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

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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.

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References

  • Adams N, Boice R (1981) Mouse (Mus) burrows: effects of age, strain, and domestication. Anim Learn Behav 9:140–144

    Google Scholar 

  • Berry RJ (1968) The ecology of an island population of the house mouse. J Anim Ecol 37(2):445–470

    Article  Google Scholar 

  • 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):649–661

    Article  PubMed  CAS  Google Scholar 

  • Boice R, Adams N (1980) Outdoor enclosures for feralizing rats and mice. Behav Res Meth Instrum 12:577–582

    Google Scholar 

  • 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):285–293

    Article  Google Scholar 

  • Bolles RC (1970) Species-specific defense reactions and avoidance learning. Psychol Rev 77(1):32–48

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bouchard PR, Lynch CB (1989) Burrowing behavior in wild house mice: variation within and between populations. Behav Genet 19(3):447–456

    Article  PubMed  CAS  Google Scholar 

  • Bouwknecht JA, Paylor R (2002) Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains. Behav Brain Res 136:489–501

    Article  PubMed  Google Scholar 

  • 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 126:223–229

    Article  PubMed  CAS  Google Scholar 

  • 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 132:107–124

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Dodart JC, Mathis C, Ungerer A (1997) Scopolamine-induced deficits in a two-trial object recognition task in mice. Neuroreport 8(5):1173–1178

    Article  PubMed  CAS  Google Scholar 

  • 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):249–259

    Article  PubMed  CAS  Google Scholar 

  • File SE (1996) Recent developments in anxiety, stress, and depression. Pharmacol Biochem Behav 54(1):3–12

    Article  PubMed  CAS  Google Scholar 

  • 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):301–315

    Article  Google Scholar 

  • Gyertyán I (1995) Analysis of the marble burying response: marbles serve to measure digging rather than evoke burying. Behav Pharmacol 6:24–31

    Article  PubMed  Google Scholar 

  • 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):21–26

    Article  PubMed  CAS  Google Scholar 

  • Hughes BO, Duncan IJH (1988) The notion of ethological ‘need’, models of motivation and animal welfare. Anim Behav 36(6):1696–1707

    Article  Google Scholar 

  • 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):210–214

    Article  Google Scholar 

  • 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 68:65–70

    Article  PubMed  CAS  Google Scholar 

  • Kitaoka A (1994) Defensive aspects of burrowing behavior in rats (Rattus norvegicus): a descriptive and correlational study. Behav Processes 31:13–28

    Article  Google Scholar 

  • 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):1933–1939

    Article  PubMed  CAS  Google Scholar 

  • Londei T, Valentini AMV, Leone VG (1998) Investigative burying by laboratory mice may involve non-functional, compulsive, behaviour. Behav Brain Res 94:249–254

    Article  PubMed  CAS  Google Scholar 

  • Masuda Y, Ishigooka S, Matsuda Y (2000) Digging behavior of ddY mouse. Exp Anim 49(3):235–237

    Article  PubMed  CAS  Google Scholar 

  • McNab BK (1966) The metabolism of fossorial rodents: a study of convergence. Ecology 47(5):712–733

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Njung’e K, Handley SL (1991a) Evaluation of marble-burying behavior as a model of anxiety. Pharmacol Biochem Behav 38(1):63–67

    Article  PubMed  Google Scholar 

  • 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 104:105–112

    PubMed  Google Scholar 

  • Pinel JPJ, Treit D (1978) Burying as a defensive response in rats. J Comp Physiol Psychol 92(4):708–712

    Article  Google Scholar 

  • 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):359–365

    Article  PubMed  CAS  Google Scholar 

  • Poling A, Cleary J, Monaghan M (1981) Burying by rats in response to aversive and nonaversive stimuli. J Exp Anal Behav 35:31–44

    Article  PubMed  Google Scholar 

  • 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 105:207–217

    Article  PubMed  CAS  Google Scholar 

  • Ruffer DG (1965) Burrows and burrowing behavior of Onychomys leucogaster. J Mammal 46(2):241–247

    Article  Google Scholar 

  • Schmid-Holmes S, Drickamer LC, Robinson AS, Gillie LL (2001) Burrows and burrow-cleaning behavior of house mice (Mus musculus domesticus). Am Midl Nat 146:53–62

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Studier EH, Baca TP (1968) Atmospheric conditions in artificial rodent burrows. Southwest Nat 13(4):401–410

    Article  Google Scholar 

  • 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 90:197–200

    Article  PubMed  CAS  Google Scholar 

  • Terlecki LJ, Pinel JPJ, Treit D (1979) Conditioned and unconditioned defensive burying in the rat. Learn Motiv 10:337–350

    Article  Google Scholar 

  • Treit D, Fundytus M (1989) Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 31:959–962

    Article  Google Scholar 

  • Treit D, Pinel JPJ, Fibiger HC (1981) Conditioned defensive burying: a new paradigm for the study of anxiolytic agents. Pharmacol Biochem Behav 15(4):619–626

    Article  PubMed  CAS  Google Scholar 

  • Trullas R, Skolnick P (1993) Differences in fear motivated behaviors among inbred mouse strains. Psychopharmacology 111:323–331

    Article  PubMed  CAS  Google Scholar 

  • van Gaalen MM, Steckler T (2000) Behavioural analysis of four mouse strains in an anxiety test battery. Behav Brain Res 115:95–106

    Article  PubMed  Google Scholar 

  • Webster DG, Williams MH, Owens RD, Geiger VB, Dewsbury DA (1981) Digging behavior in 12 taxa of muroid rodents. Anim Learn Behav 9(2):173–177

    Google Scholar 

  • Wilkie DM, MacLennan AJ, Pinel JPJ (1979) Rat defensive behavior: burying noxious food. J Exp Anal Behav 31(3):299–306

    Article  PubMed  CAS  Google Scholar 

Download references

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.

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Authors and Affiliations

  1. Department of Neuroscience, Baylor College of Medicine, Houston, TX, 77030, USA

    Alexia Thomas & Richard Paylor

  2. Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA

    April Burant, Nghiem Bui, Deanna Graham, Lisa A. Yuva-Paylor & Richard Paylor

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  1. Alexia Thomas
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  2. April Burant
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Correspondence to Richard Paylor.

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Thomas, A., Burant, A., Bui, N. et al. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology 204, 361–373 (2009). https://doi.org/10.1007/s00213-009-1466-y

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  • DOI: https://doi.org/10.1007/s00213-009-1466-y

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