The interstrain differences in laboratory mouse cognitive abilities (elementary logic task, attention, memory)

Abstract

Mice of two strains, selected, respectively, for successful solution of puzzle-box test (addressed to “object permanence” rule operation) and for non-solution of this test, were tested for short term memory, attention to moving object and neophagia. The data obtained demonstrated, that mice, selected for successful “object permanence” test solution demonstrated higher scores in recent memory and attention indices. It was suggested, that interstrain differences discovered should be addressed to differences in the “executive functions” expression.

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About the authors

O. V. Perepelkina

Lomonosov Moscow State University

Email: ingapoletaeva@mail.ru
Russian Federation, Moscow

I. I. Poletaeva

Lomonosov Moscow State University

Author for correspondence.
Email: ingapoletaeva@mail.ru
Russian Federation, Moscow

References

  1. Крушинский Л.В. Элементарная рассудочная деятельность. Изд-во URSS, 2014.
  2. Перепелкина О.В., Маркина Н.В., Голибродо В.А., Лильп И Г., Полетаева И.И. Селекция мышей на высокий уровень способности к экстраполяции при низком уровне тревожности. Журн. высш. нервн. деят. им. И.П.Павлова. 2011. 61 (6): 13–23.
  3. Перепелкина О.В., Тарасова А.Ю., Голибродо В.А., Лильп И.Г., Полетаева И.И. Поведение мышей, селектированных на высокие значения когнитивного признака. Журн. высш. нервн. деят. им. И.П.Павлова. 2018. 68 (4): 434–447.
  4. Перепелкина О.В., Лильп И.Г., Маркина Н.В., Голибродо В.А., Полетаева И.И. Первый опыт селекции лабораторных мышей на высокую способность к экстраполяции. В сб. Формирование поведения животных в норме и патологии. К 100-летию со дня рождения Л.В. Крушинского. Под ред. И.И. Полетаевой, З.А. Зориной. М.: Языки славянских культур, 2013. 162–188.
  5. Полетаева И.И., Романова Л.Г. Хромосомные мутации и способность лабораторных мышей к экстраполяции направления движения стимула. В сб. Формирование поведения животных в норме и патологии. К 100-летию со дня рождения Л.В. Крушинского. Под ред. И.И. Полетаевой, З.А. Зориной. М.: Языки славянских культур, 2013. 133–150.
  6. Ben Abdallah N.M.-B. Т., Fuss J., M., Galsworthy M.J., Bobsin K., Colacicco G., Deacon R.M.J., 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 (1): 42–52. https://doi.org/10.1016/j.expneurol.2010.09.008
  7. Brigman J.L., Powell E.M., Mittleman G., Young J W. Examining the genetic and neural components of cognitive flexibility using mice. Physiol. Behav. 2012. 107 (5): 666–669. https://doi.org/10.1016/j.physbeh.2011.12.024 (5)
  8. Carli M., Invernizzi R.W. Serotoninergic and dopaminergic modulation of cortico-striatal circuit in executive and attention deficits induced by NMDA receptor hypofunction in the 5-choice serial reaction time task. Front Neural Circuits. 2014; 8: 58. eCollection 2014
  9. https://doi.org/10.3389/fncir.2014.00058
  10. Cascella M., Al Khalili Y. Short-term memory impairment. 2023. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024 Jan. PMID: 31424720
  11. Cooper R.P. Cognitive Control: Componential or Emergent? Top Cogn Sci. 2010.;2 (4): 598–613. https://doi.org/10.1111/j.1756-8765.2010.01110.x
  12. Ene H.M., Kara N.Z., Barak N., Ben-Mordechai T.R., Einat H. Effects of repeated asenapine in a battery of tests for anxiety-like behaviours in mice. Acta Neuropsychiatr 2016 Apr. 28 (2): 85–91. https://doi.org/10.1017/neu.2015.53
  13. Galsworthy M.J., Paya-Cano J.L., Monleon S., Plomin R. Evidence for general cognitive ability (g) in heterogeneous stock mice and an analysis of potential confounds. Genes Brain Behav. 2002. 1 (2): 88–95. https://doi.org/10.1034/j.1601-183x.2002.10204.x
  14. Georgiou P., Panos Zanos P., Mou T-Ch.M., An X., Gerhard D.M., Dilyan I., Dryanovski D.J., Potter L.E., Highland J.N., Jenne C.E., Stewart B.W., Pultorak K.J., Yuan P., Powels C.F., Lovett J., Pereira E.F.R., Clark S.M., Tonelli L.H., Moaddel R., Zarate C.A.Jr., Duman R.S., Thompson S.M., Gould T.D. Experimenters’ sex modulates mouse behaviors and neural responses to ketamine via corticotropin releasing factor. Nat Neurosci 2022 Sep; 25 (9): 1191–1200. https://doi.org/10.1038/s41593-022-01146-x
  15. Giménez-Llort L., Schiffmann S.N., Shmidt T., Canela L., Camón L., Wassholm M., Canals M., Terasmaa A., Fernández-Teruel A., Tobeña A., Popova E, Ferré S., Agnati L., Ciruela F., Martínez E., Scheel-Kruger J. L.C., Franco R., Fuxe K., Bader M. Working memory deficits in transgenic rats overexpressing human adenosine A2A receptors in the brain. Neurobiol. Learn. Mem. 2007. 87 (1): 42–56. https://doi.org/10.1016/j.nlm.2006.05.004
  16. Hamilton D.A., Brigman J.L. Behavioral flexibility in rats and mice: contributions of distinct frontocortical regions. Genes Brain Behav .2015. 14 (1): 4–21. doi: 10.1111/gbb.12191
  17. Hen R., Dulawa S.C. Recent advances in animal models of chronic antidepressant effects: the novelty-induced hypophagia test. Neurosci Biobehav Rev. 2005. 29 (4-5): 771–783. https://doi.org/10.1016/j.neubiorev.2005.03.017
  18. Holmes A., Wellman C L. Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci Biobehav Rev. 2009. 33 (6): 773–783. https://doi.org/10.1016/j.neubiorev.2008.11.005
  19. Jian-Min C., Zhi-Yuan W., Ke L, Cheng Z., Shi-Xuan W., Yi-Wei C., Guan-Yi L., Rui S., Xiao-Mei Z., Jin L., Ning W. Assessment of lisdexamfetamine on executive function in rats: A translational cognitive research. Exp Neurol. 2024. 374:114718. Epub 2024 Feb 8. PMID: 38336285. https://doi.org/10.1016/j.expneurol.2024.114718
  20. Nilsson S.R.O., Alsiöa J., Somerville E.M., Clifton P.G. The rat’s not for turning: Dissociating the psychological components of cognitive inflexibility Neurosci. Biobehav. Rev, 2015. V. 56. P 1–14.
  21. Perepelkina O.V., Poletaeva I.I. Selection of Mice for Object Permanence Cognitive Task Solution. Neurol Int. 2022. 14(3): 696–706. PMID: 36135993. https://doi.org/10.3390/neurolint14030058
  22. Perepelkina O.V., Poletaeva I.I. Cognitive Test Solution in Mice with Different Brain Weights after Atomoxetine Neurol Int. 2023 May 15; 15 (2): 649–660. https://doi.org/10.3390/neurolint15020041
  23. Reimer A. E., de Oliveira A.R, Brandão M. L. Glutamatergic mechanisms of the dorsal periaqueductal gray matter modulate the expression of conditioned freezing and fear-potentiated startle. Neurosci. 2012. 219: 72–81. https://doi.org/10.1016/j.neuroscience.2012.06.005
  24. Rozeske R.R, Jercog D., Karalis N., Chaudun F., Khoder S., Delphine G., Winke N., Herry C. Prefrontal-periaqueductal gray-projecting neurons mediate context fear discrimination. Neuron, 2018. 97 (4): 898–910. doi: 10.1016/j.neuron.2017.12.044
  25. Sable H.J.K., Lester D.B., Potter J.L., Nolen H.G., Cruthird D.M., Estes L.M., Johnson A.D., Regan S.L., Williams M.T., Vorhees C.V. An assessment of executive function in two different rat models of attention-deficit hyperactivity disorder: Spontaneously hypertensive versus Lphn3 knockout rats. Genes Brain Behav. 2021. 20(8): e12767. Epub 2021 Sep 8. PMID: 34427038. https://doi.org/10.1111/gbb.12767
  26. Talpos J., Shoaib M. Executive function. Handb Exp Pharmacol. 2015. 228: 191–213. https://doi.org/10.1007/978-3-319-16522-6_6
  27. Yegla B., Foster T.C., Kumar A. Behavior model for assessing decline in executive function during aging and neurodegenerative disease. Methods Mol. Biol. 2011. 2019: 441–449. https://doi.org/10.1007/978-1-4939-9554-7
  28. Zhong P., Cao Q., Yan Z. Selective impairment of circuits between prefrontal cortex glutamatergic neurons and basal forebrain cholinergic neurons in a tauopathy mouse model. Cereb Cortex. 2022. 32 (24): 5569–5579. doi: 10.1093/cercor/bhac036.PMID: 35235649.
  29. Zucca P., Milos N., Vallortigara G. Piagetian object permanence and its development in Eurasian jays (Garrulus glandarius). Anim. Cogn. 2007. 10 (2): 243–258. https://doi.org/10.1007/s10071-006-0063-2

Supplementary files

Supplementary Files
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1. JATS XML
2. Fig. 1. (а) – the schematic view of the experimental device for puzzle-box test. 1 – the brightly lit box compartment. 2 – the dark compartment, 3 – the underpass, leading to dark compartment. (б) – the photograph of the experimental box for puzzle-box test with mouse inside, (в) – the photograph of the experimental box for attention test, (г) – mouse near the object, (д) – the set of objects presented to animals in this test

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3. Fig. 2. The proportions of animals (%, ordinate) in the course of selection (F1-F9), which solved successfully the stages of puzzle-box test, when the underpass was blocked by a plug. The sign “+” – the scores for “plus” strain, “-” – for “minus” strain. Co – the scores of mice from control non-selected population. The first test presentation with a “plug”– light grey columns, the second “plug” presentation – dark grey columns. *, *** – the statistically significant differences from scores of “minus” strain, ### – differences from control population scores, p < 0.05 (Fisher φ test for alternative proportions differences)

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4. Fig. 3. The proportions of mice (%, ordinate), which performed the second “plug” stage with shorter latencies than those at first “plug” presentation. Light grey columns – “plus” strain, dark grey columns – “minus” strain, black columns – non-selected genetically heterogenous control population. *** – statistically significant differences from scores of the “minus” strain and of control population (Fisher φ test for alternative proportions differences)

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5. Fig. 4. The latencies, L (s, ordinate, mean ± st.err.) of the reactions of F6, F7 and F9 male mice to moving new objects (attention test). 1 – L of the first approach to the object, shown as the first, 2 – L of the first approach to object, shown as the fifth. Designations as in fig. 3. Number of animals: “plus” strain – F6, n = 14, F7, n = 16, F9, n = 10, strain “minus” – F6, n = 18, F7, n = 13, F9, n = 7, control population – F6, n = 10, F7, n = 12, not tested in F9. * – significant difference, р < 0.05 (one-factor ANOVA, factor “genotype”, Fisher post hoc LSD test)

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6. Fig. 5. The mean scores contact numbers (ordinate, mean ± st.err.) with the object in mice of F6, F7 and F9 during 40 sec of its movement along the box perimeter. 1 – the object, shown as the first, 2 – the object, shown as the fifth. Designations as in Fig. 3

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