Neurobehavioral Testing as Cognitive Function Evaluation tool in Experimentally Induced Neurodegeneration in Mice

Cover Page

Cite item

Full Text

Abstract

Neurodegeneration is a complex and multifactorial process presenting one of the major issues of fundamental science and clinical medicine due to its high prevalence, multiple nosological entities, and variations in pathogenesis. Translational research contributes to the study of neurodegenerative diseases, with modeling of such pathologies being an important part of this research. Behavioral testing in various animal models of neurodegenerative diseases allows to assess the model validity and reliability, as well as to investigate the potential efficacy of pharmacotherapy and other management approaches. In this overview we present test batteries that evaluate behavior, cognitive performance, and emotional states in animals with experimentally induced neurodegeneration.

About the authors

Yulia A. Panina

Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University

Author for correspondence.
Email: yulia.panina@list.ru
ORCID iD: 0000-0002-8675-3489

Cand. Sci. (Med.), Associate Professor, Department of Biological Chemistry with Courses in Medical, Pharmaceutical and Toxicological Chemistry; Researcher, Research Institute of Molecular Medicine and Pathobiochemistry

Russian Federation, Krasnoyarsk

Olga L. Lopatina

Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University

Email: ol.lopatina@gmail.com
ORCID iD: 0000-0002-7884-2721

D. Sci. (Biol.), Associate Professor; Professor, Department of Biological Chemistry with Courses in Medical, Pharmaceutical and Toxicological Chemistry, Head of Social Neuroscience Laboratory

Russian Federation, Krasnoyarsk

Angelina I. Mosyagina

Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University

Email: angelina.mosiagina@gmail.com
ORCID iD: 0000-0002-7344-7925

Junior Researcher, Research Institute of Molecular Medicine and Pathobiochemistry

Russian Federation, Krasnoyarsk

Yulia K. Komleva

Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University

Email: yuliakomleva@mail.ru
ORCID iD: 0000-0001-5742-8356

D. Sci. (Med.), Associate Professor; Professor, Department of Biological Chemistry with Courses in Medical, Pharmaceutical and Toxicological Chemistry

Russian Federation, Krasnoyarsk

Andrey V. Morgun

Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University

Email: 441682@mail.ru
ORCID iD: 0000-0002-9644-5500

D. Sci. (Med.), Head, Department of Outpatient Pediatrics and Propaedeutics of Childhood Diseases with a PE-Course

Russian Federation, Krasnoyarsk

Yana V. Gorina

Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University

Email: yana_20@bk.ru
ORCID iD: 0000-0002-3341-1557

D. Sci. (Biol.), Associate Professor; Associate Professor, Department of Biological Chemistry with Courses in Medical, Pharmaceutical and Toxicological Chemistry, Senior Researcher, Social Neuroscience Laboratory 

Russian Federation, Krasnoyarsk

Elena D. Hilazheva

Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University

Email: elena.hilazheva@mail.ru
ORCID iD: 0000-0002-9718-1260

Senior Lecturer, Department of Biological Chemistry with Courses in Medical, Pharmaceutical and Toxicological Chemistry; Researcher, Research Institute of Molecular Medicine and Pathobiochemistry

