Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Segmentation of spatial experience by hippocampal theta sequences

Nature Neuroscience volume 15, pages 1032–1039 (2012)Cite this article

Subjects

Abstract

The encoding and storage of experience by the hippocampus is essential for the formation of episodic memories and the transformation of individual experiences into semantic structures such as maps and schemas. The rodent hippocampus compresses ongoing experience into repeating theta sequences, but the factors determining the content of theta sequences are not understood. Here we first show that the spatial paths represented by theta sequences in rats extend farther in front of the rat during acceleration and higher running speeds and begin farther behind the rat during deceleration. Second, the length of the path is directly related to the length of the theta cycle and the number of gamma cycles in it. Finally, theta sequences represent the environment in segments or 'chunks'. These results imply that information encoded in theta sequences is subject to powerful modulation by behavior and task variables. Furthermore, these findings suggest a potential mechanism for the cognitive 'chunking' of experience.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Distinct populations of theta sequences on the two-choice T maze.
Figure 2: Examples of ahead sequences while rats were located at the choice point.
Figure 3: Examples of ahead and behind sequences.
Figure 4: Characteristics of theta sequence ahead and behind length.
Figure 5: Theta period and gamma cycles vary as functions of path length.
Figure 6: Ahead length, behind length and path distribution vary according to landmarks on the maze.
Figure 7: Segmented representation of space by theta sequences.
Figure 8: Relationships between rat behavior and the represented path.

Similar content being viewed by others

References

  1. Cohen, N.J. & Eichenbaum, H. Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, Massachusetts, USA, 1993).

  2. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon Press, Oxford, UK, 1978).

  3. Hassabis, D., Kumaran, D., Vann, S.D. & Maguire, E.A. Patients with hippocampal amnesia cannot imagine new experiences. Proc. Natl. Acad. Sci. USA 104, 1726–1731 (2007).

    Article  CAS  Google Scholar 

  4. Schacter, D.L., Addis, D.R. & Buckner, R.L. Remembering the past to imagine the future: the prospective brain. Nat. Rev. Neurosci. 8, 657–661 (2007).

    Article  CAS  Google Scholar 

  5. Morris, G., Nevet, A., Arkadir, D., Vaadia, E. & Bergman, H. Midbrain dopamine neurons encode decisions for future action. Nat. Neurosci. 9, 1057–1063 (2006).

    Article  CAS  Google Scholar 

  6. Redish, A.D. Beyond the Cognitive Map: From Place Cells to Episodic Memory (MIT Press, Cambridge, Massachusetts, USA, 1999).

  7. Vanderwolf, C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407–418 (1969).

    Article  CAS  Google Scholar 

  8. Skaggs, W.E., McNaughton, B.L., Wilson, M.A. & Barnes, C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149–172 (1996).

    Article  CAS  Google Scholar 

  9. Dragoi, G. & Buzsaki, G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50, 145–157 (2006).

    Article  CAS  Google Scholar 

  10. Foster, D.J. & Wilson, M.A. Hippocampal theta sequences. Hippocampus 17, 1093–1099 (2007).

    Article  Google Scholar 

  11. Tsodyks, M.V., Skaggs, W.E., Sejnowski, T.J. & McNaughton, B.L. Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus 6, 271–280 (1996).

    Article  CAS  Google Scholar 

  12. Jensen, O. & Lisman, J.E. Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn. Mem. 3, 279–287 (1996).

    Article  CAS  Google Scholar 

  13. Maurer, A.P. & McNaughton, B.L. Network and intrinsic cellular mechanisms underlying theta phase precession of hippocampal neurons. Trends Neurosci. 30, 325–333 (2007).

    Article  CAS  Google Scholar 

  14. Malhotra, S., Cross, R.W.A. & van der Meer, M.A.A. Theta phase precession beyond the hippocampus. Rev. Neurosci. 23, 39–65 (2012).

    Article  Google Scholar 

  15. O'Keefe, J. & Recce, M. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330 (1993).

    Article  CAS  Google Scholar 

  16. Geisler, C., Robbe, D., Zugaro, M., Sirota, A. & Buzsáki, G. Hippocampal place cell assemblies are speed-controlled oscillators. Proc. Natl. Acad. Sci. USA 104, 8149–8154 (2007).

    Article  CAS  Google Scholar 

  17. Schmidt, R. et al. Single-trial phase precession in the hippocampus. J. Neurosci. 29, 13232–13241 (2009).

    Article  CAS  Google Scholar 

  18. Geisler, C. et al. Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus. Proc. Natl. Acad. Sci. USA 107, 7957–7962 (2010).

