Cortex
Volume 46, Issue 2 , Pages 256-263, February 2010

Sleep-dependent directional coupling between human neocortex and hippocampus

  • Tobias Wagner

      Affiliations

    • Department of Epileptology, University of Bonn, Germany
    • Helmholtz-Institute for Radiation and Nuclear Physics, University of Bonn, Germany
    • Corresponding Author InformationCorresponding author. Department of Epileptology, University of Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany.
  • ,
  • Nikolai Axmacher

      Affiliations

    • Department of Epileptology, University of Bonn, Germany
    • Life and Brain Center for Academic Research, University of Bonn, Germany
  • ,
  • Klaus Lehnertz

      Affiliations

    • Department of Epileptology, University of Bonn, Germany
    • Helmholtz-Institute for Radiation and Nuclear Physics, University of Bonn, Germany
    • Interdisciplinary Center for Complex Systems, University of Bonn, Germany
  • ,
  • Christian E. Elger

      Affiliations

    • Department of Epileptology, University of Bonn, Germany
    • Life and Brain Center for Academic Research, University of Bonn, Germany
  • ,
  • Jürgen Fell

      Affiliations

    • Department of Epileptology, University of Bonn, Germany

Received 25 November 2008; received in revised form 12 April 2009 and 18 May 2009; accepted 22 May 2009. published online 24 June 2009.

Action editor Mike Kopelman

Abstract 

Complex interactions between neocortex and hippocampus are the neural basis of memory formation. Two-step theories of memory formation suggest that initial encoding of novel information depends on the induction of rapid plasticity within the hippocampus, and is followed by a second sleep-dependent step of memory consolidation. These theories predict information flow from the neocortex into the hippocampus during waking state and in the reverse direction during sleep. However, experimental evidence that interactions between hippocampus and neocortex have a predominant direction which reverses during sleep rely on cross-correlation analysis of data from animal experiments and yielded inconsistent results. Here, we investigated directional coupling in intracranial EEG data from human subjects using a phase-modeling approach which is well suited to reveal functional interdependencies in oscillatory data. In general, we observed that the anterior hippocampus predominantly drives nearby and remote brain regions. Surprisingly, however, the influence of neocortical regions on the hippocampus significantly increased during sleep as compared to waking state. These results question the standard model of hippocampal–neocortical interactions and suggest that sleep-dependent consolidation is accomplished by an active retrieval of hippocampal information by the neocortex.

Keywords: EEG, Directionality, Sleep, Hippocampus, Neocortex

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PII: S0010-9452(09)00165-8

doi:10.1016/j.cortex.2009.05.012

Cortex
Volume 46, Issue 2 , Pages 256-263, February 2010