Animal cognition (reasoning) in the light of genetic ideas

The historical overview is presented of genetic experiments in L.V. Krushinsky’s laboratory in Moscow State University. L.V. Krushinsky stated the three-component concept of animal behavior. He claimed that animal behavior has not only innate species specific behavior and the learning ability, but should be supplemented by another mental category, reasoning the ability for elementary logic operarions. Being rather lonesome at the beginning, Krushinsky got the spiritual support from D.K. Belyaev and B.L. Astaurov. The attempt to study the genetic bases of reasoning ability was performed in Krushinsky’s lab using the trait “extrapolation problem solving”, which meant the ability of an unexperienced naïve animal to find the food bait when it moved aside and disappeared from (not “in”) the view. The selection for high scores of this trait in the hybrid rat population (Norway rat × laboratory strain cross) was started. Initially the hybrid rats solved this problem in the statistically significant proportions, while the animals from further selection generations demonstrated the dramatic increase of anxiety (in spite of extensive handling of these animals), which made further experiments impossible. Much later another selection experiment started in which mice of a genetically heterogeneous population were selected for high scores of extrapolation problem and concomitantly for the lack-ofanxiety signs during the testing procedure. This selection for a cognitive trait produced some positive results, although the direct response to selection was very weak. The data obtained show the intricate connection between the mouse ability to solve the problem and the processes of anxiety, which in turn looks as non-uniform by its nature and mechanisms. The data from experiments performed in classical genetics should be combined with the new knowledge concerning the role of single genes determining animal behavior.

1. Allen B.D., Singer A.C., Boyden E.S. Principles of designing interpretable optogenetic behavior experiments. Learn. Mem. 2015;22:232-238. DOI 10.1101/lm.038026.114.

2. Ben Abdallah N.M., Fuss J., Trusel M., Galsworthy M.J., Bobsin K., Colacicco G., Deacon R.M., Riva M.A., Kellendonk C., Sprengel R., Lipp H.-P., Gass P. The puzzle box as a simple and efficient behavioral test for exploring impairments of general cognition and executive functions in mouse models of schizophrenia. Exp. Neurol. 2011;227:42-52. http://dx.doi.org/10.1016/j.expneurol.2010.09.008.

3. Braida D., Sacerdote P., Panerai A.E., Bianchi M., Aloisi A.M., Iosuè S., Sala M. DNA fragmentation factor 45 knockout mice exhibit longer memory retention in the novel object recognition task compared to wild-type mice. Physiol. Behav. 2002;76:315-332.

4. Champtiaux N., Changeux J.P. Knockout and knockin mice to investigate the role of nicotinic receptors in the central nervous system. Prog. Brain Res. 2004;145:235-251.

5. De Bundel D., Schallier A., Loyens E., Fernando R., Miyashita H., Van Liefferinge J., Vermoesen K., Bannai S., Sato H., Michotte Y., Smolders I., Massie A. Loss of system x(c)- does not induce oxidative stress but decreases extracellular glutamate in hippocampus and influences spatial working memory and limbic seizure susceptibility. J. Neurosci. 2011;31:5792-5803.

6. Dong J., Horvath S. Understanding network concepts in modules BMC. Syst. Biol. 2007;1;24. http://www.biomedcentral.com/1752-0509/1/24.

7. Driscoll P., Battig K. Behavioral, emotional and neurochemical profiles of rats selected for extreme differences in active, two-way avoidance performance. Genetics of the Brain. Ed. I.Lieblich. Amsterdam: Elsevier Biomedical Press, 1982;95-123.

8. Duffy L., Cappas E., Lai D., Boucher A.A., Karl T. Cognition in transmembrane domain neuregulin 1 mutant mice. Neuroscience. 2010; 170:800-807.

9. Dziewczapolski G., Glogowski C.M., Masliah E., Heinemann S.F. Deletion of the alpha 7 nicotinic acetylcholine receptor gene improves cognitive deficits and synaptic pathology in a mouse model of Alzheimer’s disease. J. Neurosci. 2009;29:8805-8815.

10. Fujino T., Leslie J.H., Eavri R., Chen J.L., Lin W.C., Flanders G.H., Borok E., Horvath T.L., Nedivi E. CPG15 regulates synapse stability in the developing and adult brain. Genes Dev. 2011;25:2674-2685.

11. Golibrodo V.A., Perepelkina O.V., Lilp I.G., Poletaeva I.I. The behavior of mice selected for cognitive trait in hyponeophagia test. Zh. Vyssh. Nerv. Deiat. Im. I.P. Pavlova. 2014;64:639- 645. Russian. PMID:25975140.

12. Innis N.K. Tolman and Tryon. Early research on the inheritance of the ability to learn. Am. Psychol. 1992;47:190-197. PMID:1567088.

13. Josselyn S.A., Shi C., Carlezon W.A. Jr., Neve R.L., Nestler E.J., Davis M. Long-term memory is facilitated by cAMP response elementbinding protein overexpression in the amygdala. J. Neurosci. 2001; 21:2404-2412. PMID:11264314.

14. Knowles E.E., Mathias S.R., McKay D.R., Sprooten E., Blangero J., Almasy L., Glahn D.C. Genome-wide analyses of working-memory ability: a review. Curr. Behav. Neurosci. Rep. 2014;1:224-233.

15. Kos A., Loohuis N.F., Glennon J.C., Celikel T., Martens G.J., Tiesinga P.H., Aschrafi A. Recent developments in optical neuromodulation technologies. Mol. Neurobiol. 2013;47:172-185. DOI 10.1007/s12035-012-8361-y.

