Corticosterone level and central dopaminergic activity involved in agile and exploratory behaviours in formosan wood mice (Apodemus semotus)

Original Paper
  • 22 Downloads

Abstract

The native Formosan wood mouse (Apodemus semotus) is the dominant rodent in Taiwan. In their natural environment, Formosan wood mice exhibit high locomotor activity, including searching and exploratory behaviours, which is observed similarly in the laboratory environment. How the behavioural responses of Formosan wood mice exhibit in elevated plus maze and marble burying tests remains unclear. How corticosterone levels and central dopaminergic activities are related to the behaviours in these tests is also unclear. This study compared the behaviours of Formosan wood mice with that of C57BL/6J mice using the elevated plus maze and marble burying tests, and measured the corticosterone levels and central dopaminergic activities. Formosan wood mice showed greater locomotor and exploratory activity than the C57BL/6J mice. Similarly, the marble burying and rearing numbers were higher for Formosan wood mice. High locomotor and exploratory behaviours were strongly correlated with corticosterone levels after acute mild restraint stress in Formosan wood mice. The anxiolytic, diazepam, reduced the high exploratory activity, corticosterone levels and central dopaminergic activities. The high locomotor and exploratory behaviours of Formosan wood mice are related to the corticosterone levels and central dopaminergic activities. These data may explain Formosan wood mice dominance in the intermediate altitude of Taiwan.

Keywords

Glucocorticoid Locomotion Medial prefrontal cortex Striatum Taiwan wood mice 

Abbreviations

DA

Dopamine

DOPAC

3,4-Dihydroxyphenylacetic acid

MPFC

Medial prefrontal cortex

NA

Nucleus accumbens

ST

Striatum

Notes

Acknowledgements

We are grateful for the technical assistance from C. Y. Lee, R. J. Chen and the Laboratory Animal Center at Tzu Chi University. We would like to thank Editor-in-Chief, Professor Friedrich G. Barth, for his insightful comments, and Professors M. H. Wang and L. K. Lin for helpful comments. We would like to thank Ms. Natasha Tomicic for her help with language editing. This study was supported in part by Ministry of Science and Technology in Taiwan (103-2410-H-277-001 to SCY and 99-2320-B-320-011-MY3, 104-2320-B-320-005 and 105-2320-B-320-011-MY3 to KRS) and the Tzu Chi Foundation (TCRPP103015, TCRPP105002 and TCMRC-P-103007 to KRS). The funding agency had no role in experimental design, data collection and analysis, decision to publish, or preparation of the manuscript. All procedures and experimental protocols in studies involving animals were in accordance with the ethical standards and were approved by the Institutional Animal Care and Use Committee of Tzu Chi University. The institutional guidelines were followed for the care and use of animals and conducted in accordance with the European Community Council Directive of 24th November 1986 (86/609/EEC).

Author contributions

KRS and SCY contributed to study concept and design, acquisition of data, research performance, statistical analysis, interpretation of data, and approval of the final version of the manuscript; SCY contributed to drafting of the manuscript. All authors reviewed the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests related to this work.

Supplementary material

359_2018_1259_MOESM1_ESM.pdf (251 kb)
Supplementary material 1 (PDF 250 KB)

