Book contents
- The Cambridge Handbook of Animal Cognition
- The Cambridge Handbook of Animal Cognition
- Copyright page
- Dedication
- Contents
- Figures, Tables, and Boxes
- Contributors
- Acknowledgments
- Introduction
- Part I Communication and Language
- Part II Memory and Recall
- 6 Memory and Recall Overview
- 7 A Fish Memory Tale
- 8 Memory in Hummingbirds
- 9 Event Memory in Rats
- 10 Primate Recall Memory
- Part III Social Cognition
- Part IV Social Learning and Teaching
- Part V Numerical and Quantitative Abilities
- Part VI Innovation and Problem-Solving
- Index
- References
9 - Event Memory in Rats
from Part II - Memory and Recall
Published online by Cambridge University Press: 01 July 2021
Book contents
- The Cambridge Handbook of Animal Cognition
- The Cambridge Handbook of Animal Cognition
- Copyright page
- Dedication
- Contents
- Figures, Tables, and Boxes
- Contributors
- Acknowledgments
- Introduction
- Part I Communication and Language
- Part II Memory and Recall
- 6 Memory and Recall Overview
- 7 A Fish Memory Tale
- 8 Memory in Hummingbirds
- 9 Event Memory in Rats
- 10 Primate Recall Memory
- Part III Social Cognition
- Part IV Social Learning and Teaching
- Part V Numerical and Quantitative Abilities
- Part VI Innovation and Problem-Solving
- Index
- References
Summary
People remember specific earlier events that happened to them by using episodic memory. Accordingly, researchers have sought to evaluate the hypothesis that nonhumans retrieve episodic memories. The central hypothesis of an animal model of episodic memory proposes that, at the moment of memory assessment, the animal retrieves a memory of the specific earlier event. Testing this hypothesis requires the elimination of the hypothesis that animals solve such problems by using non-episodic memory. Most of the research on event memory in nonhumans focuses on memory of a single event. Here, I describe approaches that we have used with rats to move from episodic memory of one event to two events, to many events, and to sequentially ordered events. These studies focus on source memory, binding of episodic memories, remembering items-in-context, and the replay of episodic memories. Connections between episodic memory and hippocampal replay are explored. These approaches may be used to explore the evolution of cognition.
Keywords
- Type
- Chapter
- Information
- The Cambridge Handbook of Animal Cognition , pp. 190 - 209Publisher: Cambridge University PressPrint publication year: 2021
References
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.2005.02.009CrossRefGoogle Scholar
Babb, S. J. & Crystal, J. D. (2006a). Discrimination of what, when, and where is not based on time of day. Learning & Behavior, 34, 124–130. doi: 10.3758/bf03193188Google Scholar
Babb, S. J. & Crystal, J. D. (2006b). Episodic-like memory in the rat. Current Biology, 16, 1317–1321. https://doi.org/10.1016/j.cub.2006.05.025Google Scholar
Basile, B. M. & Hampton, R. R. (2017). Dissociation of item and source memory in rhesus monkeys. Cognition, 166, 398–406. https://doi.org/10.1016/j.cognition.2017.06.009CrossRefGoogle ScholarPubMed
Beran, Michael J. (2014). Animal memory: Rats bind event details into episodic memories. Current Biology, 24(24), R1159–R1160. doi: 10.1016/j.cub.2014.11.019Google Scholar
Buzsáki, G. (2015). Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning. Hippocampus, 25(10), 1073–1188. doi: 10.1002/hipo.22488Google Scholar
Carlesimo, G. A., Serra, L., Fadda, L., Cherubini, A., Bozzali, M., & Caltagirone, C. (2007). Bilateral damage to the mammillo-thalamic tract impairs recollection but not familiarity in the recognition process: A single case investigation. Neuropsychologia, 45(11), 2467–2479.Google Scholar
Carr, M. F., Jadhav, S. P., & Frank, L. M. (2011). Hippocampal replay in the awake state: A potential substrate for memory consolidation and retrieval. Nature Neuroscience, 14(2), 147–153.Google Scholar
Carr, M. F., Karlsson, M. P., & Frank, L. M. (2012). Transient slow gamma synchrony underlies hippocampal memory replay. Neuron, 75(4), 700–713.Google Scholar
Cheng, S., Werning, M., & Suddendorf, T. (2016). Dissociating memory traces and scenario construction in mental time travel. Neuroscience and Biobehavioral Reviews, 60, 82–89. https://doi.org/10.1016/j.neubiorev.2015.11.011Google Scholar
Clayton, N. S. & Dickinson, A. (1998). Episodic-like memory during cache recovery by scrub jays. Nature, 395(6699), 272–274.Google Scholar
Crystal, J. D. (2013). Remembering the past and planning for the future in rats. Behavioural Processes, 93(0), 39–49. http://dx.doi.org/10.1016/j.beproc.2012.11.014CrossRefGoogle ScholarPubMed
Crystal, J. D. (2016a). Animal models of source memory. Journal of the Experimental Analysis of Behavior, 105(1), 56–67. doi: 10.1002/jeab.173Google Scholar
Crystal, J. D. (2016b). Comparative cognition: Action imitation using episodic memory. Current Biology, 26(23), R1226-R1228. doi: 10.1016/j.cub.2016.10.010CrossRefGoogle ScholarPubMed
Crystal, J. D. (2018). Animal models of episodic memory. Comparative Cognition & Behavior Reviews, 13, 105–122. doi: 10.3819/ccbr.2018.130012Google Scholar
Crystal, J. D., Alford, W. T., Zhou, W., & Hohmann, A. G. (2013). Source memory in the rat. Current Biology, 23(5), 387–391. http://dx.doi.org/10.1016/j.cub.2013.01.023Google Scholar
Crystal, J. D. & Alford, W. T. (2014). Validation of a rodent model of source memory. Biology Letters, 10(3), 20140064. doi: 10.1098/rsbl.2014.0064CrossRefGoogle ScholarPubMed
Crystal, J. D. & Smith, A. E. (2014). Binding of episodic memories in the rat. Current Biology, 24(24), 2957–2961. doi: 10.1016/j.cub.2014.10.074Google Scholar
Crystal, J. D. & Suddendorf, T. (2019). Episodic memory in nonhuman animals? Current Biology, 29(24), R1291–R1295. https://doi.org/https://doi.org/10.1016/j.cub.2019.10.045Google Scholar
Davidson, T. J., Kloosterman, F., & Wilson, M. A. (2009). Hippocampal replay of extended experience. Neuron, 63(4), 497–507. https://doi.org/10.1016/j.neuron.2009.07.027Google Scholar
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. doi: 10.1073/pnas.1617025113CrossRefGoogle ScholarPubMed
Dere, E., Huston, J. P., & De Souza Silva, M. A. (2005a). Episodic-like memory in mice: Simultaneous assessment of object, place and temporal order memory. Brain Research Protocols, 16, 10–19.CrossRefGoogle ScholarPubMed
Dere, E., Huston, J. P., & de Souza Silva, M. A. (2005b). Integrated memory for objects, places, and temporal order: Evidence for episodic-like memory in mice. Neurobiology of Learning and Memory, 84, 214–221.CrossRefGoogle ScholarPubMed
Dere, E., Dere, D., de Souza Silva, M. A., Huston, J. P., & Zlomuzica, A. (2017). Fellow travellers: Working memory and mental time travel in rodents. Behavioural Brain Research, 352(2018), 2–7. https://doi.org/10.1016/j.bbr.2017.03.026Google Scholar
Devkar, D. T. & Wright, A. A. (2016). Event-based proactive interference in rhesus monkeys. Psychonomic Bulletin & Review, 23(5), 1474–1482. doi: 10.3758/s13423-016-1005-xGoogle Scholar
Diba, K. & Buzsáki, G. (2007). Forward and reverse hippocampal place-cell sequences during ripples. Nature Neuroscience, 10, 1241. doi: 10.1038/nn1961 www.nature.com/articles/nn1961#supplementary-informationGoogle Scholar
Eacott, M. J. & Easton, A. (2010). Episodic memory in animals: Remembering which occasion. Neuropsychologia, 48(8), 2273–2280. http://dx.doi.org/10.1016/j.neuropsychologia.2009.11.002Google Scholar
Eacott, M. J., Easton, A., & Zinkivskay, A. (2005). Recollection in an episodic-like memory task in the rat. Learning & Memory, 12(3), 221–223.Google Scholar
Eacott, M. J. & Norman, G. (2004). Integrated memory for object, place, and context in rats: A possible model of episodic-like memory? The Journal of Neuroscience, 24(8), 1948–1953.Google Scholar
Ego-Stengel, V. & Wilson, M. A. (2010). Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus, 20(1), 1–10.Google Scholar
Eichenbaum, H. (2000). A cortical-hippocampal system for declarative memory. National Review of Neuroscience., 1(1), 41–50. doi: 10.1038/35036213CrossRefGoogle ScholarPubMed
Eichenbaum, H. (2007). Comparative cognition, hippocampal function, and recollection. Comparative Cognition & Behavior Reviews, 2), 47–66.Google Scholar
Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007). The medial temporal lobe and recognition memory. Annual Review of Neuroscience, 30, 123–152. doi: 10.1146/annurev.neuro.30.051606.094328CrossRefGoogle ScholarPubMed
Eichenbaum, H., Sauvage, M., Fortin, N., Komorowski, R., & Lipton, P. (2012). Towards a functional organization of episodic memory in the medial temporal lobe. Neuroscience Biobehavior Review, 36(7), 1597–1608. doi: 10.1016/j.neubiorev.2011.07.006CrossRefGoogle ScholarPubMed
Eldridge, L. L., Knowlton, B. J., Furmanski, C. S., Bookheimer, S. Y., & Engel, S. A. (2000). Remembering episodes: A selective role for the hippocampus during retrieval. Nature Neuroscience, 3(11), 1149–1152.CrossRefGoogle ScholarPubMed
Ergorul, C. & Eichenbaum, H. (2004). The hippocampus and memory for ‘what’, ‘where’, and ‘when’. Learning & Memory, 11(4), 397–405.Google Scholar
Fortin, N. J., Wright, S. P., & Eichenbaum, H. (2004). Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature, 431(7005), 188–191.Google Scholar
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.CrossRefGoogle Scholar
Hofer, A., Siedentopf, C. M., Ischebeck, A., Rettenbacher, M. A., Verius, M., Golaszewski, S. M., Felber, S., & Fleischhacker, W. W. (2007). Neural substrates for episodic encoding and recognition of unfamiliar faces. Brain and Cognition, 63(2), 174–181.Google Scholar
Hunsaker, M. R., Lee, B., & Kesner, R. P. (2008). Evaluating the temporal context of episodic memory: The role of CA3 and CA1. Behavioural Brain Research, 188(2), 310–315. doi: 10.1016/j.bbr.2007.11.015Google Scholar
Iordanova, M. D., Good, M. A., & Honey, R. C. (2008). Configural learning without reinforcement: Integrated memories for correlates of what, where, and when. Quarterly Journal of Experimental Psychology, 61(12), 1785–1792.Google Scholar
Iordanova, M. D., Burnett, D. J., Aggleton, J. P., Good, M., & Honey, R. C. (2009). The role of the hippocampus in mnemonic integration and retrieval: Complementary evidence from lesion and inactivation studies. European Journal of Neuroscience, 30(11), 2177–2189. doi: 10.1111/j.1460-9568.2009.07010.xCrossRefGoogle ScholarPubMed
Iordanova, M. D., Burnett, D. J., Good, M., & Honey, R. C. (2011). Pattern memory involves both elemental and configural processes: Evidence from the effects of hippocampal lesions. Behavioral Neuroscience, 125(4), 567.Google Scholar
