Environmental standardization: cure or cause of poor reproducibility in animal experiments? (original) (raw)

References

  1. US Department of Agriculture, Animal and Plant Health Inspection Service. Animal Welfare Act 22 (Riverdale: U.S. Department of Agriculture, 1990).
  2. NRC (National Research Council). Guide for the Care and Use of Laboratory Animals (Washington, National Academy Press, 1996).
  3. Beynen, A.C., Gärtner, K. & van Zutphen, L.F.M. Standardization of animal experimentation In Principles of Laboratory Animal Science (eds., van Zutphen, L.F.M., Baumans, V. & Beynen, A.C.) 103–110 (Elsevier, Amsterdam, 2003).
    Google Scholar
  4. Festing, M.F.W. Good experimental design and statistics can save animals, but how can it be promoted? Altern. Lab. Anim. 32, 133–135 (2004).
    CAS PubMed Google Scholar
  5. Festing, M.F.W. Refinement and reduction through the control of variation. Altern. Lab. Anim. 32, 259–263 (2004).
    CAS PubMed Google Scholar
  6. Quinn, G.P. & Keough, M.J. Hypothesis testing. In Experimental Design and Data Analysis for Biologists (eds., Quinn, G.P. & Keough, M.J.) 32–57 (Cambridge University Press, 2002).
    Chapter Google Scholar
  7. Crabbe, J.C., Wahlsten, D. & Dudek, B.C. Genetics of mouse behaviour: interactions with laboratory environment. Science 284, 1670–1672 (1999).
    Article CAS Google Scholar
  8. Wahlsten, D. Standardizing tests of mouse behavior: reasons, recommendations, and reality. Physiol. Behav. 73, 695–705 (2001).
    Article CAS Google Scholar
  9. Würbel, H. Behavioral phenotyping enhanced—beyond (environmental) standardization. Genes Brain Behav. 1, 3–8 (2002).
    Article Google Scholar
  10. Campbell, D.T. Factors relevant to the validity of experiments in social settings. Psychol. Bull. 54, 297–312 (1957).
    Article CAS Google Scholar
  11. Lehner, P.N. Handbook of Ethological Methods, 2nd edn (Cambridge University Press, Cambridge, 1996).
    Google Scholar
  12. Guala, F. Experimental localism and external validity. Philos. Sci. 70, 1195–1205 (2003).
    Article Google Scholar
  13. Van der Staay, F.J. Animal models of behavioral dysfunctions: Basic concepts and classifications, and an evaluation strategy. Brain Res. Brain Res. Rev. 52, 131–159 (2006).
    Article Google Scholar
  14. Crestani, F., Martin, J.R., Möhler, H. & Rudolph, U. Resolving differences in GABAA receptor mutant mouse studies. Nat. Neurosci. 3, 1059 (2000).
    Article CAS Google Scholar
  15. Wahlsten, D., et al. Different data from different labs: lessons from studies of gene-environment interaction. J. Neurobiol. 54, 283–311 (2003).
    Article Google Scholar
  16. Wolfer, D.P. et al. Laboratory animal welfare: cage enrichment and mouse behaviour. Nature 432, 821–822 (2004).
    Article CAS Google Scholar
  17. Kafkafi, N., Benjamini, Y., Sakov, A., Elmer, G.I. & Golani, I. Genotype-environment interactions in mouse behavior: A way out of the problem. Proc. Natl. Acad. Sci. USA 102, 4619–4624 (2005).
    Article CAS Google Scholar
  18. Lewejohann, L. et al. Environmental bias? Effects of housing conditions, laboratory environment and experimenter on behavioral tests. Genes Brain Behav. 5, 64–72 (2006).
    Article CAS Google Scholar
  19. Mandillo, S. et al. Reliability, robustness and reproducibility in mouse behavioral phenotyping: a cross-laboratory study. Physiol. Genomics 34, 243–255 (2008).
    Article Google Scholar
  20. Chesler, E.J., Wilson, S.G., Lariviere, W.R., Rodriguez-Zas, S.L. & Mogil, J.S. Identification and ranking of genetic and laboratory environment factors influencing a behavioral trait, thermal nociception, via computational analysis of a large data archive. Neurosci. Biobehav. Rev. 26, 907–923 (2002).
    Article Google Scholar
  21. Valdar, W. et al. Genetic and environmental effects on complex traits in mice. Genetics 174, 959–984 (2006).
    Article CAS Google Scholar
  22. Wahlsten, D., Bachmanov, A., Finn, D.A. & Crabbe, J.C. Stability of inbred mouse strain differences in behavior and brain size between laboratories and across decades. Proc. Natl. Acad. Sci. USA 103, 16364–16369 (2006).
    Article CAS Google Scholar
  23. Andrews, N. & File, S.E. Handling history of rats modifies behavioural effects of drugs in the elevated plus-maze test of anxiety. Eur. J. Pharmacol. 235, 109–112 (1993).
    Article CAS Google Scholar