References

  1. An XL, Zou JX, Wu RY, Yang Y, Tai FD, Zeng SY, Jia R, Zhang X, Liu EQ, Broders H (2011) Strain and sex differences in anxiety-like and social behaviors in C57BL/6J and BALB/cJ mice. Exp Anim 60:111–123CrossRefPubMedGoogle Scholar
  2. Bardo MT, Donohew RL, Harrington NG (1996) Psychobiology of novelty seeking and drug seeking behavior. Behav Brain Res 77:23–43CrossRefPubMedGoogle Scholar
  3. Bouwknecht JA, van der Gugten J, Groenink L, Olivier B, Paylor RE (2004) Behavioral and physiological mouse models for anxiety: effects of flesinoxan in 129S6/SvEvTac and C57BL/6J mice. Eur J Pharmacol 494:45–53CrossRefPubMedGoogle Scholar
  4. Broekkamp CL, Rijk HW, Joly-Gelouin D, Lloyd KL (1986) Major tranquillizers can be distinguished from minor tranquillizers on the basis of effects on marble burying and swim-induced grooming in mice. Eur J Pharmacol 126:223–229CrossRefPubMedGoogle Scholar
  5. Bronikowski AM, Carter PA, Swallow JG, Girard IA, Rhodes JS, Garland T Jr (2001) Open-field behavior of house mice selectively bred for high voluntary wheel-running. Behav Genet 31:309–316CrossRefPubMedGoogle Scholar
  6. Buesching CD, Newman C, Twell R, Macdonald DW (2008) Reasons for arboreality in wood mice Apodemus sylvaticus and Bank voles Myodes glareolus. Mamm Biol 73:318–324CrossRefGoogle Scholar
  7. Carola V, D’Olimpio F, Brunamonti E, Mangia F, Renzi P (2002) Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res 134:49–57CrossRefPubMedGoogle Scholar
  8. Deacon RM (2006) Digging and marble burying in mice: simple methods for in vivo identification of biological impacts. Nat Protoc 1:122–124CrossRefPubMedGoogle Scholar
  9. Depino AM, Gross C (2007) Simultaneous assessment of autonomic function and anxiety-related behavior in BALB/c and C57BL/6 mice. Behav Brain Res 177:254–260CrossRefPubMedGoogle Scholar
  10. Ebada ME, Kendall DA, Pardon MC (2016) Corticosterone and dopamine D2/D3 receptors mediate the motivation for voluntary wheel running in C57BL/6J mice. Behav Brain Res 311:228–238CrossRefPubMedGoogle Scholar
  11. Franklin KBJ, Paxinos G (1997) The mouse brain in stereotaxic coordinates. Academic Press, San DiegoGoogle Scholar
  12. Gil-Bea FJ, Aisa B, Schliebs R, Ramirez MJ (2007) Increase of locomotor activity underlying the behavioral disinhibition in tg2576 mice. Behav Neurosci 121:340–344CrossRefPubMedGoogle Scholar
  13. Gorton LM, Vuckovic MG, Vertelkina N, Petzinger GM, Jakowec MW, Wood RI (2010) Exercise effects on motor and affective behavior and catecholamine neurochemistry in the MPTP-lesioned mouse. Behav Brain Res 213:253–262CrossRefPubMedPubMedCentralGoogle Scholar
  14. Graf EN et al (2013) Corticosterone acts in the nucleus accumbens to enhance dopamine signaling and potentiate reinstatement of cocaine seeking. J Neurosci 33:11800–11810CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hauser T, Klaus F, Lipp HP, Amrein I (2009) No effect of running and laboratory housing on adult hippocampal neurogenesis in wild caught long-tailed wood mouse. BMC Neurosci 10:43CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hayashi E, Kuratani K, Kinoshita M, Hara H (2010) Pharmacologically distinctive behaviors other than burying marbles during the marble burying test in mice. Pharmacology 86:293–296CrossRefPubMedGoogle Scholar
  17. Huang BM, Lin LK, Alexander PS (1997) Annual reproductive cycle of the Formosan wood mouse, Apodemus semotus. Zool Stud 36:17–25Google Scholar
  18. Kalivas PW, Stewart J (1991) Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res Brain Res Rev 16:223–244CrossRefPubMedGoogle Scholar
  19. Kennedy HF, Elwood RW (1988) Strain differences in the inhibition of infanticide in male mice (Mus musculus). Behav Neural Biol 50:349–353CrossRefPubMedGoogle Scholar
  20. Kuroda N (1952) Mammalogical history of Formosa with zoogeography and bioliography. Quart J Taiwan Mus 4:262–304Google Scholar
  21. Kuwahara S, Mizukami T, Omura M, Hagihara M, Iinuma Y, Shimizu Y, Tamada H, Tsukamoto Y, Nishida T, Sasaki F (2000) Seasonal changes in the hypothalamo-pituitary-testes axis of the Japanese wood mouse (Apodemus speciosus). Anat Rec 260:366–372CrossRefPubMedGoogle Scholar
  22. Lalonde R, Strazielle C (2008) Relations between open-field, elevated plus-maze, and emergence tests as displayed by C57/BL6J and BALB/c mice. J Neurosci Methods 171:48–52CrossRefPubMedGoogle Scholar
  23. Lee CY, Alexander PS, Yang VVC, Yu JYL (2001) Seaonal reproductive activity of male Formosan wood mice (Apodemus semotus): relationships to androgen levels. J Mammal 82:700–708CrossRefGoogle Scholar
  24. Lejeune H, Huynen MC, Ferrara A (2000) Temporal differentiation in two strains of small rodents: a wood mouse (Apodemus sylvaticus) and an albino mouse (Mus musculus OF1). Behav Processes 52:155–169CrossRefPubMedGoogle Scholar
