Volume 600, Issue 17 pp. 4019-4037
Research Article

In vivo low-intensity magnetic pulses durably alter neocortical neuron excitability and spontaneous activity

Manon Boyer

Manon Boyer

Sorbonne Université & CNRS, IBPS-B2A, UMR 8256 Biological Adaptation and Ageing, Paris, France

Sorbonne Université, Paris Brain Institute–ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, team ‘Network dynamics and cellular excitability’, Paris, France

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Paul Baudin

Paul Baudin

Sorbonne Université, Paris Brain Institute–ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, team ‘Network dynamics and cellular excitability’, Paris, France

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Chloé Stengel

Chloé Stengel

Sorbonne Université, Paris Brain Institute–ICM, INSERM, CNRS, Pitié-Salpêtrière Hospital, team Cerebral Dynamics, Plasticity and Rehabilitation Group, FRONTLAB team, Paris, France

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Antoni Valero-Cabré

Antoni Valero-Cabré

Sorbonne Université, Paris Brain Institute–ICM, INSERM, CNRS, Pitié-Salpêtrière Hospital, team Cerebral Dynamics, Plasticity and Rehabilitation Group, FRONTLAB team, Paris, France

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Ann M. Lohof

Ann M. Lohof

Sorbonne Université & CNRS, IBPS-B2A, UMR 8256 Biological Adaptation and Ageing, Paris, France

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Stéphane Charpier

Stéphane Charpier

Sorbonne Université, Paris Brain Institute–ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, team ‘Network dynamics and cellular excitability’, Paris, France

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Rachel M. Sherrard

Corresponding Author

Rachel M. Sherrard

Sorbonne Université & CNRS, IBPS-B2A, UMR 8256 Biological Adaptation and Ageing, Paris, France

Corresponding authors R. M. Sherrard: UMR 8256 Biological Adaptation and Ageing, Boite 256, Sorbonne Université, 9 Quai St Bernard, 75005 Paris, France. Email: [email protected]

Severine Mahon: Paris Brain Institute–ICM, INSERM U1127, Pitié-Salpêtrière Hospital, Paris 75013 France. Email: [email protected]

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Séverine Mahon

Corresponding Author

Séverine Mahon

Sorbonne Université, Paris Brain Institute–ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, team ‘Network dynamics and cellular excitability’, Paris, France

Corresponding authors R. M. Sherrard: UMR 8256 Biological Adaptation and Ageing, Boite 256, Sorbonne Université, 9 Quai St Bernard, 75005 Paris, France. Email: [email protected]

Severine Mahon: Paris Brain Institute–ICM, INSERM U1127, Pitié-Salpêtrière Hospital, Paris 75013 France. Email: [email protected]

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First published: 28 July 2022
Citations: 4

Handling Editors: David Wyllie & Jing-Ning Zhu

The peer review history is available in the Supporting Information section of this article (https://doi.org/10.1113/JP283244#support-information-section).

R. M. Sherrard and S. Mahon contributed equally to this work.

This article was first published as a preprint. Boyer M, Baudin P, Stengel C, Valero-Cabré A, Lohof AM, Charpier S, Sherrard RM & Mahon S. 2022. In vivo low-intensity magnetic pulses durably alter neocortical neuron excitability and spontaneous activity. bioRxiv DOI: 10.1101/2022.03.18.484911

Abstract

Magnetic brain stimulation is a promising treatment for neurological and psychiatric disorders. However, a better understanding of its effects at the individual neuron level is essential to improve its clinical application. We combined focal low-intensity repetitive transcranial magnetic stimulation (LI-rTMS) to the rat somatosensory cortex with intracellular recordings of subjacent pyramidal neurons in vivo. Continuous 10 Hz LI-rTMS reliably evoked firing at ∼4–5 Hz during the stimulation period and induced durable attenuation of synaptic activity and spontaneous firing in cortical neurons, through membrane hyperpolarization and a reduced intrinsic excitability. However, inducing firing in individual neurons by repeated intracellular current injection did not reproduce the effects of LI-rTMS on neuronal properties. These data provide a novel understanding of mechanisms underlying magnetic brain stimulation showing that, in addition to inducing biochemical plasticity, even weak magnetic fields can activate neurons and enduringly modulate their excitability.

Key points

  • Repetitive transcranial magnetic stimulation (rTMS) is a promising technique to alleviate neurological and psychiatric disorders caused by alterations in cortical activity.
  • Our knowledge of the cellular mechanisms underlying rTMS-based therapies remains limited.
  • We combined in vivo focal application of low-intensity rTMS (LI-rTMS) to the rat somatosensory cortex with intracellular recordings of subjacent pyramidal neurons to characterize the effects of weak magnetic fields at single cell level.
  • Ten minutes of LI-rTMS delivered at 10 Hz reliably evoked action potentials in cortical neurons during the stimulation period, and induced durable attenuation of their intrinsic excitability, synaptic activity and spontaneous firing.
  • These results help us better understand the mechanisms of weak magnetic stimulation and should allow optimizing the effectiveness of stimulation protocols for clinical use.

Data availability statement

All data are available in the main text.