Jadhav, S. P., Kemere, C., German, P. W., & Frank, L. M. (2012). Awake hippocampal sharp-wave ripples support spatial memory. Science, 336(6087), 1454–1458. 10.1126/science.1217230Google Scholar
Janowsky, J. S., Shimamura, A. P., & Squire, L. R. (1989). Source memory impairment in patients with frontal lobe lesions. Neuropsychologia, 27(8), 1043–1056. http://dx.doi.org/10.1016/0028-3932(89)90184-XCrossRefGoogle ScholarPubMed
Johnson, M. K., Hashtroudi, S., & Lindsay, D. S. (1993). Source monitoring. Psychological Bulletin, 114(1), 3–28. doi: 10.1037/0033-2909.114.1.3Google Scholar
Kart-Teke, E., De Souza Silva, M. A., Huston, J. P., & Dere, E. (2006). Wistar rats show episodic-like memory for unique experiences. Neurobiology of Learning and Memory, 85, 173–182.Google Scholar
Kesner, R. P., Hunsaker, M. R., & Warthen, M. W. (2008). The CA3 subregion of the hippocampus is critical for episodic memory processing by means of relational encoding in rats. Behavioral Neuroscience, 122(6), 1217–1225. doi: 10.1037/a0013592CrossRefGoogle ScholarPubMed
Kesner, R. P. & Hunsaker, M. R. (2010). The temporal attributes of episodic memory. Behavioural Brain Research, 215(2), 299–309. doi: 10.1016/j.bbr.2009.12.029Google Scholar
Kheifets, A., Freestone, D., & Gallistel, C. R. (2017). Theoretical implications of quantitative properties of interval timing and probability estimation in mouse and rat. Journal of the Experimental Analysis of Behavior, 108, 39–72. doi: 10.1002/jeab.261Google Scholar
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.2016.05.028Google Scholar
Lancet, D. (1986). Vertebrate olfactory reception. Annual Review of Neuroscience, 9(1), 329–355.Google Scholar
Mitchell, K. J. & Johnson, M. K. (2009). Source monitoring 15 years later: What have we learned from fMRI about the neural mechanisms of source memory? Psychological Bulletin, 135(4), 638–677. doi: 10.1037/a0015849CrossRefGoogle ScholarPubMed
Mori, K., Nagao, H., & Yoshihara, Y. (1999). The olfactory bulb: Coding and processing of odor molecule information. Science, 286(5440), 711–715. doi: 10.1126/science.286.5440.711Google Scholar
Moser, M.-B., Rowland, D. C., & Moser, E. I. (2015). Place cells, grid cells, and memory. Cold Spring Harbor Perspectives in Biology, 7(2). doi: 10.1101/cshperspect.a021808Google Scholar
Ólafsdóttir, H. F., Carpenter, F., & Barry, C. (2017). Task demands predict a dynamic switch in the content of awake hippocampal replay. Neuron, 96(4), 925–935.e926. doi: https://doi.org/10.1016/j.neuron.2017.09.035Google Scholar
Ólafsdóttir, H. F., Bush, D., & Barry, C. (2018). The role of hippocampal replay in memory and planning. Current Biology, 28(1), R37–R50. doi: 10.1016/j.cub.2017.10.073Google Scholar
Panoz-Brown, D. E., Corbin, H. E., Dalecki, S. J., Gentry, M., Brotheridge, S., Sluka, C. M., Wu, J.-E., & Crystal, J. D. (2016). Rats remember items in context using episodic memory. Current Biology, 26(20), 2821–2826. http://dx.doi.org/10.1016/j.cub.2016.08.023Google Scholar
Panoz-Brown, D., Iyer, V., Carey, L. M., Sluka, C. M., Rajic, G., Kestenman, J., Gentry, M., Brotheridge, S., Somekh, I., Corbin, H. E., Tucker, K. G., Almeida, B., Hex, S. B., Garcia, K. D., Hohmann, A. G., & 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.2018.04.006Google Scholar
Pavlides, C. & Winson, J. (1989). Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. The Journal of Neuroscience, 9(8), 2907–2918. doi: 10.1523/jneurosci.09-08-02907.1989Google Scholar
Pfeiffer, B. E. & Foster, D. J. (2013). Hippocampal place-cell sequences depict future paths to remembered goals. Nature, 497(7447), 74–79.CrossRefGoogle ScholarPubMed
