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The role of inhibition in oscillatory wave dynamics in the cortex

Authors

  • Ying Xiao,

    1. Center for Neural Engineering, Department of Engineering Science and Mechanics, Pennsylvania State University, University Park, PA, USA
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  • Xiao-ying Huang,

    1. Department of Physiology and Biophysics, Georgetown University Medical Center, Washington, DC, USA
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  • Stephen Van Wert,

    1. Center for Neural Engineering, Department of Engineering Science and Mechanics, Pennsylvania State University, University Park, PA, USA
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  • Ernest Barreto,

    1. School of Physics, Astronomy, and Computational Sciences, The Center for Neural Dynamics and The Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA, USA
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  • Jian-young Wu,

    1. Department of Physiology and Biophysics, Georgetown University Medical Center, Washington, DC, USA
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  • Bruce J. Gluckman,

    1. Center for Neural Engineering, Department of Engineering Science and Mechanics, Pennsylvania State University, University Park, PA, USA
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  • Steven J. Schiff

    1. Center for Neural Engineering, Department of Engineering Science and Mechanics, Pennsylvania State University, University Park, PA, USA
    2. Department of Neurosurgery and Department of Physics, Pennsylvania State University, University Park, PA, USA
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    • Present address: W311 Millennium Science Complex, The Pennsylvania State University, University Park, PA 16802, USA


Steven J. Schiff, *present address below.
E-mail: sschiff@psu.edu

Abstract

Cortical oscillations arise during behavioral and mental tasks, and all temporal oscillations have particular spatial patterns. Studying the mechanisms that generate and modulate the spatiotemporal characteristics of oscillations is important for understanding neural information processing and the signs and symptoms of dynamical diseases of the brain. Nevertheless, it remains unclear how GABAergic inhibition modulates these oscillation dynamics. Using voltage-sensitive dye imaging, pharmacological methods, and tangentially cut occipital neocortical brain slices (including layers 3–5) of Sprague-Dawley rat, we found that GABAa disinhibition with bicuculline can progressively simplify oscillation dynamics in the presence of carbachol in a concentration-dependent manner. Additionally, GABAb disinhibition can further simplify oscillation dynamics after GABAa receptors are blocked. Both GABAa and GABAb disinhibition increase the synchronization of the neural network. Theta frequency (5–15-Hz) oscillations are reliably generated by using a combination of GABAa and GABAb antagonists alone. These theta oscillations have basic spatiotemporal patterns similar to those generated by carbachol/bicuculline. These results are illustrative of how GABAergic inhibition increases the complexity of patterns of activity and contributes to the regulation of the cortex.

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