Transcranial ultrasonic stimulation modulates single-neuron discharge in macaques performing an antisaccade task

Wattiez, Nicolas; Constans, Charlotte; Thomas, Daniel; Daye, Pierre; Tanter, Mickaël; Aubry, Jean‐François; Pouget, Pierre

doi:10.1016/j.brs.2017.07.007

Cited by 120 publications

(94 citation statements)

References 45 publications

(48 reference statements)

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“…This has raised some questions about a possible acoustic confound or distractor in some US stimulation experiments. Although the authors did not report their reason for doing so in their study (Wattiez et al, 2017), Wattiez et al attempted to reduce these airconducted audible artifacts in their study on non-human primates by using a procedure not unlike ours: they prolonged the rise and fall times at the beginning and the end of each US pulse. However, they chose a much shorter rise and fall time (5 ms) compared with ours (12ms) and they did not report on any comparisons between prolonged rise and fall times and rectangular envelope sonications.…”

Section: Discussionmentioning

confidence: 89%

“…Menz et al (Menz et al, 2013) demonstrated reproducible activation of salamander retina to US stimulation in an isolated retina preparation. Modulation of the neural activity from ultrasound stimulation has been demonstrated in C.elegans nematodes (Kubanek et al, 2018), and in several mammals including pigs (Dallapiazza et al, 2018), sheep , non-human primates (Deffieux et al, 2013, Wattiez et al, 2017 and humans . Transcranial ultrasound stimulation in rodents has resulted in motor responses such as whole body twitches (Tufail et al, 2010, King et al, 2013, Ye et al, 2016.…”

Section: Introductionmentioning

confidence: 99%

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Elimination of peripheral auditory pathway activation does not affect motor responses from ultrasound neuromodulation

Mohammadjavadi

Xia

et al. 2018

Preprint

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Recent studies in a variety of animal models including rodents, monkeys, and humans suggest that transcranial focused ultrasound (tFUS) has considerable promise for noninvasively modulating neural activity with the ability to target deep brain structures. However, concerns have been raised that motor responses evoked by tFUS may be due to indirect activation of the auditory pathway rather than direct activation of motor circuits. In this study, tFUS-induced electromyography (EMG) signals were recorded and analyzed in wild-type (WT) normal hearing mice and two strains of genetically deaf mice to examine the involvement of the peripheral auditory system in tFUS-stimulated motor responses. In addition, auditory brainstem responses (ABRs) were measured to elucidate the effect of the tFUS stimulus envelope on auditory and motor responses. We also varied the tFUS stimulation duration to measure its effect on motor response duration. We show, first, that the sharp edges in a tFUS rectangular envelope stimulus activate the peripheral afferent auditory pathway and, second, that smoothing these edges eliminates the auditory responses without affecting the motor responses in normal hearing WT mice. We further show that by eliminating peripheral auditory activity using two different strains of deaf knockout mice, motor responses are the same as in normal hearing WT mice. Finally, we demonstrate a high correlation between tFUS pulse duration and EMG response duration. These results support the concept that tFUS-evoked motor responses are not a result of stimulation of the peripheral auditory system.

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Section: Discussionmentioning

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Elimination of peripheral auditory pathway activation does not affect motor responses from ultrasound neuromodulation

Mohammadjavadi

Xia

et al. 2018

Preprint

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“…13,17, 22,34 The current surge of interest in it as a noninvasive neurostimulation modality has been triggered by the following relatively recent findings: 1) FUS can elicit neuromodulatory effects in the CNS by using relatively short stimuli; 59 2) short stimuli of low intensity can trigger visible movements upon motor cortex stimulation in rodents; 25–27,35,38, 56,62 and 3) the method has been safely used in primates, including humans. 9,21,32–34,60 Given the enormous potential of this neurostimulation modality in causal brain mapping and treatments of deep brain circuits, work is currently under way to provide the information necessary for effective use. In particular, researchers are beginning to elucidate how FUS stimulates neurons and which FUS parameters mediate effective excitation or inhibition.…”

Section: Transcranial Focused Ultrasoundmentioning

confidence: 99%

“…27,31 In this regard, interestingly, recent neuromodulation studies in large mammals including humans used stimuli that were applied for ≥ 100 msec. 9,32–34,60 …”

Section: Effective Stimulation Protocolsmentioning

confidence: 99%

Neuromodulation with transcranial focused ultrasound

Kubanek

2018

Neurosurgical Focus

141

124

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The understanding of brain function and the capacity to treat neurological and psychiatric disorders rest on the ability to intervene in neuronal activity in specific brain circuits. Current methods of neuromodulation incur a tradeoff between spatial focus and the level of invasiveness. Transcranial focused ultrasound (FUS) is emerging as a neuromodulation approach that combines noninvasiveness with focus that can be relatively sharp even in regions deep in the brain. This may enable studies of the causal role of specific brain regions in specific behaviors and behavioral disorders. In addition to causal brain mapping, the spatial focus of FUS opens new avenues for treatments of neurological and psychiatric conditions. This review introduces existing and emerging FUS applications in neuromodulation, discusses the mechanisms of FUS effects on cellular excitability, considers the effects of specific stimulation parameters, and lays out the directions for future work.

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“…We therefore conclude that our stimulus, at least in part, excited neurons within the FEF. This finding is supported by a study that recorded neuronal responses within supplementary eye fields in response to ultrasonic FEF stimulation in an anti-saccade task (Wattiez et al, 2017).…”

Section: Discussionmentioning

confidence: 55%

Transcranial ultrasound selectively biases decision-making in primates

Kubanek¹,

Brown²,

Ye³

et al. 2018

Preprint

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Transcranial focused ultrasound has the promise to evolve into a transformative noninvasive way to modulate activity of neuronal circuits deep in the brain. The approach may enable systematic and causal mapping of how individual brain circuits are involved in specific behaviors and behavioral disorders. Previous studies demonstrated neuromodulatory potential, but the e↵ect polarity, size, and spatial specificity have been di cult to assess. Here, we engaged non-human primates (macaca mulatta) in an established task that provides a well defined framework to characterize the neuromodulatory e↵ects. In this task, subjects decide whether to look at a right or a left target, guided by one the targets appearing first. Previous studies showed that excitation/inhibition of oculomotor circuits leads to contralateral/ipsilateral biases in this choice behavior. We found that brief, low-intensity ultrasound stimuli (300 ms, 0.6 MPa, 270 kHz) delivered to the animals' left/right frontal eye fields bias the animals' decisions to the right/left visual hemifield. The e↵ect was modest, about on the order of that produced when injecting moderate amounts of potent neuromodulatory drugs into the same regions in this task. The polarity of the e↵ects suggested a neuronal excitation within the stimulated regions. No e↵ects were observed when we applied the same stimuli to control brain regions not involved in oculomotor target selection. Together, using an established paradigm, we found that transcranial ultrasound is capable of modulating neurons to the extent of biasing choice behavior of non-human primates. A demonstration of tangible, brain-region-specific e↵ects on behavior of primates constitutes a critical step toward applying this noninvasive neuromodulation method in investigations of how specific neural circuits are involved in specific behaviors or disease signs. Sato et al., 2018). In these studies, applications of low-intensity stimuli to peri-motor regions often lead to visible movements of the limbs or other body parts. There have been concerns that the small size of the rodent brain, relative to the dimensions of the focal spot, results in reflections, Li

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Transcranial ultrasonic stimulation modulates single-neuron discharge in macaques performing an antisaccade task

Cited by 120 publications

References 45 publications

Elimination of peripheral auditory pathway activation does not affect motor responses from ultrasound neuromodulation

Elimination of peripheral auditory pathway activation does not affect motor responses from ultrasound neuromodulation

Neuromodulation with transcranial focused ultrasound

Transcranial ultrasound selectively biases decision-making in primates

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