Skip to main content
SpringerLink
Log in

How Does the Hippocampus Support the Spatial and Temporal Attributes of Memory?

  • Chapter
  • First Online:
The Neurobiological Basis of Memory

Abstract

Ray Kesner long ago proposed that the hippocampus supports the organization of memories by their spatial and temporal attributes, and he generated compelling evidence for this proposal through many creative experimental analyses of the effects on memory resulting from damage to the hippocampus. Here I describe some of that evidence and other studies of the firing properties of hippocampal neurons that offer insight into the mechanisms of spatial and temporal organization that underlie hippocampal dependent memory. Hippocampal neurons parse the layout of spatial contexts by “place cells” that represent memories in the locations where they occur, and they parse the temporal organization of experiences by “time cells” that represent the moments when memories occur. The combination of mapping place and time constitutes a mechanism for organizing spatial–temporal context as a fundamental attribute of the memory capacity supported by the hippocampus.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ainge, J. A., Tamosiunaite, M., Woergoetter, F., & Dudchenko, P. A. (2007). Hippocampal CA1 place cells encode intended destination on a maze with multiple choice points. The Journal of Neuroscience, 27, 9769–9779. doi:10.1523/JNEUROSCI.2011-07.2007.

    Article  PubMed  Google Scholar 

  • Bower, M. R., Euston, D. R., & McNaughton, B. L. (2005). Sequential-context-dependent hippocampal activity is not necessary to learn sequences with repeated elements. The Journal of Neuroscience, 25, 1313–1323. doi:10.1523/JNEUROSCI.2901-04.2005.

    Article  PubMed  Google Scholar 

  • Buhusi, C. V., & Meck, W. H. (2005). What makes us tick? Functional and neural mechanisms of interval timing. Nature Reviews Neuroscience, 6, 755–765. doi:10.1038/nrn1764.

    Article  PubMed  Google Scholar 

  • Dragoi, G., & Tonegawa, S. (2011). Preplay of future place cell sequences by hippocampal cellular assemblies. Nature, 469, 397–401. doi:10.1038/nature09633.

    Article  PubMed Central  PubMed  Google Scholar 

  • Dupret, D., O’Neill, J., Pleydell-Bouverie, B., & Csicsvari, J. (2010). The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nature Neuroscience, 13, 995–1002. doi:10.1038/nn.2599.

    Article  PubMed Central  PubMed  Google Scholar 

  • Eichenbaum, H. (2004). Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron, 44, 109–120. doi:10.1016/j.neuron.2004.08.028.

    Article  PubMed  Google Scholar 

  • Eichenbaum, H. (2013). Memory on time. Trends in Cognitive Sciences, 17, 81–88. doi: 10.1016/j.tics.2012.12.007.

    Article  PubMed Central  PubMed  Google Scholar 

  • Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M., & Tanila, H. (1999). The hippocampus, memory, and place cells: Is it spatial memory or a memory space? Neuron, 23, 209–226. doi:10.1016/j.neuron.2013.04.015.

    Article  PubMed  Google Scholar 

  • Etienne, A. S., & Jeffery, K. J. (2004). Path integration in mammals. Hippocampus, 14, 180–192. doi:10.1002/hipo.10173.

    Article  PubMed  Google Scholar 

  • Farovik, A., Dupont, L. M., & Eichenbaum, H. (2010). Distinct roles for dorsal CA3 and CA1 in memory for sequential nonspatial events. Learning & Memory, 17, 12–17. doi: 10.1101/lm.1616209.

    Article  Google Scholar 

  • Ferbinteanu, J., & Shapiro, M. L. (2003). Prospective and retrospective memory coding in the hippocampus. Neuron, 40, 1227–1239. doi:10.1016/S0896-6273(03)00752-9.

    Article  PubMed  Google Scholar 

  • Fortin, N. J., Agster, K. L., & Eichenbaum, H. B. (2002). Critical role of the hippocampus in memory for sequences of events. Nature Neuroscience, 5, 458–462. doi:10.1038/nn834.

    PubMed Central  PubMed  Google Scholar 

  • Frank, L. M., Brown, E. N., & Wilson, M. (2000). Trajectory encoding in the hippocampus and entorhinal cortex. Neuron, 27, 169–178. doi:10.1016/S0896-6273(00)00018-0.