Russian Federation, Krasnoyarsk

References

  1. Roy D.S., Arons A., Mitchell T.I.et al. Memory retrieval by activating engram cells in mouse models of early Alzheimer’s disease. Nature. 2016;531(7595):508–512. doi: 10.1038/nature17172
  2. Urbach Y.K., Bode F.J., Nguyen H.P. et al. Neurobehavioral tests in rat models of degenerative brain diseases. Methods Mol. Biol. 2010;597:333–356. doi: 10.1007/978-1-60327-389-3_24
  3. van der Staay F.J., Arndt S.S., Nordquist R.E. Evaluation of animal models of neurobehavioral disorders. Behav. Brain Funct. 2009;5:11. doi: 10.1186/1744-9081-5-11
  4. Doyle A., McGarry M.P., Lee N.A., Lee J.J. The construction of transgenic and gene knockout/knockin mouse models of human disease. Transgenic Res. 2012;21(2):327–349. doi: 10.1007/s11248-011-9537-3
  5. Vandamme T.F. Rodent models for human diseases. Eur. J. Pharmacol. 2015;759:84–89. doi: 10.1016/j.ejphar.2015.03.046
  6. Dutta S., Sengupta P. Men and mice: relating their ages. Life Sci. 2016;152:244–248. doi: 10.1016/j.lfs.2015.10.025
  7. Groisberg R., Maitra A., Subbiah V. Of mice and men: lost in translation. Ann. Oncol. 2019;30(4):499–500. doi: 10.1093/annonc/mdz041
  8. Ellenbroek B., Youn J. Rodent models in neuroscience research: is it a rat race? DMM Dis. Model Mech. 2016;9(10):1079–1087. doi: 10.1242/dmm.026120
  9. Brown R.E. Behavioural phenotyping of transgenic mice. Can. J. Exp. Psychol. 2007;61(4):328–344. doi: 10.1037/cjep2007033
  10. Adam Y., Kim J.J., Lou S. et al. Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics. Nature. 2019; 569(7756):413–417. doi: 10.1038/s41586-019-1166-7
  11. Yamada T., Yang Y., Valnegri P. et al. Sensory experience remodels genome architecture in neural circuit to drive motor learning. Nature. 2019:569(7758):708–713. doi: 10.1038/s41586-019-1190-7
  12. Boguski M.S. The mouse that roared. Nature. 2002;420(6915):515–516. doi: 10.1038/420515a
  13. Ukai H., Sumiyama K., Ueda H.R. Next-generation human genetics for organism-level systems biology. Curr. Opin. Biotechnol. 2019;58:137–145. doi: 10.1016/j.copbio.2019.03.003
  14. Котеров А.Н., Ушенкова Л.Н., Зубенкова Э.С. и др. Соотношение возрастов основных лабораторных животных (мышей, крыс, хомячков и собак) и человека: актуальность для проблемы возрастной радиочувствительности и анализ опубликованных данных. Медицинская радиология и радиационная безопасность. 2018;63(1):5–27. Koterov A.N., Ushenkova L.N., Zubenkova E.S. et al. The relationship between the age of the based laboratory animals (mice, rats, hamsters and dogs) and the age of human: actuality for the age-ralated radiosensitivity problem and the analysis of published data. Med. Radiol. Radiat. Safety. 2018;63(1):5–27. (In Russ.) doi: 10.12737/article_5a82e4a3908213.56647014
  15. Miller R.A., Harrison D.E., Astle C.M. et al. Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2011;66(2):191–201. doi: 10.1093/gerona/glq178
  16. Yuan R., Peters L.L., Paigen B. Mice as a mammalian model for research on the genetics of aging. ILAR J. 2011;52(1):4–15. doi: 10.1093/ilar.52.1.4
  17. Seifert B., Eckenstaler R., Ronicke R. et al. Amyloid-beta induced changes in vesicular transport of BDNF in hippocampal neurons. Neural Plast. 2016;2016:4145708. doi: 10.1155/2016/4145708
