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GABAB receptor-mediated presynaptic inhibition reverses inter-columnar covariability of synaptic actions by intracortical axons in the rat barrel cortex

Authors

  • Hajime Sato,

    1. Department of Neuroscience and Oral Physiology, Osaka University Graduate School of Dentistry, Suita, Osaka, Japan
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    • H.S., H.T. and M.S. contributed equally to this work.
  • Hiroki Toyoda,

    1. Department of Neuroscience and Oral Physiology, Osaka University Graduate School of Dentistry, Suita, Osaka, Japan
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    • H.S., H.T. and M.S. contributed equally to this work.
  • Mitsuru Saito,

    1. Department of Neuroscience and Oral Physiology, Osaka University Graduate School of Dentistry, Suita, Osaka, Japan
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    • H.S., H.T. and M.S. contributed equally to this work.
  • Masayuki Kobayashi,

    1. Department of Pharmacology, Nihon University School of Dentistry, Tokyo, Japan
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  • Daniel Althof,

    1. Department of Neuroanatomy, Institute of Anatomy and Cell Biology, University of Freiburg, Freiburg, Germany
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  • Ákos Kulik,

    1. Department of Neuroanatomy, Institute of Anatomy and Cell Biology, University of Freiburg, Freiburg, Germany
    2. Department of Physiology II, University of Freiburg, Freiburg, Germany
    3. BIOSS Centre for Biological Studies, University of Freiburg, Freiburg, Germany
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  • Youngnam Kang

    Corresponding author
    • Department of Neuroscience and Oral Physiology, Osaka University Graduate School of Dentistry, Suita, Osaka, Japan
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Correspondence: Youngnam Kang, as above.

E-mail: kang@dent.osaka-u.ac.jp.

Abstract

Intracortical axons originating from pyramidal cells in layer 3 of the rat somatosensory cortex are shared between adjacent columns, and receive the presynaptic inhibition that is mediated by the GABAB receptor. Synaptic actions by intracortical axons of single layer 3 pyramidal cells covary between the two adjacent columns in response to stimulation of layer 3 of either column. We examined whether GABAB receptor-mediated presynaptic inhibition affects the covariability of synaptic actions by intracortical axons between adjacent columns in slice preparations of the rat barrel cortex. Paired stimulations of superficial layer 3 evoked first and second excitatory postsynaptic currents (EPSCs) of varying amplitudes, yielding varying paired-pulse depression of EPSCs in layer 3 pyramidal cells that were located in the stimulated column, but not in its adjacent column. The amplitude of the second EPSC was inversely proportional to that of the first EPSC in layer 3 pyramidal cells in the stimulated column, yielding a negative correlation coefficient between the first and second EPSCs. Baclofen and CGP55845 attenuated paired-pulse depression and abolished the inverse relationship. Simultaneous recordings from two layer 3 pyramidal cells in the stimulated and adjacent columns revealed a positive correlation between the paired first EPSC amplitudes and a negative correlation between the paired second EPSC amplitudes, which, respectively, indicate the positive and negative covariability of synaptic actions by intracortical axons between the two adjacent columns. These results suggest that GABAB receptor-mediated presynaptic inhibition can reverse the positive covariability of inter-columnar synaptic actions, which may serve as a basis for inter-columnar desynchronisation.

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