    Article  PubMed  Google Scholar 

  • Gallistel, C. R. (1990). The organization of learning. Cambridge: MIT Press.

    Google Scholar 

  • Gibbon, J., Church, R. M., & Meck, W. H. (1984). Scalar timing in memory. Annals of the New York Academy of Sciences, 423, 52–77. doi:10.1111/j.1749-6632.1984.tb23417.x.

    Google Scholar 

  • Gilbert, P. E., & Kesner, R. P. (2003). Localization of function within the dorsal hippocampus: the role of the CA3 subregion in paired-associate learning. Behavioral Neuroscience, 117, 1385–1394. doi:10.1037/0735-7044.117.6.1385.

    Article  PubMed  Google Scholar 

  • Gill, P. R., Mizumori, S. J., & Smith, D. M. (2011). Hippocampal episode fields develop with learning. Hippocampus, 21, 1240–1249. doi:10.1002/hipo.20832.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ginther, M. R., Walsh, D. F., & Ramus, S. J. (2011). Hippocampal neurons encode different episodes in an overlapping sequence of odors task. The Journal of Neuroscience, 31, 2706–2711. doi:10.1523/JNEUROSCI.3413-10.2011.

    Article  PubMed Central  PubMed  Google Scholar 

  • Gothard, K. M., Skaggs, W. E., McNaughton B. L. (1996) Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. The Journal of Neuroscience, 16, 8027–8040.

    PubMed  Google Scholar 

  • Griffin, A. L., Eichenbaum, H., & Hasselmo, M. E. (2007). Spatial representations of hippocampal CA1 neurons are modulated by behavioral context in a hippocampus-dependent memory task. The Journal of Neuroscience, 27, 2416–2423. doi: 10.1523/JNEUROSCI.4083-06.2007.

    Article  PubMed  Google Scholar 

  • Gupta, A. S., van der Meer, M. A., Touretzky, D. S., & Redish, A. D. (2010). Hippocampal replay is not a simple function of experience. Neuron, 65, 695–705. doi:10.1016/j.neuron.2010.01.034.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hunsaker, M. R., Thorup, J. A., Welch, T., & Kesner, R. P. (2006). The role of CA3 and CA1 in the acquisition of an object-trace-place paired associate task. Behavioral Neuroscience, 120, 1252–1256. doi:10.1037/0735-7044.120.6.1252.

    Article  PubMed  Google Scholar 

  • Jacobs, N. S., Allen, T. A., Nguyen, N., & Fortin, N. J. (2013). Critical role of the hippocampus in memory for elapsed time. The Journal of Neuroscience, 33, 13888–13893. doi:10.1523/JNEUROSCI.1733-13.2013.

    Article  PubMed  Google Scholar 

  • Jadhav, S. P., Kemere, C., German, P. W., & Frank, L. M. (2012). Awake hippocampal sharp-wave ripples support spatial memory. Science, 336, 1454–1458. doi:10.1126/science.1217230.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ji, D., & Wilson, M. A. (2007). Coordinated memory replay in the visual cortex and hippocampus during sleep. Nature Neuroscience, 10, 100–107. doi:10.1038/nn1825.

    Article  PubMed  Google Scholar 

  • Johnson, A., & Redish, A. D. (2007). Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. The Journal of Neuroscience, 27, 12176–12189. doi:10.1523/JNEUROSCI.3761-07.2007.

    Article  PubMed  Google Scholar 

  • Karlsson, M. P., & Frank, L. M. (2009). Awake replay of remote experiences in the hippocampus. Nature Neuroscience, 12, 913–918. doi:10.1038/nn.2344.

    Article  PubMed Central  PubMed  Google Scholar 

  • Kesner, R. P. (1990). Learning and memory in rats with an emphasis on the role of the hippocampal formation. In: R. P. Kesner & D. S. Olton (Eds.), Neurobiology of comparative cognition (pp. 179–205). New Jersey: Erlbaum.

    Google Scholar 

  • Kesner, R. P., & DiMattia, B. V. (1987). Neurobiology of an attribute model of memory. In: A. R. Morrison & A. N. Epstein (Eds.), Progress in psychobiology and physiological psychology (pp. 207–277). New York: Academic.

