Concept Fatigue with the Three R’s

  • Jan Lauwereyns


The three R’s as defined by Russell and Burch have come to occupy a central position in animal research. A careful examination of the original definitions and aims shows these to be a product of their time, no longer in line with contemporary perspectives. A particular point of interest is the reliance on the concept of “humanity.” This is contrasted with more recent ideas about “speciesism” and the moral status of nonhuman animals. As a case study, I focus on the use of nonhuman primates in basic neuroscience research; the historical analysis illustrates how the changing context implies a changing perspective on the ethical validity of research. Yet, the three R’s fail as guidelines to translate the changes in context to commensurate changes in conduct.


Animal ethics Replacement Reduction Refinement Historical analysis 


  1. Andre, C., & Velasquez, M. (1991). Who counts? Issues in Ethics, 4(1). Available at:
  2. Balls, M. (2010). The principles of humane experimental technique: Timeless insights and unheeded warnings [Special Issue]. ALTEX, 27, 19–23.Google Scholar
  3. Barack, D. L., Chang, S. W. C., & Platt, M. L. (2017). Posterior cingulate neurons dynamically signal decisions to disengage during foraging. Neuron, 96, 339–347.CrossRefGoogle Scholar
  4. Beauchamp, T. L. (2011). Rights theory and animal rights. In T. L. Beauchamp & R. G. Frey (Eds.), The Oxford Handbook of Animal Ethics (pp. 198–227). New York: Oxford University Press.CrossRefGoogle Scholar
  5. Bentham, J. (1823). An Introduction to the Principles of Morals and Legislation. A new edition, corrected by the author (Vol. II). London: W. Pickering.Google Scholar
  6. Boden, M. A. (2006). Mind as Machine. A History of Cognitive Science (Vols. 1 and 2). New York: Oxford University Press.Google Scholar
  7. Buchanan-Smith, H. M., Rennie, A. E., Vitale, A., Pollo, S., Prescott, M. J., & Morton, D. B. (2005). Harmonising the definition of refinement. Animal Welfare, 14, 379–384.Google Scholar
  8. Copp, D. (2011). Animals, fundamental moral standing, and speciesism. In T. L. Beauchamp & R. G. Frey (Eds.), The Oxford Handbook of Animal Ethics (pp. 276–303). New York: Oxford University Press.CrossRefGoogle Scholar
  9. Cornwall, W. (2017). Revamp animal research rules, report urges. Science, 358, 434.CrossRefGoogle Scholar
  10. Driver, J. (2011). A Humean account of the status and character of animals. In T. L. Beauchamp & R. G. Frey (Eds.), The Oxford Handbook of Animal Ethics (pp. 144–171). New York: Oxford University Press.CrossRefGoogle Scholar
  11. Editorial. (1999). Science and terrorism in Europe. Nature Neuroscience, 2, 99–100.Google Scholar
  12. Editorial. (2000). Legal challenges to animal experimentation. Nature Neuroscience, 3, 523.Google Scholar
  13. Editorial. (2001). Primate research faces extinction. Nature Neuroscience, 4, 111.Google Scholar
  14. Goldberg, A. M. (2010). The principles of Humane experimental technique: Is it relevant today? [Special Issue]. ALTEX, 27, 25–27.Google Scholar
  15. Goodall, J. (1964). Tool-using and aimed throwing in a community of free-living chimpanzees. Nature, 201, 1264–1266.CrossRefGoogle Scholar
  16. Hauser, M. D., Chomsky, N., & Fitch, W. T. (2002). The faculty of language: What is it, who has it, and how did it evolve? Science, 298, 1569–1579.CrossRefGoogle Scholar
  17. Hubel, D. H. (1988). Eye, Brain, and Vision. Scientific American Library. New York: W. H. Freeman.Google Scholar
  18. Hume, D. (1740/2002). A Treatise of Human Nature (D. F. Norton & M. J. Norton, Eds.). New York: Oxford University Press.Google Scholar
  19. Kabadayi, C., & Osvath, M. (2017). Ravens parallel great apes in flexible planning for tool-use and bartering. Science, 357, 202–204.CrossRefGoogle Scholar
  20. Kaiser, J. (2015, November 18). NIH to end all support for chimpanzee research. Science, News online.
  21. Kalof, L. (Ed.). (2017). The Oxford Handbook of Animal Studies. New York: Oxford University Press.Google Scholar
  22. Kim, H. F., Amita, H., & Hikosaka, O. (2017). Indirect pathway of caudal basal ganglia for rejection of valueless visual objects. Neuron, 94, 920–930.CrossRefGoogle Scholar
  23. LaFollette, H. (2011). Animal experimentation in biomedical research. In T. L. Beauchamp & R. G. Frey (Eds.), The Oxford Handbook of Animal Ethics (pp. 796–825). New York: Oxford University Press.CrossRefGoogle Scholar
  24. Laidre, M. E. (2012). Niche construction drives social dependence in hermit crabs. Current Biology, 22, R861–R863.CrossRefGoogle Scholar
  25. Lauwereyns, J. (2012). Brain and the Gaze: On the Active Boundaries of Vision. Cambridge, MA: The MIT Press.Google Scholar
