Advertisement

Animal Cognition

, Volume 22, Issue 6, pp 931–946 | Cite as

Motoric self-regulation by sled dogs and pet dogs and the acute effect of carbohydrate source in sled dogs

  • Debbie M. KellyEmail author
  • Jennifer L. Adolphe
  • Alizée Vernouillet
  • J. Andrew McCausland
  • Alexandra Rankovic
  • Adronie Verbrugghe
Original Paper

Abstract

Inhibitory control is a term used to envelop a collection of processes that allow an organism to refrain from engaging in an inappropriate prepotent or responsive behavior. Studies have examined the propensity of inhibitory control by nonhuman animals, from the cognitively complex processes involved in self-control to potentially less cognitively taxing processes such as motoric self-regulation. Focusing on canines, research has suggested that the domestication process as well as experiences during ontogeny contribute to inhibitory control. Diet may also play an important role in an individual’s ability to self-regulate. This study examined this possibility by investigating motoric self-regulation in sled dogs, using three well-established tasks (i.e., A-not-B Bucket, Cylinder, and A-not-B Barrier tasks), performed after consumption of one of three dietary treatments with different glycemic index values. We also compared the performance of sled dogs during these tasks with results previously obtained from pet dogs. Overall, the results show many similarities in the performance of sled dogs and pet dogs on the motoric self-regulation tasks, with the notable exception that sled dogs may have a stronger spatial perseveration during the A-not-B Bucket task. Previous research findings reporting a lack of correlation among these tasks are also supported. Finally, during the early postprandial phase (period after consumption), dietary treatments with different glycemic index values did not influence self-regulatory performance for sled dogs.

Keywords

Carbohydrate Glycemic index Inhibitory control Motoric self-regulation Sled dogs 

Notes

Acknowledgments

We would very much like to thank the owner’s of the sled dogs for lending us the facilities and access to their sled dogs to perform our experiments. We would like to thank Laura Stiles for assistance with data scoring. AdV, DMK, JA designed the study; DMK, AlV and JAM conducted the behavioral experiments; AdV, JA, AR designed the nutritional components, AlV and DMK analyzed the data, and all authors contributed to writing and editing the manuscript.

Funding

This study was funded by a Natural Science & Engineering Research Council Collaborative Research Development grant (#CRDPJ488705–15) in partnership with Petcurean Pet Nutrition to AdV, DMK and JA. JA is an employee with Petcurean Pet Nutrition.

Compliance with ethical standards

Conflict of interest

Authors AdV, DMK and JA received funding by a Natural Science & Engineering Research Council Collaborative Research Development grant (#CRDPJ488705–15) in partnership with Petcurean Pet Nutrition to JA, who is an employee with Petcurean Pet Nutrition. Authors AdV, DMK and JA 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.

Supplementary material

10071_2019_1285_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 16 kb)

