J Vet Sci.  2016 Dec;17(4):563-567. 10.4142/jvs.2016.17.4.563.

Learning, memory and exploratory similarities in genetically identical cloned dogs

• Shin CW
• Kim GA
• Park WJ
• Park KY
• Jeon JM
• Oh HJ
• Kim MJ
• Lee BC

• KMID: 2412613
• DOI: http://doi.org/10.4142/jvs.2016.17.4.563

Abstract

Somatic cell nuclear transfer allows generation of genetically identical animals using donor cells derived from animals with particular traits. To date, few studies have investigated whether or not these cloned dogs will show identical behavior patterns. To address this question, learning, memory and exploratory patterns were examined using six cloned dogs with identical nuclear genomes. The variance of total incorrect choice number in the Y-maze test among cloned dogs was significantly lower than that of the control dogs. There was also a significant decrease in variance in the level of exploratory activity in the open fields test compared to age-matched control dogs. These results indicate that cloned dogs show similar cognitive and exploratory patterns, suggesting that these behavioral phenotypes are related to the genotypes of the individuals.

Keyword

cloned dogs; exploratory; learning and memory; similarity; somatic cell nuclear transfer

MeSH Terms

Animals
Cloning, Organism/*veterinary
Dogs/genetics/*physiology
*Exploratory Behavior
Female
*Learning
*Memory

Figure

• 

  Fig. 1 Cognitive performance among cloned dogs (Cl) and control dogs (Co) based on the Y-maze testing apparatus. (A) Times to reach the obligatory preferred arm of the Y-maze. The variation between Cl and Co was compared using a permutation test. (B) Times to reach the non-preferred site of the Y-maze during reversal learning. The variation between Cl and Co was compared using the permutation test. (C) Total incorrect (TIC) number for Cl and Co. (D) Total incorrect number before the first correct (IBFC) choice during reversal learning. (E) Total incorrect choices after the first correct choice (IAFC) among each dog. p < 0.05 indicates statistical significance.

Reference

1. Araujo JA, Chan ADF, Winka LL, Seymour PA, Milgram NW. Dose-specific effects of scopolamine on canine cognition: impairment of visuospatial memory, but not visuospatial discrimination. Psychopharmacology (Berl). 2004; 175:92–98.

2. Baughman HM, Schermer JA, Veselka L, Harris J, Vernon PA. A behavior genetic analysis of trait emotional intelligence and alexithymia: a replication. Twin Res Hum Genet. 2013; 16:554–559.

3. Blokland GAM, McMahon KL, Thompson PM, Martin NG, de Zubicaray GI, Wright MJ. Heritability of working memory brain activation. J Neurosci. 2011; 31:10882–10890.

4. Boenigk K, Hamann H, Distl O. Genetic analysis of the outcome of behavioural tests in puppies of the Hovawart breed. Dtsch Tierarztl Wochenschr. 2005; 112:265–271.

5. Caston J, Chianale C, Delhaye-Bouchaud N, Mariani J. Role of the cerebellum in exploration behavior. Brain Res. 1998; 808:232–237.

6. Cheung CHM, Wood AC, Paloyelis Y, Arias-Vasquez A, Buitelaar JK, Franke B, Miranda A, Mulas F, Rommelse N, Sergeant JA, Sonuga-Barke EJ, Faraone SV, Asherson P, Kuntsi J. Aetiology for the covariation between combined type ADHD and reading difficulties in a family study: the role of IQ. J Child Psychol Psychiatry. 2012; 53:864–873.

7. Choi J, Lee JH, Oh HJ, Kim MJ, Kim GA, Park EJ, Jo YK, Lee SI, Hong DG, Lee BC. Behavioral analysis of cloned puppies derived from an elite drug-detection dog. Behav Genet. 2014; 44:68–76.

8. Cotman CW, Head E, Muggenburg BA, Zicker S, Milgram NW. Brain aging in the canine: a diet enriched in antioxidants reduces cognitive dysfunction. Neurobiol Aging. 2002; 23:809–818.

9. Head E, Callahan H, Cummings BJ, Cotman CW, Ruehl WW, Muggenberg BA, Milgram NW. Open field activity and human interaction as a function of age and breed in dogs. Physiol Behav. 1997; 62:963–971.

10. Head E, Nukala VN, Fenoglio KA, Muggenburg BA, Cotman CW, Sullivan PG. Effects of age, dietary, and behavioral enrichment on brain mitochondria in a canine model of human aging. Exp Neurol. 2009; 220:171–176.

11. Hong SG, Jang G, Kim MK, Oh HJ, Park JE, Kang JT, Koo OJ, Kim DY, Lee BC. Dogs cloned from fetal fibroblasts by nuclear transfer. Anim Reprod Sci. 2009; 115:334–339.

12. Hong SG, Kim MK, Jang G, Oh HJ, Park JE, Kang JT, Koo OJ, Kim T, Kwon MS, Koo BC, Ra JC, Kim DY, Ko C, Lee BC. Generation of red fluorescent protein transgenic dogs. Genesis. 2009; 47:314–322.

13. Jang G, Hong SG, Oh HJ, Kim MK, Park JE, Kim HJ, Kim DY, Lee BC. A cloned toy poodle produced from somatic cells derived from an aged female dog. Theriogenology. 2008; 69:556–563.

14. Kelley AE, Cador M, Stinus L. Exploration and its measurement: a psychopharmacological perspective. In : Boulton AA, Baker GB, editors. Psychopharmacology: Neuromethods. Humana Press: Clifton;1989. Vol. 13.

