Low intensity rTMS has sex-dependent effects on the local response of glia following a penetrating cortical stab injury

Clarke, Darren; Penrose, Marissa A.; Harvey, Alan R.; Rodger, Jennifer; Bates, Kristyn A.

doi:10.1016/j.expneurol.2017.06.019

Cited by 21 publications

(18 citation statements)

References 64 publications

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“…According to the above results ( Figure 2D ), we conclude that neither LPS nor 10 Hz rMS significantly affect cell viability. This finding corroborates previous work in which no negative or even neuroprotective effects of rTMS have been reported ( 37 – 39 ).…”

Section: Resultssupporting

confidence: 93%

Interleukin 10 Restores Lipopolysaccharide-Induced Alterations in Synaptic Plasticity Probed by Repetitive Magnetic Stimulation

et al. 2020

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Systemic inflammation is associated with alterations in complex brain functions such as learning and memory. However, diagnostic approaches to functionally assess and quantify inflammation-associated alterations in synaptic plasticity are not well-established. In previous work, we demonstrated that bacterial lipopolysaccharide (LPS)-induced systemic inflammation alters the ability of hippocampal neurons to express synaptic plasticity, i.e., the long-term potentiation (LTP) of excitatory neurotransmission. Here, we tested whether synaptic plasticity induced by repetitive magnetic stimulation (rMS), a non-invasive brain stimulation technique used in clinical practice, is affected by LPS-induced inflammation. Specifically, we explored brain tissue cultures to learn more about the direct effects of LPS on neural tissue, and we tested for the plasticity-restoring effects of the anti-inflammatory cytokine interleukin 10 (IL10). As shown previously, 10 Hz repetitive magnetic stimulation (rMS) of organotypic entorhino-hippocampal tissue cultures induced a robust increase in excitatory neurotransmission onto CA1 pyramidal neurons. Furthermore, LPS-treated tissue cultures did not express rMS-induced synaptic plasticity. Live-cell microscopy in tissue cultures prepared from a novel transgenic reporter mouse line [C57BL/6-Tg(TNFa-eGFP)] confirms that ex vivo LPS administration triggers microglial tumor necrosis factor alpha (TNFα) expression, which is ameliorated in the presence of IL10. Consistent with this observation, IL10 hampers the LPS-induced increase in TNFα, IL6, IL1β, and IFNγ and restores the ability of neurons to express rMS-induced synaptic plasticity in the presence of LPS. These findings establish organotypic tissue cultures as a suitable model for studying inflammation-induced alterations in synaptic plasticity, thus providing a biological basis for the diagnostic use of transcranial magnetic stimulation in the context of brain inflammation.

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Section: Resultssupporting

confidence: 93%

Interleukin 10 Restores Lipopolysaccharide-Induced Alterations in Synaptic Plasticity Probed by Repetitive Magnetic Stimulation

et al. 2020

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“…As such, there is little information about the effects of BHFS in the literature. Studies using BHFS LI-rTMS in mice have shown increased structural plasticity of visual pathway topography in the midbrain, thalamus and cortex 23 , 24 and altered density of GFAP astrocytes in a mouse model of brain injury 71 , possibly via intracellular calcium increases and changes in gene expression 27 . However, how these cellular and molecular changes might relate to resting-state network changes remains unclear.…”

Section: Resultsmentioning

confidence: 99%

Resting-state fMRI study of brain activation using low-intensity repetitive transcranial magnetic stimulation in rats

