Year 2022,
, 938 - 945, 29.09.2022
Bahar Dalkiran
,
Burcu Açıkgöz
,
Ayfer Dayı
References
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- 2. Hall JE, Guyton AC. Guyton and Hall textbook of medical physiology. 13 th edition. Philadelphia, Saunders Elsevier, 2016.
- 3. Gasparini L, Racchi M, Binetti G, Trabucchi M, Solerte SB, Alkon D, et al.Peripheralmarkers in testing pathophysiological hypotheses and diagnosingAlzheimer's disease. FASEB J. 1998 Jan;12(1):17-34.
- 4. Waxman A, Chugani H, Seibyl J. Medical imaging in neurological disorders.J Am Pharm Assoc (Wash). 2002 Sep-Oct;42(5 Suppl 1):S48-9.
- 5. Phelps EA, LeDoux JE. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron. 2005;48(2):175-187. doi:10.1016/j.neuron.2005.09.025
6. Morgane PJ, Galler JR, Mokler DJ. A review of systems and networks of the limbic forebrain/limbic midbrain. Prog Neurobiol. 2005 Feb;75(2):143-60.
- 7. Mineur YS, Obayemi A, Wigestrand MB, Fote GM, Calarco AC, Li AM, et al. Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior. Proc Natl Acad Sci U S A. 2013;110(9):3573-3578. doi:10.1073/pnas.1219731110
- 8. Morris R. Developments of a water-maze procedure for studying spatial-learning in the rat. J. Neurosci. Methods. (1984) 11, 47–60.
- 9. Shultz SR, McDonald SJ, Corrigan F, Semple BD, Salberg S, Zamani A, et al. Clinical Relevance of Behavior Testing in Animal Models of Traumatic Brain Injury. J Neurotrauma. 2020;37(22):2381-2400. doi:10.1089/neu.2018.6149
- 10. Quillfeldt, J. Behavioral Methods to Study Learning and Memory in Rats. (2015) 10.1007/978-3-319-11578-8_17.
- 11. Buresová O, Bures J, Oitzl MS, Zahálka A. Radial maze in the water tank: an aversively motivated spatial working memory task. Physiol Behav. 1985;34(6):1003-1005. doi:10.1016/0031-9384(85)90028-9
- 12. Liu L, Ikonen S, Heikkinen T, Heikkilä M, Puoliväli J, van Groen T, et al. Effects of fimbria-fornix lesion and amyloid pathology on spatial learning and memory in transgenic APP+PS1 mice. Behav Brain Res. 2002;134(1-2):433-445. doi:10.1016/S0166-4328(02)00058-X
- 13. Tanila H. Testing cognitive functions in rodent disease models: Present pitfalls and future perspectives. Behav Brain Res. 2018;352(May 2017):23-27. doi:10.1016/j.bbr.2017.05.040
- 14. Vorhees CV, Williams MT. Assessing spatial learning and memory in rodents. ILAR J. 2014;55(2):310-332. doi:10.1093/ilar/ilu013
- 15. Moser MB, Moser EI, Forrest E, Andersen P, Morris RG. Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci U S A. 1995;92(21):9697-9701. doi:10.1073/pnas.92.21.9697
- 16. Wu C, Yang L, Li Y, Dong Y, Yang B, Tucker LD, et al. Effects of Exercise Training on Anxious-Depressive-like Behavior in Alzheimer Rat. Med Sci Sports Exerc. 2020;52(7):1456-1469. doi:10.1249/MSS.0000000000002294
- 17. Mc Gaugh JL. Time-dependent processes in memory storage. Science (80-). 1966;153(3742):1351-1358. doi:10.1126/science.153.3742.1351
- 18. Deacon RMJ, Bannerman DM, Kirby BP, Croucher A, Rawlins JNP. Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behav Brain Res. 2002;133(1):57-68. doi:10.1016/S0166-4328(01)00451-X
- 19. Cordner ZA, Tamashiro KLK. Effects of high-fat diet exposure on learning & memory. Physiol Behav. 2015;152:363-371. doi:10.1016/j.physbeh.2015.06.008
- 20. Sohn E, Lim HS, Kim YJ, Kim BY, Jeong SJ. Annona atemoya Leaf Extract Improves Scopolamine-Induced Memory Impairment by Preventing Hippocampal Cholinergic Dysfunction and Neuronal Cell Death. Int J Mol Sci. 2019;20(14). doi:10.3390/ijms20143538
- 21. Matsumoto J, Uehara T, Urakawa S, Takamura Y, Sumiyoshi Y, Suzuki M et al. 3D video analysis of the novel object recognition test in rats. Behav Brain Res. 2014;272:16-24. doi:10.1016/j.bbr.2014.06.047
- 22. Berlyne DE. Novelty and curiosity as determinants of exploratory behavior. BrJ Psychol 1950;41:68–80
- 23. Ennaceur A, Delacour JA. New one-trial test for neurobiological studies ofmemory in rats. 1: Behavioral data. Behav Brain Res 1988;31(1):47–59
- 24. Bevins RA, Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study ‘recognition memory’. Nat Protoc2006;1(3):1306–11
- 25. Antunes M, Biala G. The novel object recognition memory: Neurobiology, test procedure, and its modifications. Cogn Process. 2012;13(2):93-110. doi:10.1007/s10339-011-0430-z
- 26. Barnes, CA. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol. 1979 Feb;93(1):74-104.
- 27. Gawel K, Gibula E, Marszalek-Grabska M, Filarowska J, Kotlinska JH. Assessment of spatial learning and memory in the Barnes maze task in rodents—methodological consideration. Naunyn Schmiedebergs Arch Pharmacol. 2019;392(1):1-18. doi:10.1007/s00210-018-1589-y
- 28. Kennard J, Woodruff-Pak D. Age Sensitivity of Behavioral Tests and Brain Substrates of Normal Aging in Mice. Front Aging Neurosci. 2011;3:9. doi:10.3389/fnagi.2011.00009
- 29. Negrón-Oyarzo I, Neira D, Espinosa N, Fuentealba P, Aboitiz F. Prenatal stress produces persistence of remote memory and disrupts functional connectivity in the hippocampal-prefrontal cortex axis. Cereb Cortex. 2015;25(9):3132-3143. doi:10.1093/cercor/bhu108
- 30. Rodriguez GA, Burns MP, Weeber EJ, Rebeck GW. Young APOE4 targeted replacement mice exhibit poor spatial learning and memory, with reduced dendritic spine density in the medial entorhinal cortex. doi:10.1101/lm.030031.112
- 31. Crews FT, Boettiger CA. Impulsivity, frontal lobes and risk for addiction. Pharmacol Biochem Behav. 2009;93(3):237-247. doi:10.1016/j.pbb.2009.04.018
- 32. Chawla A, Cordner ZA, Boersma G, Moran TH. Cognitive impairment and gene expression alterations in a rodent model of binge eating disorder. Physiol Behav. 2017;180:78-90. doi:10.1016/j.physbeh.2017.08.004
- 33. Stewart S, Cacucci F, Lever C. ‘Which Memory Task for My Mouse? A Systematic Review of Spatial Memory Performance in the Tg2576 Alzheimer’s Mouse Model’. 1 Jan. 2011: 105 – 1
- 34. Olton DS, Samuelson RJ. Remembrance of places passed: Spatial memory in rats. J Exp Psychol Anim Behav Process. 1976;2(2):97-116. doi:10.1037/0097-7403.2.2.97
- 35. Stafstrom CE. Behavioral and Cognitive Testing Procedures in Animal Models of Epilepsy. Models of Seizures and Epilepsy. 613-628. 10.1016/B978-012088554-1/50051-7.
- 36. Soblosky JS, Tabor SL, Matthews MA, Davidson JF, Chorney DA, Carey ME. Reference memory and allocentric spatial localization deficits after unilateral cortical brain injury in the rat. Behav Brain Res. 1996;80(1-2):185-194. doi:10.1016/0166-4328(96)00034-4
- 37. Mei J, Kohler J, Winter Y, Spies C, Endres M, Banneke S, et al. Automated radial 8-arm maze: A voluntary and stress-free behavior test to assess spatial learning and memory in mice. Behav Brain Res. 2020;381. doi:10.1016/j.bbr.2019.112352.
Behavioral Tests Used in the Evaluation of Learning and Memory in Experimental Animals
Year 2022,
, 938 - 945, 29.09.2022
Bahar Dalkiran
,
Burcu Açıkgöz
,
Ayfer Dayı
Abstract
Learning and memory regulate the necessary mental processes such as evaluating stimuli from the environment and developing appropriate behaviors. People consciously or unconsciously resort to memory functions in every process they perform. Experiences that emerge through interaction with the environment lead to changes and shaping of behaviors. Thus, learning of different behavioral phenomena takes place. Memory ensures that this learned behavioral information is stored and used when necessary. The central nervous system is capable of storing and processing information in mammals.