16. Krushinsky L.V. Experimental Studies of Elementary Reasoning. Evolutionary, Physiological and Genetic Aspects of Behavior. New Dehli: Oxonian Press, 1990.

17. Krushinsky L.V., Astaurova N.V., Kouznetzova L.V., Otchinskaya E.I., Poletaeva I.I., Romanova L.G., Sotskaya M.N. The Role of genetic factors in determining the extrapolation ability in animals. Current Problems in Behavioural Genetics. Eds. V.K. Fedorov, V.V. Ponomarenko. Leningrad: Nauka, 1975;98-110.

18. Leitinger B., Poletaeva I.I., Wolfer D.P., Lipp H.-P. Swimming navigation, open-field activity, and extrapolation behavior of two inbred mouse strains with Robertsonian translocation of chromosomes 8 and 17. Behav. Genet. 1994;24:273-284. PMID:7945157.

19. Luria A.R. The Essentials in Neuropsychology. Academia Publ. Center, 2003.

20. McQuade J.M.S., Vorhees C.V., Xu M., Zhang J. Cognitive function in young and adult IL (interleukin)-6 deficient mice. Behav. Brain Res. 2004;153:423-429.

21. Milhaud J.M., Halley H., Lassalle J.M. Two QTLs located on chromosomes 1 and 5 modulate different aspects of the performance of mice of the B × D Ty RI strain series in the Morris navigation task. Behav. Genet. 2002;32:69-78.

22. Mizumori S.J., Tryon V.L. Integrative hippocampal and decision-making neurocircuitry during goal-relevant predictions and encoding. Prog. Brain. Res. 2015;219:217-242. DOI 10.1016/bs.pbr.2015.03.010.

23. Mohammed A.H. Genetic dissection of nicotine-related behaviour: a review of animal studies. Behav. Brain Res. 2000;113:35-41. PMID:10942030.

24. Nadler J.J., Zou F., Huang H., Moy S.S., Lauder J., Crawley J.N., Threadgill D.W., Wright F.A., Magnuson T.R. Plasticity, large-scale gene expression differences across brain regions and inbred strains correlate with a behavioral phenotype. Genetics. 2006;174:1229-1236.

25. O’Connor R.M., Finger B.C., Flor P.J., Cryan J.F. Metabotropic glutamate receptor 7: At the interface of cognition and emotion. Eur. J. Pharmacol. 2010;639:123-131.

26. Owen E.H., Logue S.F., Rasmussen D.L., Wehner J.M. Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F1 hybrids: implications of genetic background for single gene mutations and quantitative trait loci analyses. Neuroscience. 1997;80:1087-1099.

27. Perepelkina O.V., Golibrodo V.A., Lilp I.G., Poletaeva I.I. Selection of laboratory mice for the high scores of logic task solutions: the correlated changes in behavior. Adv. Biosci. Biotechnol. 2014;5:294-300. http://dx.doi.org/10.4236/abb.2014.54036.

28. Perepelkina O.V., Golibrodo V.A., Lilp I.G., Poletaeva I.I. Selection of mice for high scores of elementary logical task solution. Dokl. Biol. Sci. 2015;460:52-56. DOI 10.1134/S0012496615010159. PMID: 25773252.

29. Perepelkina O.V., Markina N.V., Golibrodo V.A., Lil’p I.G., Poletaeva I.I. Selection of mice for high level of extrapolation capacity with cobcommitant low anxiety level. Zh. Vyssh. Nerv. Deyat. Im. I.P. Pavlova. 2011;61:742-749.

30. Poletaeva I.I., Romanova L.G., Popova N.V. Genetic aspects of animal reasoning. Behav. Gen. 1993;23:467-475. http://dx.doi.org/10.1007/BF01067982.

31. Poletaeva I.I., Zorina Z.A. Physiological and genetic approaches to study animal cognitive behavior. Russ. J. Cogn. Sci. 2014;1:31-55.

32. Powell C.M. Gene targeting of presynaptic proteins in synaptic plasticity and memory: across the great divide. Neurobiol. Learn. Mem. 2006;85:2-15.

33. Ren K., Thinschmidt J., Liu J., Ai L., Papke R.L., King M.A., Hughes J.A., Meyer E.M. alpha7 Nicotinic receptor gene delivery into mouse hippocampal neurons leads to functional receptor expression, improved spatial memory-related performance, and tau hyperphosphorylation. Neuroscience. 2007;145:314-322.

34. Reznikova Z. Animal Intelligence. From Individual to Social Cognition. Cambridge: Cambridge University Press, 2007.

35. Scott R., Bourtchuladze R., Gossweiler S., Dubnau J., Tully T. CREB and the discovery of cognitive enhancers. J. Mol. Neurosci. 2002;19: 171-177. PMID12212777.

36. Senechal Y., Kelly P.H., Cryan J.F., Natt F., Dev K.K. Amyloid precursor protein knockdown by siRNA impairs spontaneous alternation in adult mice. J. Neurochem. 2007;102;1928-1940.

37. Shapiro M. Plasticity, hippocampal place cells, and cognitive maps (reprinted). Arch. Neurol. 2001;58:874-881. www.archneurol.com.

38. Silva A.J. Molecular and cellular cognitive studies of the role of synaptic plasticity in memory. J. Neurobiol. 2003;54:224-237. PMID: 12486706.

39. Tolman E.C. Purposive behavior in animals and man. London, Appleton-Century, 1932.

40. Zucca P., Milos N., Vallortigara G. Piagetian object permanence and its development in eurasian jays (Garrulus glandarius). Anim. Cogn. 2007;10:243-258. http://dx.doi.org/10.1007/s10071-006-0063-2.