Repetitive Transcranial Magnetic Stimulation Elicits Rate-Dependent Brain Network Responses in Non-Human Primates

Salinas, F.; Narayana, Shalini; Zhang, Wei; Fox, Peter T.; Szabó, C. Ákos

doi:10.1016/j.brs.2013.03.002

Cited by 20 publications

(27 citation statements)

References 73 publications

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“…Cerebral blood flow was measured during 3 Hz, 5 Hz, 10 Hz, and 15 Hz TMS applied to M1. The data demonstrated that the CBF response was optimal at 5 Hz rTMS not only at the site of stimulation, but also in the connected motor areas (Salinas et al, 2013). In addition, we found no significant CBF changes at any rTMS frequency in the homologous contralateral M1 hand region.…”

Section: Discussionmentioning

confidence: 98%

Concurrent TMS to the primary motor cortex augments slow motor learning

et al. 2014

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Transcranial magnetic stimulation (TMS) has shown promise as a treatment tool, with one FDA approved use. While TMS alone is able to up- (or down-) regulate a targeted neural system, we argue that TMS applied as an adjuvant is more effective for repetitive physical, behavioral and cognitive therapies, that is, therapies which are designed to alter the network properties of neural systems through Hebbian learning. We tested this hypothesis in the context of a slow motor learning paradigm. Healthy right-handed individuals were assigned to receive 5 Hz TMS (TMS group) or sham TMS (sham group) to the right primary motor cortex (M1) as they performed daily motor practice of a digit sequence task with their non-dominant hand for 4 weeks. Resting cerebral blood flow (CBF) was measured by normalH215O PET at baseline and after 4 weeks of practice. Sequence performance was measured daily as the number of correct sequences performed, and modeled using a hyperbolic function. Sequence performance increased significantly at 4 weeks relative to baseline in both groups. The TMS group had a significant additional improvement in performance, specifically, in the rate of skill acquisition. In both groups, an improvement in sequence timing and transfer of skills to non-trained motor domains was also found. Compared to the sham group, the TMS group demonstrated increases in resting CBF specifically in regions known to mediate skill learning namely, the M1, cingulate cortex, putamen, hippocampus, and cerebellum. These results indicate that TMS applied concomitantly augments behavioral effects of motor practice, with corresponding neural plasticity in motor sequence learning network. These findings are the first demonstration of the behavioral and neural enhancing effects of TMS on slow motor practice and have direct application in neurorehabilitation where TMS could be applied in conjunction with physical therapy.

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Section: Discussionmentioning

confidence: 98%

Concurrent TMS to the primary motor cortex augments slow motor learning

et al. 2014

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“…> 1 Hz) will produce excitatory brain activity in all nodes of the targeted brain network. In this study, we extend our previous results 8,9 by investigating the effective connectivity of the baboon’s motor network—at different rTMS frequencies—to determine if 5 Hz rTMS is the optimal frequency for stimulation of all of the nodes within the motor network.…”

Section: Introductionmentioning

confidence: 60%

“…11 The data acquired in these five animals was used in prior publications 8,9 ; the results from these prior publications were reanalyzed in this study to assess the effective connectivity of the baboon’s motor network. Each animal was pre-screened—using electroencephalography 12 —to ensure that only animals with no neurological deficits were enrolled in the study.…”

Section: Methodsmentioning

confidence: 99%

“…Cubic regions of interest (ROIs; 3 mm x 3 mm x 3 mm) were selected from the statistical parametric imaging results of the “All rTMS vs. Rest” experiment presented in Salinas et al, 8 which demonstrated the highest levels of brain activity during rTMS while targeting the motor cortex (Figure 1). These regions included the: targeted dorsal precentral (L-M1), ipsilateral dorsal premotor (L-PM), supplementary motor area (SMA), contralateral anterior cingulate (R-Cg), contralateral cerebellum (R-Cb), ipsilateral caudate (L-Cd), contralateral thalamus (R-Th), ipsilateral parietal operculum (L-SII), ipsilateral insula (L-Ins), and contralateral anterior intraparietal sulcus (R-AIP).…”

Section: Methodsmentioning

confidence: 99%

“…In our previous study, 8 we reported that a unimodal relationship (peaking at 5 Hz rTMS) existed between rTMS frequency and the cerebral blood flow (CBF) of the motor network during concurrent positron emission tomographic (PET) imaging. We also found that some of the nodes in the motor network were maximally inhibited at 5 Hz rTMS.…”

Section: Introductionmentioning

confidence: 99%

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Repetitive Transcranial Magnetic Stimulation Educes Frequency-Specific Causal Relationships in the Motor Network

et al. 2016

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Background Repetitive transcranial magnetic stimulation (rTMS) has the potential to treat brain disorders by modulating the activity of disease-specific brain networks, yet the rTMS frequencies used are delivered in a binary fashion—excitatory (> 1 Hz) and inhibitory (≤1 Hz). Objective To assess the effective connectivity of the motor network at different rTMS stimulation rates during positron-emission tomography (PET) and confirm that not all excitatory rTMS frequencies act on the motor network in the same manner. Methods We delivered image-guided, supra-threshold rTMS at 3 Hz, 5 Hz, 10 Hz, 15 Hz and rest (in separate randomized sessions) to the primary motor cortex (M1) of the lightly anesthetized baboon during PET imaging. Each rTMS/PET session was analyzed using normalized cerebral blood flow (CBF) measurements. Path analysis—using structural equation modeling (SEM)—was employed to determine the effective connectivity of the motor network at all rTMS frequencies. Once determined, the final model of the motor network was used to assess any differences in effective connectivity at each rTMS frequency. Results The exploratory SEM produced a very well fitting final network model (χ2 = 18.04, df = 21, RMSEA = 0.000, p = 0.647, TLI = 1.12) using seven nodes of the motor network. 5 Hz rTMS produced the strongest path coefficients in four of the seven connections, suggesting that this frequency is the optimal rTMS frequency for stimulation the motor network (as a whole), however, the premotor → cerebellum connection was optimally stimulated at 10 Hz rTMS and the supplementary motor area → caudate connection was optimally driven at 15 Hz rTMS. Conclusion(s) We have demonstrated that 1) 5 Hz rTMS revealed the strongest path coefficients (i.e. causal influence) on the nodes of the motor network, 2) stimulation at “excitatory” rTMS frequencies did not produce increased CBF in all nodes of the motor network, 3) specific rTMS frequencies may be used to target specific none-to-node interactions in the stimulated brain network, and 4) more research needs to be performed to determine the optimum frequency for each brain circuit and/or node.

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Low‐frequency rTMS targeting individual self‐initiated finger‐tapping task activation modulates the amplitude of local neural activity in the putamen

Wang

Deng

et al. 2022

Human Brain Mapping

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Repetitive transcranial magnetic stimulation (rTMS) has been used in the clinical treatment of Parkinson's disease (PD). Most of rTMS studies on PD used high‐frequency stimulation; however, excessive nonvoluntary movement may represent abnormally cortical excitability, which is likely to be suppressed by low‐frequency rTMS. Decreased neural activity in the basal ganglia on functional magnetic resonance imaging (fMRI) is a characteristic of PD. In the present study, we found that low‐frequency (1 Hz) rTMS targeting individual finger‐tapping activation elevated the amplitude of local neural activity (percentage amplitude fluctuation, PerAF) in the putamen as well as the functional connectivity (FC) of the stimulation target and basal ganglia in healthy participants. These results provide evidence for our hypothesis that low‐frequency rTMS over the individual task activation site can modulate deep brain functions, and that FC might serve as a bridge transmitting the impact of rTMS to the deep brain regions. It suggested that a precisely localized individual task activation site can act as a target for low‐frequency rTMS when it is used as a therapeutic tool for PD.

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Repetitive Transcranial Magnetic Stimulation Elicits Rate-Dependent Brain Network Responses in Non-Human Primates

Cited by 20 publications

References 73 publications

Concurrent TMS to the primary motor cortex augments slow motor learning

Concurrent TMS to the primary motor cortex augments slow motor learning

Repetitive Transcranial Magnetic Stimulation Educes Frequency-Specific Causal Relationships in the Motor Network

Low‐frequency rTMS targeting individual self‐initiated finger‐tapping task activation modulates the amplitude of local neural activity in the putamen

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