Seewoo

Feindel

Etherington

et al. 2018

Sci Rep

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Repetitive transcranial magnetic stimulation (rTMS) is a non-invasive neuromodulation technique used to treat many neuropsychiatric conditions. However, the mechanisms underlying its mode of action are still unclear. This is the first rodent study using resting-state functional MRI (rs-fMRI) to examine low-intensity (LI) rTMS effects, in an effort to provide a direct means of comparison between rodent and human studies. Using anaesthetised Sprague-Dawley rats, rs-fMRI data were acquired before and after control or LI-rTMS at 1 Hz, 10 Hz, continuous theta burst stimulation (cTBS) or biomimetic high-frequency stimulation (BHFS). Independent component analysis revealed LI-rTMS-induced changes in the resting-state networks (RSN): (i) in the somatosensory cortex, the synchrony of resting activity decreased ipsilaterally following 10 Hz and bilaterally following 1 Hz stimulation and BHFS, and increased ipsilaterally following cTBS; (ii) the motor cortex showed bilateral changes following 1 Hz and 10 Hz stimulation, a contralateral decrease in synchrony following BHFS, and an ipsilateral increase following cTBS; and (iii) hippocampal synchrony decreased ipsilaterally following 10 Hz, and bilaterally following 1 Hz stimulation and BHFS. The present findings demonstrate that LI-rTMS modulates functional links within the rat RSN with frequency-specific outcomes, and the observed changes are similar to those described in humans following rTMS.

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“…Although many studies have investigated the role of rTMS frequency on brain excitability and function, less focus has been given to the role of intensity, perhaps because the mechanisms activated by rTMS have always been assumed to involve traditional forms of synaptic plasticity such as long-term potentiation and long-term depression, which require action potential firing 29 . However, recent work in humans and in animal models has shown that LI-rTMS and MI-rTMS (subthreshold) can have a notable effect on the brain 5 , 22 , 30 , 31 . In our study, both MI-rTMS and HI-rTMS reduced FST hyperactivity in the OB model despite being sub- and at-threshold, respectively, and causing different neurobiologic outcomes and recruiting different mechanisms of action, as described.…”

Section: Discussionmentioning

confidence: 99%

Medium- and high-intensity rTMS reduces psychomotor agitation with distinct neurobiologic mechanisms

Heath¹,

Lindberg

Makowiecki

et al. 2018

Transl Psychiatry

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Definitive data are lacking on the mechanism of action and biomarkers of repetitive transcranial magnetic stimulation (rTMS) for the treatment of depression. Low-intensity rTMS (LI-rTMS) has demonstrated utility in preclinical models of rTMS treatments but the effects of LI-rTMS in murine models of depression are unknown. We examined the behavioral and neurobiologic changes in olfactory bulbectomy (OB) mice with medium-intensity rTMS (MI-rTMS) treatment and fluoxetine hydrochloride. We then compared 10-Hz rTMS sessions for 3 min at intensities (measured at the cortical surface) of 4 mT (LI-rTMS), 50 mT (medium-intensity rTMS [MI-rTMS]), or 1 T (high-intensity rTMS [HI-rTMS]) 5 days per week over 4 weeks in an OB model of agitated depression. Behavioral effects were assessed with forced swim test; neurobiologic effects were assessed with brain levels of 5-hydroxytryptamine, brain-derived neurotrophic factor (BDNF), and neurogenesis. Peripheral metabolomic changes induced by OB and rTMS were monitored through enzyme-linked immunosorbent assay and ultrapressure liquid chromatography-driven targeted metabolomics evaluated with ingenuity pathway analysis (IPA). MI-rTMS and HI-rTMS attenuated psychomotor agitation but only MI-rTMS increased BDNF and neurogenesis levels. HI-rTMS normalized the plasma concentration of α-amino-n-butyric acid and 3-methylhistidine. IPA revealed significant changes in glutamine processing and glutamate signaling in the OB model and following MI-rTMS and HI-rTMS treatment. The present findings suggest that MI-rTMS and HI-rTMS induce differential neurobiologic changes in a mouse model of agitated depression. Further, α-amino-n-butyric acid and 3-methylhistidine may have utility as biomarkers to objectively monitor the response to rTMS treatment of depression.

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Low intensity rTMS has sex-dependent effects on the local response of glia following a penetrating cortical stab injury

Cited by 21 publications

References 64 publications

Interleukin 10 Restores Lipopolysaccharide-Induced Alterations in Synaptic Plasticity Probed by Repetitive Magnetic Stimulation

Interleukin 10 Restores Lipopolysaccharide-Induced Alterations in Synaptic Plasticity Probed by Repetitive Magnetic Stimulation

Resting-state fMRI study of brain activation using low-intensity repetitive transcranial magnetic stimulation in rats

Medium- and high-intensity rTMS reduces psychomotor agitation with distinct neurobiologic mechanisms

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