    Google Scholar 

  • Kesner, R. P., & Hunsaker, M. R. (2010). The temporal attributes of episodic memory. Behavioural Brain Research, 215, 299–309. doi:10.1016/j.bbr.2009.12.029.

    Article  PubMed  Google Scholar 

  • Kesner, R. P., & Novak, J. (1982). Serial position curve in rats: Role of the dorsal hippocampus. Science, 218, 173–175. doi:10.1126/science.7123228.

    Article  PubMed  Google Scholar 

  • Kesner, R. P., Gilbert, P. E., & Barua, L. A. (2002). The role of the hippocampus in memory for the temporal order of a sequence of odors. Behavioral Neuroscience, 116, 286–290. doi:10.1037/0735-7044.116.2.286.

    Article  PubMed  Google Scholar 

  • Kesner, R. P., Hunsaker M. R., & Gilbert, P.E. (2005). The role of CA1 in the acquisition of an object–trace–odor paired associate task. Behavioral Neuroscience, 119, 781–786. doi:10.1037/0735-7044.119.3.781

    Article  PubMed  Google Scholar 

  • Komorowski, R. W., Manns, J. R., & Eichenbaum, H. (2009). Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where. The Journal of Neuroscience, 29, 9918–9929. doi:10.1523/JNEUROSCI.1378-09.2009.

    Article  PubMed Central  PubMed  Google Scholar 

  • Komorowski, R. W., Garcia, C. G., Wilson, A., Hattori, S., Howard, M. W., & Eichenbaum, H. (2013). Ventral hippocampal neurons are shaped by experience to represent behaviorally relevant contexts. The Journal of Neuroscience, 33, 8079–8087. doi:10.1523/JNEUROSCI.5458–12.2013.

    Article  PubMed Central  PubMed  Google Scholar 

  • Kraus, B. J., Robinson II, R. J., White, J. A., Eichenbaum, H., & Hasselmo, M. E. (2013). Hippocampal “time cells”: Time versus path integration. Neuron, 78, 1090–1101. doi:10.1016/j.neuron.2013.04.015.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee, I., Griffin, A. L., Zilli, E. A., Eichenbaum, H., & Hasselmo, M. E. (2006). Gradual translocation of spatial correlates of neuronal firing in the hippocampus toward prospective locations. Neuron, 51, 639–650. doi:10.1016/j.neuron.2006.06.033.

    Article  PubMed  Google Scholar 

  • Lenck-Santini, P. P., Save, E., & Poucet, B. (2001). Place-cell firing does not depend on the direction of turn in a Y-maze alternation task. The European Journal of Neuroscience, 13, 1055–1058. doi:10.1046/j.0953-816x.2001.01481.x.

    Article  PubMed  Google Scholar 

  • MacDonald, C. J. (2014). Prospective and retrospective duration memory in the hippocampus: Is time in the foreground or background? Proceedings of the Royal Society B: Biological Processes, 2014 Jan 20; 369(1637), 20120463.

    Google Scholar 

  • MacDonald, C. J., Lepage, K. Q., Eden, U. T., & Eichenbaum, H. (2011). Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron, 71, 737–749. doi:10.1016/j.neuron.2011.07.012.

    Article  PubMed Central  PubMed  Google Scholar 

  • MacDonald, C. J., Place, R., Carrow, S., & Eichenbaum, H. (2013). Distinct hippocampal time cell sequences represent odor memories in immobilized rats. The Journal of Neuroscience, 33, 14607–14616. doi:10.1523/JNEUROSCI.1537-13.2013.

    Article  PubMed Central  PubMed  Google Scholar 

  • Manns, J. R., & Eichenbaum, H. (2005). Time and treason to the trisynaptic teachings: theoretical comment on Kesner et Al. (2005). Behavioral Neuroscience, 119, 1140–1143. doi:10.1037/0735-7044.119.4.1140.

    Article  PubMed  Google Scholar 

  • Manns, J. R., & Eichenbaum, H. (2009). A cognitive map for object memory in the hippocampus. Learning and Memory, 16, 616–624. doi:10.1101/lm.1484509.