  18. Spangenberg E.E., Lee R.J., Najafi A.R. et al. Eliminating microglia in Alzheimer’s mice prevents neuronal loss without modulating amyloid-β pathology. Brain. 2016;139(4):1265–1281. doi: 10.1093/brain/aww016
  19. Woodling N.S., Colas D., Wang Q. et al. Cyclooxygenase inhibition targets neurons to prevent early behavioural decline in Alzheimer’s disease model mice. Brain. 2016;139(7):2063–2081. doi: 10.1093/brain/aww117
  20. Gasparotto J., Ribeiro C.T., Bortolin R.C. et al. Targeted inhibition of RAGE in substantia nigra of rats blocks 6-OHDA-induced dopaminergic denervation. Sci. Rep. 2017;7(1):8795. doi: 10.1038/s41598-017-09257-3
  21. Lu X., Kim-Han J.S., Harmon S. et al. The Parkinsonian mimetic, 6-OHDA, impairs axonal transport in dopaminergic axons. Mol. Neurodegener. 2014;9(1):17. doi: 10.1186/1750-1326-9-17
  22. Innos J., Hickey M.A. Using rotenone to model Parkinson’s disease in mice: a review of the role of pharmacokinetics. 2021;4(5):1223–1239. doi: 10.1021/acs.chemrestox.0c00522
  23. Bentea E., De Pauw L., Verbruggen L. et al. Aged xCT-deficient mice are less susceptible for lactacystin-, but not 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-, induced degeneration of the nigrostriatal pathway. Front. Cell Neurosci. 2021;15: 796635. doi: 10.3389/fncel.2021.796635
  24. Goedert M. Filamentous nerve cell inclusions in neurodegenerative diseases: Tauopathies and α-synucleinopathies. Philos. Trans. R. Soc. B Biol. Sci. 1999;354(1386):1101–1118. doi: 10.1098/rstb.1999.0466
  25. Pir G.J., Choudhary B., Kaniyappan S. et al. Suppressing tau aggregation and toxicity by an anti-aggregant tau fragment. Mol. Neurobiol. 2019;56(5):3751–3767. doi: 10.1007/s12035-018-1326-z
  26. Engstrom A.K., Snyder J.M., Maeda N., Xia Z. Gene-environment interaction between lead and Apolipoprotein E4 causes cognitive behavior deficits in mice. Mol. Neurodegener. 2017;12(1):14. doi: 10.1186/s13024-017-0155-2
  27. Leung L., Andrews-Zwilling Y., Yoon S.Y. et al. Apolipoprotein E4 causes age- and sex-dependent impairments of hilar GABAergic interneurons and learning and memory deficits in mice. PLoS One. 2012;7(12):e53569. doi: 10.1371/journal.pone.0053569
  28. Cai Y., An S.S.A., Kim S. Mutations in presenilin 2 and its implications in Alzheimer’s disease and other dementia-associated disorders. Clin. Interv. Aging. 2015;10:1163-1172. doi: 10.2147/CIA.S85808
  29. Xia D., Watanabe H., Wu B. et al. Presenilin-1 knockin mice reveal loss-of-function mechanism for familial Alzheimer’s disease. Neuron. 2015;85(5):967–981. doi: 10.1016/j.neuron.2015.02.010
  30. Unger M.S., Schernthaner P., Marschallinger J. et al. Microglia prevent peripheral immune cell invasion and promote an anti-inflammatory environment in the brain of APP-PS1 transgenic mice. J. Neuroinflammation. 2018;15(1):274. doi: 10.1186/s12974-018-1304-4
  31. Balakrishnan K., Rijal Upadhaya A., Steinmetz J. et al. Impact of amyloid β aggregate maturation on antibody treatment in APP23 mice. Acta Neuropathol. Commun. 2015;3:41. doi: 10.1186/s40478-015-0217-z
  32. De Retana S.F., Marazuela P., Solé M. et al. Peripheral administration of human recombinant ApoJ/clusterin modulates brain beta-amyloid levels in APP23 mice. Alzheimer’s Res. Ther. 2019;11(1):42. doi: 10.1186/s13195-019-0498-8
  33. Bouter Y., Kacprowski T., Weissmann R. et al. Deciphering the molecular profile of plaques, memory decline and neuron loss in two mouse models for Alzheimer’s disease by deep sequencing. Front. Aging Neurosci. 2014;6:75. doi: 10.3389/fnagi.2014.00075
  34. Colby-Milley J., Cavanagh C., Jego S. et al. Sleep-wake cycle dysfunction in the TgCRND8 mouse model of Alzheimer’s disease: from early to advanced pathological stages. PLoS One. 2015;10(6):e0130177. doi: 10.1371/journal.pone.0130177
  35. Kalia L.V., Kalia S.K., McLean P.J. et al. α-Synuclein oligomers and clinical implications for Parkinson disease. Ann. Neurol. 2013;73(2):155–169. doi: 10.1002/ana.23746
  36. Ferrante R.J. Mouse models of Huntington’s disease and methodological considerations for therapeutic trials. Biochim. Biophys. Acta. 2009;1792(6):506–520. doi: 10.1016/j.bbadis.2009.04.001
  37. Pouladi M.A., Morton A.J., Hayden M.R. Choosing an animal model for the study of Huntington’s disease. Nat. Rev. Neurosci. 2013;14(10):708–721. doi: 10.1038/nrn3570
  38. Saxena M. Animal models for Huntington’s and Parkinson’s diseases. Mater. Methods. 2013;3:205. doi: 10.13070/mm.en.3.205
  39. Худякова Н.А., Баженова Т.В. Поведенческая активность линейных и нелинейных мышей разных цветовых вариаций в тесте «Открытое поле». Вестник Удмуртского университета. Серия «Биология. Науки о Земле». 2012;2:89–93. Khudyakova N.A., Bazhenova T.B. Behavioral activity of linear and nonlinear mice of different color variations in the test “open field”. Vestnik Udmurtskogo universiteta. Seriya «Biologiya. Nauki o Zemle». 2012;2:89–92. (In Russ.)
  40. Albanese S., Greco A., Auletta L., Mancini M. Mouse models of neurodegenerative disease: preclinical imaging and neurovascular component. Brain Imaging Behav. 2018;12(4):1160–1196. doi: 10.1007/s11682-017-9770-3
  41. Blesa J., Przedborski S. Parkinson’s disease: animal models and dopaminergic cell vulnerability. Front. Neuroanat. 2014;8:155. doi: 10.3389/fnana.2014.00155
  42. Blesa J., TrigoDamas I., Quiroga‐Varela A., Lopez‐Gonzalez del Rey N. Animal models of Parkinson’s Disease. In: Dorszewska J., Kozubski W. (eds.) Challenges in Parkinson's disease. London; 2016.
  43. Perusini J.N., Cajigas S.A., Cohensedgh O. et al. Optogenetic stimulation of dentate gyrus engrams restores memory in Alzheimer’s disease mice. Hippocampus. 2017;27(10):1110–1122. doi: 10.1002/hipo.22756
  44. Kitamura T., Saitoh Y., Takashima N. et al. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell. 2009;139(4):814–827. doi: 10.1016/j.cell.2009.10.020
  45. Lisman J., Buzsáki G., Eichenbaum H. et al. Viewpoints: how the hippocampus contributes to memory, navigation and cognition. Nat. Neurosci. 2017;20(11):1434–1447. doi: 10.1038/nn.4661
  46. Cembrowski M.S., Phillips M.G., DiLisio S.F. et al. Dissociable Structural and Functional Hippocampal Outputs via Distinct Subiculum Cell Classes. Cell. 2018;173(5):280–1292.e18. doi: 10.1016/j.cell.2018.03.031
  47. Wang S.H., Morris R.G.M. Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu. Rev. Psychol. 2010;61:49–79:C1-4. doi: 10.1146/annurev.psych.093008.100523
  48. Tonegawa S., Liu X., Ramirez S., Redondo R. Memory engram cells have come of age. Neuron. 2015;87(5):918–931. doi: 10.1016/j.neuron.2015.08.002
  49. Squire L.R. Memory systems of the brain: a brief history and current perspective. Neurobiol. Learn Mem. 2004;82(3):171–177. doi: 10.1016/j.nlm.2004.06.005
  50. Knierim J.J. The hippocampus. Curr. Biol. 2015;25(23):R1116–R1121. doi: 10.1016/j.cub.2015.10.049
  51. Guitar N.A., Roberts W.A. The interaction between working and reference spatial memories in rats on a radial maze. Behav. Processes. 2015;112:100–107. doi: 10.1016/j.beproc.2014.10.007
  52. Roy D.S., Kitamura T., Okuyama T. et al. Distinct neural circuits for the formation and retrieval of episodic memories. Cell. 2017;170(5):1000–1012.e19. doi: 10.1016/j.cell.2017.07.013
  53. Çevik M.Ö. Habituation, sensitization, and Pavlovian conditioning. Front. Integr. Neurosci. 2014;8:13. doi: 10.3389/fnint.2014.00013
  54. Cartoni E., Balleine B., Baldassarre G. Appetitive Pavlovian-instrumental transfer: a review. Neurosci. Biobehav. Rev. 2016;71:829–848. doi: 10.1016/j.neubiorev.2016.09.020
  55. Ullman M.T., Pullman M.Y. A compensatory role for declarative memory in neurodevelopmental disorders. Neurosci. Biobehav. Rev. 2015;51:205–222. doi: 10.1016/j.neubiorev.2015.01.008
  56. Tonegawa S., McHugh T.J. The ins and outs of hippocampal circuits. Neuron. 2008;57(2):175–177. doi: 10.1016/j.neuron.2008.01.005
  57. Горина Я.В., Иптышев А.М., Лопатина О.Л. и др. Анализ пространственной памяти у ЖИРЗ-нокаутных животных. Сибирское медицинское обозрение. 2017;(6):50–56. Gorina Y.V., Iptyshev A.M. Lopatina O.L. et al. The analysys of spatial memory in NLRP3-knockout animals. Sib. Med. Rev. 2017;(6):50–56. (In Russ.) DOI: 10.20ЗЗЗ/25001З6-2017-6-50-56
  58. Denny C.A., Kheirbek M.A., Alba E.L. et al. Hippocampal memory traces are differentially modulated by experience, time, and adult neurogenesis. Neuron. 2014; 83(1):189–201. doi: 10.1016/j.neuron.2014.05.018
  59. Poppenk J., Evensmoen H.R., Moscovitch M., Nadel L. Long-axis specialization of the human hippocampus. Trends Cogn. Sci. 2013;17(5):230–240. doi: 10.1016/j.tics.2013.03.005
  60. Salmina A.B., Komleva Y.K., Lopatina O.L., Birbrair A. Pericytes in Alzheimer’s disease: novel clues to cerebral amyloid angiopathy pathogenesis. Adv. Exp. Med. Biol. 2019;1147:147–166. doi: 10.1007/978-3-030-16908-4_7
  61. da Silva R.C.R., de Carvalho R.L.S., Dourado M.C.N. Deficits in emotion processing in Alzheimer’s disease: asystematic review. Dement. Neuropsychol. 2021;15(3):314–330. doi: 10.1590/1980-57642021dn15-030003
  62. Teegarden S. Behavioral phenotyping in rats and mice. Mater. Methods. 2012;2:122. doi: 10.13070/mm.en.2.122
  63. Kasai S., Yoshihara T., Lopatina O. et al. Selegiline ameliorates depression-like behavior in mice lacking the CD157/BST1 gene, a risk factor for Parkinson’s disease. Front. Behav. Neurosci. 2017;11:75. doi: 10.3389/fnbeh.2017.00075
  64. Porsolt R.D., Le Pichon M., Jalfre M. Depression: A new animal model sensitive to antidepressant treatments. Nature. 1977;266(5604):730–732. doi: 10.1038/266730a0
  65. Cryan J.F., Mombereau C. In search of a depressed mouse: utility of models for studying depression-related behavior in genetically modified mice. Mol. Psychiatry. 2004;9(4):326–357. doi: 10.1038/sj.mp.4001457
  66. Slattery D.A., Cryan J.F. Using the rat forced swim test to assess antidepressant-like activity in rodents. Nat. Protoc. 2012;7(6):1009–1014. doi: 10.1038/nprot.2012.044
  67. Castagné V., Porsolt R.D., Moser P. Early behavioral screening for antidepressants and anxiolytics. Drug Dev Res. 2006;67:729–742. doi: 10.1002/ddr.20145.