  24. Rampon, C. et al. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 3, 238–244 (2000).
    Article CAS Google Scholar
  25. Cabib, S., Orsini, C., Le Moal, M. & Piazza, P.V. Abolition and reversal of strain differences in behavioural responses to drugs of abuse after brief experience. Science 289, 463–465 (2000).
    Article CAS Google Scholar
  26. Kas, M.J.H. & Van Ree, J.M. Dissecting complex behaviours in the post-genomic era. Trends Neurosci. 27, 366–369 (2004).
    Article CAS Google Scholar
  27. Izidio, G.S., Lopes, D.M., Spricigio, L. & Ramos, A. Common variations in the pretest environment influence genotypic comparisons in models of anxiety. Genes Brain Behav. 4, 412–419 (2005).
    Article CAS Google Scholar
  28. Öbrink, K.J. & Rehbinder, C. Animal definition: a necessity for the validity of animal experiments. Lab. Anim. 34, 121–130 (2000).
    Article Google Scholar
  29. van der Staay, F.J. & Steckler, T. Behavioural phenotyping of mouse mutants. Behav. Brain Res. 125, 3–12 (2001).
    Article CAS Google Scholar
  30. van der Staay, F.J. & Steckler, T. The fallacy of behavioral phenotyping without standardisation. Genes Brain Behav. 1, 9–13 (2002).
    Article CAS Google Scholar
  31. Würbel, H. Behaviour and the standardization fallacy. Nat. Genet. 26, 263 (2000).
    Article Google Scholar
  32. De Witt, T.J. Scheiner, S.M. Phenotypic Plasticity. Functional and Conceptual Approaches. (Oxford University Press, 2004).
    Google Scholar
  33. Latham, N. & Mason, G. From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory. Appl. Anim. Behav. Sci. 86, 261–289 (2004).
    Article Google Scholar
  34. Silver, L.M. Mouse genetics: concepts and applications (Oxford University Press, New York, 1995).
  35. Silva, A. J., et al. Mutant mice and neuroscience: recommendations concerning genetic background. Neuron 19, 755–759 (1997).
    Article Google Scholar
  36. Beynen, A.C., Festing, M.F.M. & van Montfort, M.A.J. Design of animal experiments In Principles of Laboratory Animal Science (eds., van Zutphen, L.F.M., Baumans, V. & Beynen, A.C.) 219–249 (Elsevier, Amsterdam, 2003).
    Google Scholar
  37. Baggerly, K.A. Reproducibility of SELDI-TOF protein patterns in serum: comparing datasets from different experiments. Bioinformatics 20, 777 (2004).
    Article CAS Google Scholar
  38. Anderson, C.A., Lindsay, J.J. & Bushman, B.J. Research in the psychological laboratory: truth or triviality? Curr. Dir. Psychol. Sci. 8, 3–9 (1999).
    Article Google Scholar
  39. Vissers, G., Heyne, G., Peters, V. & Guerts, J. The validity of laboratory research in social and behavioral science. Qual. Quant. 35, 129–145 (2001).
    Article Google Scholar
  40. Boehm, G.W. et al. Learning and memory in autoimmune BXSB mouse: Effects of neocorticaol ectopias and environmental enrichment. Brain Res. 726, 11–22 (1996).
    Article CAS Google Scholar
  41. Chapillon, P., Manneche, C., Belzung, C. & Caston, J. Rearing environmental enrichment in two inbred strain of mice: 1. Effects on emotional reactivity. Behav. Genet. 29, 41–46 (1999).
    Article CAS Google Scholar
  42. Cudilo, E., Al Naemi, H., Marmorstein, L. & Baldwin, A.L. Knockout mice: is it just genetics? Effect of enriched housing on Fibulin-4+/− mice. PLoS ONE 2, e229, (2007).
    Article Google Scholar
  43. Hascoet, M., Colombel, M.-C. & Bourin, M. Influence of age on behavioural response in the light/dark paradigm. Physiol. Behav. 66, 567–570 (1999).
    Article CAS Google Scholar
  44. Imhof, J.T., Coelho, Z.M.I., Schmitt, M.L., Morato, G.S. & Carobrez, A.P. Influence of age and gender on performance of rats in the elevated plus maze apparatus. Behav. Brain Res. 56, 177–180 (1993).
    Article CAS Google Scholar
  45. Poon, A.M. et al. Effect of cage size on ultradian locomotor rhythms of laboratory mice. Physiol. Behav. 62, 1253–1258 (1997).
    Article CAS Google Scholar
  46. Soffie, M., Hahn, K., Terao, E. & Eclancher, F. Behavioural and glial changes in old rats following environmental enrichment. Behav. Brain Res. 101, 37–49 (1999).
    Article CAS Google Scholar
  47. Van de Weerd, H.A., Baumans, V., Koolhaas, J.M. & van Zutphen, L.F. Strain specific behavioral response to environmental enrichment in the mouse. J. Exp. Anim. Sci. 36, 117–127 (1994).
    CAS PubMed Google Scholar
  48. Russell, W.M.S. & Burch, R.L. The principles of humane experimental technique (Methuen, London, 1959).

Download references