Systematic examination of low-intensity ultrasound parameters on human motor cortex excitability and behavior

Fomenko, Anton; Chen, Kai‐Hsiang Stanley; Nankoo, Jean-François; Saravanamuttu, James; Wang, Yanqiu; El-Baba, Mazen; Xia, Xue; Seerala, Shakthi Sanjana; Hynynen, Kullervo; Lozano, Andrés M.; Chen, Robert

doi:10.7554/elife.54497

Cited by 99 publications

(137 citation statements)

References 80 publications

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“…Efficient induction of such assemblies can provide a powerful means to trigger or suppress a specific behavior (8,11), and can potentially guide us in understanding brain diseases (12) and to design more efficient brain machine interfaces (13). As with other perturbation techniques (14)(15)(16)(17), it is crucial to understand how parameters of stimulation, including the pattern of activation of specific neurons and the general state of the network dynamics, can be optimized for an efficient induction. This optimization can, however, be complicated, given the complex connectivity and dynamics of cortical networks.…”

Section: Introductionmentioning

confidence: 99%

Excitatory-inhibitory balance modulates the formation and dynamics of neuronal assemblies in cortical networks

Sadeh

Clopath

2021

Preprint

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Repetitive activation of subpopulation of neurons in cortical networks leads to the formation of neuronal assemblies, which can guide learning and behavior. Recent technological advances have made the artificial induction of such assemblies feasible, yet how various patterns of activation can shape their emergence in different operating regimes is not clear. Here we studied this question in large-scale cortical networks composed of excitatory (E) and inhibitory (I) neurons. We found that the dynamics of the network in which neuronal assemblies are embedded is important for their induction. In networks with strong E-E coupling at the border of E-I balance, increasing the number of perturbed neurons enhanced the potentiation of ensembles. This was, however, accompanied by off-target potentiation of connections from unperturbed neurons. When strong E-E connectivity was combined with dominant E-I interactions, formation of ensembles became specific. Counter-intuitively, increasing the number of perturbed neurons in this regime decreased the average potentiation of individual synapses, leading to an optimal assembly formation at intermediate sizes. This was due to potent lateral inhibition in this regime, which also slowed down the formation of neuronal assemblies, resulting in a speed-accuracy trade-off in the performance of the networks in pattern completion and behavioral discrimination. Our results therefore suggest that the two regimes might be suited for different cognitive tasks, with fast regimes enabling crude detections and slow but specific regimes favoring finer discriminations. Functional connectivity inferred from recent experiments in mouse cortical networks seems to be consistent with the latter regime, but we show that recurrent and top-down mechanisms can dynamically modulate the networks to switch between different states. Our work provides a framework to study how neuronal perturbations can lead to network-wide plasticity under biologically realistic conditions, and sheds light on the design of future experiments to optimally induce behaviorally relevant neuronal assemblies.

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Section: Introductionmentioning

confidence: 99%

Excitatory-inhibitory balance modulates the formation and dynamics of neuronal assemblies in cortical networks

Sadeh

Clopath

2021

Preprint

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“…There is evidence that GABAergic interneurons within the superior colliculus downregulate the activity of the nucleus itself [ 40 , 46 , 47 , 48 , 49 ]. Also, a recent study demonstrated that TUS increases GABAergic inhibition at the cortical level [ 9 ]. Accordingly, TUS may enhance the activity of superior colliculus GABAergic interneurons and, in turn, produce an overall reduction in superior colliculus output to the nucleus raphe magnus, thus leading to an increased R2 area ( Figure 4 ).…”

Section: Discussionmentioning

confidence: 99%

“…In humans, TUS of the primary motor cortex decreased corticospinal excitability and intracortical facilitation, increased GABAergic inhibition and reduced motor reaction task performance [ 8 , 9 ]. Conversely, motor evoked potential (MEP) amplitude was facilitated immediately after stimulation [ 10 ].…”

Section: Introductionmentioning

confidence: 99%

Effects of Transcranial Ultrasound Stimulation on Trigeminal Blink Reflex Excitability

et al. 2021

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Recent evidence indicates that transcranial ultrasound stimulation (TUS) modulates sensorimotor cortex excitability. However, no study has assessed possible TUS effects on the excitability of deeper brain areas, such as the brainstem. In this study, we investigated whether TUS delivered on the substantia nigra, superior colliculus, and nucleus raphe magnus modulates the excitability of trigeminal blink reflex, a reliable neurophysiological technique to assess brainstem functions in humans. The recovery cycle of the trigeminal blink reflex (interstimulus intervals of 250 and 500 ms) was tested before (T0), and 3 (T1) and 30 min (T2) after TUS. The effects of substantia nigra-TUS, superior colliculus-TUS, nucleus raphe magnus-TUS and sham-TUS were assessed in separate and randomized sessions. In the superior colliculus-TUS session, the conditioned R2 area increased at T1 compared with T0, while T2 and T0 values did not differ. Results were independent of the interstimulus intervals tested and were not related to trigeminal blink reflex baseline (T0) excitability. Conversely, the conditioned R2 area was comparable at T0, T1, and T2 in the nucleus raphe magnus-TUS and substantia nigra-TUS sessions. Our findings demonstrate that the excitability of brainstem circuits, as evaluated by testing the recovery cycle of the trigeminal blink reflex, can be increased by TUS. This result may reflect the modulation of inhibitory interneurons within the superior colliculus.

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“…ON/OFF cycling is a frequently used parameter, particularly for the anterior nucleus of thalamus stimulation in epilepsy patients (Fisher et al, 2010). It is a potential approach to reduce energy delivery; however, acute stimulation studies showed a decreased treatment effect with cycling DBS compared to conventional DBS in ET (Swan et al, 2016), PD (Montgomery, 2005), and epilepsy (Molnar et al, 2006) patients.…”

Section: Cycling Dbsmentioning

confidence: 99%

Implantable Pulse Generators for Deep Brain Stimulation: Challenges, Complications, and Strategies for Practicality and Longevity

Sarica

Iorio-Morin

Aguirre-Padilla

et al. 2021

Front. Hum. Neurosci.

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Deep brain stimulation (DBS) represents an important treatment modality for movement disorders and other circuitopathies. Despite their miniaturization and increasing sophistication, DBS systems share a common set of components of which the implantable pulse generator (IPG) is the core power supply and programmable element. Here we provide an overview of key hardware and software specifications of commercially available IPG systems such as rechargeability, MRI compatibility, electrode configuration, pulse delivery, IPG case architecture, and local field potential sensing. We present evidence-based approaches to mitigate hardware complications, of which infection represents the most important factor. Strategies correlating positively with decreased complications include antibiotic impregnation and co-administration and other surgical considerations during IPG implantation such as the use of tack-up sutures and smaller profile devices.Strategies aimed at maximizing battery longevity include patient-related elements such as reliability of IPG recharging or consistency of nightly device shutoff, and device-specific such as parameter delivery, choice of lead configuration, implantation location, and careful selection of electrode materials to minimize impedance mismatch. Finally, experimental DBS systems such as ultrasound, magnetoelectric nanoparticles, and near-infrared that use extracorporeal powered neuromodulation strategies are described as potential future directions for minimally invasive treatment.

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Systematic examination of low-intensity ultrasound parameters on human motor cortex excitability and behavior

Cited by 99 publications

References 80 publications

Excitatory-inhibitory balance modulates the formation and dynamics of neuronal assemblies in cortical networks

Excitatory-inhibitory balance modulates the formation and dynamics of neuronal assemblies in cortical networks

Effects of Transcranial Ultrasound Stimulation on Trigeminal Blink Reflex Excitability

Implantable Pulse Generators for Deep Brain Stimulation: Challenges, Complications, and Strategies for Practicality and Longevity

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