Research on learning and memory in humans is limited due to ethical rules. Therefore, different experimental tests evaluating learning and memory states in rodents have been designed to find effective treatment strategies. The aim of this review is to provide information about the most commonly used learning and memory tests in experimental animals.
References
- 1. Pittenger C, Kandel ER. In search of general mechanisms for long-lasting plasticity: Aplysia and the hippocampus. Philos Trans R Soc Lond B Biol Sci. 2003 Apr 29;358(1432):757-63.
- 2. Hall JE, Guyton AC. Guyton and Hall textbook of medical physiology. 13 th edition. Philadelphia, Saunders Elsevier, 2016.
- 3. Gasparini L, Racchi M, Binetti G, Trabucchi M, Solerte SB, Alkon D, et al.Peripheralmarkers in testing pathophysiological hypotheses and diagnosingAlzheimer's disease. FASEB J. 1998 Jan;12(1):17-34.
- 4. Waxman A, Chugani H, Seibyl J. Medical imaging in neurological disorders.J Am Pharm Assoc (Wash). 2002 Sep-Oct;42(5 Suppl 1):S48-9.
- 5. Phelps EA, LeDoux JE. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron. 2005;48(2):175-187. doi:10.1016/j.neuron.2005.09.025
6. Morgane PJ, Galler JR, Mokler DJ. A review of systems and networks of the limbic forebrain/limbic midbrain. Prog Neurobiol. 2005 Feb;75(2):143-60.
- 7. Mineur YS, Obayemi A, Wigestrand MB, Fote GM, Calarco AC, Li AM, et al. Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior. Proc Natl Acad Sci U S A. 2013;110(9):3573-3578. doi:10.1073/pnas.1219731110
- 8. Morris R. Developments of a water-maze procedure for studying spatial-learning in the rat. J. Neurosci. Methods. (1984) 11, 47–60.
- 9. Shultz SR, McDonald SJ, Corrigan F, Semple BD, Salberg S, Zamani A, et al. Clinical Relevance of Behavior Testing in Animal Models of Traumatic Brain Injury. J Neurotrauma. 2020;37(22):2381-2400. doi:10.1089/neu.2018.6149
- 10. Quillfeldt, J. Behavioral Methods to Study Learning and Memory in Rats. (2015) 10.1007/978-3-319-11578-8_17.
- 11. Buresová O, Bures J, Oitzl MS, Zahálka A. Radial maze in the water tank: an aversively motivated spatial working memory task. Physiol Behav. 1985;34(6):1003-1005. doi:10.1016/0031-9384(85)90028-9
- 12. Liu L, Ikonen S, Heikkinen T, Heikkilä M, Puoliväli J, van Groen T, et al. Effects of fimbria-fornix lesion and amyloid pathology on spatial learning and memory in transgenic APP+PS1 mice. Behav Brain Res. 2002;134(1-2):433-445. doi:10.1016/S0166-4328(02)00058-X
- 13. Tanila H. Testing cognitive functions in rodent disease models: Present pitfalls and future perspectives. Behav Brain Res. 2018;352(May 2017):23-27. doi:10.1016/j.bbr.2017.05.040
- 14. Vorhees CV, Williams MT. Assessing spatial learning and memory in rodents. ILAR J. 2014;55(2):310-332. doi:10.1093/ilar/ilu013
- 15. Moser MB, Moser EI, Forrest E, Andersen P, Morris RG. Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci U S A. 1995;92(21):9697-9701. doi:10.1073/pnas.92.21.9697
- 16. Wu C, Yang L, Li Y, Dong Y, Yang B, Tucker LD, et al. Effects of Exercise Training on Anxious-Depressive-like Behavior in Alzheimer Rat. Med Sci Sports Exerc. 2020;52(7):1456-1469. doi:10.1249/MSS.0000000000002294
- 17. Mc Gaugh JL. Time-dependent processes in memory storage. Science (80-). 1966;153(3742):1351-1358. doi:10.1126/science.153.3742.1351
- 18. Deacon RMJ, Bannerman DM, Kirby BP, Croucher A, Rawlins JNP. Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behav Brain Res. 2002;133(1):57-68. doi:10.1016/S0166-4328(01)00451-X