    Article  PubMed Central  PubMed  Google Scholar 

  • Manns, J. R., Zilli, E. A., Ong, K. C., Hasselmo, M. E., & Eichenbaum, H. (2007) Hippocampal CA1 spiking during encoding and retrieval: Relation to theta phase. Neurobiology of Learning and Memory, 87, 9–20. doi:10.1016/j.nlm.2006.05.007.

    Article  PubMed  Google Scholar 

  • Mauk, M. D., & Buonomano, D. V. (2004). The neural basis of temporal processing. Annual Review of Neuroscience, 27, 307–340. doi:10.1146/annurev.neuro.27.070203.144247.

    Article  PubMed  Google Scholar 

  • McNaughton, B. L., Barnes, C. A., Gerrard, J. L., Gothard, K., Jung, M. W., Knierim, J. J., Kudrimoti, H., Qin, Y., Skaggs, W. E., Suster, M., & Weaver, K. L. (1996). Deciphering the hippocampal polyglot: The hippocampus as a path integration system. The Journal of Experimental Biology, 199, 173–185.

    PubMed  Google Scholar 

  • McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., & Moser, M. B. (2006). Path integration and the neural basis of the ‘cognitive map’. Nature Reviews Neuroscience, 7, 663–678. doi:10.1038/nrn1932.

    Article  PubMed  Google Scholar 

  • Moita, M. A. P., Rosis, S., Zhou, Y., LeDoux, J. E., & Blair, H. T. (2003). Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron, 37, 485–497. doi:10.1016/S0896-6273(03)00033-3.

    Article  PubMed  Google Scholar 

  • Meck, W. H., Church, R. M., & Olton, D. S. (1984). Hippocampus, time, and memory. Behavioral Neuroscience 98, 3–22.

    Google Scholar 

  • Moser, E. I., Kropff, E., & Moser, M. B. (2008). Place cells, grid cells, and the brain’s spatial representation system. Annual Review of Neuroscience, 31, 69–89. doi:10.1146/annurev.neuro.31.061307.090723.

    Article  PubMed  Google Scholar 

  • Naya, Y., & Suzuki, W. A. (2011). Integrating what and when across the primate medial temporal lobe. Science, 333, 773–776. doi:10.1126/science.1206773.

    Article  PubMed  Google Scholar 

  • O’Keefe, J., & Nadel, L. (1978). The Hippocampus as a cognitive map. Oxford: Oxford University Press.

    Google Scholar 

  • Olton, D. S. (1986). Hippocampal function and memory for temporal context. In: R. L. Isaacson & K. H. Pribram (Eds.), The Hippocampus (pp. 281–298). Philadelphia: Springer US.

    Chapter  Google Scholar 

  • Pastalkova, E., Itskov, V., Amarasingham, A., & Buzsáki, G. (2008). Internally generated cell assembly sequences in the rat hippocampus. Science, 321, 1322–1327. doi:10.1126/science.1159775.

    Article  PubMed Central  PubMed  Google Scholar 

  • Paz, R., Gelbard-Sagiv, H., Mukamel, R., Harel, M., Malach, R., & Fried, I. (2010). A neural substrate in the human hippocampus for linking successive events. Proceedings of the National Academy of Sciences of the United States of America, 107, 6046–6051. doi:10.1073/pnas.0910834107.

    Article  PubMed Central  PubMed  Google Scholar 

  • Pfeiffer, B. E., & Foster, D. J. (2013). Hippocampal place-cell sequences depict future paths to remembered goals. Nature, 497, 74–79. doi:10.1038/nature12112.

    Article  PubMed Central  PubMed  Google Scholar 

  • Rawlins, J. N. P. (1985). Associations across time: The hippocampus as a temporary memory store. Behavioral and Brain Sciences, 8, 479–528. doi:10.1017/S0140525X00001291.

    Article  Google Scholar 

  • Redish, A. D., Rosenzweig, E. S., Bohanick, J. D., McNaughton, B. L., & Barnes, C. A. (2000). Dynamics of hippocampal ensemble activity realignment: time versus space. The Journal of Neuroscience, 20, 9298–9309.

