The soma and neurites of primary afferent neurons in the guinea-pig intestine respond differentially to deformation

Authors

  • W. A. A. Kunze,

    Corresponding author
    1. Department of Anatomy and Cell Biology, University of Melbourne, Parkville, Victoria 3010, Australia
    • Corresponding author
      W. A. A. Kunze: Department of Anatomy & Cell Biology, University of Melbourne, Parkville, Victoria 3010, Australia. Email: w.kunze@anatomy.unimelb.edu.au

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  • N. Clerc,

    1. Laboratoire de Neurobiologie, CNRS, 31 Ch J. Aiguier, 13402 Marseille Cedex 20, France
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  • J. B. Furness,

    1. Department of Anatomy and Cell Biology, University of Melbourne, Parkville, Victoria 3010, Australia
    2. Howard Florey Institute, University of Melbourne, Parkville, Victoria 3010, Australia
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  • M. Gola

    1. Department of Anatomy and Cell Biology, University of Melbourne, Parkville, Victoria 3010, Australia
    2. Laboratoire de Neurobiologie, CNRS, 31 Ch J. Aiguier, 13402 Marseille Cedex 20, France
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Abstract

  • 1Intrinsic primary afferent neurons in the small intestine are exposed to distortion of their processes and of their cell bodies. Recordings of mechanosensitivity have previously been made from these neurons using intracellular microelectrodes, but this form of recording has not permitted detection of generator potentials from the processes, or of responses to cell body distortion.
  • 2We have developed a technique to record from enteric neurons in situ using patch electrodes. The mechanical stability of the patch recordings has allowed recording in cell-attached and whole cell configuration during imposed movement of the neurons.
  • 3Pressing with a fine probe initiated generator potentials (14 ± 9 mV) from circumscribed regions of the neuron processes within the same myenteric ganglion, at distances from 100 to 500 μm from the cell body that was patched. Generator potentials persisted when synaptic transmission was blocked with high Mg2+, low Ca2+ solution.
  • 4Soma distortion, by pressing down with the whole cell recording electrode, inhibited action potential firing. Consistent with this, moderate intra-electrode pressure (10 mbar; 1 kPa) increased the opening probability of large-conductance (BK) potassium channels, recorded in cell-attached mode, but suction was not effective. In outside-out patches, suction, but not pressure, increased channel opening probability. Mechanosensitive BK channels have not been identified on other neurons.
  • 5The BK channels had conductances of 195 ± 25 pS. Open probability was increased by depolarization, with a half-maximum activation at a patch potential of 20 mV and a slope factor of 10 mV. Channel activity was blocked by charybdotoxin (20 nM).
  • 6Stretch that increased membrane area under the electrode by 15 % was sufficient to double open probability. Similar changes in membrane area occur when the intestine changes diameter and wall tension under physiological conditions. Thus, the intestinal intrinsic primary afferent neurons are detectors of neurite distortion and of compression of the soma, these stimuli having opposite effects on neuron excitability.

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