Skip to main content

Advertisement

Log in

Validation of a rodent model of episodic memory

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Babb SJ, Crystal JD (2005) Discrimination of what, when, and where: implications for episodic-like memory in rats. Learn Motiv 36(2):177–189

    Article  Google Scholar 

  • Babb SJ, Crystal JD (2006a) Discrimination of what, when, and where is not based on time of day. Learn Behav 34(2):124–130

    Article  PubMed  Google Scholar 

  • Babb SJ, Crystal JD (2006b) Episodic-like memory in the rat. Curr Biol 16(13):1317–1321

    Article  PubMed  CAS  Google Scholar 

  • 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):1861–1870

    PubMed  Google Scholar 

  • Blaisdell A, Cook R (2005) Integration of spatial maps in pigeons. Anim Cogn 8:7–16

    Article  PubMed  Google Scholar 

  • 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):147–157

    Article  PubMed  CAS  Google Scholar 

  • 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 385–409

    Chapter  Google Scholar 

  • Brown MF (1992) Does a cognitive map guide choices in the radial-arm maze? J Exp Psychol Anim Behav Process 18(1):56–66

    Article  PubMed  CAS  Google Scholar 

  • 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):195–214

    Article  PubMed  CAS  Google Scholar 

  • Chamizo VD, Rodrigo T, Mackintosh NJ (2006) Spatial integration with rats. Learn Behav 34:348–354

    Article  PubMed  Google Scholar 

  • Cheng K, Shettleworth SJ, Huttenlocher J, Rieser JJ (2007) Bayesian integration of spatial information. Psychol Bull 133:625–637

    Article  PubMed  Google Scholar 

  • 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):1153–1163

    Article  PubMed  CAS  Google Scholar 

  • Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395(6699):272–274

    Article  PubMed  CAS  Google Scholar 

  • Clayton NS, Dickinson A (1999a) Memory for the content of caches by scrub jays (Aphelocoma coerulescens). J Exp Psychol Anim Behav Process 25(1):82–91

    Article  PubMed  CAS  Google Scholar 

  • Clayton NS, Dickinson A (1999b) Motivational control of caching behaviour in the scrub jay, Aphelocoma coerulescens. Anim Behav 57(2):435–444

    Article  PubMed  Google Scholar 

  • 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):403–416

    Article  PubMed  CAS  Google Scholar 

  • 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):17–29

    Article  PubMed  CAS  Google Scholar 

  • Clayton NS, Bussey TJ, Dickinson A (2003a) Can animals recall the past and plan for the future? Nat Rev Neurosci 4(8):685–691

    Article  PubMed  CAS  Google Scholar 

  • 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):14–22

    Article  PubMed  Google Scholar 

  • Crystal JD (2009) Elements of episodic-like memory in animal models. Behav Process 80(3):269–277

    Article  Google Scholar 

  • Crystal JD (2010) Episodic-like memory in animals. Behav Brain Res 215:235–243

    Article  PubMed  Google Scholar 

  • de Kort SR, Dickinson A, Clayton NS (2005) Retrospective cognition by food-caching western scrub-jays. Learn Motiv 36(2):159–176

    Article  Google Scholar 

  • 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):10–19

    Article  Google Scholar 

  • 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):746–751

    Article  PubMed  Google Scholar 

  • Eriksen JL, Janus CG (2007) Plaques, tangles, and memory loss in mouse models of neurodegeneration. Behav Genet 37(1):79–100

    Article  PubMed  Google Scholar 

  • Feeney M, Roberts WA, Sherry D (2009) Memory for what, where, and when in the black-capped chickadee. Anim Cogn 12(6):767–777

    Article  PubMed  Google Scholar 

  • Gallistel CR (1990) The organization of learning. MIT Press, Cambridge

    Google Scholar 

  • 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):245–259

    Article  Google Scholar 

  • 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):143–152

    Article  PubMed  Google Scholar 

  • 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):20–32

    Article  PubMed  CAS  Google Scholar 

  • 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–e1333

    Article  PubMed  Google Scholar 

  • 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 2673–2708

    Chapter  Google Scholar 

  • 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):795–810

    Article  PubMed  Google Scholar 

  • 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):281–287

    Article  PubMed  CAS  Google Scholar 

  • Liscic RM, Storandt M, Cairns NJ, Morris JC (2007) Clinical and psychometric distinction of frontotemporal and Alzheimer dementias. Arch Neurol 64(4):535–540

