Psychopharmacology

, Volume 204, Issue 2, pp 361–373 | Cite as

Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety

  • Alexia Thomas
  • April Burant
  • Nghiem Bui
  • Deanna Graham
  • Lisa A. Yuva-Paylor
  • Richard Paylor
Original Investigation

Abstract

Rationale

An increasing number of investigators utilize the marble-burying assay despite the paucity of information available regarding what underlies the behavior.

Objectives

We tested the possibility that a genetic component underlies marble burying in mice and if there is a genetic correlation with other anxiety-like traits. Since findings reported in the literature indicate that marble-burying behavior reflects an anxiety-like response, we explored the assumption that the novel nature of a marble induces this anxiety. Finally, we investigated how the natural response of a mouse to dig relates to the marble-burying phenomenon.

Methods

We examined ten different inbred mouse strains to determine if marble-burying behavior is genetically regulated and correlated with anxiety-like traits in two other assays. We employed multiple variants of the “traditional” marble-burying assay to address how issues such as the novelty of marbles and digging behavior contribute to marble burying.

Results

Marble-burying behavior varied across strain and did not correlate with anxiety measures in other assays. Multiple tests conducted to reduce the novelty of marbles failed to alter burying behavior. Additionally, digging behavior correlated with marble burying, and the presence of marbles did not significantly impact the digging response.

Conclusions

Our results indicate that mouse marble burying is genetically regulated, not correlated with other anxiety-like traits, not stimulated by novelty, and is a repetitive behavior that persists/perseveres with little change across multiple exposures. Marble burying is related to digging behavior and may in fact be more appropriately considered as an indicative measure of repetitive digging.

Keywords

Marble burying Anxiety Perseverative Obsessive–compulsive Digging 

Notes

Acknowledgments

This work was supported by the Baylor Fragile X Center and the Baylor EKS IDDRC (NICHD, HD24064). A.T. and A.B. received partial support from NIGMS training grants T32 GM08307 and TM GM008507, respectively. We would like to thank Dr. Corinne Spencer, Shannon Hamilton, and Randi-Michelle Cowin for their valuable input and suggestions during the course of this study.

References

  1. Adams N, Boice R (1981) Mouse (Mus) burrows: effects of age, strain, and domestication. Anim Learn Behav 9:140–144Google Scholar
  2. Berry RJ (1968) The ecology of an island population of the house mouse. J Anim Ecol 37(2):445–470CrossRefGoogle Scholar
  3. Boice R (1977) Burrows of wild and albino rats: effects of domestication, outdoor raising, age, experience, and maternal state. J Comp Physiol Psychol 91(3):649–661PubMedCrossRefGoogle Scholar
  4. Boice R, Adams N (1980) Outdoor enclosures for feralizing rats and mice. Behav Res Meth Instrum 12:577–582Google Scholar
  5. Bolivar VJ, Caldarone BJ, Reilly AA, Flaherty L (2000) Habituation of activity in an open field: a survey of inbred strains and F1 hybrids. Behav Genet 20(4):285–293CrossRefGoogle Scholar
  6. Bolles RC (1970) Species-specific defense reactions and avoidance learning. Psychol Rev 77(1):32–48CrossRefGoogle Scholar
  7. Borsini F, Podhorna J, Marazziti D (2002) Do animal models of anxiety predict anxiolytic-like effects of antidepressants? Psychopharmacology 163:121–141 doi: 10.1007/s00213-002-1155-6 PubMedCrossRefGoogle Scholar
  8. Bouchard PR, Lynch CB (1989) Burrowing behavior in wild house mice: variation within and between populations. Behav Genet 19(3):447–456PubMedCrossRefGoogle Scholar
  9. Bouwknecht JA, Paylor R (2002) Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains. Behav Brain Res 136:489–501PubMedCrossRefGoogle Scholar
  10. 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 126:223–229PubMedCrossRefGoogle Scholar
  11. Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, Wehner JM, Wynshaw-Boris A, Paylor R (1997) Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology 132:107–124PubMedCrossRefGoogle Scholar
  12. Deacon RMJ, Rawlins JNP (2005) Hippocampal lesions, species-typical behaviours and anxiety in mice. Behav Brain Res 156:241–249 doi: 10.1016/j.bbr.2004.05.027 PubMedCrossRefGoogle Scholar
  13. De Boer SF, Koolhaas JM (2003) Defensive burying in rodents: ethology, neurobiology and psychopharmacology. Eur J Pharmacol 463:145–161 doi: 10.1016/S0014-2999(03)01278-0 PubMedCrossRefGoogle Scholar
  14. Dodart JC, Mathis C, Ungerer A (1997) Scopolamine-induced deficits in a two-trial object recognition task in mice. Neuroreport 8(5):1173–1178PubMedCrossRefGoogle Scholar
  15. Dudek BC, Adams N, Boice R, Abbott ME (1983) Genetic influences on digging behaviors in mice (Mus musculus) in laboratory and seminatural settings. J Comp Psychol 97(3):249–259PubMedCrossRefGoogle Scholar
  16. File SE (1996) Recent developments in anxiety, stress, and depression. Pharmacol Biochem Behav 54(1):3–12PubMedCrossRefGoogle Scholar
  17. Fleming TH, Brown GJ (1975) An experimental analysis of seed hoarding and burrowing behavior in two species of Costa Rican heteromyid rodents. J Mammal 56(2):301–315CrossRefGoogle Scholar
  18. Gyertyán I (1995) Analysis of the marble burying response: marbles serve to measure digging rather than evoke burying. Behav Pharmacol 6:24–31PubMedCrossRefGoogle Scholar
  19. Homanics GE, Quinlan JJ, Firestone LL (1999) Pharmacologic and behavioral responses of inbred C57BL/6J and strain 129/SvJ mouse lines. Pharmacol Biochem Behav 63(1):21–26PubMedCrossRefGoogle Scholar
  20. Hughes BO, Duncan IJH (1988) The notion of ethological ‘need’, models of motivation and animal welfare. Anim Behav 36(6):1696–1707CrossRefGoogle Scholar
  21. Hughes BO, Duncan IJH, Brown MF (1989) The performance of nest building by domestic hens: is it more important than construction of a nest? Anim Behav 37(2):210–214CrossRefGoogle Scholar
  22. Ichimaru Y, Egawa T, Sawa A (1995) 5-HT1A-receptor subtype mediates the effect of fluvoxamine, a selective serotonin reuptake inhibitor, on marble-burying behavior in mice. Jpn J Pharmacol 68:65–70PubMedCrossRefGoogle Scholar
  23. Kitaoka A (1994) Defensive aspects of burrowing behavior in rats (Rattus norvegicus): a descriptive and correlational study. Behav Processes 31:13–28CrossRefGoogle Scholar
  24. Li X, Morrow D, Witkin JM (2006) Decreases in nestlet shredding of mice by serotonin uptake inhibitors: comparison with marble burying. Life Sci 78(17):1933–1939PubMedCrossRefGoogle Scholar
  25. Londei T, Valentini AMV, Leone VG (1998) Investigative burying by laboratory mice may involve non-functional, compulsive, behaviour. Behav Brain Res 94:249–254PubMedCrossRefGoogle Scholar