  68. Cryan J.F., Holmes A. Model organisms: the ascent of mouse: advances in modelling human depression and anxiety. Nat. Rev. Drug Discov. 2005;4(9):775–790. doi: 10.1038/nrd1825
  69. Cryan J.F., Mombereau C., Vassout A. The tail suspension test as a model for assessing antidepressant activity: Review of pharmacological and genetic studies in mice. Neurosci. Biobehav. Rev. 2005;29(4–5):571–625. doi: 10.1016/j.neubiorev.2005.03.009
  70. Steru L., Chermat R., Thierry B., Simon P. The tail suspension test: A new method for screening antidepressants in mice. Psychopharmacology (Berl.). 1985;85(3):367–70. doi: 10.1007/BF00428203
  71. Ripoll N., David D.J.P., Dailly E. et al. Antidepressant-like effects in various mice strains in the tail suspension test. Behav. Brain Res. 2003;143(2):193–200. doi: 10.1016/s0166-4328(03)00034-2
  72. Schechter M.D., Calcagnetti D.J. Trends in place preference conditioning with a cross-indexed bibliography; 1957–1991. Neurosci. Biobehav. Rev. 1993;17(1):21–41. doi: 10.1016/s0149-7634(05)80228-3
  73. Deacon R.M.J. Measuring motor coordination in mice. J. Vis. Exp. 2013;(75):e2609. doi: 10.3791/2609
  74. Meredith G.E., Kang U.J. Behavioral models of Parkinson’s disease in rodents: a new look at an old problem. Mov. Disord. 2006;21(10):1595–1606. doi: 10.1002/mds.21010
  75. Glajch K.E., Fleming S.M., Surmeier D.J., Osten P. Sensorimotor assessment of the unilateral 6-hydroxydopamine mouse model of Parkinson’s disease. Behav. Brain Res. 2012;230(2):309–316. doi: 10.1016/j.bbr.2011.12.007
  76. Roy S. Synuclein and dopamine: the Bonnie and Clyde of Parkinson’s disease. Nat. Neurosci. 2017;20(11):1514–1515. doi: 10.1038/nn.4660
  77. Carter R.J., Lione L.A., Humby T. et al. Characterization of progressive motor deficits in mice transgenic for the human Huntington’s disease mutation. J. Neurosci. 1999;19(8):3248–3257. doi: 10.1523/JNEUROSCI.19-08-03248.1999
  78. Lopatina O., Yoshihara T., Nishimura T. et al. Anxiety- and depression-like behavior in mice lacking the CD157/BST1 gene, a risk factor for Parkinson’s disease. Front. Behav. Neurosci. 2014;8:133. doi: 10.3389/fnbeh.2014.00133
  79. Fleming S.M., Ekhator O.R., Ghisays V. Assessment of sensorimotor function in mouse models of Parkinson’s disease. J. Vis. Exp. 2013;(76):50303. doi: 10.3791/50303
  80. Pacala J.T., Yueh B. Hearing deficits in the older patient: “I didn’t notice anything.” JAMA. 2012;307(11):1185–1194. doi: 10.1001/jama.2012.305
  81. Rönnberg J., Danielsson H., Rudner M. et al. Hearing loss is negatively related to episodic and semantic long-term memory but not to short-term memory. J. Speech, Lang Hear Res. 2011;54(2):705–726. doi: 10.1044/1092-4388(2010/09-0088)
  82. Fritze T., Teipel S., Óvári A. et al. Hearing impairment affects dementia incidence. An analysis based on longitudinal health claims data in Germany. PLoS One. 2016;11(7):e0156876. doi: 10.1371/journal.pone.0156876
  83. Hung S.C., Liao K.F., Muo C.H. et al. Hearing loss is associated with risk of Alzheimer’s disease: A case-control study in older people. J. Epidemiol. 2015;25(8):517–521. doi: 10.2188/jea.JE20140147
  84. O’Leary T.P., Shin S., Fertan E. et al. Reduced acoustic startle response and peripheral hearing loss in the 5xFAD mouse model of Alzheimer’s disease. Genes, Brain Behav. 2017;16(5):554–563. doi: 10.1111/gbb.12370
