Temporal foundations of episodic memory.

Animal models of episodic memory Episodic memory Long interval timing Oscillator Pacemaker accumulator Rat Short interval timing Time of occurrence

Journal

Learning & behavior
ISSN: 1543-4508
Titre abrégé: Learn Behav
Pays: United States
ID NLM: 101155056

Informations de publication

Date de publication:
06 Nov 2023
Historique:
accepted: 13 10 2023
medline: 7 11 2023
pubmed: 7 11 2023
entrez: 6 11 2023
Statut: aheadofprint

Résumé

A fundamental question in the development of animal models of episodic memory concerns the role of temporal processes in episodic memory. Gallistel, (1990) developed a framework in which animals remember specific features about an event, including the time of occurrence of the event and its location in space. Gallistel proposed that timing is based on a series of biological oscillators, spanning a wide range of periods. Accordingly, a snapshot of the phases of multiple oscillators provides a representation of the time of occurrence of the event. I review research on basic timing mechanisms that may support memory for times of occurrence. These studies suggest that animals use biological oscillators to represent time. Next, I describe recently developed animal models of episodic memory that highlight the importance of temporal representations in memory. One line of research suggests that an oscillator representation of time supports episodic memory. A second line of research highlights the flow of events in time in episodic memory. Investigations that integrate time and memory may advance the development of animal models of episodic memory.

Identifiants

pubmed: 37932642
doi: 10.3758/s13420-023-00608-x
pii: 10.3758/s13420-023-00608-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : SBE Office of Multidisciplinary Activities
ID : NSF/BCS-1946039

Informations de copyright

© 2023. The Psychonomic Society, Inc.

Références

Babb, S. J., & Crystal, J. D. (2005). Discrimination of what, when, and where: Implications for episodic-like memory in rats. Learning & Motivation, 36, 177–189. https://doi.org/10.1016/j.lmot.2005.02.009
doi: 10.1016/j.lmot.2005.02.009
Babb, S. J., & Crystal, J. D. (2006). Discrimination of what, when, and where is not based on time of day. Learning & Behavior, 34, 124–130. https://doi.org/10.3758/bf03193188
doi: 10.3758/bf03193188
Babb, S. J., & Crystal, J. D. (2006). Episodic-like memory in the rat. Current Biology, 16, 1317–1321. https://doi.org/10.1016/j.cub.2006.05.025
doi: 10.1016/j.cub.2006.05.025 pubmed: 16824919
Behncke, H. (2000). Periodical cicadas. Journal of Mathematical Biology, 40(5), 413–431. https://doi.org/10.1007/s002850000024
doi: 10.1007/s002850000024 pubmed: 10885591
Bird, L. R., Roberts, W. A., Abroms, B. D., Kit, K. A., & Crupi, C. (2003). Spatial memory for food hidden by rats (Rattus norvegicus) on the radial maze: Studies of memory for where, what, and when. Journal of Comparative Psychology, 117(2), 176–187.
doi: 10.1037/0735-7036.117.2.176 pubmed: 12856788
Buhusi, C. V., & Meck, W. H. (2005). What makes us tick? Functional and neural mechanisms of interval timing. Nature Reviews Neuroscience, 6(10), 755–765.
doi: 10.1038/nrn1764 pubmed: 16163383
Cheng, K. (2022). Oscillators and servomechanisms in orientation and navigation, and sometimes in cognition. Proceedings of the Royal Society B, 289(1974), 20220237. https://doi.org/10.1098/rspb.2022.0237
doi: 10.1098/rspb.2022.0237 pubmed: 35538783 pmcid: 9091845
Cheng, K. (2023). From representations to servomechanisms to oscillators: My journey in the study of cognition. Animal Cognition, 26(1), 73–85. https://doi.org/10.1007/s10071-022-01677-7
doi: 10.1007/s10071-022-01677-7 pubmed: 36029388
Clayton, N. S., Bussey, T. J., & Dickinson, A. (2003). Can animals recall the past and plan for the future? Nature Reviews Neuroscience, 4(8), 685–691.
doi: 10.1038/nrn1180 pubmed: 12894243
Clayton, N. S., & Dickinson, A. (1998). Episodic-like memory during cache recovery by scrub jays. Nature, 395(6699), 272–274. https://doi.org/10.1038/26216
doi: 10.1038/26216 pubmed: 9751053
Crystal, J. D. (1999). Systematic nonlinearities in the perception of temporal intervals. Journal of Experimental Psychology: Animal Behavior Processes, 25(1), 3–17.
Crystal, J. D. (2001a). Circadian time perception. Journal of Experimental Psychology: Animal Behavior Processes, 27(1), 68–78.
Crystal, J. D. (2001b). Nonlinear time perception. Behavioural Processes, 55(1), 35–49.
Crystal, J. D. (2006a). Long-interval timing is based on a self sustaining endogenous oscillator. Behavioural Processes, 72, 149–160.
Crystal, J. D. (2006b). Time, place, and content. Comparative Cognition & Behavior Reviews, 1, 53–76.  https://comparative-cognition-and-behavior-reviews.org/wp/wp-content/uploads/2013/10/vol_1_crystal.pdf
Crystal, J. D. (2010). Time: What animals know. In N. S. Clayton, J. Moore, & M. Breed (Eds.), Encyclopedia of Animal Behavior (pp. 429–437). Academic Press.
doi: 10.1016/B978-0-12-813251-7.00092-4
Crystal, J. D. (2012). Sensitivity to time: Implications for the representation of time. In E. A. Wasserman & T. R. Zentall (Eds.), The Oxford handbook of comparative cognition (pp. 434–450). Oxford University Press.
Crystal, J. D. (2013). Remembering the past and planning for the future in rats. Behavioural Processes, 93, 39–49. https://doi.org/10.1016/j.beproc.2012.11.014
doi: 10.1016/j.beproc.2012.11.014 pubmed: 23219951
Crystal, J. D. (2015). Rats time long intervals: Evidence from several cases. International Journal of Comparative Psychology, 28, 1–9.
doi: 10.46867/ijcp.2015.28.02.01
Crystal, J. D. (2016). Animal models of source memory. Journal of the Experimental Analysis of Behavior, 105(1), 56–67. https://doi.org/10.1002/jeab.173
doi: 10.1002/jeab.173
Crystal, J. D. (2018). Animal models of episodic memory. Comparative Cognition & Behavior Reviews, 13, 105–122. https://doi.org/10.3819/ccbr.2018.130012
doi: 10.3819/ccbr.2018.130012
Crystal, J. D. (2021a). Evaluating evidence from animal models of episodic memory. Journal of Experimental Psychology: Animal Learning and Cognition, 47(3), 337–356. https://doi.org/10.1037/xan0000294
Crystal, J. D. (2021b). Event memory in rats. In A. Kaufman, J. Call, & J. Kaufman (Eds.), Cambridge handbook of animal cognition (pp. 190–209). Cambridge University Press.
Crystal, J. D. (2022). Episodic memory in animals. In M. Kruase, K. Hollis, & M. Papini (Eds.), Evolution of learning and memory mechanisms (pp. 302–316). Cambridge University Press.
doi: 10.1017/9781108768450.021
Crystal, J. D., & Baramidze, G. T. (2007). Endogenous oscillations in short-interval timing. Behavioural Processes, 74(2), 152–158. https://doi.org/10.1016/j.beproc.2006.10.008
doi: 10.1016/j.beproc.2006.10.008 pubmed: 17118575
Crystal, J. D., Church, R. M., & Broadbent, H. A. (1997). Systematic nonlinearities in the memory representation of time. Journal of Experimental Psychology: Animal Behavior Processes, 23(3), 267–282.
pubmed: 9206024
Crystal, J. D., & Suddendorf, T. (2019). Episodic memory in nonhuman animals? Current Biology, 29(24), R1291–R1295. https://doi.org/10.1016/j.cub.2019.10.045
doi: 10.1016/j.cub.2019.10.045 pubmed: 31846670
Dede, A. J. O., Frascino, J. C., Wixted, J. T., & Squire, L. R. (2016). Learning and remembering real-world events after medial temporal lobe damage. Proceedings of the National Academy of Sciences, 113(47), 13480–13485. https://doi.org/10.1073/pnas.1617025113
doi: 10.1073/pnas.1617025113
Eichenbaum, H. (2000). A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience, 1(1), 41–50. https://doi.org/10.1038/35036213
doi: 10.1038/35036213 pubmed: 11252767
Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007). The medial temporal lobe and recognition memory. Annual Review of Neuroscience, 30(1), 123–152. https://doi.org/10.1146/annurev.neuro.30.051606.094328
doi: 10.1146/annurev.neuro.30.051606.094328 pubmed: 17417939 pmcid: 2064941
Gallistel, C. R. (1990). The organization of learning. MIT Press.
Gerkema, M. P. (2002). Ultradian rhythms. In V. Kumar (Ed.), Biological rhythms (pp. 207–215). Springer. https://doi.org/10.1007/978-3-662-06085-8_17
doi: 10.1007/978-3-662-06085-8_17
Gibbon, J., Fairhurst, S., & Goldberg, B. (1997). Cooperation, conflict and compromise between circadian and interval clocks in pigeons. In C. M. Bradshaw & E. Szabadi (Eds.), Time and behaviour: Psychological and neurobehavioural analyses (pp. 329–384). Elsevier.
doi: 10.1016/S0166-4115(97)80060-X
Glass, L., & Winfree, A. T. (1984). Discontinuities in phase-resetting experiments., 246(2), R251–R258. https://doi.org/10.1152/ajpregu.1984.246.2.R251
doi: 10.1152/ajpregu.1984.246.2.R251
Hampton, R. R., Hampstead, B. M., & Murray, E. A. (2005). Rhesus monkeys (Macaca mulatta) demonstrate robust memory for what and where, but not when, in an open-field test of memory. Learning & Motivation, 36(2), 245–259.
doi: 10.1016/j.lmot.2005.02.004
Henson, R. N. A., Rugg, M. D., Shallice, T., Josephs, O., & Dolan, R. J. (1999). Recollection and familiarity in recognition memory: An event-related functional magnetic resonance imaging study. Journal of Neuroscience, 99, 3962–3972.
doi: 10.1523/JNEUROSCI.19-10-03962.1999
Hofer, A., Siedentopf, C. M., Ischebeck, A., Rettenbacher, M. A., Verius, M., Golaszewski, S. M., ..., & Fleischhacker, W. W. (2007). Neural substrates for episodic encoding and recognition of unfamiliar faces. Brain and Cognition, 63(2), 174–181. https://doi.org/10.1016/j.bandc.2006.11.005
Isomura, A., & Kageyama, R. (2014). Ultradian oscillations and pulses: Coordinating cellular responses and cell fate decisions. Development, 141(19), 3627–3636. https://doi.org/10.1242/dev.104497
doi: 10.1242/dev.104497
Johnson, C. H. (1990). An atlas of phase response curves for circadian and circatidal rhythms. Vanderbilt University.
Kirkpatrick-Steger, K., Miller, S. S., Betti, C. A., & Wasserman, E. A. (1996). Cyclic responding by pigeons on the peak timing procedure. Journal of Experimental Psychology: Animal Behavior Processes, 22, 447–460.
pubmed: 8865612
Kumar, V., Wingfield, J. C., Dawson, A., Ramenofsky, M., Rani, S., & Bartell, P. (2010). Biological clocks and regulation of seasonal reproduction and migration in birds. Physiological and Biochemical Zoology, 83(5), 827–835. https://doi.org/10.1086/652243
doi: 10.1086/652243 pubmed: 20604684
Kurth-Nelson, Z., Economides, M., Dolan, Raymond J., & Dayan, P. (2016). Fast sequences of non-spatial state representations in humans. Neuron, 91(1), 194–204. https://doi.org/10.1016/j.neuron.2016.05.028
doi: 10.1016/j.neuron.2016.05.028 pubmed: 27321922 pmcid: 4942698
Langille, J. J., Gallistel, C. R. (2020). The search for the engram: Should we look for plastic synapses or information-storing molecules? Neurobiology of Learning and Memory, 107164. https://doi.org/10.1016/j.nlm.2020.107164
MacGregor, D. J., & Lincoln, G. A. (2008). A physiological model of a circannual oscillator. Journal of Biological Rhythms, 23(3), 252–264. https://doi.org/10.1177/0748730408316796
