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Rhinal-Hippocampal Information Flow Reverses Between Memory Encoding and Retrieval

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Neural Information Processing (ICONIP 2016)

Part of the book series: Lecture Notes in Computer Science ((LNTCS,volume 9947))

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Abstract

The medial temporal lobe is crucial for the encoding and retrieval of episodic long-term memories. It is widely assumed that memory encoding is associated with information transfer from sensory regions via the rhinal cortex into the hippocampus. Retrieval of information should then be associated with transfer in the reverse direction. However, experimental evidence for this mechanism is still lacking. Here, we show in human intracranial EEG data during two independent recognition memory paradigms that rhinal-hippocampal information flow significantly changes its directionality from encoding to retrieval. Using a novel phase-based method to analyze directional coupling of oscillations, coupling values were more positive (i.e., from rhinal cortex to the hippocampus) during encoding as compared to retrieval. These effects were observed in the delta (1–3 Hz) range where rhinal-hippocampal post-stimulus phase synchronization increased most robustly across both experiments.

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References

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

    Article  Google Scholar 

  2. Squire, L.R., Stark, C.E., Clark, R.E.: The medial temporal lobe. Ann. Rev. Neurosci. 27, 279–306 (2004)

    Article  Google Scholar 

  3. Eichenbaum, H., Yonelinas, A.P., Ranganath, C.: The medial temporal lobe and recognition memory. Ann. Rev. Neurosci. 30, 123–152 (2007)

    Article  Google Scholar 

  4. Hasselmo, M.E.: What is the function of hippocampal theta rhythm? Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 15, 936–949 (2005)

    Article  Google Scholar 

  5. Carr, M.F., Frank, L.M.: A single microcircuit with multiple functions: state dependent information processing in the hippocampus. Curr. Opin. Neurobiol. 22, 704–708 (2012)

    Article  Google Scholar 

  6. Buzsáki, G., Draguhn, A.: Neuronal oscillations in cortical networks. Science 304, 1926–1929 (2004)

    Article  Google Scholar 

  7. Fell, J., Axmacher, N.: The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 12, 105–118 (2011)

    Article  Google Scholar 

  8. Osterhage, H., Mormann, F., Wagner, T., Lehnertz, K.: Detecting directional coupling in the human epileptic brain: limitations and potential pitfalls. Phys. Rev. E 77, 011914 (2008)

    Article  Google Scholar 

  9. Rosenblum, M.G., Pikovsky, A.S.: Detecting direction of coupling in interacting oscillators. Phys. Rev. E 64, 045202 (2001)

    Article  Google Scholar 

  10. Wagner, T., Fell, J., Lehnertz, K.: Detection of transient directional couplings based on phase synchronization. New J. Phys. 12, 053031 (2010)

    Article  Google Scholar 

  11. Maris, E., Oostenveld, R.: Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 164, 177–190 (2007)

    Article  Google Scholar 

  12. Fernández, G., Effern, A., Grunwald, T., Pezer, N., Lehnertz, K., Dümpelmann, M., Van Roost, D., Elger, C.E.: Real-time tracking of memory formation in the human rhinal cortex and hippocampus. Science 285, 1582–1585 (1999)

    Article  Google Scholar 

  13. Axmacher, N., Haupt, S., Fernández, G., Elger, C.E., Fell, J.: The role of sleep in declarative memory consolidation - direct evidence by intracranial EEG. Cereb. Cortex 18, 500–507 (2008)

    Article  Google Scholar 

  14. Axmacher, N., Cohen, M.X., Fell, J., Haupt, S., Dümpelmann, M., Elger, C.E., Schlaepfer, T.E., Lenartz, D., Sturm, V., Ranganath, C.: Intracranial EEG correlates of expectancy and memory formation in the human hippocampus and nucleus accumbens. Neuron 65, 541–549 (2010)

    Article  Google Scholar 

  15. Lachaux, J.P., Rodriguez, E., Martinerie, J., Varela, F.J.: Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194–208 (1999)

    Article  Google Scholar 

  16. Bruns, A.: Fourier-, Hilbert- and wavelet-based signal analysis: are they really different approaches? J. Neurosci. Methods 137, 321–332 (2004)

    Article  Google Scholar 

  17. Kralemann, B., Cimponeriu, L., Rosenblum, M.G., Pikovsky, A.S., Mrowka, R.: Phase dynamics of coupled oscillators reconstructed from data. Phys. Rev. E 77, 066205 (2008)

    Article  MathSciNet  Google Scholar 

  18. Staresina, B.P., Fell, J., Do Lam, A.T., Axmacher, N., Henson, R.N.: Memory signals are temporally dissociated in and across human hippocampus and perirhinal cortex. Nat. Neurosci. 15, 1167–1173 (2012)

    Article  Google Scholar 

  19. Mormann, F., Kornblith, S., Quiroga, R.Q., Kraskov, A., Cerf, M., Fried, I., Koch, C.: Latency and selectivity of single neurons indicate hierarchical processing in the human medial temporal lobe. J. Neurosci. 28, 8865–8872 (2008)

    Article  Google Scholar 

  20. Nobre, A.C., McCarthy, G.: Language-related field potentials in the anterior-medial temporal lobe: II. Effects of word type and semantic priming. J. Neurosci. 15, 1090–1098 (1995)

    Google Scholar 

  21. Grunwald, T., Beck, H., Lehnertz, K., Blümcke, I., Pezer, N., Kurthen, M., Fernández, G., Van Roost, D., Heinze, H.J., Kutas, M., Elger, C.E.: Evidence relating human verbal memory to hippocampal N-methyl-D-asparate receptors. Proc. Natl. Acad. Sci. U.S.A. 96, 12085–12089 (1999)

    Article  Google Scholar 

  22. Jutras, M.J., Buffalo, E.A.: Synchronous neural activity and memory formation. Curr. Opin. Neurobiol. 20, 150–155 (2010)

    Article  Google Scholar 

  23. Fell, J., Ludowig, E., Rosburg, T., Axmacher, N., Elger, C.E.: Phase-locking within human mediotemporal lobe predicts memory formation. Neuroimage 43, 410–419 (2008)

    Article  Google Scholar 

  24. Lega, B.C., Jacobs, J., Kahana, M.: Human hippocampal theta oscillations and the formation of episodic memories. Hippocampus 22, 748–761 (2011)

    Article  Google Scholar 

  25. Clemens, Z., Borbély, C., Weiss, B., Eröss, L., Szücs, A., Kelemen, A., Fabó, D., Rásonyi, G., Janszky, J., Halász, P.: Increased mesiotemporal delta activity characterizes virtual navigation in humans. Neurosci. Res. 76, 67–75 (2013)

    Article  Google Scholar 

  26. Watrous, A.J., Tandon, N., Conner, C.R., Pieters, T., Ekstrom, A.D.: Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nat. Neurosci. 16, 349–356 (2013)

    Article  Google Scholar 

  27. Watrous, A.J., Lee, D.J., Izadi, A., Gurkoff, G.G., Shahlaie, K., Ekstrom, A.D.: A comparative study of human and rat hippocampal low-frequency oscillations during spatial navigation. Hippocampus 23, 656–661 (2013)

    Article  Google Scholar 

  28. Hanslmayr, S., Staudigl, T.: How brain oscillations form memories - a processing based perspective on oscillatory subsequent memory effects. Neuroimage 85, 648–655 (2014)

    Article  Google Scholar 

  29. Buzsáki, G., Logothetis, N., Singer, W.: Scaling brain size, keeping timing, evolutionary preservation of brain rhythms. Neuron 80, 751–764 (2013)

    Article  Google Scholar 

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Author information

Authors and Affiliations

  1. Department of Epileptology, University of Bonn, Bonn, Germany

    Juergen Fell, Tobias Wagner, Bernhard P. Staresina & Christian E. Elger

  2. Department of Psychology, University of Birmingham, Birmingham, UK

    Bernhard P. Staresina

  3. Center for Neuroscience and Department of Psychology, University of California, Davis, USA

    Charan Ranganath

  4. Department of Psychology, Ruhr-University Bochum, Bochum, Germany

    Nikolai Axmacher

  5. German Center for Neurodegenerative Diseases, Bonn, Germany

    Nikolai Axmacher

Authors
  1. Juergen Fell
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  2. Tobias Wagner
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  3. Bernhard P. Staresina
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  4. Charan Ranganath
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  5. Christian E. Elger
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  6. Nikolai Axmacher
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Corresponding author

Correspondence to Juergen Fell .

Editor information

Editors and Affiliations

  1. The University of Tokyo, Tokyo, Japan

    Akira Hirose

  2. Kobe University, Kobe, Japan

    Seiichi Ozawa

  3. Okinawa Institute of Science and Technology Graduate University, Onna, Japan

    Kenji Doya

  4. Nara Institute of Science and Technology, Ikoma, Japan

    Kazushi Ikeda

  5. Kyungpook National University, Daegu, Korea (Republic of)

    Minho Lee

  6. Chinese Academy of Sciences, Beijing, China

    Derong Liu

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Fell, J., Wagner, T., Staresina, B.P., Ranganath, C., Elger, C.E., Axmacher, N. (2016). Rhinal-Hippocampal Information Flow Reverses Between Memory Encoding and Retrieval. In: Hirose, A., Ozawa, S., Doya, K., Ikeda, K., Lee, M., Liu, D. (eds) Neural Information Processing. ICONIP 2016. Lecture Notes in Computer Science(), vol 9947. Springer, Cham. https://doi.org/10.1007/978-3-319-46687-3_11

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  • DOI: https://doi.org/10.1007/978-3-319-46687-3_11

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  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-46686-6

  • Online ISBN: 978-3-319-46687-3

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