    Article  CAS  Google Scholar 

  19. Gupta, A.S., Van der Meer, M.A.A., Touretzky, D.S. & Redish, A.D. Hippocampal replay is not a simple function of experience. Neuron 65, 695–705 (2010).

    Article  CAS  Google Scholar 

  20. Foster, D.J. & Wilson, M.A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680–683 (2006).

    Article  CAS  Google Scholar 

  21. Diba, K. & Buzsáki, G. Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 10, 1241–1242 (2007).

    Article  CAS  Google Scholar 

  22. Carr, M.F., Jadhav, S.P. & Frank, L.M. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 14, 147–153 (2011).

    Article  CAS  Google Scholar 

  23. Gupta, A.S. Behavioral Correlates of Hippocampal Neural Sequences PhD thesis, (Carnegie Mellon Univ, 2011).

  24. Johnson, A. & Redish, A.D. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27, 12176–12189 (2007).

    Article  CAS  Google Scholar 

  25. Gothard, K.M., Hoffman, K.L., Battaglia, F.P. & McNaughton, B.L. Dentate gyrus and CA1 ensemble activity during spatial reference frame shifts in the presence and absence of visual input. J. Neurosci. 21, 7284–7292 (2001).

    Article  CAS  Google Scholar 

  26. Maurer, A.P., Burke, S.N., Lipa, P., Skaggs, W.E. & Barnes, C.A. Greater running speeds result in altered hippocampal phase sequence dynamics. Hippocampus 22, 737–747 (2012).

    Article  Google Scholar 

  27. Lisman, J. & Redish, A.D. Prediction, sequences and the hippocampus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1193–1201 (2009).

    Article  Google Scholar 

  28. Royer, S., Sirota, A., Patel, J. & Buzsáki, G. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J. Neurosci. 30, 1777–1787 (2010).

    Article  CAS  Google Scholar 

  29. van der Meer, M.A.A. & Redish, A.D. Theta phase precession in rat ventral striatum links place and reward information. J. Neurosci. 31, 2843–2854 (2011).

    Article  CAS  Google Scholar 

  30. Wood, E.R., Dudchenko, P.A., Robitsek, R.J. & Eichenbaum, H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623–633 (2000).

    Article  CAS  Google Scholar 

  31. Frank, L.M., Brown, E.N. & Wilson, M. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169–178 (2000).

    Article  CAS  Google Scholar 

  32. Ferbinteanu, J. & Shapiro, M.L. Prospective and retrospective memory coding in the hippocampus. Neuron 40, 1227–1239 (2003).

    Article  CAS  Google Scholar 

  33. Ji, D. & Wilson, M.A. Firing rate dynamics in the hippocampus induced by trajectory learning. J. Neurosci. 28, 4679–4689 (2008).

    Article  CAS  Google Scholar 

  34. Yartsev, M.M. Dissociating the effects of past and future on neural encoding of sequences in the hippocampus. J. Neurosci. 28, 8383–8384 (2008).

    Article  CAS  Google Scholar 

  35. Buzsáki, G. Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15, 827–840 (2005).

    Article  Google Scholar 

  36. Hasselmo, M.E. The role of hippocampal regions CA3 and CA1 in matching entorhinal input with retrieval of associations between objects and context: Theoretical comment on Lee et al. (2005). Behav. Neurosci. 119, 342–345 (2005).

    Article  Google Scholar 

  37. Hasselmo, M.E. A model of episodic memory: mental time travel along encoded trajectories using grid cells. Neurobiol. Learn. Mem. 92, 559–573 (2009).

    Article  Google Scholar 

  38. Muller, R.U. & Kubie, J.L. The firing of hippocampal place cells predicts the future position of freely moving rats. J. Neurosci. 9, 4101–4110 (1989).

    Article  CAS  Google Scholar 

  39. Battaglia, F.P., Sutherland, G.R. & McNaughton, B.L. Local sensory cues and place cell directionality: additional evidence of prospective coding in the hippocampus. J. Neurosci. 24, 4541–4550 (2004).

    Article  CAS  Google Scholar 

  40. Huxter, J.R., Senior, T.J., Allen, K. & Csicsvari, J. Theta phase–specific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat. Neurosci. 11, 587–594 (2008).

    Article  CAS  Google Scholar 

  41. Lisman, J.E. & Idiart, M.A. Storage of 7 ± 2 short-term memories in oscillatory subcycles. Science 267, 1512–1515 (1995).