  26. Masuda Y, Ishigooka S, Matsuda Y (2000) Digging behavior of ddY mouse. Exp Anim 49(3):235–237PubMedCrossRefGoogle Scholar
  27. McNab BK (1966) The metabolism of fossorial rodents: a study of convergence. Ecology 47(5):712–733CrossRefGoogle Scholar
  28. Milner LC, Crabbe JC (2008) Three murine anxiety models: results from multiple inbred strain comparisons. Genes Brain Behav 7:496–505 doi: 10.1111/j.1601-183X.2007.00385.x PubMedCrossRefGoogle Scholar
  29. Nicolas LB, Kolb Y, Prinssen EPM (2006) A combined marble burying-locomotor activity test in mice: a practical screening test with sensitivity to different classes of anxiolytics and antidepressants. Eur J Pharmacol 547:106–115 doi: 10.1016/j.ejphar.2006.07.015 PubMedCrossRefGoogle Scholar
  30. Njung’e K, Handley SL (1991a) Evaluation of marble-burying behavior as a model of anxiety. Pharmacol Biochem Behav 38(1):63–67PubMedCrossRefGoogle Scholar
  31. Njung’e K, Handley SL (1991b) 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 104:105–112PubMedGoogle Scholar
  32. Pinel JPJ, Treit D (1978) Burying as a defensive response in rats. J Comp Physiol Psychol 92(4):708–712CrossRefGoogle Scholar
  33. Pinel JPJ, Symons LA, Christensen BK, Tees RC (1989) Development of defensive burying in Rattus norvegicus: experience and defensive responses. J Comp Psychol 103(4):359–365PubMedCrossRefGoogle Scholar
  34. Poling A, Cleary J, Monaghan M (1981) Burying by rats in response to aversive and nonaversive stimuli. J Exp Anal Behav 35:31–44PubMedCrossRefGoogle Scholar
  35. Rogers DC, Jones DNC, Nelson PR, Jones CM, Quilter CA, Robinson TL, Hagan JJ (1999) Use of SHIRPA and discriminant analysis to characterise marked differences in the behavioural phenotype of six inbred mouse strains. Behav Brain Res 105:207–217PubMedCrossRefGoogle Scholar
  36. Ruffer DG (1965) Burrows and burrowing behavior of Onychomys leucogaster. J Mammal 46(2):241–247CrossRefGoogle Scholar
  37. Schmid-Holmes S, Drickamer LC, Robinson AS, Gillie LL (2001) Burrows and burrow-cleaning behavior of house mice (Mus musculus domesticus). Am Midl Nat 146:53–62CrossRefGoogle Scholar
  38. Sherwin CM, Haug E, Terkelsen N, Vadgama M (2004) Studies on the motivation for burrowing by laboratory mice. Appl Anim Behav Sci 88:343–358 doi: 10.1016/j.applanim.2004.03.009 CrossRefGoogle Scholar
  39. Studier EH, Baca TP (1968) Atmospheric conditions in artificial rodent burrows. Southwest Nat 13(4):401–410CrossRefGoogle Scholar
  40. Takeuchi H, Yatsugi S, Yamaguchi T (2002) Effect of YM992, a novel antidepressant with selective serotonin re-uptake inhibitory and 5-HT2A receptor antagonistic activity, on a marble-burying behavior test as an obsessive-compulsive disorder model. Jpn J Pharmacol 90:197–200PubMedCrossRefGoogle Scholar
  41. Terlecki LJ, Pinel JPJ, Treit D (1979) Conditioned and unconditioned defensive burying in the rat. Learn Motiv 10:337–350CrossRefGoogle Scholar
  42. Treit D, Fundytus M (1989) Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 31:959–962CrossRefGoogle Scholar
  43. Treit D, Pinel JPJ, Fibiger HC (1981) Conditioned defensive burying: a new paradigm for the study of anxiolytic agents. Pharmacol Biochem Behav 15(4):619–626PubMedCrossRefGoogle Scholar
  44. Trullas R, Skolnick P (1993) Differences in fear motivated behaviors among inbred mouse strains. Psychopharmacology 111:323–331PubMedCrossRefGoogle Scholar
  45. van Gaalen MM, Steckler T (2000) Behavioural analysis of four mouse strains in an anxiety test battery. Behav Brain Res 115:95–106PubMedCrossRefGoogle Scholar
  46. Webster DG, Williams MH, Owens RD, Geiger VB, Dewsbury DA (1981) Digging behavior in 12 taxa of muroid rodents. Anim Learn Behav 9(2):173–177Google Scholar
  47. Wilkie DM, MacLennan AJ, Pinel JPJ (1979) Rat defensive behavior: burying noxious food. J Exp Anal Behav 31(3):299–306PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Alexia Thomas
    • 1
  • April Burant
    • 2
  • Nghiem Bui
    • 2
  • Deanna Graham
    • 2
  • Lisa A. Yuva-Paylor
    • 2
  • Richard Paylor
    • 1
    • 2
  1. 1.Department of NeuroscienceBaylor College of MedicineHoustonUSA
  2. 2.Molecular and Human GeneticsBaylor College of MedicineHoustonUSA

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