Low-intensity repetitive magnetic stimulation lowers action potential threshold and increases spike firing in layer 5 pyramidal neurons in vitro

Alex Tang, I. Hong, L.J. Boddington, Andrew Garrett, S. Etherington, J.N.J. Reynolds, Jennifer Rodger

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    Abstract

    © 2016 IBRORepetitive transcranial magnetic stimulation (rTMS) has become a popular method of modulating neural plasticity in humans. Clinically, rTMS is delivered at high intensities to modulate neuronal excitability. While the high-intensity magnetic field can be targeted to stimulate specific cortical regions, areas adjacent to the targeted area receive stimulation at a lower intensity and may contribute to the overall plasticity induced by rTMS. We have previously shown that low-intensity rTMS induces molecular and structural plasticity in vivo, but the effects on membrane properties and neural excitability have not been investigated. Here we investigated the acute effect of low-intensity repetitive magnetic stimulation (LI-rMS) on neuronal excitability and potential changes on the passive and active electrophysiological properties of layer 5 pyramidal neurons in vitro. Whole-cell current clamp recordings were made at baseline prior to subthreshold LI-rMS (600 pulses of iTBS, n = 9 cells from 7 animals) or sham (n = 10 cells from 9 animals), immediately after stimulation, as well as 10 and 20 min post-stimulation. Our results show that LI-rMS does not alter passive membrane properties (resting membrane potential and input resistance) but hyperpolarises action potential threshold and increases evoked spike-firing frequency. Increases in spike firing frequency were present throughout the 20 min post-stimulation whereas action potential (AP) threshold hyperpolarization was present immediately after stimulation and at 20 min post-stimulation. These results provide evidence that LI-rMS alters neuronal excitability of excitatory neurons. We suggest that regions outside the targeted region of high-intensity rTMS are susceptible to neuromodulation and may contribute to rTMS-induced plasticity.
    Original languageEnglish
    Pages (from-to)64-71
    Number of pages8
    JournalNeuroscience
    Volume335
    Early online date24 Aug 2016
    DOIs
    Publication statusPublished - 29 Oct 2016

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    Pyramidal Cells
    Action Potentials
    Neuronal Plasticity
    Membranes
    Transcranial Magnetic Stimulation
    Magnetic Fields
    Membrane Potentials
    Neurons
    In Vitro Techniques

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    Tang, Alex ; Hong, I. ; Boddington, L.J. ; Garrett, Andrew ; Etherington, S. ; Reynolds, J.N.J. ; Rodger, Jennifer. / Low-intensity repetitive magnetic stimulation lowers action potential threshold and increases spike firing in layer 5 pyramidal neurons in vitro. In: Neuroscience. 2016 ; Vol. 335. pp. 64-71.
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    Low-intensity repetitive magnetic stimulation lowers action potential threshold and increases spike firing in layer 5 pyramidal neurons in vitro. / Tang, Alex; Hong, I.; Boddington, L.J.; Garrett, Andrew; Etherington, S.; Reynolds, J.N.J.; Rodger, Jennifer.

    In: Neuroscience, Vol. 335, 29.10.2016, p. 64-71.

    Research output: Contribution to journalArticle

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    AU - Tang, Alex

    AU - Hong, I.

    AU - Boddington, L.J.

    AU - Garrett, Andrew

    AU - Etherington, S.

    AU - Reynolds, J.N.J.

    AU - Rodger, Jennifer

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    AB - © 2016 IBRORepetitive transcranial magnetic stimulation (rTMS) has become a popular method of modulating neural plasticity in humans. Clinically, rTMS is delivered at high intensities to modulate neuronal excitability. While the high-intensity magnetic field can be targeted to stimulate specific cortical regions, areas adjacent to the targeted area receive stimulation at a lower intensity and may contribute to the overall plasticity induced by rTMS. We have previously shown that low-intensity rTMS induces molecular and structural plasticity in vivo, but the effects on membrane properties and neural excitability have not been investigated. Here we investigated the acute effect of low-intensity repetitive magnetic stimulation (LI-rMS) on neuronal excitability and potential changes on the passive and active electrophysiological properties of layer 5 pyramidal neurons in vitro. Whole-cell current clamp recordings were made at baseline prior to subthreshold LI-rMS (600 pulses of iTBS, n = 9 cells from 7 animals) or sham (n = 10 cells from 9 animals), immediately after stimulation, as well as 10 and 20 min post-stimulation. Our results show that LI-rMS does not alter passive membrane properties (resting membrane potential and input resistance) but hyperpolarises action potential threshold and increases evoked spike-firing frequency. Increases in spike firing frequency were present throughout the 20 min post-stimulation whereas action potential (AP) threshold hyperpolarization was present immediately after stimulation and at 20 min post-stimulation. These results provide evidence that LI-rMS alters neuronal excitability of excitatory neurons. We suggest that regions outside the targeted region of high-intensity rTMS are susceptible to neuromodulation and may contribute to rTMS-induced plasticity.

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