  26. Lauwereyns, J., Takikawa, Y., Kawagoe, R., Kobayashi, S., Koizumi, M., Coe, B., et al. (2002a). Feature-based anticipation of cues that predict reward in monkey caudate nucleus. Neuron, 33, 463–473.CrossRefGoogle Scholar
  27. Lauwereyns, J., Watanabe, K., Coe, B., & Hikosaka, O. (2002b). A neural correlate of response bias in monkey caudate nucleus. Nature, 418, 413–417.CrossRefGoogle Scholar
  28. Moore, D. W. (2003, May 21). Public lukewarm on animal rights. GALLUP News. Available at:
  29. Morris, C. W. (2011). The idea of moral standing. In T. L. Beauchamp & R. G. Frey (Eds.), The Oxford Handbook of Animal Ethics (pp. 255–275). New York: Oxford University Press.CrossRefGoogle Scholar
  30. Newport, F. (2008, May 15). Post-derby tragedy, 38% support banning animal racing. GALLUP News. Available at:
  31. (2017, December 5). The Nobel prize in physiology or medicine 1981. Nobel Media A B 2014. Available at:
  32. Nussbaum, M. (2011). The capabilities approach and animal entitlements. In T. L. Beauchamp & R. G. Frey (Eds.), The Oxford Handbook of Animal Ethics (pp. 228–251). New York: Oxford University Press.CrossRefGoogle Scholar
  33. Olsson, I. A. S., Franco, N. H., Weary, D. M., & Sandøe, P. (2012). The 3Rs principle: Mind the ethical gap! ALTEX Proceedings, 1/12, Proceedings of WC8, 29, 333–336. Google Scholar
  34. Project R&R. (2017). International bans: Countries banning or limiting chimpanzee research. Available at:
  35. Rifkin, R. (2015, May 18). In U.S., more say animals should have same rights as people. GALLUP News: Social Issues. Available at:
  36. Roelfsema, P. R., & Treue, S. (2014). Basic neuroscience research with nonhuman primates: A small but indispensable component of biomedical research. Neuron, 82, 1200–1204.CrossRefGoogle Scholar
  37. Rowlands, M. J., & Monsó, S. (2017). Animals as reflexive thinkers: The aponoian paradigm. In L. Kalof (Ed.), The Oxford Handbook of Animal Studies (pp. 319–341). New York: Oxford University Press.Google Scholar
  38. Russell, W. M. S., & Burch, R. L. (1959/1992). The Principles of Humane Experimental Technique. Wheathampstead: Universities Federation for Animal Welfare. Available at ALTWEB:
  39. Sandel, M. J. (2009). Justice: What’s the Right Thing to Do. New York: Farrar, Straus and Giroux.Google Scholar
  40. Singer, P. (1975/2009). Animal Liberation. New York: HarperCollins.Google Scholar
  41. Singer, P. (1981/2011). The Expanding Circle: Ethics, Evolution, and Moral Progress. Princeton, NJ: Princeton University Press.Google Scholar
  42. Tannenbaum, J., & Bennett, B. J. (2015). Russell and Burch’s 3Rs then and now: The need for clarity in definition and purpose. Journal of the American Association for Laboratory Animal Science, 54, 120–132.PubMedPubMedCentralGoogle Scholar
  43. The Jane Goodall Institute Australia. (2017). About Dr. Jane Goodall. Available at:
  44. Traxler, M. J., Boudewyn, M., & Loudermilk, J. (2012). What’s special about human language? The contents of the “narrow language faculty” revisited. Language and Linguistics Compass, 6, 611–621.CrossRefGoogle Scholar
  45. Vicari, G., & Adenzato, M. (2014). Is recursion language-specific? Evidence of recursive mechanisms in the structure of intentional action. Consciousness and Cognition, 26, 169–188.CrossRefGoogle Scholar
  46. White, B. J., Kan, J. Y., Levy, R., Itti, L., & Munoz, D. P. (2017). Superior colliculus encodes visual saliency before the primary visual cortex. Proceedings of the National Academy of Sciences of the United States of America, 114, 9451–9456.CrossRefGoogle Scholar
  47. Wrangham, R. (2004). Killer species. Daedalus, 133, 25–35.CrossRefGoogle Scholar
  48. Wurtz, R. H. (1965). Steady potential shifts during arousal and deep sleep in the cat. Electroencephalography and Clinical Neurophysiology, 18, 649–662.CrossRefGoogle Scholar
  49. Wurtz, R. H. (1969a). Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. Journal of Neurophysiology, 32, 987–994.CrossRefGoogle Scholar
  50. Wurtz, R. H. (1969b). Response of striate cortex neurons to stimuli during rapid eye movements in the monkey. Journal of Neurophysiology, 32, 975–986.CrossRefGoogle Scholar
  51. Wurtz, R. H. (1969c). Visual receptive fields of striate cortex neurons in awake monkeys. Journal of Neurophysiology, 32, 975–986.CrossRefGoogle Scholar
  52. Wurtz, R. H., & Olds, J. (1963). Amygdaloid stimulation and operant conditioning in the rat. Journal of Comparative and Physiological Psychology, 56, 941–949.CrossRefGoogle Scholar

Copyright information

© The Author(s) 2018

Authors and Affiliations

  1. 1.Kyushu UniversityFukuokaJapan

Personalised recommendations