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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Scoville, W.B., Milner, B.: Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11–21 (1957)
Squire, L.R., Stark, C.E., Clark, R.E.: The medial temporal lobe. Ann. Rev. Neurosci. 27, 279–306 (2004)
Eichenbaum, H., Yonelinas, A.P., Ranganath, C.: The medial temporal lobe and recognition memory. Ann. Rev. Neurosci. 30, 123–152 (2007)
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)
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)
Buzsáki, G., Draguhn, A.: Neuronal oscillations in cortical networks. Science 304, 1926–1929 (2004)
Fell, J., Axmacher, N.: The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 12, 105–118 (2011)
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)
Rosenblum, M.G., Pikovsky, A.S.: Detecting direction of coupling in interacting oscillators. Phys. Rev. E 64, 045202 (2001)
Wagner, T., Fell, J., Lehnertz, K.: Detection of transient directional couplings based on phase synchronization. New J. Phys. 12, 053031 (2010)
Maris, E., Oostenveld, R.: Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 164, 177–190 (2007)
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)
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)
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)
Lachaux, J.P., Rodriguez, E., Martinerie, J., Varela, F.J.: Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194–208 (1999)
Bruns, A.: Fourier-, Hilbert- and wavelet-based signal analysis: are they really different approaches? J. Neurosci. Methods 137, 321–332 (2004)
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)
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)
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)
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)
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)
Jutras, M.J., Buffalo, E.A.: Synchronous neural activity and memory formation. Curr. Opin. Neurobiol. 20, 150–155 (2010)
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)
Lega, B.C., Jacobs, J., Kahana, M.: Human hippocampal theta oscillations and the formation of episodic memories. Hippocampus 22, 748–761 (2011)
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)
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)
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)
Hanslmayr, S., Staudigl, T.: How brain oscillations form memories - a processing based perspective on oscillatory subsequent memory effects. Neuroimage 85, 648–655 (2014)
Buzsáki, G., Logothetis, N., Singer, W.: Scaling brain size, keeping timing, evolutionary preservation of brain rhythms. Neuron 80, 751–764 (2013)
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing AG
About this paper
Cite this paper
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
Download citation
DOI: https://doi.org/10.1007/978-3-319-46687-3_11
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-46686-6
Online ISBN: 978-3-319-46687-3
eBook Packages: Computer ScienceComputer Science (R0)