  85. Ison J.R., Hoffman H.S. Reflex modification in the domain of startle: II. The anomalous history of a robust and ubiquitous phenomenon. Psychol. Bull. 1983;94(1):3–17
  86. Swerdlow N.R., Braff D.L., Geyer MA. Animal models of deficient sensorimotor gating: what we know, what we think we know, and what we hope to know soon. Behav. Pharmacol. 2000;11(3-4):185–204. doi: 10.1097/00008877-200006000-00002
  87. File S.E. Factors controlling measures of anxiety and responses to novelty in the mouse. Behav. Brain Res. 2001;125(1–2):151–157. doi: 10.1016/s0166-4328(01)00292-3
  88. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 2003;463(1–3):3–33. doi: 10.1016/s0014-2999(03)01272-x
  89. Bains R.S., Cater H.L., Sillito R.R. et al. Analysis of individual mouse activity in group housed animals of different inbred strains using a novel automated home cage analysis system. Front. Behav. Neurosci. 2016;10:106. doi: 10.3389/fnbeh.2016.00106
  90. Bains R.S., Wells S., Sillito R.R. et al. Assessing mouse behaviour throughout the light/dark cycle using automated in-cage analysis tools. J. Neurosci. Methods. 2018;300:37–47. doi: 10.1016/j.jneumeth.2017.04.014
  91. Salmina A.B., Lopatina O.L., Kuvacheva N.V., Higashida H. Integrative neurochemistry and neurobiology of social recognition and behavior analyzed with respect to CD38-dependent brain oxytocin secretion. Curr. Top. Med. Chem. 2015;13(23):2965–2977. doi: 10.2174/15680266113136660211
  92. Blanco-Gandía M.C., Mateos-García A., García-Pardo M.P. et al. Effect of drugs of abuse on social behaviour: a review of animal models. Behav. Pharmacol. 2015;26(6):541–570. doi: 10.1097/FBP.0000000000000162
  93. Kaidanovich-Beilin O., Lipina T., Vukobradovic I. et al. Assessment of social interaction behaviors. J. Vis. Exp. 2011;(48):2473. doi: 10.3791/2473
  94. Ichinose W., Cherepanov S.M., Shabalova A.A. et al. Development of a highly potent analogue and a long-acting analogue of oxytocin for the treatment of social impairment-like behaviors. J. Med. Chem. 2019;62(7):3297–3310. doi: 10.1021/acs.jmedchem.8b01691
  95. Jacobs S., Huang F., Tsien J., Wei W. Social recognition memory test in rodents. Bio. Protocol. 2016;6(9):1–12. doi: 10.21769/BioProtoc.1804
  96. Kercmar J., Büdefeld T., Grgurevic N. et al. Adolescent social isolation changes social recognition in adult mice. Behav. Brain Res. 2011;216(2):647–651. doi: 10.1016/j.bbr.2010.09.007
  97. Jin D., Liu H.X., Hirai H. et al. CD38 is critical for social behaviour by regulating oxytocin secretion. Nature. 2007;446(7131):41–45. doi: 10.1038/nature05526
  98. Liu H.X., Lopatina O.L., Higashida C. et al. Displays of paternal mouse pup retrieval following communicative interaction with maternal mates. Nat. Commun. 2013;4:1346. doi: 10.1038/ncomms2336

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. A diagram of neurobehavioral testing in experimental mouse models of neurodegeneration.

Download (246KB)
Indexing metadata
3. Fig. 2. The fear conditioning test to reveal the interaction between the auditory cortex, the hippocampus, and the amigdala nuclei in formation of the emotional memory.

Download (105KB)
Indexing metadata

Copyright (c) 2023 Panina Y.A., Lopatina O.L., Mosyagina A.I., Komleva Y.K., Morgun A.V., Gorina Y.V., Hilazheva E.D.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies