar to the variation observed in Radolfzell, with the exception of a slight difference in neocortex winter decrease – more emphasized in Gugny – and a quite different pattern in the cerebellum. However, the lack of overall brain mass increase in spring in Gugny may be due to early sampling and the results in Lázaro et al. (2018b) from Radolfzell might describe these patterns better.
Interestingly, the structural changes described in Russia (Yaskin, 1994) largely differ from both Radolfzell and Gugny. The only brain region with a similar pattern is the neocortex, which is the structure that shows the greatest winter decline in all three populations – 37% decline in Russia and Gugny, 28% in Radolfzell – although this is followed by a 18% spring regrowth in Russia, which we did not observe in the other populations. The paleocortex of Russian shrews shrinks/regrows 28/12% in mass respectively, more pronounced than the intermediate values in the corresponding regions – rhinal and piriform cortices – in Gugny (21/6%), and the less pronounced changes in Radolfzell (18/4%). This is the only brain structure that matches our expectation of a geographic and/or environmental gradient, with the Polish population intermediate between Russia and Germany. Hippocampus changes are much greater in Russia (29/33%) than in Gugny (10/5%) and Radolfzell (10/8%), while the olfactory bulbs, which did not change seasonally in Russia, showed strong changes both in Radolfzell (14/14%) and Gugny (24/12%). These inconsistencies refute the hypothesis of a simple linear geographic trend. Instead, the differences in brain structure between populations and seasons might reflect local adaptations to specific climatic or habitat features. Nevertheless, we must also point out differences in the used methods. We used volumetric estimations derived from tracing brain regions in fixed, sectioned, and stained sections, while Yaskin (1994) weighed dissected tissue.