- 19. Cordner ZA, Tamashiro KLK. Effects of high-fat diet exposure on learning & memory. Physiol Behav. 2015;152:363-371. doi:10.1016/j.physbeh.2015.06.008
- 20. Sohn E, Lim HS, Kim YJ, Kim BY, Jeong SJ. Annona atemoya Leaf Extract Improves Scopolamine-Induced Memory Impairment by Preventing Hippocampal Cholinergic Dysfunction and Neuronal Cell Death. Int J Mol Sci. 2019;20(14). doi:10.3390/ijms20143538
- 21. Matsumoto J, Uehara T, Urakawa S, Takamura Y, Sumiyoshi Y, Suzuki M et al. 3D video analysis of the novel object recognition test in rats. Behav Brain Res. 2014;272:16-24. doi:10.1016/j.bbr.2014.06.047
- 22. Berlyne DE. Novelty and curiosity as determinants of exploratory behavior. BrJ Psychol 1950;41:68–80
- 23. Ennaceur A, Delacour JA. New one-trial test for neurobiological studies ofmemory in rats. 1: Behavioral data. Behav Brain Res 1988;31(1):47–59
- 24. Bevins RA, Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study ‘recognition memory’. Nat Protoc2006;1(3):1306–11
- 25. Antunes M, Biala G. The novel object recognition memory: Neurobiology, test procedure, and its modifications. Cogn Process. 2012;13(2):93-110. doi:10.1007/s10339-011-0430-z
- 26. Barnes, CA. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol. 1979 Feb;93(1):74-104.
- 27. Gawel K, Gibula E, Marszalek-Grabska M, Filarowska J, Kotlinska JH. Assessment of spatial learning and memory in the Barnes maze task in rodents—methodological consideration. Naunyn Schmiedebergs Arch Pharmacol. 2019;392(1):1-18. doi:10.1007/s00210-018-1589-y
- 28. Kennard J, Woodruff-Pak D. Age Sensitivity of Behavioral Tests and Brain Substrates of Normal Aging in Mice. Front Aging Neurosci. 2011;3:9. doi:10.3389/fnagi.2011.00009
- 29. Negrón-Oyarzo I, Neira D, Espinosa N, Fuentealba P, Aboitiz F. Prenatal stress produces persistence of remote memory and disrupts functional connectivity in the hippocampal-prefrontal cortex axis. Cereb Cortex. 2015;25(9):3132-3143. doi:10.1093/cercor/bhu108
- 30. Rodriguez GA, Burns MP, Weeber EJ, Rebeck GW. Young APOE4 targeted replacement mice exhibit poor spatial learning and memory, with reduced dendritic spine density in the medial entorhinal cortex. doi:10.1101/lm.030031.112
- 31. Crews FT, Boettiger CA. Impulsivity, frontal lobes and risk for addiction. Pharmacol Biochem Behav. 2009;93(3):237-247. doi:10.1016/j.pbb.2009.04.018
- 32. Chawla A, Cordner ZA, Boersma G, Moran TH. Cognitive impairment and gene expression alterations in a rodent model of binge eating disorder. Physiol Behav. 2017;180:78-90. doi:10.1016/j.physbeh.2017.08.004
- 33. Stewart S, Cacucci F, Lever C. ‘Which Memory Task for My Mouse? A Systematic Review of Spatial Memory Performance in the Tg2576 Alzheimer’s Mouse Model’. 1 Jan. 2011: 105 – 1
- 34. Olton DS, Samuelson RJ. Remembrance of places passed: Spatial memory in rats. J Exp Psychol Anim Behav Process. 1976;2(2):97-116. doi:10.1037/0097-7403.2.2.97
- 35. Stafstrom CE. Behavioral and Cognitive Testing Procedures in Animal Models of Epilepsy. Models of Seizures and Epilepsy. 613-628. 10.1016/B978-012088554-1/50051-7.
- 36. Soblosky JS, Tabor SL, Matthews MA, Davidson JF, Chorney DA, Carey ME. Reference memory and allocentric spatial localization deficits after unilateral cortical brain injury in the rat. Behav Brain Res. 1996;80(1-2):185-194. doi:10.1016/0166-4328(96)00034-4
- 37. Mei J, Kohler J, Winter Y, Spies C, Endres M, Banneke S, et al. Automated radial 8-arm maze: A voluntary and stress-free behavior test to assess spatial learning and memory in mice. Behav Brain Res. 2020;381. doi:10.1016/j.bbr.2019.112352.