References

  1. Adolphe JL, Drew MD, Huang Q, Silver TI, Weber LP (2012) Postprandial impairment of flow-mediated dilation and elevated methylglyoxal after simple but not complex carbohydrate consumption in dogs. Nutr Res 32(4):278–284.  https://doi.org/10.1016/j.nutres.2012.03.002 CrossRefPubMedGoogle Scholar
  2. Adolphe J, Silver T, Childs H, Drew M, Weber L (2014) Short-term obesity results in detrimental metabolic and cardiovascular changes that may not be reversed with weight loss in an obese dog model. Brit J Nutr 112(4):647–656.  https://doi.org/10.1017/S0007114514001214 CrossRefPubMedGoogle Scholar
  3. Amici F, Aureli F, Call J (2008) Fission-fusion dynamics, behavioral flexibility, and inhibitory control in primates. Curr Biol 18(18):1415–1419.  https://doi.org/10.1016/j.cub.2008.08.020 CrossRefPubMedGoogle Scholar
  4. Atkinson FS, Foster-Powell K, Brand-Miller JC (2008) International tables of glycemic index and glycemic load values: 2008. Diabetes Care 31(12):2281–2283.  https://doi.org/10.2337/dc08-1239 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Axelsson E, Ratnakumar A, Arendt ML, Maqbool K, Webster MT, Perloski M et al (2013) The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495(7441):360–364.  https://doi.org/10.1038/nature11837 CrossRefPubMedGoogle Scholar
  6. Barclay AW, Petocz P, McMillan-Price J, Flood VM, Prvan T, Mitchell P, Brand-Miller JC (2008) Glycemic index, glycemic load, and chronic disease risk—a meta-analysis of observational studies. Am J Clin Nutr 87(3):627–637.  https://doi.org/10.1093/ajcn/87.3.627 CrossRefPubMedGoogle Scholar
  7. Barrera G, Alterisio A, Scandurra A, Bentosela M, D’Aniello B (2018) Training improves inhibitory control in water rescue dogs. Anim Cogn 22(1):127–131.  https://doi.org/10.1007/s10071-018-1224-9 CrossRefPubMedGoogle Scholar
  8. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67(1):1–48.  https://doi.org/10.18637/jss.v067.i01 CrossRefGoogle Scholar
  9. Benton D, Ruffin M, Lassel T, Nabb S, Messaoudi M, Vinoy S et al (2003) The delivery rate of dietary carbohydrates affects cognitive performance in both rats and humans. Psychopharm 166(1):86–90.  https://doi.org/10.1007/s00213-002-1334-5 CrossRefGoogle Scholar
  10. Beran MJ (2015) The comparative science of “self-control”: what are we talking about? Front Psychol 6:51.  https://doi.org/10.3389/fpsyg.2015.00051 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Beurms S, Miller HC (2016) Sharing more than the sofa: what dogs can teach us about human self-control. Curr Dir Psychol Sci 25(5):351–356.  https://doi.org/10.1177/0963721416664392 CrossRefGoogle Scholar
  12. Bray E, MacLean E, Hare B (2014) Context specificity of inhibitory control in dogs. Anim Cogn 17(1):15–31.  https://doi.org/10.1007/s10071-013-0633-z CrossRefPubMedGoogle Scholar
  13. Bray E, MacLean E, Hare B (2015) Increasing arousal enhances inhibitory control in calm but not excitable dogs. Anim Cogn 18(6):1317–1329.  https://doi.org/10.1007/s10071-015-0901-1 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Brucks D, Marshall-Pescini S, Wallis L, Huber L, Range F (2017) Measures of dogs’ inhibitory control abilities do not correlate across tasks. Front Psychol 8:849.  https://doi.org/10.3389/fpsyg.2017.00849 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Carciofi AC, Takakura FS, de Oliveira LD et al (2008) Effects of six carbohydrate sources on dog diet digestibility and post-prandial glucose and insulin response. J Anim Physiol Anim Nutr 92(3):326–336.  https://doi.org/10.1111/j.1439-0396.2007.00794.x CrossRefGoogle Scholar
  16. Davis MS, Geor RJ, Williamson KK (2018) Effect of endurance conditioning on nsulin-mediated glucose clearance in dogs. Med Sci Sports Exerc 50:2494–2499CrossRefGoogle Scholar
  17. Diamond A (1990) Developmental time course in human infants and infant monkeys, and the neural bases of, inhibitory control in reaching. Ann N Y Acad Sci 608:637–669CrossRefGoogle Scholar
  18. Fagnani J, Barrera G, Carballo F, Bentosela M (2016) Is previous experience important for inhibitory control? A comparison between shelter and pet dogs in A-not-B and cylinder tasks. Anim Cogn 19(6):1165–1172.  https://doi.org/10.1007/s10071-016-1024-z CrossRefGoogle Scholar
  19. Flint R, Turek C (2003) Glucose effects on a continuous performance test of attention in adults. Behav Brain Res 142(1–2):217–228.  https://doi.org/10.1016/S0166-4328(03)00002-0 CrossRefPubMedGoogle Scholar