    PubMed  Google Scholar 

  • Robitsek, J. R., White, J. A., & Eichenbaum, H. (2013). Place cell activation predicts subsequent memory. Behavioural Brain Research, 254, 65–72. doi:10.1016/j.bbr.2012.12.034.

    Article  PubMed Central  PubMed  Google Scholar 

  • Shapiro, M. L., Kennedy, P. J., & Ferbinteanu, J. (2006). Representing episodes in the mammalian brain. Current Opinion in Neurobiology, 16, 701–709. doi:10.1016/j.conb.2006.08.017.

    Article  PubMed  Google Scholar 

  • Singer, A. C., Carr, M. F., Karlsson, M. P., & Frank, L. M. (2013). Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task. Neuron, 77, 1163–1173. doi:10.1016/j.neuron.2013.01.027.

    Article  PubMed Central  PubMed  Google Scholar 

  • Squire, L. R. (2009). Memory and brain systems: 1969–2009. The Journal of Neuroscience, 29, 12711–12716. doi:10.1523/JNEUROSCI.3575-09.2009.

    Article  PubMed Central  PubMed  Google Scholar 

  • Wilson, M. A., & McNaughton, B. L. (1994). Reactivation of hippocampal ensemble memories during sleep. Science, 265, 676–679. doi:10.1126/science.8036517.

    Article  PubMed  Google Scholar 

  • Wood, E. R., Dudchenko, P. A., & Eichenbaum, H. (1999). The global record of memory in hippocampal neuronal activity. Nature, 397, 613–616. doi:10.1038/17605.

    Article  PubMed  Google Scholar 

  • Wood, E. R., Dudchenko, P. A., Robitsek, R. J., & Eichenbaum, H. (2000). Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron, 27, 623–633. doi:10.1016/S0896-6273(00)00071-4

    Article  PubMed  Google Scholar 

  • Yin, B., & Troger, A. B. (2011). Exploring the 4th dimension: Hippocampus, time, and memory revisited. Frontiers in Integrative Neuroscience, 5, Article 36. doi:10.3389/fnint.2011.00036.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Center for Memory and Brain, Boston University, 2 Cummington Mall, 02215, Boston, MA, USA

    Howard Eichenbaum PhD & Benjamin J. Kraus PhD

  2. Picower Institute for Learning and Memory, Massachusetts Institute of Technology, 77 Massachusetts Ave, 02139, Cambridge, MA, USA

    Robert Komorowski PhD

  3. Picower Institute for Learning and Memory, RIKEN-MIT Center for Neural Circuit Genetics, Massachusetts Institute of Technology, 43 Vassar St., 02139, Cambridge, MA, USA

    Christopher J. MacDonald PhD

  4. The MathWorks, Inc., 3 Apple Hill Road, Natick, MA, USA

    Benjamin J. Kraus PhD

  5. Department of Surgery, Jamaica Hospital Medical Center, 8900 Van Wyck Expressway Jamaica, 11418, Jamaica, NY, USA

    Jonathan Robitsek

Authors
  1. Howard Eichenbaum PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert Komorowski PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher J. MacDonald PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Benjamin J. Kraus PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jonathan Robitsek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Howard Eichenbaum PhD .

Editor information

Editors and Affiliations

  1. Department of Psychology, Radford University, Radford, Virginia, USA

    Pamela A. Jackson

  2. Department of Cognitive Science, University of California-San Diego, La Jolla, California, USA

    Andrea A. Chiba

  3. Department of Neurological Surgery and Center for Neuroscience, University of California-Davis, Davis, California, USA

    Robert F. Berman

  4. Department of Psychology, University of Illinois at Chicago, Chicago, Illinois, USA

    Michael E. Ragozzino

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Eichenbaum, H., Komorowski, R., MacDonald, C., Kraus, B., Robitsek, J. (2016). How Does the Hippocampus Support the Spatial and Temporal Attributes of Memory?. In: Jackson, P., Chiba, A., Berman, R., Ragozzino, M. (eds) The Neurobiological Basis of Memory. Springer, Cham. https://doi.org/10.1007/978-3-319-15759-7_2

Download citation

Publish with us

Policies and ethics

Search

Navigation