    Article  CAS  Google Scholar 

  42. Lisman, J. The theta/gamma discrete phase code occurring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 15, 913–922 (2005).

    Article  Google Scholar 

  43. Miller, G.A. The magical number seven, plus or minus two: some limits on our capacity for processing information. Psychol. Rev. 63, 81–97 (1956).

    Article  CAS  Google Scholar 

  44. Newell, A. Unified Theories of Cognition (Harvard University Press, 1990).

  45. Newell, A. & Simon, H. Human Problem Solving (Prentice-Hall, Englewood Cliffs, New Jersey, USA, 1972).

  46. Mulder, A.B., Tabuchi, E. & Wiener, S.I. Neurons in hippocampal afferent zones of rat striatum parse routes into multi-pace segments during maze navigation. Eur. J. Neurosci. 19, 1923–1932 (2004).

    Article  Google Scholar 

  47. Robbe, D. & Buzsáki, G. Alteration of theta timescale dynamics of hippocampal place cells by a cannabinoid is associated with memory impairment. J. Neurosci. 29, 12597–12605 (2009).

    Article  CAS  Google Scholar 

  48. Davidson, T.J., Kloosterman, F. & Wilson, M.A. Hippocampal replay of extended experience. Neuron 63, 497–507 (2009).

    Article  CAS  Google Scholar 

  49. Jackson, J.C., Johnson, A. & Redish, A.D. Hippocampal sharp waves and reactivation during awake states depend on repeated sequential experience. J. Neurosci. 26, 12415–12426 (2006).

    Article  CAS  Google Scholar 

  50. Schmitzer-Torbert, N.C., Jackson, J., Henze, D., Harris, K. & Redish, A.D. Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131, 1–11 (2005).

    Article  CAS  Google Scholar 

  51. Schmitzer-Torbert, N. & Redish, A.D. Neuronal activity in the rodent dorsal striatum in sequential navigation: separation of spatial and reward responses on the multiple T task. J. Neurophysiol. 91, 2259–2272 (2004).

    Article  Google Scholar 

  52. Zhang, K., Ginzburg, I., McNaughton, B.L. & Sejnowski, T.J. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J. Neurophysiol. 79, 1017–1044 (1998).

    Article  CAS  Google Scholar 

  53. Janabi-Sharifi, F., Hayward, V. & Chen, C.S.J. Discrete-time adaptive windowing for velocity estimation. IEEE Trans. Control Syst. Technol. 8, 1003–1009 (2000).

    Article  Google Scholar 

Download references

Acknowledgements

We thank C. Boldt, K.D. Seeland and A.P. Steiner for technical assistance and A. Johnson and the members of the Redish lab for discussion. This work was supported by US National Institutes of Health grants (R01 MH-080318 and F30 MH-091821), the Pennsylvania Department of Health and a US National Science Foundation Integrative Graduate Education and Research Traineeship grant (DGE-0549352).

Author information

Authors and Affiliations

  1. Robotics Institute, Carnegie Mellon University, Pittsburgh, Pennsylvania, USA

    Anoopum S Gupta

  2. Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, Pennsylvania, USA

    Anoopum S Gupta & David S Touretzky

  3. School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA

    Anoopum S Gupta

  4. Department of Biology, University of Waterloo, Waterloo, Ontario, Canada

    Matthijs A A van der Meer

  5. Centre for Theoretical Neuroscience, University of Waterloo, Waterloo, Ontario, Canada

    Matthijs A A van der Meer

  6. Computer Science Department, Carnegie Mellon University, Pittsburgh, Pennsylvania, USA

    David S Touretzky

  7. Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota, USA

    A David Redish

Authors
  1. Anoopum S Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthijs A A van der Meer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David S Touretzky
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A David Redish
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.S.G., M.A.A.v.d.M. and A.D.R. designed the experiment; D.S.T. and A.D.R. supervised the project; A.S.G. and M.A.A.v.d.M. carried out the experiments; A.S.G. analyzed the data; and A.S.G., M.A.A.v.d.M., D.S.T. and A.D.R. wrote the paper.

Corresponding author

Correspondence to A David Redish.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–9 (PDF 2447 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gupta, A., van der Meer, M., Touretzky, D. et al. Segmentation of spatial experience by hippocampal theta sequences. Nat Neurosci 15, 1032–1039 (2012). https://doi.org/10.1038/nn.3138

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3138

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing