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Growth of the Hippocampus in Bank Voles (Clethrionomys glareolus, Rodentia) from Different Seasonal Generations

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Abstract

Age-related variations in the hippocampus mass in the late postnatal ontogeny of bank voles (Clethrionomys glareolus) from the spring and autumn generations are considered in a comparative aspect. The mass of the hippocampus of the spring voles increases regularly over their short life cycle and approaches the values maximum for the species at two months of age. In the autumn voles, a two-peak growth curve is detected, the hippocampus increasing until September, after which an autumn-winter regression of the mass of this brain region was observed. The hippocampal growth of autumn voles resumed at the age of 7–9 months and coincided with the beginning of the period of reproduction. The hippocampus of autumn voles reached a definitive size at the age of 10–11 months. The results obtained characterize specific features of hippocampal growth in spring and autumn voles. The mechanisms that switch the alternative types of ontogeny of the seasonal generations are discussed.

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REFERENCES

  1. Amrein, I., Isler, K., and Lipp, H.-P., Comparing adult hippocampal neurogenesis in mammalian species and orders: influence of chronological age and life history stage, Eur. J. Neurosci., 2011, vol. 34, no. 6, pp. 978–987.

    Article  PubMed  Google Scholar 

  2. Amstislavskaya, T.S. and Balakhonov, V.S., Mitotic activity and its relationship with lifespan and metabolic rate in seasonal generations of the subarctic population of the vole Clethrionomys rutilus, Ekologiya, 1974, no. 4, pp. 80–83.

  3. Bartkowska, K., Djavadian, R.L., Taylor, J.R.E., and Turlejski, K., Generation recruitment and death of brain cells throughout the life cycle of Sorex shrews (Lypotyphla), Eur. J. Neurosci., 2008, vol. 27, pp. 1710–1721.

    Article  PubMed  Google Scholar 

  4. Burger, D.K., Saucier, J.M., Iwaniuk, A.N., and Saucier, D.M., Seasonal and sex differences in the hippocampus of wild rodents, Behav. Brain Res., 2013, vol. 236, pp. 131–138.

    Article  PubMed  Google Scholar 

  5. Burger, D.K., Gulbrandsen, T., Saucier, D.M., and Iwaniuk, A.N., The effects of season and sex on dentate gyrus size and neurogenesis in a wild rodent, Richardson’s ground squirrel (Urocitellus richardsonii), Neuroscience, 2014, vol. 272, pp. 240–251.

    Article  CAS  PubMed  Google Scholar 

  6. Cameron, H.A. and Glover, L.R., Adult neurogenesis: beyond learning and memory, Annu. Rev. Psychol., 2015, vol. 66, pp. 53–81.

    Article  PubMed  Google Scholar 

  7. Dark, J., Spears, N., Whaling, C.S., Wade, G.N., Meyer, J.S., and Zucker, I., Long day lengths promote brain growth in meadow voles, Dev. Brain Res., 1990, vol. 53, pp. 264–269.

    Article  CAS  Google Scholar 

  8. Donahue, C.P., Kosik, K.S., and Shors, T.J., Growth hormone is produced within the hippocampus where it responds to age, sex, and stress, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 6031–6036.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Duarte-Guterman, P., Yagi, S., Chow, C., and Galea, L.A.M., Hippocampal learning, memory, and neurogenesis: effects of sex and estrogens across the lifespan in adults. Horm. Behav., 2015, vol. 75, pp. 37–52.

    Article  CAS  Google Scholar 

  10. Filaretov, A.A., Nervnaya regulyatsiya gipofizarno-adrenokortikal’noi sistemy (Nervous Regulation of the Pituitary–Adrenocortical System), Leningrad: Nauka, 1979.

  11. Fuchs, E., Flügge, G., Ohl, F., Lucassen, P., Vollmann-Honsdorf, G.K., and Michaelis, T., Psychosocial stress, glucocorticoids, and structural alterations in the tree shrew hippocampus, Physiol. Behav., 2001, vol. 73, pp. 285–291.

    Article  CAS  PubMed  Google Scholar 

  12. Galea, L.A.M., Perrot-Sinal, T.S., Kavaliers, M., and Ossenkopp, K.P., Relations of hippocampal volume and dentate gyrus width to gonadal hormone levels in male and female meadow voles, Brain Res., 1999, vol. 821, pp. 383–391.

    Article  CAS  PubMed  Google Scholar 

  13. Galea, L.A.M., Uban, K.A., Epp, J.R., Brummelte, S., Barha, C.K., Wilson, W.L., Lieblich, S.E., and Pawluski, J.L., Endocrine regulation of cognition and neuroplasticity: our pursuit to unveil the complex interaction between hormones, the brain, and behaviour, Can. J. Exp. Psychol., 2008, vol. 62, no. 4, pp. 247–260.

    Article  PubMed  Google Scholar 

  14. Gould, E., How widespread is adult neurogenesis in mammals?, Nat. Rev. Neurosci., 2007, pp. 481–488.

  15. Haitlinger, R., Morphological analysis of the Wroclaw population of Clethrionomys glareolus (Schreber, 1780), Acta Theriol., 1965, vol. 10, pp. 243–272.

    Article  Google Scholar 

  16. Ivanter, E.V., Populyatsionnaya ekologiya melkikh mlekopitayushchikh taezhnogo Severo-Zapada SSSR (The Population Ecology of Small Mammals of the Taiga of the North-West of the USSR), Leningrad: Nauka, 1975.

  17. Jacobs, L.F. and Menzel, R., Navigation outside of the box: what the lab can learn from the field and what the field can learn from the lab, Mov. Ecol., 2014, vol. 2, no. 1, pp. 1–22.

    Article  CAS  Google Scholar 

  18. Jacobs, L.F. and Schenk, F., Unpacking the cognitive map: the parallel map theory of hippocampal function, Psychol. Rev., 2003, vol. 110, no. 2, pp. 285–315.

    Article  PubMed  Google Scholar 

  19. Jacobson, L. and Sapolsky, R., The role of hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis, Endocrinol. Rev., 1991, vol. 12, pp. 118–134.

    Article  CAS  Google Scholar 

  20. Karlsson, A.F., Age-differential homing tendencies in displaced bank voles, Clethrionomys glareolus, Anim. Behav., 1984, vol. 32, pp. 515–519.

    Article  Google Scholar 

  21. Koikegami, H., Amygdala and other related limbic structures experimental studies on the anatomy and function, Acta Med. Biol., 1964, vol. 12, pp. 73–266.

    CAS  PubMed  Google Scholar 

  22. Kravchenko, L.B., Zav’yalov, and Moskvitina, N.S., Sexual maturation and age-related dynamics of corticosterone in two species of forest voles (Clethrionomys, Rodentia, Cricetidae), Zool. Zh., 2011, vol. 90, no. 12, pp. 1522–1529.

    Google Scholar 

  23. Krebs, J.R., Sherry, D.F., Healey, S.D., Perry, V.H., and Vaccarino, A.L., Hippocampal specialization of food-storing birds, Proc. Natl. Acad. Sci. U. S. A., 1989, vol. 86, pp. 1388–1392.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lavenex, P., Steele, M.A., and Jacobs, L.F., The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels, Eur. J. Neurosci., 2000, vol. 12, pp. 643–648.

    Article  CAS  PubMed  Google Scholar 

  25. Lopatina, N.G., Ponomarenko, V.V., and Smirnova, G.P., The hypothesis of nervous regulation of the process of realization of hereditary information, in Problemy vysshei nervnoi deyatel’nosti i neirofiziologii (Problems of Higher Nervous Activity and Neurophysiology), Leningrad: Nauka, 1975, pp. 107–120.

  26. Maklakov, K.V., Olenev, G.V., and Kryazhimskii, F.V., Types of ontogeny and territorial distribution of small rodents, Russ. J. Ecol., 2004, vol. 35, no. 5, pp. 324–331.

    Article  Google Scholar 

  27. Mihok, S., Chitty’s hypothesis and behaviour in subarctic red-backed voles Clethrionomys gappery, Oikos, 1981, vol. 36, pp. 281–295.

    Article  Google Scholar 

  28. Mizoguchi, K., Kunishita, T., Chui, D.H., and Tabira, T., Stress induces neuronal death in the hippocampus of castrated rats, Neurosci. Lett., 1992, vol. 138, pp. 157–160.

    Article  CAS  PubMed  Google Scholar 

  29. O’Keefe, J. and Nadel, L., The Hippocampus as a Cognitive Map, Oxford: Clarendon Press, 1978.

    Google Scholar 

  30. Olenev, G.V., Determining the age of cyclomorphic rodents: functional–ontogenetic determination, ecological aspects, Russ. J. Ecol., 2009, vol. 40, no. 2, pp. 93–104.

    Article  Google Scholar 

  31. Pawluski, J.L. and Galea, L.A., Hippocampal morphology is differentially affected by reproductive experience in the mother, J. Neurobiol., 2006, vol. 66, no. 1, pp. 71–81.

    Article  PubMed  Google Scholar 

  32. Praag, H., van Schinder, A.F., Christie, B.R., Toni, N., Palmer, T.D., and Gage, F.H., Functional neurogenesis in the adult hippocampus, Nature, 2002, vol. 415, pp. 1030–1034.

    Article  PubMed  CAS  Google Scholar 

  33. Pyter, L.M., Reader, B.F., and Nelson, R.J., Short photoperiods impair spatial learning and alter hippocampal dendritic morphology in adult male white-footed mice (Peromyscus leucopus), J. Neurosci., 2005, vol. 25, no. 18, pp. 4521–4526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Riss, W., Barstein, S.D., and Johnson, R.W., Hippocampal or pyriform lobe damage in infancy and endocrine development of rats, Am. J. Physiol., 1963, vol. 204, pp. 861–866.

    Article  CAS  PubMed  Google Scholar 

  35. Rosell, D.R. and Siever, L.J., The neurobiology of aggression and violence, CNS Spectrums, 2015, vol. 20, pp. 254–279.

    Article  PubMed  Google Scholar 

  36. Sacher, G.A. and Staffeldt, E.F., Relation of gestation time to brain weight for placental mammals: implications for the theory of vertebrate growth, Am. Nat., 1974, vol. 108, no. 963, pp. 593–615.

    Article  Google Scholar 

  37. Shtainlekhner, S. and Pukhal’skii, V., Seasonal regulation of reproduction of small mammals, Sib. Ekol. Zh., 1999, no. 1, pp. 23–35.

  38. Shvarts, S.S., Ishchenko, V.G., Ovchinnikova, N.A., Olenev, V.G., Pokrovskii, A.V., and Pyastolova, O.A., Alternation of generations and lifespan of rodents, Zh. Obshch. Biol., 1964, vol. 25, no. 6, pp. 417–433.

    CAS  PubMed  Google Scholar 

  39. Spritzer, M.D., Panning, A.W., Engelman, S.M., Prince, W.T., Casler, A.E., et al., Seasonal and sex differences in cell proliferation, neurogenesis, and cell death within the dentate gyrus of adult wild-caught meadow voles, Neuroscience, 2017, vol. 360, pp. 155–165.

    Article  CAS  PubMed  Google Scholar 

  40. Tarakhtii, E.A. and Davydova, Yu.A., Seasonal variation in hematological indices in bank vole (Clethrionomys glareolus) in different reproductive states, Biol. Bull. (Moscow), 2007, vol. 34, no. 1, pp. 9–19.

    Article  CAS  Google Scholar 

  41. Tupikova, N.V., Sidorova, G.A., and Konovalova, E.A., Determinant of the age of forest voles, in Fauna i ekologiya gryzunov (Fauna and Ecology of Rodents), Moscow: Mosk. Gos. Univ., 1970, no. 9, pp. 160–167.

  42. Turlejski, K., Michalski, A., Bartkowska, K., Shchipanov, N.A., Tumasian, F., Taylor, J., and Djavadian, R., New data on brain mechanisms of the Dehnel effect and age-dependent behavior in Sorex araneus, in Advances in Biology of Shrews III. Materials of the International Conference, Moscow: KMK Scientific Press, 2010, pp. 69–70.

  43. Walton, J.C., Aubrecht, T.G., Weil, Z.M., Leuner, B., and Nelson, R.J., Photoperiodic regulation of hippocampal neurogenesis in adult male white-footed mice (Peromyscus leucopus), Eur. J. Neurosci., 2014, vol. 40, pp. 2674–2679.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Workman, J.L., Bowers, S.L., and Nelson, R.J., Enrichment and photoperiod interact to affect spatial learning and hippocampal dendritic morphology in white-footed mice (Peromiscus leucopus), Eur. J. Neurosci., 2009, vol. 29, pp. 161–170.

    PubMed  Google Scholar 

  45. Workman, J.L., Manny, N., Walton, J.C., and Nelson, R.J., Short day length alter stress and depressive-like responses, and hippocampal morphology in Siberian hamsters, Horm. Behav., 2011, vol. 60, pp. 520–528.

    Article  CAS  PubMed  Google Scholar 

  46. Yaskin, V.A., The response of bank voles to winter conditions, drought, and changes in population density, Ekologiya, 1981, no. 1, pp. 46–54.

  47. Yaskin, V.A., Seasonal changes in brain morphology in small mammals, in Winter Ecology of Small Mammals, Special Publication of Carnegie Museum of Natural History no. 10, Pittsburgh, 1984, pp. 183–191.

  48. Yaskin, V.A., Seasonal and annual variability of the features of the growth of the brain of narrow-headed voles (Microtus gregalis), Zool. Zh., 1988, vol. 67, no. 3, pp. 438–447.

    Google Scholar 

  49. Yaskin, V.A., Seasonal changes in the size of the brain and skull of small mammals, Zh. Obshch. Biol., 1989, vol. 50, no. 4, pp. 470–480.

    Google Scholar 

  50. Yaskin, V.A., The annual cycle of spatial behavior and hippocampal volume in Sorex, in Advances in the Biology of Shrews II, Special Publication of the International Society of Shrew Biologists no. 01, New York, 2005, pp. 373–385.

  51. Yaskin, V.A., Seasonal modulation of sex-related differences in hippocampus size and spatial behavior in bank voles, Clethrionomys glareolus (Rodentia, Cricetidae), Russ. J. Ecol., 2013, vol. 44, no. 3, pp. 221–226.

    Article  Google Scholar 

  52. Yaskin, V.A., A rapid method for assessing the macromorphological features of the brain of small mammals, Zool. Zh., 2016, vol. 95, no. 3, pp. 366–369.

    Google Scholar 

  53. Yaskin, V.A., Features of brain growth in the back vole (Clethrionomys glareolus, Rodentia) of different seasonal generations, Zool. Zh., 2018, vol. 97, no. 3, pp. 343–347.

    Google Scholar 

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  1. Biological Faculty, Moscow State University, 119992, Moscow, Russia

    V. A. Yaskin

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Yaskin, V.A. Growth of the Hippocampus in Bank Voles (Clethrionomys glareolus, Rodentia) from Different Seasonal Generations. Biol Bull Russ Acad Sci 47, 1051–1058 (2020). https://doi.org/10.1134/S1062359020080154

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