  20. Glady Y, Genty E, Roeder J (2012) Brown Lemus (Eulemus fulvus) can master the qualitative version of the reverse-reward contingency. PLoS One 7(10):1–7.  https://doi.org/10.1371/jounal.pone.0048378 CrossRefGoogle Scholar
  21. Graham PA, Maskell IE, Nash AS (1994) Canned high fiber diet and postprandial glycemia in dogs with naturally occurring diabetes mellitus. J Nutr 124(12 Suppl):2712S–2715S.  https://doi.org/10.1093/jn/124.suppl_12.2712S CrossRefPubMedGoogle Scholar
  22. Hall JA, Melendez LD, Jewell DE, Kaltenboeck B (2013) Using gross energy improves metabolizable energy predictive equations for pet foods whereas undigested protein and fiber content predict stool quality. PLoS ONE 8(1):e54405CrossRefGoogle Scholar
  23. Jenkins DJ, Wolever TM, Taylor RH, Barker H, Fielden H, Baldwin JM et al (1981) Glycemic index of foods: a physiological basis for carbohydrate exchange. Am J Clin Nutr 34(3):362–366.  https://doi.org/10.1093/ajcn/34.3.362 CrossRefPubMedGoogle Scholar
  24. 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(4):160104.  https://doi.org/10.1098/rsos.160104 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kabadayi C, Bobrowicz K, Osvath M (2018) The detour paradigm in animal cognition. Anim Cogn 21(1):21–35.  https://doi.org/10.1007/s10071-017-1152-0 CrossRefGoogle Scholar
  26. Kawano H, Motoyama T, Hirashima O, Hirai N, Miyao Y, Sakamoto T et al (1999) Hyperglycemia rapidly suppresses flow-mediated endothelium-dependent vasodilation of brachial artery. J Am Coll Cardiol 34(1):146–154CrossRefGoogle Scholar
  27. Laflamme D (1997) Development and validation of a body score system for dogs. Canine Pract 22(4):10–15Google Scholar
  28. Lamport DJ, Lawton CL, Mansfield MW, Dye L (2009) Impairments in glucose tolerance can have a negative impact on cognitive function: a systematic research review. Neurosci Biobehav Rev 33(3):394–413.  https://doi.org/10.1016/j.neubiorev.2008.10.008 CrossRefPubMedGoogle Scholar
  29. Lamport DJ, Hoyle E, Lawton CL, Mansfield MW, Dye L (2011) Evidence for a second meal cognitive effect: glycaemic responses to high and low glycaemic index evening meals are associated with cognition the following morning. Nutr Neurosci 14(2):66–71.  https://doi.org/10.1179/1476830511Y.0000000002 CrossRefPubMedGoogle Scholar
  30. Lucon-Xiccato T, Gatto E, Bisazza A (2017) Fish perform like mammals and birds in inhibitory motor control tasks. Sci Rep 7(1):13144.  https://doi.org/10.1038/s41598-017-13447-4 CrossRefPubMedPubMedCentralGoogle Scholar
  31. MacLean EL, Hare B, Nunn CL, Addessi E, Amici F, Anderson RC et al (2014) The evolution of self-control. Proc Natl Acad Sci USA 111(20):E2140–E2148.  https://doi.org/10.1073/pnas.1323533111 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Marshall-Pescini S, Viranyi Z, Range F (2015) The effect of domestication on inhibitory control: wolves and dogs compared. PLoS One 10(2):e0118469.  https://doi.org/10.1371/journal.pone.0118469 CrossRefPubMedPubMedCentralGoogle Scholar
  33. McCance RA, Lawrence RD (1929) The carbohydrate content of foods. Lancet 213(5520):1264–1265Google Scholar
  34. McNay EC, Fries TM, Gold PE (2000) Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task. Proc Natl Acad Sci USA 97(6):2881–2885.  https://doi.org/10.1073/pnas.050583697 CrossRefPubMedGoogle Scholar
  35. Miller HC, Pattison KF, DeWall CN, Rayburn-Reeves R, Zentall TR (2010) Self-control without a “self”? Common self-control process in humans and dogs. Psych Sci 21(4):534–538.  https://doi.org/10.1177/0956797610364968 CrossRefGoogle Scholar
  36. Miller HC, Pattison KF, Laude JR, Zentall TR (2015) Self-regulatory depletion in dogs: insulin release is not necessary for the replenishment of persistence. Behav Processes, 110:22–26. https://www.ncbi.nlm.nih.gov/pubmed/25264236.  https://doi.org/10.1016/j.beproc.2014.09.030 CrossRefGoogle Scholar
  37. Node K, Inoue T (2009) Postprandial hyperglycemia as an etiological factor in vascular failure. Cardiovasc Diabetol 8:23.  https://doi.org/10.1186/1475-2840-8-23 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Parrish AE, Emerson ID, Rossettie MS, Beran MJ (2016) Testing the glucose hypothesis among capuchin monkeys: Does glucose boost self-control? Behav Sci (Basel) 6(3):16.  https://doi.org/10.3390/bs6030016 CrossRefGoogle Scholar
