Pulsed focused ultrasound changes nerve conduction of earthworm giant axonal fibers

Yoo, Sarah H; Croce, Phillip; Margolin, Ryan W.; Lee, Stephanie D.; Lee, Wonhye

doi:10.1097/wnr.0000000000000745

Cited by 8 publications

(9 citation statements)

References 23 publications

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“…Efforts to elucidate how US modulates neural activity have been confounded by US activation of mechanosensory structures, including auditory hair cells (Guo et al, 2018;Sato et al, 2018). To circumvent these and other complicating factors, we and other groups have examined how US influences neurons on a foundational level in tractable invertebrate systems (Wright et al, 2015(Wright et al, , 2017Yoo et al, 2017;Kubanek et al, 2018;Dedola et al, 2020), mammalian cell culture (Muratore et al, 2009;Qiu et al, 2019), or slice (Rinaldi et al, 1991;Bachtold et al, 1998;Tyler et al, 2008;Prieto et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Focused Ultrasound Neuromodulation and the Confounds of Intracellular Electrophysiological Investigation

Collins

Mesce

2020

eNeuro

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Focused ultrasound (US) can modulate neuronal activity noninvasively with high spatial specificity. In intact nervous systems, however, efforts to determine its enigmatic mode of efficacy have been confounded by the indirect effects of US on mechanosensitive sensory cells and the inability to target equivalent populations of cells with precision across preparations. Single-cell approaches, either via cultured mammalian neurons or tractable invertebrate neural systems, hold great promise for elucidating the cellular mechanisms underlying the actions of US. Here, we present evidence from the medicinal leech, Hirudo verbana, that researchers should apply caution when using US in conjunction with single-cell electrophysiological recording techniques, including sharp-electrode intracellular recording. Although we found that US could elicit depolarization of the resting membrane potential of single neurons, a finding with precedent, we determined that this effect and others could be reliably mimicked via subtle manual displacement of the recording electrode. Because focused US is known to induce resonance of recording electrodes, we aimed to determine how similarly US-induced depolarizations matched those produced by micro movements of a sharp glass electrode, a phenomenon we believe can account for purported depolarizations measured in this manner. Furthermore, we show that when clonally related homologous neurons, which are essentially isopotential, are impaled before the application of focused US, they show a statistically significant change in their membrane potential as compared with the homologous cells that received US with no initial impalement. Future investigations into US's cellular effects should attempt to control for potential electrode resonance or use alternative recording strategies.

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Section: Introductionmentioning

confidence: 99%

Focused Ultrasound Neuromodulation and the Confounds of Intracellular Electrophysiological Investigation

Collins

Mesce

2020

eNeuro

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“…19,20 We transcranially applied low-intensity FUS (210 mW/cm 2 spatial-peak temporal-average intensity; I spta ) to the somatosensory areas of the rat brain for 10 min at a low duty cycle (5%; in a pulsed mode), far lower than the level that could alter the tissue temperature. 21 Concurrently, we measured electroencephalographic (EEG) SEP induced by the unilateral electrical stimulation of the hind limb before and up to 35 min after the sonication to examine the presence of differential SEP features affected by FUS. The sham sessions (i.e., without sonication using the same experimental setup) were also conducted to provide the control condition.…”

Section: Introductionmentioning

confidence: 99%

Focused ultrasound brain stimulation to anesthetized rats induces long‐term changes in somatosensory evoked potentials

Yoo

Yoon

Croce

et al. 2017

Int J Imaging Syst Tech

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Low-intensity transcranial focused ultrasound (FUS) has emerged as a non-invasive brain stimulation modality that can reach deep brain areas with high spatial specificity. Previous studies have identified transient effects of FUS on the brain excitability and accompanying physiological responses. Yet the presence of long-lasting effects of FUS, which extend on the order of half an hour or more, has not been probed. We transcranially applied FUS to the somatosensory areas of the anesthetized rats for 10 min at a low duty cycle (5%) and intensity, far below the level that could alter the tissue temperature. Concurrently, we measured electroencephalographic (EEG) somatosensory evoked potentials (SEP) induced by the unilateral electrical stimulation of the hind limb before and after the sonication. Compared to the control sham condition that did not involve sonication, differential SEP features were evident and persisted beyond 35 min after the administration of FUS. The presence of this non-transient neuromodulatory effect may provide early evidence that FUS-mediated brain stimulation has the potential to induce neuroplasticity.

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“…These effects in mammalian systems range from neuronal excitation (e.g., Tyler et al, 2008;Tufail et al, 2010;Yoo et al, 2011;Kim et al, 2012Kim et al, , 2014Downs et al, 2018) to inhibition (e.g., Anderson et al, 1951;Fry et al, 1958;Takagi et al, 1960;Shealy and Henneman, 1962;Rinaldi et al, 1991;Min et al, 2011;Legon et al, 2014;Kim et al, 2015). Invertebrate preparations including C. elegans, earthworms and crayfish share similar disparities, with reports of both neuronal excitation (Kubanek et al, 2018;Lin et al, 2019) and inhibition (Wright et al, 2017;Yoo et al, 2017;Zhou et al, 2017).…”

Section: Introductionmentioning

confidence: 96%

“…One potential factor contributing to this variability is the use, by most studies, of response measures of multiunit activity, including compound action potentials ( Tsui et al, 2005 ; Wright et al, 2015 ; Yoo et al, 2017 ), event-related potentials ( Legon et al, 2014 , 2018b ; Kim et al, 2015 ), and BOLD signals ( Yoo et al, 2011 ; Ai et al, 2016 , 2018 ). Population-level measurements can be difficult to interpret, as effects that appear to be direct on target tissues may result from mechanical activation of synaptically-coupled sensory neurons.…”

Section: Introductionmentioning

confidence: 99%

The Inhibitory Thermal Effects of Focused Ultrasound on an Identified, Single Motoneuron

Collins

Legon

Mesce

2021

eNeuro

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Focused ultrasound (US) is an emerging neuromodulation technology that has gained much attention due to its ability to modulate, noninvasively, neuronal activity in a variety of animals, including humans. However, there has been considerable debate about exactly which types of neurons can be influenced and what underlying mechanisms are in play. Are US-evoked motor changes driven indirectly by activated mechanosensory inputs, or more directly via central interneurons or motoneurons?Although it has been shown that US can mechanically depolarize mechanosensory neurons, there are no studies that have yet tested how identified motoneurons respond directly to US and what the underlying mechanism might be. Here, we examined the effects of US on a single, identified motoneuron within a well-studied and tractable invertebrate preparation, the medicinal leech, Hirudo verbana. Our approach aimed to clarify single neuronal responses to US, which may be obscured in other studies whereby US is applied across a diverse population of cells. We found that US has the ability to inhibit tonic spiking activity through a predominately thermal mechanism. USevoked effects persisted after blocking synaptic inputs, indicating that its actions were direct. Experiments also revealed that US-comparable heating blocked the axonal conduction of spontaneous action potentials. Finally, we found no evidence that US had significant mechanical effects on the neurons tested, a finding counter to prevailing views. We conclude that a non-sensory neuron can be directly inhibited via a thermal mechanism, a finding that holds promise for clinical neuromodulatory applications.

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Pulsed focused ultrasound changes nerve conduction of earthworm giant axonal fibers

Cited by 8 publications

References 23 publications

Focused Ultrasound Neuromodulation and the Confounds of Intracellular Electrophysiological Investigation

Focused Ultrasound Neuromodulation and the Confounds of Intracellular Electrophysiological Investigation

Focused ultrasound brain stimulation to anesthetized rats induces long‐term changes in somatosensory evoked potentials

The Inhibitory Thermal Effects of Focused Ultrasound on an Identified, Single Motoneuron

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