15. Kim GA, Oh HJ, Kim MJ, Jo YK, Choi J, Park JE, Park EJ, Lim SH, Yoon BI, Kang SK, Jang G, Lee BC. Survival of skin graft between transgenic cloned dogs and non-transgenic cloned dogs. PLoS One. 2014; 9:e108330.

16. Kim GA, Oh HJ, Park JE, Kim MJ, Park EJ, Lim SH, Kang SK, Jang G, Lee BC. Employing mated females as recipients for transfer of cloned dog embryos. Reprod Fertil Dev. 2013; 25:700–706.

17. Kim MJ, Oh HJ, Park JE, Kim GA, Hong SG, Jang G, Kwon MS, Koo BC, Kim T, Kang SK, Ra JC, Ko C, Lee BC. Generation of transgenic dogs that conditionally express green fluorescent protein. Genesis. 2011; 49:472–478.

18. Lindberg S, Strandberg E, Swelson L. Genetic analysis of hunting behaviour in Swedish Flatcoated Retrievers. Appl Anim Behav Sci. 2004; 88:289–298.

19. Milgram NW. Cognitive experience and its effect on age-dependent cognitive decline in beagle dogs. Neurochem Res. 2003; 28:1677–1682.

20. Milgram NW, Head E, Zicker SC, Ikeda-Douglas CJ, Murphey H, Muggenburg B, Siwak C, Tapp D, Cotman CW. Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: a two-year longitudinal study. Neurobiol Aging. 2005; 26:77–90.

21. Miller G, Zhu G, Wright MJ, Hansell NK, Martin NG. The heritability and genetic correlates of mobile phone use: a twin study of consumer behavior. Twin Res Hum Genet. 2012; 15:97–106.

22. Oh HJ, Hong SG, Park JE, Kang JT, Kim MJ, Kim MK, Kang SK, Kim DY, Jang G, Lee BC. Improved efficiency of canine nucleus transfer using roscovitine-treated canine fibroblasts. Theriogenology. 2009; 72:461–470.

23. Oh HJ, Kim MK, Jang G, Kim HJ, Hong SG, Park JE, Park K, Park C, Sohn SH, Kim DY, Shin NS, Lee BC. Cloning endangered gray wolves (Canis lupus) from somatic cells collected postmortem. Theriogenology. 2008; 70:638–647.

24. Rosado B, González-Martínez A, Pesini P, García-Belenguer S, Palacio J, Villegas A, Suárez ML, Santamarina G, Sarasa M. Effect of age and severity of cognitive dysfunction on spontaneous activity in pet dogs – part 1: locomotor and exploratory behaviour. Vet J. 2012; 194:189–195.

25. Ruefenacht S, Gebhardt-Henrich S, Miyake T, Gaillard C. A behaviour test on German Shepherd dogs: heritability of seven different traits. Appl Anim Behav Sci. 2002; 79:113–132.

26. Saetre P, Strandberg E, Sundgren PE, Pettersson U, Jazin E, Bergström TF. The genetic contribution to canine personality. Genes Brain Behav. 2006; 5:240–248.

27. Sanders DN, Kanazono S, Wininger FA, Whiting REH, Flournoy CA, Coates JR, Castaner LJ, O’Brien DP, Katz ML. A reversal learning task detects cognitive deficits in a Dachshund model of late-infantile neuronal ceroid lipofuscinosis. Genes Brain Behav. 2011; 10:798–804.

28. Siwak CT, Tapp PD, Milgram NW. Effect of age and level of cognitive function on spontaneous and exploratory behaviors in the beagle dog. Learn Mem. 2001; 8:317–325.

29. Tamashiro KLK, Sakai RR, Yamazaki Y, Wakayama T, Yanagimachi R. Developmental, behavioral, and physiological phenotype of cloned mice. Adv Exp Med Biol. 2007; 591:72–83.

30. Tamashiro KLK, Wakayama T, Yamazaki Y, Akutsu H, Woods SC, Kondo S, Yanagimachi R, Sakai RR. Phenotype of cloned mice: development, behavior, and physiology. Exp Biol Med (Maywood). 2003; 228:1193–1200.

31. Tapp PD, Siwak CT, Estrada J, Head E, Muggenburg BA, Cotman CW, Milgram NW. Size and reversal learning in the beagle dog as a measure of executive function and inhibitory control in aging. Learn Mem. 2003; 10:64–73.

32. Trzaskowski M, Davis OSP, DeFries JC, Yang J, Visscher PM, Plomin R. DNA evidence for strong genome-wide pleiotropy of cognitive and learning abilities. Behav Genet. 2013; 43:267–273.

33. van den Berg L, Schilder MBH, de Vries H, Leegwater PAJ, van Oost BA. Phenotyping of aggressive behavior in golden retriever dogs with a questionnaire. Behav Genet. 2006; 36:882–902.

34. van Soelen IL, Brouwer RM, van Leeuwen M, Kahn RS, Hulshoff Pol HE, Boomsma DI. Heritability of verbal and performance intelligence in a pediatric longitudinal sample. Twin Res Hum Genet. 2011; 14:119–128.

35. Vandenberg SG. Primary mental abilities or general intelligence? Evidence from twin studies. Eugen Soc Symp. 1968; 4:146–160.

36. Willison E, Sundgren PE. Behaviour test for eight-week old puppies—heritabilities of tested behaviour traits and its correspondence to later behaviour. Appl Anim Behav Sci. 1998; 58:151–162.