Animal Cognition

, Volume 22, Issue 3, pp 317–329 | Cite as

Context-specific response inhibition and differential impact of a learning bias in a lizard

  • Birgit SzaboEmail author
  • Daniel W. A. Noble
  • Martin J. Whiting
Original Paper


Response inhibition (inhibiting prepotent responses) is needed for reaching a more favourable goal in situations where reacting automatically would be detrimental. Inhibiting prepotent responses to resist the temptation of a stimulus in certain situations, such as a novel food item, can directly affect an animal’s survival. In humans and dogs, response inhibition varies between contexts and between individuals. We used two contextually different experiments to investigate response inhibition in the eastern water skink (Eulamprus quoyii): reversal of a visual two-choice discrimination and a cylinder detour task. During the two-choice task, half of our lizards were able to reach an initial learning criterion, but, thereafter, did not show consistent performance. Only two individuals reached a more stringent criterion, but subsequently failed during reversals. Furthermore, half of our animals were not able to inhibit a pre-existing side preference which affected their ability to learn during the two-choice task. Skinks were, however, able to achieve a detour around a cylinder performing at levels comparable to brown lemurs, marmosets, and some parrot species. A comparison between the tasks showed that reaching the initial criterion was associated with low success during the detour task, indicating that response inhibition could be context-specific in the water skink. To the best of our knowledge, this is the first study to examine inhibitory control and motor self-regulation in a lizard species.


Cognition Executive function Non-avian reptile Squamate 



We would like to thank Maiana Lenoir (ML) for her help catching skinks and helping collect data; Sebastian Hoefer (SH) for his time coding videos and Catarina Vila Pouca for her help with the analysis of the side bias. This project was funded by Macquarie University.


The study was funded by Macquarie University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practise at which the studies were conducted.

Supplementary material

10071_2019_1245_MOESM1_ESM.pdf (347 kb)
Supplementary material 1 (PDF 346 KB)


