Skip to main content
SpringerLink
Log in

Theta Phase Coding in Human Hippocampus: A Combined Approach of a Computational Model and Human Brain Activity Analyses

  • Chapter
Dynamic Brain - from Neural Spikes to Behaviors (NN 2007)

Part of the book series: Lecture Notes in Computer Science ((LNTCS,volume 5286))

Included in the following conference series:

Abstract

The hippocampus is known to maintain episodic memory in humans, but its neural mechanism is an open question. The rat hippocampus is well investigated and known to have a particular neural synchronization between firing and local field potential (LFP) called ’theta phase precession’ that encodes spatio-temporal input sequences to the hippocampus. According to anatomical similarity between the rat and human hippocampus, similar dynamics are expected in the human hippocampus, while it is still unknown if the phase precession dynamics could contribute to memory formation of complex information in episodic memory. In this paper, we evaluate the human hippocampal dynamics by using a combined approach of a computational model and human brain activity analyses. A series of computational and experimental analyses provides integrative understanding of human hippocampal dynamics and its function.

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 34.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 49.95
Price excludes VAT (USA)
  • Compact, lightweight 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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Grillner, S.: The motor infrastructure: from ion channels to neuronal networks. Nat. Rev. Neurosci. 4(7), 573–586 (2003)

    Article  Google Scholar 

  2. Engel, A.K., Konig, P., Kreiter, A.K., Schillen, T.B., Singer, W.: Temporal coding in the visual cortex: new vistas on integration in the nervous system. Trends Neurosci. 15(6), 218–226 (1992)

    Article  Google Scholar 

  3. Squire, L.R.: Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99(2), 195–231 (1992)

    Article  Google Scholar 

  4. Marr, D.: Simple memory: A theory for archicortex. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 262, 23–81 (1971)

    Article  Google Scholar 

  5. van Hoesen, G.W.: The parahippocampal gyrus. New observations regarding its cortical connections in the monkey. Trends Neurosci. 5, 345–350 (1982)

    Google Scholar 

  6. Scoville, W.B., Milner, B.: Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry. 20, 11–21 (1957)

    Article  Google Scholar 

  7. Tulving, E.: Elements of episodic memory. Clarendon Press, Oxford (1983)

    Google Scholar 

  8. Bland, B.H.: The physiology and pharmacology of hippocampal formation theta rhythms. Progress in Neurobiology 26, 1–54 (1986)

    Article  Google Scholar 

  9. Ekstrom, A.D., Caplan, J.B., Ho, E., Shattuck, K., Fried, I., Kahana, M.J.: Human Hippocampal Theta Activity During Virtual Navigation. Hippocampus 15, 881–889 (2005)

    Article  Google Scholar 

  10. Kay, L.M.: Theta oscillations and sensorimotor performance. PNAS 102(10), 3863–3868 (2005)

    Article  Google Scholar 

  11. FitzHugh, R.: Impulses and physiological states in theoretical models of nerve membrane. Biophysical Journal 1, 445–466 (1961)

    Article  Google Scholar 

  12. Hoppensteadt, F.C.: An introduction to the mathematics of neurons. Cambridge University Press, Cambridge (1986)

    MATH  Google Scholar 

  13. O’Keefe, J., Recce, M.L.: Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330 (1993)

    Article  Google Scholar 

  14. 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  Google Scholar 

  15. Burgess, N., Barry, C., O’Keefe, J.: An oscillatory interference model of grid cell firing. Hippocampus 17(9), 801–812 (2007)

    Article  Google Scholar 

  16. 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  Google Scholar 

  17. Jensen, O., Lisman, J.E.: Hippocampal CA3 region predicts memory sequence: Accounting for the phase precession of place cells. Learning and Memory 3, 279–287 (1996)

    Article  Google Scholar 

  18. Wallenstein, G.V., Hasselmo, M.E.: GABAergic modulation of hippocampal population activity: Sequence learning, place field development, and the phase precession effect. Journal of Neurophysiology 78, 393–408 (1997)

    Google Scholar 

  19. Mehta, M.R., Lee, A.K., Wilson, M.A.: Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417, 741–746 (2002)

    Article  Google Scholar 

  20. Harris, K.D., Henze, D.A., Hirase, H., Leinekugel, X., Dragoi, G., Czuko, A., Buzsaki, G.: Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417, 738–741 (2002)

    Article  Google Scholar 

  21. Yamaguchi, Y.: A theory of hippocampal memory based on theta phase precession. Biol. Cybern. 89, 1–9 (2003)

    MATH  Google Scholar 

  22. Sato, N., Yamaguchi, Y.: Memory encoding by theta phase precession in the hippocampal network. Neural Comput. 15(10), 2379–2397 (2003)

    Article  MATH  Google Scholar 

  23. Wu, Z., Yamaguchi, Y.: Input-dependent learning rule for the memory of spatiotemporal sequences in hippocampal network with theta phase precession. Biol. Cybern. 90(2), 113–124 (2004)

    Article  MATH  Google Scholar 

  24. Wagatsuma, H., Yamaguchi, Y.: Cognitive map formation through sequence encoding by theta phase precession. Neural Comput. 16(12), 2665–2697 (2004)

    Article  MATH  Google Scholar 

  25. Hafting, T., Fyhn, M.H., Moser, M., Moser, E.I.: Phase precession and phase locking in entorhinal gridc ells. Society for Neuroscience Abstracts, Program No. 68.8 (2006)

    Google Scholar 

  26. Smith, M.L., Milner, B.: The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19, 781–793 (1981)

    Article  Google Scholar 

  27. Stepankova, K., Fenton, A.A., Pastalkova, E., Kalina, M., Bohbot, V.D.: Object-location impairment in patient with thermal lesions to the right or left hippocampus. Neuropsychologia 42, 1017–1028 (2004)

    Article  Google Scholar 

  28. Gaffan, D.: Scene-specific memory for objects: a model of episodic memory impairment in monkeys with fornix transection. J. Cognit. Neurosci. 6, 305–320 (1994)

    Article  Google Scholar 

  29. Eacott, M.J., Norman, G.: Integrated memory for object, place, and context in rats: a possible model of episodic-like memory? J. Neurosci. 24, 1948–1953 (2004)

    Article  Google Scholar 

  30. Suzuki, W.A., Amaral, D.G.: The perirhinal and parahippocampal cortices of the Macaque monkey: cortical afferents. J. Comp. Neurol. 350, 179–205 (1994)

    Article  Google Scholar 

  31. Epstein, R., Kanwisher, N.: A cortical representation of the local visual environment. Nature 392, 598–601 (1998)

    Article  Google Scholar 

  32. Rolls, E.T.: Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 9, 467–480 (1999)

    Article  Google Scholar 

  33. de Araujo, I.E., Rolls, E.T., Stringer, S.M.: A view model which accounts for the spatial fields of hippocampal primate spatial view cells and rat place cells. Hippocampus 11(6), 699–706 (2001)

    Article  Google Scholar 

  34. Sato, N., Yamaguchi, Y.: On-line formation of a hierarchical cognitive map for object-place association by theta phase coding. Hippocampus 15, 963–978 (2005)

    Article  Google Scholar 

  35. Rolls, E.T., Stringer, S.M., Trappenberg, T.P.: A unified model of spatial and episodic memory. Proc. R. Soc. Lond. B 269, 1087–1093 (2002)

    Article  Google Scholar 

  36. Sato, N., Yamaguchi, Y.: A hierarchical representation of object-place memory obtained by theta phase coding in the hippocampus: A computational study, Program No. 581.2, Society for Neuroscience Abstracts (2005)

    Google Scholar 

  37. Stevens, A., Coupe, P.: Distortion in judged spatial relations. Cognitive Psychology 10, 422–437 (1978)

    Article  Google Scholar 

  38. McNamara, T.P., Hardy, J.K., Hirtle, S.C.: Subjective hierarchies in spatial memory. Journal of Experimental Psychology: Learning, Memory, and Cognition 15(2), 211–227 (1989)

    Google Scholar 

  39. Sato, N., Yamaguchi, Y.: Theta synchronization networks emerge during human object-place memory encoding. NeuroReport 18(5), 419–424 (2007)

    Article  Google Scholar 

  40. Croft, R.J., Barry, R.J.: Removal of ocular artifact from EEG: a review. Neurophysical Clin. 30, 5–19 (2000)

    Article  Google Scholar 

  41. Summerfield, C., Mangels, J.: Coherent theta-band EEG activity predicts item-context binding during encoding. NeuroImage 24, 692–703 (2005)

    Article  Google Scholar 

  42. Sauseng, P., Klimesch, W., Schabus, M., Doppelmayr, M.: Fronto-parietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. Int. J. Psychophysiol. 57(2), 97–103 (2005)

    Article  Google Scholar 

  43. Klimesch, W., Doppelmayr, M., Russegger, H., Pachinger, T.: Theta band power in the human scalp EEG and the encoding of new information. Neuroreport 7(7), 1235–1240 (1996)

    Article  Google Scholar 

  44. Tanaka, S.C., Doya, K., Okada, G., Ueda, K., Okamoto, Y., Yamawaki, S.: Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nature Neurosci. 7(8), 887–893 (2004)

    Article  Google Scholar 

  45. Sato, N., Yamaguchi, Y.: An evidence of a hierarchical representation of object-place memory based on theta phase coding: A computational model- human experiment combined analysis, Program No. 366.25, Society for Neuroscience Abstracts (2006)

    Google Scholar 

  46. Kepecs, A., Uchida, N., Mainen, Z.F.: The Sniff as a Unit of Olfactory Processing. Chemical Senses 31(2), 167–179 (2006)

    Article  Google Scholar 

  47. Sato, N., Yamaguchi, Y.: EEG theta regulates eye saccade generation during human object-place memory encoding. In: Proc. the 1st international conference on cognitive neurodynamics & the 3rd shanghai international conference on physiological biophysics-cognitive neurodynamics (ICCN 2007 & SICPB 2007), Shanghai, China (2007)

    Google Scholar 

  48. Ulanovsky, N., Moss, C.: Hippocampal cellular and network activity in freely moving echolocating bats. Nat. Neurosci. 10(2), 224–233 (2007)

    Article  Google Scholar 

  49. Sato, N., Ozaki, J.T., Someya, Y., Anami, K., Ogawa, S., Mizuhara, H., Yamaguchi, Y.: Subsequent memory dependent EEG theta correlates with hippocampal BOLD response in human. Program No. 667.1, Society for Neuroscience Abstracts (2007)

    Google Scholar 

  50. Mizuhara, H., Wang, L.Q., Kobayashi, K., Yamaguchi, Y.: A long-range cortical network emerging with theta oscillation in a mental task. Neuroreport 15(8), 1233–1238 (2004)

    Article  Google Scholar 

  51. Daselaar, S.M., Prince, S.E., Cabeza, R.: When less means more: deactivations during encoding that predict subsequent memory. NeuroImage 23, 921–927 (2004)

    Article  Google Scholar 

  52. Klimesch, W., Doppelmayr, M., Stadler, W., Pollhuber, D., Sauseng, P., Rohm, D.: Episodic retrieval is reflected by a process specific increase in human electroencephalographic theta activity. Neurosci. Lett. 302(1), 49–52 (2001)

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Lab. for Dynamics of Emergent Intelligence, RIKEN Brain Science Institute, Saitama, 351-0198, Japan

    Naoyuki Sato

Authors
  1. Naoyuki Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Dipartimento di Fisica “E.R. Caianiello”, Università degli Studi di Salerno, Via S. Allende, 84081, Baronissi (SA), Italy

    Maria Marinaro  & Silvia Scarpetta  & 

  2. Laboratory for Dynamics of Emergent Intelligence, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, 351-0198, Saitama, Japan

    Yoko Yamaguchi

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Sato, N. (2008). Theta Phase Coding in Human Hippocampus: A Combined Approach of a Computational Model and Human Brain Activity Analyses . In: Marinaro, M., Scarpetta, S., Yamaguchi, Y. (eds) Dynamic Brain - from Neural Spikes to Behaviors. NN 2007. Lecture Notes in Computer Science, vol 5286. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-88853-6_2

Download citation

  • DOI: https://doi.org/10.1007/978-3-540-88853-6_2

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-540-88852-9

  • Online ISBN: 978-3-540-88853-6

  • eBook Packages: Computer ScienceComputer Science (R0)

Publish with us

Policies and ethics

Search

Navigation