Advertisement

Animal Cognition

, Volume 14, Issue 3, pp 325–340 | Cite as

Validation of a rodent model of episodic memory

  • Wenyi Zhou
  • Jonathon D. CrystalEmail author
Original Paper

Abstract

Episodic memory consists of representations of specific episodes that happened in the past. Modeling episodic memory in animals requires careful examination of alternative explanations of performance. Putative evidence of episodic-like memory may be based on encoding failure or expectations derived from well-learned semantic rules. In Experiment 1, rats were tested in a radial maze with study and test phases separated by a retention interval. The replenishment of chocolate (at its study-phase location) depended on two factors: time of day (morning vs. afternoon) and the presence or absence of chocolate pellets at the start of the test phase. Because replenishment could not be decoded until the test phase, rats were required to encode the study episode. Success in this task rules out encoding failure. In Experiment 2, two identical mazes in different rooms were used. Chocolate replenishment was trained in one room, and then they were asked to report about a recent event in a different room, where they had no expectation that the memory assessment would occur. Rats successfully answered the unexpected question, ruling out use of expectations derived from well-learned semantic rules. Our behavioral methods for modeling episodic memory may have broad application for assessments of genetic, neuroanatomical, neurochemical, and neurophysiological bases of both episodic memory and memory disorders such as those that occur in Alzheimer’s disease.

Keywords

Episodic memory Episodic-like memory What-where-when memory Encoding Unexpected question Rats 

Notes

Acknowledgments

This work was supported by National Institute of Mental Health Grant R01 MH080052 (to J.D.C.).

Conflict of interest

The experiments complied with the current laws of the country in which they were performed. The authors declare that they have no conflict of interest.

References

  1. Babb SJ, Crystal JD (2005) Discrimination of what, when, and where: implications for episodic-like memory in rats. Learn Motiv 36(2):177–189CrossRefGoogle Scholar
  2. Babb SJ, Crystal JD (2006a) Discrimination of what, when, and where is not based on time of day. Learn Behav 34(2):124–130PubMedCrossRefGoogle Scholar
  3. Babb SJ, Crystal JD (2006b) Episodic-like memory in the rat. Curr Biol 16(13):1317–1321PubMedCrossRefGoogle Scholar
  4. Bäckman L, Andersson JL, Nyberg L, Winblad B, Nordberg A, Almkvist O (1999) Brain regions associated with episodic retrieval in normal aging and Alzheimer’s disease. Neurology 52(9):1861–1870PubMedGoogle Scholar
  5. Blaisdell A, Cook R (2005) Integration of spatial maps in pigeons. Anim Cogn 8:7–16PubMedCrossRefGoogle Scholar
  6. Blanchard J, Decorte L, Noguès X, Micheau J (2009) Characterization of cognition alteration across the course of the disease in app751 sl mice with parallel estimation of cerebral aβ deposition. Behav Brain Res 201(1):147–157PubMedCrossRefGoogle Scholar
  7. Bouton ME (1997) Signals for whether versus when an event will occur. In: Bouton ME, Fanselow MS (eds) Learning, motivation, and cognition: the functional behaviorism of Robert C. Bolles. American Psychological Association, Washington, DC, pp 385–409CrossRefGoogle Scholar
  8. Brown MF (1992) Does a cognitive map guide choices in the radial-arm maze? J Exp Psychol Anim Behav Process 18(1):56–66PubMedCrossRefGoogle Scholar
  9. Brown MF, Rish PA, VonCulin JE, Edberg JA (1993) Spatial guidance of choice behavior in the radial-arm maze. J Exp Psychol Anim Behav Process 19(3):195–214PubMedCrossRefGoogle Scholar
  10. Chamizo VD, Rodrigo T, Mackintosh NJ (2006) Spatial integration with rats. Learn Behav 34:348–354PubMedCrossRefGoogle Scholar
  11. Cheng K, Shettleworth SJ, Huttenlocher J, Rieser JJ (2007) Bayesian integration of spatial information. Psychol Bull 133:625–637PubMedCrossRefGoogle Scholar
  12. Christensen DZ, Bayer TA, Wirths O (2010) Intracellular aβ triggers neuron loss in the cholinergic system of the app/ps1ki mouse model of Alzheimer’s disease. Neurobiol Aging 31(7):1153–1163PubMedCrossRefGoogle Scholar
  13. Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395(6699):272–274PubMedCrossRefGoogle Scholar
  14. Clayton NS, Dickinson A (1999a) Memory for the content of caches by scrub jays (Aphelocoma coerulescens). J Exp Psychol Anim Behav Process 25(1):82–91PubMedCrossRefGoogle Scholar
  15. Clayton NS, Dickinson A (1999b) Motivational control of caching behaviour in the scrub jay, Aphelocoma coerulescens. Anim Behav 57(2):435–444PubMedCrossRefGoogle Scholar
  16. Clayton NS, Dickinson A (1999c) Scrub jays (Aphelocoma coerulescens) remember the relative time of caching as well as the location and content of their caches. J Comp Psychol 113(4):403–416PubMedCrossRefGoogle Scholar
  17. Clayton NS, Yu KS, Dickinson A (2001) Scrub jays (Aphelocoma coerulescens) form integrated memories of the multiple features of caching episodes. J Exp Psychol Anim Behav Process 27(1):17–29PubMedCrossRefGoogle Scholar
  18. Clayton NS, Bussey TJ, Dickinson A (2003a) Can animals recall the past and plan for the future? Nat Rev Neurosci 4(8):685–691PubMedCrossRefGoogle Scholar
  19. Clayton NS, Yu KS, Dickinson A (2003b) Interacting cache memories: evidence for flexible memory use by western scrub-jays (Aphelocoma californica). J Exp Psychol Anim Behav Process 29(1):14–22PubMedCrossRefGoogle Scholar
  20. Crystal JD (2009) Elements of episodic-like memory in animal models. Behav Process 80(3):269–277CrossRefGoogle Scholar
  21. Crystal JD (2010) Episodic-like memory in animals. Behav Brain Res 215:235–243PubMedCrossRefGoogle Scholar
  22. de Kort SR, Dickinson A, Clayton NS (2005) Retrospective cognition by food-caching western scrub-jays. Learn Motiv 36(2):159–176CrossRefGoogle Scholar
  23. Dere E, Huston JP, De Souza Silva MA (2005) Episodic-like memory in mice: Simultaneous assessment of object, place and temporal order memory. Brain Res Protoc 16(1–3):10–19CrossRefGoogle Scholar
  24. Egerhazi A, Berecz R, Bartok E, Degrell I (2007) Automated neuropsychological test battery (cantab) in mild cognitive impairment and in Alzheimer’s disease. Prog Neuropsychopharmacol Biol Psychiatry 31(3):746–751PubMedCrossRefGoogle Scholar
  25. Eriksen JL, Janus CG (2007) Plaques, tangles, and memory loss in mouse models of neurodegeneration. Behav Genet 37(1):79–100PubMedCrossRefGoogle Scholar
  26. Feeney M, Roberts WA, Sherry D (2009) Memory for what, where, and when in the black-capped chickadee. Anim Cogn 12(6):767–777PubMedCrossRefGoogle Scholar
  27. Gallistel CR (1990) The organization of learning. MIT Press, CambridgeGoogle Scholar
  28. Hampton RR, Hampstead BM, Murray EA (2005) Rhesus monkeys (Macaca mulatta) demonstrate robust memory for what and where, but not when, in an open-field test of memory. Learn Motiv 36(2):245–259CrossRefGoogle Scholar
  29. Hoffman ML, Beran MJ, Washburn DA (2009) Memory for “What”, “Where”, and “When” Information in rhesus monkeys (Macaca mulatta). J Exp Psychol Anim Behav Process 35(2):143–152PubMedCrossRefGoogle Scholar
  30. Hwang DY, Cho JS, Lee SH, Chae KR, Lim HJ, Min SH, Seo SJ, Song YS, Song CW, Paik SG, Sheen YY, Kim YK (2004) Aberrant expressions of pathogenic phenotype in Alzheimer’s diseased transgenic mice carrying nse-controlled appsw. Exp Neurol 186(1):20–32PubMedCrossRefGoogle Scholar
  31. Jankowsky JL, Slunt HH, Gonzales V, Savonenko AV, Wen JC, Jenkins NA, Copeland NG, Younkin LH, Lester HA, Younkin SG, Borchelt DR (2005) Persistent amyloidosis following suppression of aβ production in a transgenic model of Alzheimer disease. PLoS Med 2(12):e355–e1333PubMedCrossRefGoogle Scholar
  32. Keri RA, Siegel RE, Donald WP, Arthur PA, Susan EF, Anne ME, Robert TR (2009) Transgenic and genetic animal models. In: Pfaff DW, Fahrbach SE, Etgen AM, Rubin RT (eds) Hormones, brain and behavior. Academic Press, San Diego, pp 2673–2708CrossRefGoogle Scholar
  33. Kessels RPC, Hobbel D, Postma A (2007) Aging, context memory and binding: a comparison of “What, where and when” in youg and older adults. Int J Neurosci 117(6):795–810PubMedCrossRefGoogle Scholar
  34. Le Moal S, Reymann JM, Thomas V, Cattenoz C, Lieury A, Allain H (1997) Effect of normal aging and of Alzheimer’s disease on episodic memory. Dement Geriatr Cogn Disord 8(5):281–287PubMedCrossRefGoogle Scholar
  35. Liscic RM, Storandt M, Cairns NJ, Morris JC (2007) Clinical and psychometric distinction of frontotemporal and Alzheimer dementias. Arch Neurol 64(4):535–540PubMedCrossRefGoogle Scholar
  36. Lovasic L, Bauschke H, Janus C (2005) Working memory impairment in a transgenic amyloid precursor protein tgcrnd8 mouse model of Alzheimer’s disease. Genes Brain Behav 4(3):197–208PubMedCrossRefGoogle Scholar
  37. Maxwell MM (2009) Rnai applications in therapy development for neurodegenerative disease. Curr Pharm Des 15:3977–3991PubMedCrossRefGoogle Scholar
  38. Mazmanian DS, Roberts WA (1983) Spatial memory in rats under restricted viewing conditions. Learn Motiv 14(2):123–139CrossRefGoogle Scholar
  39. Naqshbandi M, Feeney MC, McKenzie TLB, Roberts WA (2007) Testing for episodic-like memory in rats in the absence of time of day cues: replication of Babb and Crystal. Behav Process 74(2):217–225CrossRefGoogle Scholar
  40. Nyberg L, McIntosh A, Cabeza R, Habib R, Houle S, Tulving E (1996) General and specific brain regions involved in encoding and retrieval of events: what, where, and when. Proc Natl Acad Sci USA 93:11280–11285PubMedCrossRefGoogle Scholar
  41. Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM (2003a) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer’s disease. Neurobiol Aging 24(8):1063–1070PubMedCrossRefGoogle Scholar
  42. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003b) Triple-transgenic model of Alzheimer’s disease with plaques and tangles: intracellular aβ and synaptic dysfunction. Neuron 39(3):409–421PubMedCrossRefGoogle Scholar
  43. Olton DS, Collison C (1979) Intramaze cues and odor trails fail to direct choice behavior on a elevated maze. Anim Learn Behav 7(2):221–223CrossRefGoogle Scholar
  44. Roberts WA (1998) Principles of animal cognition. McGraw-Hill, BostonGoogle Scholar
  45. Roberts WA, Feeney MC, MacPherson K, Petter M, McMillan N, Musolino E (2008) Episodic-like memory in rats: Is it based on when or how long ago? Science 320(5872):113–115PubMedCrossRefGoogle Scholar
  46. Savonenko A, Xu GM, Melnikova T, Morton JL, Gonzales V, Wong MPF, Price DL, Tang F, Markowska AL, Borchelt DR (2005) Episodic-like memory deficits in the appswe/ps1de9 mouse model of Alzheimer’s disease: relationships to ß-amyloid deposition and neurotransmitter abnormalities. Neurobiol Dis 18:602–617PubMedCrossRefGoogle Scholar
  47. Shettleworth SJ (1998) Cognition, evolutoin, and behavior. Oxford University Press, New YorkGoogle Scholar
  48. Singer RA, Zentall TR (2007) Pigeons learn to answer the question ‘where did you just peck?’ and can report peck location when unexpectedly asked. Learn Behav 35(3):184–189PubMedCrossRefGoogle Scholar
  49. Suzuki S, Augerinos G, Black AH (1980) Stimulus control of spatial behavior on the eight-arm maze in rats. Learn Motiv 11(1):1–18CrossRefGoogle Scholar
  50. Tulving E (1972) Episodic and semantic memory. In: Tulving E, Donaldson W (eds) Organization of memory. Academic Press, New York, pp 381–403Google Scholar
  51. Tulving E (1983) Elements of episodic memory. Oxford psychology series no. 2. Oxford University Press, New YorkGoogle Scholar
  52. Tulving E (1985) How many memory systems are there? Am Psychol 40(4):385–398CrossRefGoogle Scholar
  53. Tulving E (2002) Episodic memory: from mind to brain. Annu Rev Psychol 53(1):1–25PubMedCrossRefGoogle Scholar
  54. Tulving E, Markowitsch HJ (1998) Episodic and declarative memory: role of the hippocampus. Hippocampus 8(3):198–204PubMedCrossRefGoogle Scholar
  55. Ueberham U, Zobiak B, Ueberham E, Brückner MK, Boriss H, Arendt T (2006) Differentially expressed cortical genes contribute to perivascular deposition in transgenic mice with inducible neuron-specific expression of tgf-β1. Int J Dev Neurosci 24(2–3):177–186Google Scholar
  56. Volianskis A, Køstner R, Mølgaard M, Hass S, Jensen MS (2010) Episodic memory deficits are not related to altered glutamatergic synaptic transmission and plasticity in the ca1 hippocampus of the appswe/ps1 ∆e9-deleted transgenic mice model of β-amyloidosis. Neurobiol Aging 31(7):1173–1187PubMedCrossRefGoogle Scholar
  57. Wallace DG, Hines DJ, Pellis SM, Whishaw IQ (2002) Vestibular information is required for dead reckoning in the rat. J Neurosci 22(22):10009–10017PubMedGoogle Scholar
  58. Wallace DG, Martin MM, Winter SS (2008) Fractionating dead reckoning: role of the compass, odometer, logbook, and home base establishment in spatial orientation. Naturwissenschaften 95(11):1011–1026PubMedCrossRefGoogle Scholar
  59. Watanabe T, Yamagata N, Takasaki K, Sano K, Hayakawa K, Katsurabayashi S, Egashira N, Mishima K, Iwasaki K, Fujiwara M (2009) Decreased acetylcholine release is correlated to memory impairment in the tg2576 transgenic mouse model of Alzheimer’s disease. Brain Res 1249:222–228PubMedCrossRefGoogle Scholar
  60. Yoshiyama Y, Higuchi M, Zhang B, Huang S-M, Iwata N, Saido Takaomi C, Maeda J, Suhara T, Trojanowski JQ, Lee VMY (2007) Synapse loss and microglial activation precede tangles in a p301 s tauopathy mouse model. Neuron 53(3):337–351PubMedCrossRefGoogle Scholar
  61. Zentall TR (2005) Animals may not be stuck in time. Learn Motiv 36(2):208–225CrossRefGoogle Scholar
  62. Zentall TR (2006) Mental time travel in animals: a challenging question. Behav Process 72(2):173–183CrossRefGoogle Scholar
  63. Zentall TR, Clement TS, Bhatt RS, Allen J (2001) Episodic-like memory in pigeons. Psychon Bull Rev 8(4):685–690PubMedCrossRefGoogle Scholar
  64. Zentall TR, Singer RA, Stagner JP (2008) Episodic-like memory: pigeons can report location pecked when unexpectedly asked. Behav Process 79(2):93–98CrossRefGoogle Scholar
  65. Zhou W, Crystal JD (2009) Evidence for remembering when events occurred in a rodent model of episodic memory. Proc Natl Acad Sci 106(23):9525–9529PubMedCrossRefGoogle Scholar
  66. Zinkivskay A, Nazir F, Smulders T (2009) What—where—when memory in magpies (Pica pica). Anim Cogn 12(1):119–125PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.University of GeorgiaAthensUSA
  2. 2.Department of Psychological and Brain SciencesIndiana UniversityBloomingtonUSA

Personalised recommendations