    Article  PubMed  Google Scholar 

  • 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):197–208

    Article  PubMed  CAS  Google Scholar 

  • Maxwell MM (2009) Rnai applications in therapy development for neurodegenerative disease. Curr Pharm Des 15:3977–3991

    Article  PubMed  CAS  Google Scholar 

  • Mazmanian DS, Roberts WA (1983) Spatial memory in rats under restricted viewing conditions. Learn Motiv 14(2):123–139

    Article  Google Scholar 

  • 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):217–225

    Article  Google Scholar 

  • 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 93:11280–11285

    Article  PubMed  CAS  Google Scholar 

  • 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):1063–1070

    Article  PubMed  CAS  Google Scholar 

  • 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):409–421

    Article  PubMed  CAS  Google Scholar 

  • Olton DS, Collison C (1979) Intramaze cues and odor trails fail to direct choice behavior on a elevated maze. Anim Learn Behav 7(2):221–223

    Article  Google Scholar 

  • Roberts WA (1998) Principles of animal cognition. McGraw-Hill, Boston

    Google Scholar 

  • 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):113–115

    Article  PubMed  CAS  Google Scholar 

  • 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 18:602–617

    Article  PubMed  CAS  Google Scholar 

  • Shettleworth SJ (1998) Cognition, evolutoin, and behavior. Oxford University Press, New York

    Google Scholar 

  • 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):184–189

    Article  PubMed  Google Scholar 

  • Suzuki S, Augerinos G, Black AH (1980) Stimulus control of spatial behavior on the eight-arm maze in rats. Learn Motiv 11(1):1–18

    Article  Google Scholar 

  • Tulving E (1972) Episodic and semantic memory. In: Tulving E, Donaldson W (eds) Organization of memory. Academic Press, New York, pp 381–403

    Google Scholar 

  • Tulving E (1983) Elements of episodic memory. Oxford psychology series no. 2. Oxford University Press, New York

    Google Scholar 

  • Tulving E (1985) How many memory systems are there? Am Psychol 40(4):385–398

    Article  Google Scholar 

  • Tulving E (2002) Episodic memory: from mind to brain. Annu Rev Psychol 53(1):1–25

    Article  PubMed  Google Scholar 

  • Tulving E, Markowitsch HJ (1998) Episodic and declarative memory: role of the hippocampus. Hippocampus 8(3):198–204

    Article  PubMed  CAS  Google Scholar 

  • 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):177–186

    Google Scholar 

  • 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):1173–1187

    Article  PubMed  CAS  Google Scholar 

  • Wallace DG, Hines DJ, Pellis SM, Whishaw IQ (2002) Vestibular information is required for dead reckoning in the rat. J Neurosci 22(22):10009–10017

    PubMed  CAS  Google Scholar 

  • 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):1011–1026

    Article  PubMed  CAS  Google Scholar 

  • 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 1249:222–228

    Article  PubMed  CAS  Google Scholar 

  • 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):337–351

    Article  PubMed  CAS  Google Scholar 

  • Zentall TR (2005) Animals may not be stuck in time. Learn Motiv 36(2):208–225

    Article  Google Scholar 

  • Zentall TR (2006) Mental time travel in animals: a challenging question. Behav Process 72(2):173–183

    Article  Google Scholar 

  • Zentall TR, Clement TS, Bhatt RS, Allen J (2001) Episodic-like memory in pigeons. Psychon Bull Rev 8(4):685–690

    Article  PubMed  CAS  Google Scholar 

  • Zentall TR, Singer RA, Stagner JP (2008) Episodic-like memory: pigeons can report location pecked when unexpectedly asked. Behav Process 79(2):93–98

    Article  Google Scholar 

  • Zhou W, Crystal JD (2009) Evidence for remembering when events occurred in a rodent model of episodic memory. Proc Natl Acad Sci 106(23):9525–9529

    Article  PubMed  CAS  Google Scholar 

  • Zinkivskay A, Nazir F, Smulders T (2009) What—where—when memory in magpies (Pica pica). Anim Cogn 12(1):119–125

    Article  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jonathon D. Crystal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhou, W., Crystal, J.D. Validation of a rodent model of episodic memory. Anim Cogn 14, 325–340 (2011). https://doi.org/10.1007/s10071-010-0367-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-010-0367-0

Keywords

Navigation