  39. Philippou E, Constantinou M (2014) The influence of glycemic index on cognitive functioning: a systematic review of the evidence. Adv Nutr 5(2):119–130.  https://doi.org/10.3945/an.113.004960 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Piotti P, Satchell L, Lockhart T (2018) Impulsivity and behaviour problems in dogs: a reinforcement sensitivity theory perspective. Behav Processes 151:104–110.  https://doi.org/10.1016/j.beproc.2018.03.012 CrossRefPubMedGoogle Scholar
  41. Rankovic A (2018) The acute effects of starch sources on glycemic index, glycemic response, insulinemic response and satiety-related hormones in dogs. Master’s thesis dissertation, University of Guelph, Guelph, CanadaGoogle Scholar
  42. Riby LM, Lai Teik Ong D, Azmie NBM, Ooi EL, Regina C, Yeo EKW et al (2017) Impulsiveness, postprandial blood glucose, and glucoregulation affect measures of behavioral flexibility. Nutr Res 48:65–75.  https://doi.org/10.1016/j.nutres.2017.10.011 CrossRefPubMedGoogle Scholar
  43. Ryan CM, van Duinkerken E, Rosano C (2016) Neurocognitive consequences of diabetes. Am Psychol 71(7):563–576.  https://doi.org/10.1037/a0040455 CrossRefPubMedGoogle Scholar
  44. Salman MD, Hutchison J, Ruch-Gallie R, Kogan L, New JC, Kaas PH, Scarlett JM (2000) Behavioral reasons for relinquishment of dogs and cats to 12 shelters. J Appl Anim Welf Sci 3(2):93–106.  https://doi.org/10.1207/S15327604JAWS0302_2 CrossRefGoogle Scholar
  45. Santos L, Ericson B, Hauser M (1999) Constraints on problem solving and inhibition: object retrieval in cotton-top tamarins (Saguinus oedipus oedipus). J Comp Psychol 113(2):186–193.  https://doi.org/10.1037/0735-7036.113.2.186 CrossRefGoogle Scholar
  46. Schnurr TM, Reynolds AJ, Gustafson SJ, Duffy LK, Dunlap KL (2014) Conditioning causes an increase in glucose transporter-4 levels in mononuclear cells in sled dogs. Int J Biochem Cell Biol 55:227–231CrossRefGoogle Scholar
  47. Smith MA, Riby LM, Eekelen JA, Foster JK (2011) Glucose enhancement of human memory: a comprehensive research review of the glucose memory facilitation effect. Neurosci Biobehav Rev 35(3):770–783.  https://doi.org/10.1016/j.neubiorev.2010.09.008 CrossRefPubMedGoogle Scholar
  48. Stow MK, Vernouillet A, Kelly DM (2018) Neophobia does not account for motoric self-regulation performance as measured during the detour-reaching cylinder task. Anim Cogn 21(4):565–574.  https://doi.org/10.1007/s10071-018-1189-8 CrossRefGoogle Scholar
  49. Sümegi Z, Kis A, Miklosi A, Topal J (2014) Why do adult dogs (Canis familiaris) commit the A-not-B search error? J Comp Psychol 128(1):21–30.  https://doi.org/10.1037/a0033084 CrossRefPubMedGoogle Scholar
  50. Sunvold GD, Bouchard GB (1998) The glycemic response to dietary starch. In: Reinhart GA, Carey DP (eds) Recent advances in canine and feline nutrition: iams nutrition symposium proceedings, vol II. Orange Frazer Press, WilmingtonGoogle Scholar
  51. Thomas DE, Elliott EJ, Baur L (2007) Low glycaemic index or low glycaemic load diets for overweight and obesity. Cochrane Database Syst Rev.  https://doi.org/10.1002/14651858.cd005105.pub2 CrossRefPubMedGoogle Scholar
  52. Vernouillet A, Anderson J, Clary D, Kelly DM (2016) Inhibition in Clark’s nutcrackers (Nucifraga columbiana): results of a detour-reaching test. Anim Cogn 19(3):661–665.  https://doi.org/10.1007/s10071-016-0952-y CrossRefPubMedGoogle Scholar
  53. Vernouillet A, Stiles LR, Andrew McCausland J, Kelly DM (2018) Individual performance across motoric self-regulation tasks are not correlated for pet dogs. Learn Behav 46(4):522–536.  https://doi.org/10.3758/s13420-018-0354-x CrossRefPubMedGoogle Scholar
  54. Wascher TC, Schmoelzer I, Wiegratz A, Stuehlinger M, Mueller-Wieland D, Kotzka J, Enderle M (2005) Reduction of postchallenge hyperglycaemia prevents acute endothelial dysfunction in subjects with impaired glucose tolerance. Eur J Clin Invest 35(9):551–557.  https://doi.org/10.1111/j.1365-2362.2005.01550.x CrossRefPubMedGoogle Scholar
  55. Wiedmeyer CE, Johnson PJ, Cohn LA, Meadows RL (2003) Evaluation of a continuous glucose monitoring system for use in dogs, cats, and horses. J Am Vet Med Assoc 223(7):987–992CrossRefGoogle Scholar
  56. Wolever TMS, Jenkins DJA, Jenkins AL, Josse RG (1991) The glycemic index: methodology and clinical implications. Am J Clin Nutr 54(5):846–854CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of ManitobaWinnipegCanada
  2. 2.PetcureanChilliwackCanada
  3. 3.Department of Biological SciencesUniversity of ManitobaWinnipegCanada
  4. 4.Department of Clinical Studies, Ontario Veterinary CollegeUniversity of GuelphGuelphCanada

Personalised recommendations