  1. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. CrossRefGoogle Scholar
  2. Bonati B, Csermely D, Lopez P, Martin J (2010) Lateralization in the escape behaviour of the common wall lizard (Podarcis muralis). Behav Brain Res 207:1–6. CrossRefPubMedGoogle Scholar
  3. Bonati B, Csermely D, Sovrano VA (2013) Advantages in exploring a new environment with the left eye in lizards. Behav Process 97:80–83. CrossRefGoogle Scholar
  4. Bray EE, MacLean EL, Hare BA (2014) Context specificity of inhibitory control in dogs. Anim Cognit 17:15–31. CrossRefGoogle Scholar
  5. Burghardt GM (1978) Learning Processes in Reptiles. In: Gans C, Tinkle DW (eds) Biology of the reptilia. Ecology and behaviour A (Vol. 7). Academic Press, London, pp 555–681Google Scholar
  6. Carazo P, Noble DW, Chandrasoma D, Whiting MJ (2014) Sex and boldness explain individual differences in spatial learning in a lizard. Proc R Soc B Biol Sci 281:20133275. CrossRefGoogle Scholar
  7. Clark BF, Amiel JJ, Shine R, Noble DWA, Whiting MJ (2014) Colour discrimination and associative learning in hatchling lizards incubated at ‘hot’ and ‘cold’ temperatures. Behav Ecol Sociobiol 68:239–247. CrossRefGoogle Scholar
  8. Cogger HG (2014) Reptiles and amphibians of Australia, 7th edn. ed.). CSIRO PUBLISHING, VictoriaCrossRefGoogle Scholar
  9. Csermely D, Bonati B, Romani R (2010) Lateralisation in a detour test in the common wall lizard (Podarcis muralis). Laterality 15:535–547. CrossRefPubMedGoogle Scholar
  10. Daniels CB (1987) Aspects of the aquatic feeding ecology of the riparian skink Sphenomorphus quoyii. Aust J Zool 35:253–258CrossRefGoogle Scholar
  11. Diamond A (1981) Retrieval of an object from an open box: The development of visual-tactile control of reaching in the first year of life. Soc Res Child Dev Abstr 3:78Google Scholar
  12. Diamond A (1990) Developmental time course in human infants and infant monkeys, and the neural basis of the inhibitory control of reaching. In: Diamond A (ed) The development and neural bases of higher cognitive functions, Academy of Sciences, New York, pp. 637–676Google Scholar
  13. Diamond A (2013) Executive functions. Annu Rev Psychol 64:135–168. CrossRefGoogle Scholar
  14. Dias R, Robbins TW, Roberts AC (1996) Primate analogue of the Wisconsin card sorting test-effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav Neurosci 110:872–886CrossRefPubMedGoogle Scholar
  15. Falissard B (2012) psy: various procedures used in psychometry. R package version 1.1.
  16. Fleishman LJ, Loew ER, Whiting MJ (2011) High sensitivity to short wavelengths in a lizard and implications for understanding the evolution of visual systems in lizards. Proc R Soc B Biol Sci 278:2891–2899. CrossRefGoogle Scholar
  17. Gaalema DE (2011) Visual discrimination and reversal learning in rough-necked monitor lizards (Varanus rudicollis). J Comp Psychol 125:246–249. CrossRefPubMedGoogle Scholar
  18. Hews DK, Worthington RA (2001) Fighting from the right side of the brain: left visual field preference during aggression in free-ranging male tree lizards (Urosaurus ornatus). Brain Behav Evol 58:356–361CrossRefPubMedGoogle Scholar
  19. Kabadayi C, Taylor LA, von Bayern AM, Osvath M (2016) Ravens, New Caledonian crows and jackdaws parallel great apes in motor self-regulation despite smaller brains. R Soc Open Sci 3:160104. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kabadayi C, Bobrowicz K, Osvath M (2017a) The detour paradigm in animal cognition. Anim Cognit 21:21–35. CrossRefGoogle Scholar
  21. Kabadayi C, Krasheninnikova A, O’Neill L, van de Weijer J, Osvath M, von Bayern AMP (2017b) Are parrots poor at motor self-regulation or is the cylinder task poor at measuring it? Anim Cognit 20:1137–1146. CrossRefGoogle Scholar
  22. Koehler W (1925) The mentality of the ape. Kegan Paul Trench Trubner and Co. LTD, LondonGoogle Scholar
  23. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82(13):1–26. CrossRefGoogle Scholar
  24. Langkilde T, Shine R (2006) How much stress do researchers inflict on their study animals? A case study using a scincid lizard. Eulamprus heatwolei. J Exp Biol 209(Pt 6):1035–1043. CrossRefPubMedGoogle Scholar
  25. Leal M, Powell BJ (2012) Behavioural flexibility and problem-solving in a tropical lizard. Biol Lett 8:28–30. CrossRefPubMedGoogle Scholar
  26. Lucon-Xiccato T, Gatto E, Bisazza A (2017) Fish perform like mammals and birds in inhibitory motor control tasks. Sci Rep 7:13144. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lustig A, Ketter-Katz H, Katzir G (2013) Lateralization of visually guided detour behaviour in the common chameleon, Chamaeleo chameleon, a reptile with highly independent eye movements. Behav Process 100:110–115. CrossRefGoogle Scholar
  28. MacLean EL, Hare B, Nunn CL, Addessi E, Amici F, Anderson RC, Aureli F, Baker JM, Bania AE, Barnard AM, Boogert NJ, Brannon EM, Bray EE, Bray J, Brent LJ, Burkart JM, Call J, Cantlon JF, Cheke LG, Clayton NS, Delgado MM, DiVincenti LJ, Fujita K, Herrmann E, Hiramatsu C, Jacobs LF, Jordan KE, Laude JR, Leimgruber KL, Messer EJ, Moura AC, Ostojic L, Picard A, Platt ML, Plotnik JM, Range F, Reader SM, Reddy RB, Sandel AA, Santos LR, Schumann K, Seed AM, Sewall KB, Shaw RC, Slocombe KE, Su Y, Takimoto A, Tan J, Tao R, van Schaik CP, Viranyi Z, Visalberghi E, Wade JC, Watanabe A, Widness J, Young JK, Zentall TR, Zhao Y (2014) The evolution of self-control. Proc Natl Acad Sci USA 111:E2140–E2148. CrossRefPubMedGoogle Scholar
  29. McElroy EJ, Hickey KL, Reilly SM (2008) The correlated evolution of biomechanics, gait and foraging mode in lizards. J Exp Biol 211:1029–1040. CrossRefPubMedGoogle Scholar
  30. Noble DW, Carazo P, Whiting MJ (2012) Learning outdoors: male lizards show flexible spatial learning under semi-natural conditions. Biol Lett 8:946–948. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Noble DWA, Byrne RW, Whiting MJ (2014) Age-dependent social learning in a lizard. Biol Lett 10:20140430. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Qi Y, Noble DWA, Fu J, Whiting MJ (2018) Testing domain general learning in an Australian lizard. Anim Cognit. CrossRefGoogle Scholar
  33. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL Accessed Sept 2017
  34. Robins A, Chen P, Beazley LD, Dunlop SA (2005) Lateralised predatory responses in the ornate dragon lizard (Ctenophorus ornatus). NeuroReport 16:849–852CrossRefPubMedGoogle Scholar
  35. Santos LR, Ericson BN, Hauser MD (1999) Constraints on problem solving and inhibition: object retrieval in cotton-top tamarins (Saguinus oedipus oedipus). J Comp Psychol 113:186–193CrossRefGoogle Scholar
  36. Spedicato GA (2017) Discrete time Markov chains with R. R J 9:84–104CrossRefGoogle Scholar
  37. Sutherland NS, Mackintosh NJ (1971) Mechanisms of animal discrimination learning. Academic Press, New YorkGoogle Scholar
  38. Szabo B, Noble DWA, Byrne RW, Tait DS, Whiting MJ (2018) Subproblem learning and reversal of a multidimensional visual cue in a lizard: evidence for behavioural flexibility? Anim Behav 144:17–26. CrossRefGoogle Scholar
  39. Tsukayama E, Duckworth AL, Kim B (2011) Resisting everything except temptation: evidence and an explanation for domain specific impulsivity. Eur J Personal 26:318–334CrossRefGoogle Scholar
  40. Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–633CrossRefGoogle Scholar
  41. van Horik JO, Langley EJG, Whiteside MA, Laker PR, Beardsworth CE, Madden JR (2018) Do detour tasks provide accurate assays of inhibitory control? Proc R Soc B Biol Sci 285:20180150. CrossRefGoogle Scholar
  42. Venables WN, Ripley BD (2002) Modern applied statistics with S. 4th edition. Springer, New YorkCrossRefGoogle Scholar
  43. Veron JEN (1969) Ab analysis of stomach content of the water skink, Sphenomorphus quoyii. J Herpetol 3:187–189CrossRefGoogle Scholar
  44. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  45. Wilkinson A, Huber L (2012) Cold-blooded cognition: reptilian cognitive abilities. In: Vonk J, Shackelford TK (eds) The oxford handbook of comparative evolutionary psychology. Oxford, New York, pp 129–141Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesMacquarie UniversitySydneyAustralia
  2. 2.Ecology and Evolution Research Centre, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  3. 3.Ecology and Evolution, Research School of BiologyThe Australian National UniversityCanberraAustralia

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