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. doi: 10.1126/science.1152709Google Scholar
Rubin, B. D. & Katz, L. C. (2001). Spatial coding of enantiomers in the rat olfactory bulb. Nature Neuroscience, 4, 355. doi: 10.1038/85997CrossRefGoogle ScholarPubMed
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.Google Scholar
Skaggs, W. E. & McNaughton, B. L. (1996). Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science, 271(5257), 1870–1873. doi: 10.1126/science.271.5257.1870Google Scholar
Smith, A. E., Xu, Z., Lai, Y. Y., Kulkarni, P. M., Thakur, G. A., Hohmann, A. G., & Crystal, J. D. (2016). Source memory in rats is impaired by an NMDA receptor antagonist but not by PSD95-nNOS protein–protein interaction inhibitors. Behavioural Brain Research, 305, 23–29. http://dx.doi.org/10.1016/j.bbr.2016.02.021Google Scholar
Smith, A. E., Dalecki, S. J., & Crystal, J. D. (2017). A test of the reward-value hypothesis. Animal Cognition, 20(2), 215–220. doi: 10.1007/s10071-016-1040-zGoogle Scholar
Smith, A. E., Slivicki, R. A., Hohmann, A. G., & Crystal, J. D. (2017). The chemotherapeutic agent paclitaxel selectively impairs learning while sparing source memory and spatial memory. Behavioural Brain Research, 320, 48–57. http://dx.doi.org/10.1016/j.bbr.2016.11.042Google Scholar
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. doi: 10.1073/pnas.1311989110Google Scholar
Tulving, E. (1972). Episodic and Semantic Memory. In Tulving, E. & Donaldson, W. (Eds.), Organization of Memory (381–403), New York: Academic Press.Google Scholar
Tulving, E. (2002). Episodic memory: From mind to brain. Annual. Review of Psycholpgy, 53, 1–25. doi: 10.1146/annurev.psych.53.100901.135114Google Scholar
Tulving, E. & Markowitsch, H. J. (1998). Episodic and declarative memory: Role of the hippocampus. Hippocampus, 8(3), 198–204.Google Scholar
Uchida, N. & Mainen, Z. F. (2003). Speed and accuracy of olfactory discrimination in the rat. Nature Neuroscience, 6, 1224. doi: 10.1038/nn1142 www.nature.com/articles/nn1142#supplementary-informationGoogle Scholar
Wright, A. A. (2007). An experimental analysis of memory processing. Journal of the Experimental Analysis of Behavior, 88(3), 405–433.Google Scholar
Wright, A. A. (2013). Episodic memory: A rat model of source memory. Current Biology, 23(5), R198–R200. http://dx.doi.org/10.1016/j.cub.2013.01.055Google Scholar
Wright, A. A. (2018). Episodic memory: Manipulation and replay of episodic memories by rats. Current Biology, 28(11), R667–R669. https://doi.org/10.1016/j.cub.2018.04.060Google Scholar
Yonelinas, A. P. (2001). Components of episodic memory: The contribution of recollection and familiarity. Philosphical Transactions of the Royal. Society of London B Biol. Sci., 356(1413), 1363–1374. doi: 10.1098/rstb.2001.0939Google Scholar
Yonelinas, A. P. & Levy, B. J. (2002). Dissociating familiarity from recollection in human recognition memory: Different rates of forgetting over short retention intervals. Psychon Bull Review, 9(3), 575-582.CrossRefGoogle ScholarPubMed
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. doi: 10.1073/pnas.0904360106Google Scholar
Zhou, W. & Crystal, J. D. (2011). Validation of a rodent model of episodic memory. Animal Cognition, 14(3), 325–340. doi: 10.1007/s10071-010-0367-0CrossRefGoogle ScholarPubMed
Zhou, W., Hohmann, A. G., & Crystal, J. D. (2012). Rats answer an unexpected question after incidental encoding. Current Biology, 22(12), 11491153. doi: 10.1016/j.cub.2012.04.040Google Scholar
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