Recurrent excitatory postsynaptic potentials induced by synchronized fast cortical oscillations

DOI Web Site 2 Citations
  • Miles A. Whittington
    Department of Physiology and Biophysics, Imperial College School of Medicine at St. Mary’s, London W2 1PG, United Kingdom; IBM Research Division, T. J. Watson Research Center, Yorktown Heights, NY 10598; Department of Neurology, Columbia University, New York, NY 10032; and Department of Physiology, The Medical School, University of Birmingham, Birmingham B15 2TT, United Kingdom
  • Roger D. Traub
    Department of Physiology and Biophysics, Imperial College School of Medicine at St. Mary’s, London W2 1PG, United Kingdom; IBM Research Division, T. J. Watson Research Center, Yorktown Heights, NY 10598; Department of Neurology, Columbia University, New York, NY 10032; and Department of Physiology, The Medical School, University of Birmingham, Birmingham B15 2TT, United Kingdom
  • Howard J. Faulkner
    Department of Physiology and Biophysics, Imperial College School of Medicine at St. Mary’s, London W2 1PG, United Kingdom; IBM Research Division, T. J. Watson Research Center, Yorktown Heights, NY 10598; Department of Neurology, Columbia University, New York, NY 10032; and Department of Physiology, The Medical School, University of Birmingham, Birmingham B15 2TT, United Kingdom
  • Ian M. Stanford
    Department of Physiology and Biophysics, Imperial College School of Medicine at St. Mary’s, London W2 1PG, United Kingdom; IBM Research Division, T. J. Watson Research Center, Yorktown Heights, NY 10598; Department of Neurology, Columbia University, New York, NY 10032; and Department of Physiology, The Medical School, University of Birmingham, Birmingham B15 2TT, United Kingdom
  • John G. R. Jefferys
    Department of Physiology and Biophysics, Imperial College School of Medicine at St. Mary’s, London W2 1PG, United Kingdom; IBM Research Division, T. J. Watson Research Center, Yorktown Heights, NY 10598; Department of Neurology, Columbia University, New York, NY 10032; and Department of Physiology, The Medical School, University of Birmingham, Birmingham B15 2TT, United Kingdom

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<jats:p>Gamma frequency (about 20–70 Hz) oscillations occur during novel sensory stimulation, with tight synchrony over distances of at least 7 mm. Synchronization in the visual system has been proposed to reflect coactivation of different parts of the visual field by a single spatially extended object. We have shown that intracortical mechanisms, including spike doublet firing by interneurons, can account for tight long-range synchrony. Here we show that synchronous gamma oscillations in two sites also can cause long-lasting (>1 hr) potentiation of recurrent excitatory synapses. Synchronous oscillations lasting >400 ms in hippocampal area CA1 are associated with an increase in both excitatory postsynaptic potential (EPSP) amplitude and action potential afterhyperpolarization size. The resulting EPSPs stabilize and synchronize a prolonged beta frequency (about 10–25 Hz) oscillation. The changes in EPSP size are not expressed during non-oscillatory behavior but reappear during subsequent gamma-oscillatory events. We propose that oscillation-induced EPSPs serve as a substrate for memory, whose expression either enhances or blocks synchronization of spatially separated sites. This phenomenon thus provides a dynamical mechanism for storage and retrieval of stimulus-specific neuronal assemblies.</jats:p>

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