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Open Access 01-07-2018 | Original Article

Profound seasonal changes in brain size and architecture in the common shrew

Authors: Javier Lázaro, Moritz Hertel, Chet C. Sherwood, Marion Muturi, Dina K. N. Dechmann

Published in: Brain Structure and Function | Issue 6/2018

Abstract

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.

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Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis. Curr Anthropol 36:199–221CrossRef

Amrein I (2015) Adult hippocampal neurogenesis in natural populations of mammals. Cold Srping Harb Perspect Biol 7:a021295. https://doi.org/10.1101/cshperspect.a021295 CrossRef

Anderson B, Rutledge V (1996) Age and hemisphere effects on dendritic structure. Brain 119:1983–1990. https://doi.org/10.1093/brain/119.6.1983 CrossRefPubMed

Barker JM, Boonstra R, Schulte-Hostedde AI (2003) Age determination in yellow-pine chipmunks (Tamias amoenus): a comparison of eye lens masses and bone sections. Can J Zool 81:1774–1779. https://doi.org/10.1139/Z03-173 CrossRef

Barker JM, Wojtowicz JM, Boonstra R (2005) Where’s my dinner? Adult neurogenesis in free-living food-storing rodents. Genes Brain Behav 4:89–98. https://doi.org/10.1111/j.1601-183X.2004.00097.x CrossRefPubMed

Barnea A, Nottebohm F (1994) Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci USA 91:11217–11221. https://doi.org/10.1073/pnas.91.23.11217 CrossRefPubMedCentralPubMed

Barnea A, Nottebohm F (1996) Recruitment and replacement of hippocampal neurons in young and adult chickadees: an addition to the theory of hippocampal learning. Proc Natl Acad Sci USA 93:714–718. https://doi.org/10.1073/pnas.93.2.714 CrossRefPubMedCentralPubMed

Bartkowska K, Djavadian RL, Taylor JRE, Turlejski K (2008) Generation recruitment and death of brain cells throughout the life cycle of Sorex shrews (Lipotyphla). Eur J Neurosci 27:1710–1721. https://doi.org/10.1111/j.1460-9568.2008.06133.x CrossRefPubMed

Bates D, Mächler M, Bolker BM, Walker SC (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01 CrossRef

Bielak T, Pucek Z (1960) Seasonal changes in the brain weight of the common shrew (Sorex araneus Linnaeus: 1758). Acta Theriol 13:297–300

Bolhuis JJ, Macphail EM (2001) A critique of the neuroecology of learning and memory. Trends Cogn Sci 5:426–433CrossRefPubMed

Brenowitz E, Nalls B, Wingfield JC, Kroodsma DE (1991) Seasonal changes in avian song nuclei without seasonal changes in song repertoire. J Neurosci 11:1367–1374CrossRefPubMed

Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 13:336–349. https://doi.org/10.1038/nrn3214 CrossRefPubMed

Burger DK, Saucier JM, Iwaniuk AN, Saucier DM (2013) Seasonal and sex differences in the hippocampus of a wild rodent. Behav Brain Res 236:131–138. https://doi.org/10.1016/j.bbr.2012.08.044 CrossRefPubMed

Burke SN, Barnes CA (2006) Neural plasticity in the ageing brain. Nat Rev Neurosci 7:30–40. https://doi.org/10.1038/nrn1809 CrossRefPubMed

Caboń K (1956) Untersuchungen über die saisonale Veränderlichkeit der Gehirnes bei der kleinen Spitsmaus (Sorex minutus minutus L.). Ann Univ Marie Curie Sklodowska Sect C 10:93–105

Catania KC (2000) Cortical organization in insectivora: the parallel evolution of the sensory periphery and the brain. Brain Behav Evol 55:311–321CrossRefPubMed

Catania KC, Lyon DC, Mock OB, Kaas JH (1999) Cortical organization in shrews: evidence from five species. J Comp Neurol 410:55–72CrossRefPubMed

Charvet CJ, Striedter GF, Finlay BL (2011) Evo-devo and brain scaling: candidate developmental mechanisms for variation and constancy in vertebrate brain evolution. Brain Behav Evol 78:248–257. https://doi.org/10.1159/000329851 CrossRefPubMedCentralPubMed

Churchfield S (1990) The natural history of shrews. Christopher Helm, Bromley

Churchfield S, Rychlik L, Taylor JRE (2012) Food resources and foraging habits of the common shrew, Sorex araneus: does winter food shortage explain Dehnel’s phenomenon? Oikos 121:1593–1602. https://doi.org/10.1111/j.1600-0706.2011.20462.x CrossRef

Clancy B, Darlington RB, Finlay BL (2001) Translating developmental time across species. Neuroscience 105:7–17CrossRefPubMed

Clarke PG (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 181:195–213. https://doi.org/10.1007/BF00174615 CrossRefPubMed

Cowan WM, Fawcett JW, O’Leary DD, Stanfield BB (1984) Regressive events in neurogenesis. Science 225:1258–1265. https://doi.org/10.1126/science.6474175 CrossRefPubMed

de Sousa AA, Sherwood CC, Mohlberg H et al (2010) Hominoid visual brain structure volumes and the position of the lunate sulcus. J Hum Evol 58:281–292. https://doi.org/10.1016/j.jhevol.2009.11.011 CrossRefPubMed

Dehnel A (1949) Studies on the genus Sorex L. Ann Univ Marie Curie Sklodowska Sect C 4:17–102

Dickstein DL, Kabaso D, Rocher AB et al (2007) Changes in the structural complexity of the aged brain. Aging Cell 6:275–284. https://doi.org/10.1111/j.1474-9726.2007.00289.x CrossRefPubMedCentralPubMed

Dobbing J, Sands J (1973) Quantitative growth and development of human brain. Arch Dis Child 48:757–767. https://doi.org/10.1136/adc.48.10.757 CrossRefPubMedCentralPubMed

Dobbing J, Sands J (1979) Comparative aspects of the brain growth spurt. Early Hum Dev 311:79–83. https://doi.org/10.1016/0378-3782(79)90022-7 CrossRef

Duan H, Wearne SL, Rocher AB et al (2003) Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb Cortex 13:950–961. https://doi.org/10.1093/cercor/13.9.950 CrossRefPubMed

Fan L, Tang Y, Sun B et al (2010) Sexual dimorphism and asymmetry in human cerebellum: an MRI-based morphometric study. Brain Res 1353:60–73. https://doi.org/10.1016/j.brainres.2010.07.031 CrossRefPubMed

Farkas E, Luiten PGM (2001) Cerebral microvascular pathology in aging and Alzheimer’s disease. Prog Neurobiol 64:575–611. https://doi.org/10.1016/S0301-0082(00)00068-X CrossRefPubMed

Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 284:1578–1584CrossRef

Galea LAM, Kavaliers M, Ossenkopp K (1996) Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus. J Exp Biol 199:195–200PubMed

Gaulin SJC, Fitzgerald RW (1989) Sexual selection for spatial-learning ability. Anim Behav 37:322–331CrossRef

Geinisman Y, Bondareff W, Dodge JT (1978) Dendritic atrophy in the dentate gyrus of the senescent rat. Am J Anat 152:321–329. https://doi.org/10.1002/aja.1001520305 CrossRefPubMed

Gelman A, Su Y-S (2015) ARM: data analysis using regression and multilevel/hierarchical models. R package version 1.8-6

Gonda A, Herczeg G, Merilä J (2013) Evolutionary ecology of intraspecific brain size variation: a review. Ecol Evol 3:2751–2764. https://doi.org/10.1002/ece3.627 CrossRefPubMedCentralPubMed

Hofman M, Swaab DF (1992) Seasonal changes in the suprachiasmatic nucleus of man. Neurosci Lett 139:257–260CrossRefPubMed

Hofman MA, Swaab DF (2002) A brain for all season: cellular, and molecular mechanism of photoperiodic plasticity. In: Hofman MA, Boer GJ, Holtmaat AJGD et al (eds) Plasticity in the adult brain: from genes to neurotherapy, progress in brain research. Elsevier, Amsterdam, pp 255–280CrossRef

Hyvarinen H (1969) On the seasonal changes in the skeleton of the common shrew (Sorex araneus L.) and their physiological background. Aquil Ser Zool 7:2–32

Karbowski J (2007) Global and regional brain metabolic scaling and its functional consequences. BMC Biol 5:18. https://doi.org/10.1186/1741-7007-5-18 CrossRefPubMedCentralPubMed

Kaufman JA (2004) Pattern and scaling of regional cerebral glucose metabolism in mammals. Washington University, Washington

Krebs JR, Sherryt DF, Healy SD et al (1989) Hippocampal specialization of food-storing birds. Neurobiology 86:1388–1392. https://doi.org/10.1073/pnas.86.4.1388 CrossRef

Laughlin SB, de R Van Steveninck, Anderson RR JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36–41. https://doi.org/10.1038/236 CrossRefPubMed

Lavenex P, Steele MA, Jacobs LF (2000a) The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels. Eur J Neurosci 12:643–648. https://doi.org/10.1046/j.1460-9568.2000.00949.x CrossRefPubMed

Lavenex P, Steele MA, Jacobs LF (2000b) Sex differences, but no seasonal variations in the hippocampus of food-caching squirrels: a stereological study. J Comp Neurol 425:152–166CrossRefPubMed

Lázaro J, Dechmann DKN, LaPoint S et al (2017) Profound reversible seasonal changes of individual skull size in a mammal. Curr Biol 27:R1106–R1107CrossRefPubMed

Lázaro J, Hertel M, LaPoint S et al (2018) Cognitive skills of common shrews (Sorex araneus) vary with seasonal changes in skull size and brain mass. J Exp Biol 221:jeb-166595. https://doi.org/10.1242/jeb.166595 CrossRef

Magariños AM, McEwen BS, Saboureau M, Pevet P (2006) Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters. Proc Natl Acad Sci USA 103:18775–18780. https://doi.org/10.1073/pnas.0608785103 CrossRefPubMedCentralPubMed

Marner L, Nyengaard JR, Tang Y, Pakkenberg B (2003) Marked loss of myelinated nerve fibers in the human brain with age. J Comp Neurol 462:144–152. https://doi.org/10.1002/cne.10714 CrossRefPubMed

Mcnab BK, Eisenberg JF (1989) Brain size and its relation to the rate of metabolism in mammals. Am Nat 133:157–167CrossRef

Mezhzherin VA (1964) Dehnel’s phenomenon and its possible explanation. Acta Theriol 8:95–114CrossRef

Moraleva N, Telitzina A (1994) Territoriality in juveniles of the common shrew (Sorex araneus) in prepeak and peak years of population density. Spec Publ Carnegie Museum Nat Hist 18:67–76

Naumann RK, Anjum F, Roth-Alpermann C, Brecht M (2012) Cytoarchitecture, areas, and neuron numbers of the Etruscan shrew cortex. J Comp Neurol 520:2512–2530. https://doi.org/10.1002/cne.23053 CrossRefPubMed

Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804. https://doi.org/10.1242/jeb.017574 CrossRef

Nottebohm F (1981) A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 214:1368–1370. https://doi.org/10.1126/science.7313697 CrossRefPubMed

Paxinos G, Franklin KBJ (2013) The mouse brain in stereotaxic coordinates, 4th edn. Acadmic Press, San Diego

Popov VI, Bocharova LS (1992) Hibernation-induced structural changes in synaptic contacts between mossy fibers and hippocampal pyramidal neurons. Neuroscience 48:53–62CrossRefPubMed

Popov VI, Bocharova LS, Bragin a. G (1992) Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation. Neuroscience 48:45–51. https://doi.org/10.1016/0306-4522(92)90336-Z CrossRefPubMed

Pucek M (1965a) Water contents and seasonal changes of the brain-weight in shrews. Acta Theriol 10:353–367CrossRef

Pucek Z (1965b) Seasonal and age changes in the weight of internal organs of shrews. Acta Theriol 10:369–438CrossRef

Pucek Z (1970) Seasonal and age change in shrews as an adaptive process. Symp Zool Soc Lond 26:189–207

R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

Raz N, Lindenberger U, Rodrigue KM et al (2005) Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cereb Cortex 15:1676–1689. https://doi.org/10.1093/cercor/bhi044 CrossRefPubMed

Rychlik L (1998) Evolution of social systems in shrews. In: Wojcik JM, Woslan M (eds) Evolution of shrews. Mammal Research Institute, Polish Academy of Sciences, Bialowieza, pp 347–405

Scheibel ME, Scheibel AB (1978) The methods of Golgi. In: Robertson RT (ed) Neuroanatomical research techniques. New York Academic Press, New York, pp 98–144

Serafinski W (1955) Morphological and ecological investigations on Polish species of the genus Sorex L. (Insectivora, Soricidae). Acta Oecol 1:27–86

Smith GT, Brenowitz EA, Beecher MD, Wingfield JC (1997) Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J Neurosci 17:6001–6010CrossRefPubMed

Smith DE, Roberts J, Gage FH, Tuszynski MH (1999) Age-associated neuronal atrophy occurs in the primate brain and is reversible by growth factor gene therapy. Proc Natl Acad Sci 96:10893–10898CrossRefPubMedCentralPubMed

Smulders TV, Sasson AD, Devoogd TJ (1995) Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee. J Neurobiol 27:15–25CrossRefPubMed

Smulders T V., Shiflett MW, Sperling AJ, Devoogd TJ (2000) Seasonal changes in neuron numbers in the hippocampal formation of a food-hoarding bird: the black-capped chickadee. J Neurobiol 44:414–422. https://doi.org/10.1002/1097-4695(20000915)44:4<414::AID-NEU4>3.0.CO;2-ICrossRefPubMed

Spocter M, Hopkins WD, Barks SK et al (2012) Neuropil distribution in the cerebral cortex differs between humans and chimpanzees. J Comp Neurol 520:2917–2929. https://doi.org/10.1002/cne.23074 CrossRefPubMedCentralPubMed

Stephan H (1960) Methodische Studien über den quantitativen Vergleich architektonischer Struktureinheiten des Gehirns. Z Wiss Zool 164:143–172

Stockley P, Searle JB (1998) Shrew mating systems. In: Wójcik JM, Wolsan M (eds) Evolution of shrews. Mammal Research Institute, Polish Academy of Sciences, Białowieża, pp 407–424

Stockley P, Searle JB, Macdonald DW, Jones CS (1994) Alternative reproductive tactics in male common shrews: relationships between mate-searching behaviour, sperm production, and reproductive success as revealed by DNA fingerprinting. Behav Ecol Sociobiol 34:71–78. https://doi.org/10.1007/BF00175460 CrossRef

Striedter GF (2005) Principles of brain evolution. Sinauer, Sunderland

Suárez I, Bodega G, Rubio M, Fernández B (1992) Sexual dimorphism in the hamster cerebellum demonstrated by glial fibrillary acidic protein (GFAP) and vimentin immunoreactivity. Glia 5:10–16. https://doi.org/10.1002/glia.440050103 CrossRefPubMed

Taylor JRE, Rychlik L, Churchfield S (2013) Winter reduction in body mass in a very small, nonhibernating mammal: consequences for heat loss and metabolic rates. Physiol Biochem Zool 86:9–18. https://doi.org/10.1086/668484 CrossRefPubMed

Tiemeier H, Lenroot RK, Greenstein DK et al (2011) Cerebellum development during childhood and adolescence: a longitudinal morphometric MRI study. Neuroimage 49:63–70. https://doi.org/10.1016/j.neuroimage.2009.08.016.Cerebellum CrossRef

Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23:251–258CrossRefPubMed

Tramontin AD, Smith GT, Breuner CW, Brenowitz EA (1998) Seasonal plasticity and sexual dimorphism in the avian song control system: Stereological measurement of neuron density and number. J Comp Neurol 396:186–192. https://doi.org/10.1002/(SICI)1096-9861(19980629)396:2<186::AID-CNE4>3.0.CO;2-XCrossRefPubMed

Workman JL, Bowers SL, Nelson RJ (2009) Enrichment and photoperiod interact to affect spatial learning and hippocampal dendritic morphology in white-footed mice (Peromyscus leucopus). Eur J Neurosci 29:161–170. https://doi.org/10.1111/j.1460-9568.2008.06570.x CrossRefPubMed

Yaskin VA (1994) Variation in brain morphology of the common shrew. In: Merrit JF, Kirkland GL, Rose RK (eds) Advances in the biology of shrews. Carnegie Museum of Natural History, Special Publication, Pittsburgh, pp 155–161

Yaskin VA (2005) The annual cycle of spatial behavior and hippocampal volume in Sorex. In: Merrit JF, Churchfield S, Hutterer R, Sheftel BI (eds) Advances in the biology of shrews II. International Society of Shrew Biologists, New York, pp 373–385

Yopak KE, Lisney TJ, Darlington RB et al (2010) A conserved pattern of brain scaling from sharks to primates. Proc Natl Acad Sci USA 107:12946–12951. https://doi.org/10.1073/pnas.1002195107 CrossRefPubMedCentralPubMed

Title: Profound seasonal changes in brain size and architecture in the common shrew
Authors: Javier Lázaro
Moritz Hertel
Chet C. Sherwood
Marion Muturi
Dina K. N. Dechmann
Publication date: 01-07-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 6/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1666-5

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Profound seasonal changes in brain size and architecture in the common shrew

Abstract

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Abstract

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