doi: 10.1177/0748730408316796 pubmed: 18487417
Mercier, A., Sun, Z., Baillon, S., & Hamel, J.-F. (2011). Lunar rhythms in the deep sea: Evidence from the reproductive periodicity of several marine invertebrates. Journal of Biological Rhythms, 26(1), 82–86. https://doi.org/10.1177/0748730410391948
doi: 10.1177/0748730410391948 pubmed: 21252369
Naqshbandi, M., Feeney, M. C., McKenzie, T. L. B., & Roberts, W. A. (2007). Testing for episodic-like memory in rats in the absence of time of day cues: Replication of Babb and Crystal. Behavioural Processes, 74(2), 217–225. https://doi.org/10.1016/j.beproc.2006.10.010
doi: 10.1016/j.beproc.2006.10.010 pubmed: 17118573
Panoz-Brown, D. E., Corbin, H. E., Dalecki, S. J., Gentry, M., Brotheridge, S., Sluka, C. M., ..., & Crystal, J. D. (2016). Rats remember items in context using episodic memory. Current Biology, 26(20), 2821–2826. https://doi.org/10.1016/j.cub.2016.08.023
Panoz-Brown, D., Iyer, V., Carey, L. M., Sluka, C. M., Rajic, G., Kestenman, J., ..., & Crystal, J. D. (2018). Replay of episodic memories in the rat. Current Biology, 28(10), 1628-1634.e1627. https://doi.org/10.1016/j.cub.2018.04.006
Pizzo, M. J., & Crystal, J. D. (2004). Time-place learning in the eight-arm radial maze. Learning & Behavior, 32(2), 240–255.
doi: 10.3758/BF03196025
Pizzo, M. J., & Crystal, J. D. (2006). The influence of temporal spacing on time-place discrimination. Learning & Behavior, 34, 131–143.
doi: 10.3758/BF03193189
Roberts, W. A., Feeney, M. C., 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. https://doi.org/10.1126/science.1152709
doi: 10.1126/science.1152709 pubmed: 18388296
Roberts, W. A., & Roberts, S. (2002). Two tests of the stuck in-time hypothesis. Journal of General Psychology, 129(4), 415–429.
doi: 10.1080/00221300209602105 pubmed: 12494992
Schacter, D. L. (2002). The seven sins of memory: How the mind forgets and remembers. Houghton Mifflin Harcourt.
Schmitter-Edgecombe, M., & Anderson, J. W. (2007). Feeling of knowing in episodic memory following moderate to severe closed-head injury. Neuropsychology, 21(2), 224–234. https://doi.org/10.1037/0894-4105.21.2.224
doi: 10.1037/0894-4105.21.2.224 pmcid: 2262102
Staresina, B. P., Alink, A., Kriegeskorte, N., & Henson, R. N. (2013). Awake reactivation predicts memory in humans. Proceedings of the National Academy of Sciences, 110(52), 21159–21164. https://doi.org/10.1073/pnas.1311989110
doi: 10.1073/pnas.1311989110
Stein, H. V. (1951). Untersuchungen über den Zeitsinn bei Vögeln [Studies on the sense of time in birds]. J Zeitschrift für vergleichende Physiologie, 33(5), 387–403.
doi: 10.1007/BF00339232
Suddendorf, T. (2013). Mental time travel: Continuities and discontinuities. Trends in Cognitive Sciences, 17(4), 151–152. https://doi.org/10.1016/j.tics.2013.01.011
doi: 10.1016/j.tics.2013.01.011 pubmed: 23453751
Suddendorf, T., & Corballis, M. C. (1997). Mental time travel and the evolution of the human mind. Genetic, Social, & General Psychology Monographs, 123(2), 133–167.
Takahashi, J. S., Turek, F. W., & Moore, R. Y. (Eds.). (2001). Handbook of behavioral neurobiology: Circadian clocks (12th ed.). Plenum.
Tulving, E. (1972). Episodic and semantic memory. In E. Tulving & W. Donaldson (Eds.), Organization of memory (pp. 381–403). Academic Press.
Tulving, E. (1983). Elements of episodic memory. Oxford University Press.
Tulving, E. (2001). Chronesthesia: Awareness of subjective time. In D. T. Stuss & R. C. Knight (Eds.), The age of the frontal lobes (pp. 311–325). Oxford University Press.
Tulving, E. (2002). Episodic memory: From mind to brain. Annual Review of Psychology, 53(1), 1–25. https://doi.org/10.1146/annurev.psych.53.100901.135114
doi: 10.1146/annurev.psych.53.100901.135114 pubmed: 11752477
Zhou, W., & Crystal, J. D. (2009). Evidence for remembering when events occurred in a rodent model of episodic memory. Proceedings of the National Academy of Sciences of the United States of America, 106(23), 9525–9529. https://doi.org/10.1073/pnas.0904360106
doi: 10.1073/pnas.0904360106 pubmed: 19458264 pmcid: 2695044
Zhou, W., & Crystal, J. D. (2011). Validation of a rodent model of episodic memory. Animal Cognition, 14(3), 325–340. https://doi.org/10.1007/s10071-010-0367-0
doi: 10.1007/s10071-010-0367-0 pubmed: 21165663

Auteurs

Jonathon D Crystal (JD)

Department of Psychological & Brain Science, Indiana University, 1101 E 10TH ST, Bloomington, IN, 47405, USA. jcrystal@indiana.edu.

Classifications MeSH