  25. Lepicard EM, Joubert C, Hagneau I, Perez-Diaz F, Chapouthier G (2000) Differences in anxiety-related behavior and response to diazepam in BALB/cByJ and C57BL/6J strains of mice. Pharmacol Biochem Behav 67:739–748CrossRefPubMedGoogle Scholar
  26. Lin LK, Shiraishi S (1992a) Demography of the Formosan wood mouse, Apodemus semotus. J Fac Agric Kyushu Univ 36:245–266Google Scholar
  27. Lin LK, Shiraishi S (1992b) Reproductive biology of the Formosan wood mouse, Apodemus semotus. J Fac Agric Kyushu Univ 36:183–200Google Scholar
  28. Lin LK, Nishino T, Shiraishi S (1993) Postnatal growth and development of the Formosan wood mouse, Apodemus semotus. J Mamm Soc Jpn 18:1–18Google Scholar
  29. Lister RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 92:180–185PubMedGoogle Scholar
  30. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  31. Matsuda S, Matsuzawa D, Ishii D, Tomizawa H, Sutoh C, Nakazawa K, Amano K, Sajiki J, Shimizu E (2012) Effects of perinatal exposure to low dose of bisphenol A on anxiety like behavior and dopamine metabolites in brain. Prog Neuropsychopharmacol Biol Psychiatry 39:273–279CrossRefPubMedGoogle Scholar
  32. Njung’e K, Handley SL (1991) Effects of 5-HT uptake inhibitors, agonists and antagonists on the burying of harmless objects by mice; a putative test for anxiolytic agents. Br J Pharmacol 104:105–112CrossRefPubMedPubMedCentralGoogle Scholar
  33. Palkovits M (1983) Punch sampling biopsy technique. Methods Enzymol 103:368–376CrossRefPubMedGoogle Scholar
  34. Perrigo G, Belvin L, Quindry P, Kadir T, Becker J, van Look C, Niewoehner J, vom Saal FS (1993) Genetic mediation of infanticide and parental behavior in male and female domestic and wild stock house mice. Behav Genet 23:525–531CrossRefPubMedGoogle Scholar
  35. Romero LM, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc Natl Acad Sci USA 98:7366–7370CrossRefPubMedPubMedCentralGoogle Scholar
  36. Rosalino LM, Nobrega F, Santos-Reis M, Teixeira G, Rebelo R (2013) Acorn selection by the wood mouse Apodemus sylvaticus: a semi-controlled experiment in a Mediterranean environment. Zoolog Sci 30:724–730CrossRefPubMedGoogle Scholar
  37. Shieh KR, Lee HJ, Yang SC (2008) Different patterns of food consumption and locomotor activity among Taiwanese native rodents, Formosan wood mice (Apodemus semotus), and common laboratory mice, C57BL/6 (Mus musculus). Chin J Physiol 51:129–135PubMedGoogle Scholar
  38. Sorregotti T, Mendes-Gomes J, Rico JL, Rodgers RJ, Nunes-de-Souza RL (2013) Ethopharmacological analysis of the open elevated plus-maze in mice. Behav Brain Res 246:76–85CrossRefPubMedGoogle Scholar
  39. Takechi R, Hayashi F (2012) Historical effects on local variation in walnut-feeding behavior by the Japanese wood mouse, Apodemus speciosus. Zoolog Sci 29:71–78CrossRefPubMedGoogle Scholar
  40. Tosh DG, McDonald RA, Bearhop S, Llewellyn NR, Montgomery WI, Shore RF (2012) Rodenticide exposure in wood mouse and house mouse populations on farms and potential secondary risk to predators. Ecotoxicology 21:1325–1332CrossRefPubMedGoogle Scholar
  41. Verret L, Krezymon A, Halley H, Trouche S, Zerwas M, Lazouret M, Lassalle JM, Rampon C (2013) Transient enriched housing before amyloidosis onset sustains cognitive improvement in Tg2576 mice. Neurobiol Aging 34:211–225CrossRefPubMedGoogle Scholar
  42. Voikar V, Polus A, Vasar E, Rauvala H (2005) Long-term individual housing in C57BL/6J and DBA/2 mice: assessment of behavioral consequences. Genes brain behavior 4:240–252CrossRefGoogle Scholar
  43. Volle J, Brocard J, Saoud M, Gory-Faure S, Brunelin J, Andrieux A, Suaud-Chagny MF (2013) Reduced expression of STOP/MAP6 in mice leads to cognitive deficits. Schizophr Bull 39:969–978CrossRefPubMedGoogle Scholar
  44. Walf AA, Frye CA (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2:322–328CrossRefPubMedPubMedCentralGoogle Scholar
  45. Yang SC, Shieh KR (2007) Gonadal hormones-mediated effects on the stimulation of dopamine turnover in mesolimbic and nigrostriatal systems by cocaine- and amphetamine-regulated transcript (CART) peptide in male rats. Neuropharmacology 53:801–809CrossRefPubMedGoogle Scholar
  46. Yang SC, Shieh KR, Li HY (2005) Cocaine- and amphetamine-regulated transcript in the nucleus accumbens participates in the regulation of feeding behavior in rats. Neuroscience 133:841–851CrossRefPubMedGoogle Scholar
  47. Yu HT (1993) Natural history of small mammals along a subtrophical elevation gradient in central Taiwan. J Zool (Lond) 234:577–600CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PhysiologyTzu Chi UniversityHualienTaiwan
  2. 2.Holistic Education CenterTzu Chi University of Science and TechnologyHualienTaiwan

Personalised recommendations