Visuomotor Transformations Are Modulated by Focused Ultrasound over Frontal Eye Field

Lowe, Kaleb A.; Zinke, Wolf; Phipps, M. Anthony; Cosman, Josh; Maddox, Micala; Schall, Jeffrey D.; Caskey, Charles F.

doi:10.1016/j.ultrasmedbio.2020.11.022

Cited by 4 publications

(2 citation statements)

References 33 publications

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“…FUS can also directly affect behavior in rhesus macaques. Several studies have showed that FUS applied to the frontal eye field alters eye movement behavior and decision-making (Deffieux et al, 2013;Wattiez et al, 2017;Pouget et al, 2020), and altered decision-making (Khalighinejad et al 2020; Kubanek et al, 2020;Lowe et al, 2021).…”

Section: /33mentioning

confidence: 99%

Long Term Study of Motivational and Cognitive Effects of Low-intensity Focused Ultrasound Neuromodulation in the Dorsal Striatum of Nonhuman Primates

Muñoz

Meaney

Gross

et al. 2021

Preprint

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Noninvasive brain stimulation using focused ultrasound (FUS) has many potential applications as a research and clinical tool, including incorporation into neural prosthetics for cognitive rehabilitation. To develop this technology, it is necessary to evaluate the safety and efficacy of FUS neuromodulation for specific brain targets and cognitive functions. It is also important to test whether repeated long-term application of FUS to deep brain targets improves or degrades behavioral and cognitive function. To this end, we investigated the effects of FUS in the dorsal striatum of nonhuman primates (NHP) performing a visual-motor decision-making task for small or large rewards. Over the course of 2 years, we performed 129 and 147 FUS applications, respectively, in two NHP. FUS (0.5 MHz @ 0.2 - 0.8 MPa) was applied to the putamen and caudate in both hemispheres to evaluate the effects on movement accuracy, motivation, decision accuracy, and response time. Sonicating the caudate or the putamen unilaterally resulted in modest but statistically significant improvements in motivation and decision accuracy, but at the cost of slower reaction times. The effects were dose (i.e., FUS pressure) and reward dependent. There was no effect on reaching accuracy, nor was there long-term behavioral impairment or neurological trauma evident on T1-weighted, T2-weighted, or susceptibility-weighted MRI scans. Sonication also resulted in significant changes in resting state functional connectivity between the caudate and multiple cortical regions. The results indicate that applying FUS to the dorsal striatum can positively impact the motivational and cognitive aspects of decision making. The capability of FUS to improve motivation and cognition in NHPs points to its therapeutic potential in treating a wide variety of human neural diseases, and warrants further development as a novel technique for non-invasive deep brain stimulation.

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Section: /33mentioning

confidence: 99%

Long Term Study of Motivational and Cognitive Effects of Low-intensity Focused Ultrasound Neuromodulation in the Dorsal Striatum of Nonhuman Primates

Muñoz

Meaney

Gross

et al. 2021

Preprint

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“… 8 , 9 Ultrasound neuromodulation is also effective in triggering antisaccadic eye movement in non-human primates and boosting sensory performance in human subjects. 10 , 11 In contrast, our understanding of the neuromodulatory mechanism of ultrasonic waves is limited; potential molecular candidates range from cell membranes to ion channel. 12 Adding more complexity, ultrasound has a wide range of parameters, including frequency, duration, and duty cycle, which potentially lead to different biological outcomes.…”

Section: Introductionmentioning

confidence: 99%

Implantable acousto-optic window for monitoring ultrasound-mediated neuromodulation in vivo

Lee

Choi

et al. 2022

Neurophoton.

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Significance: Ultrasound has recently received considerable attention in neuroscience because it provides noninvasive control of deep brain activity. Although the feasibility of ultrasound stimulation has been reported in preclinical and clinical settings, its mechanistic understanding remains limited. While optical microscopy has become the "gold standard" tool for investigating population-level neural functions in vivo, its application for ultrasound neuromodulation has been technically challenging, as most conventional ultrasonic transducers are not designed to be compatible with optical microscopy. Aim:We aimed to develop a transparent acoustic transducer based on a glass coverslip called the acousto-optic window (AOW), which simultaneously provides ultrasound neuromodulation and microscopic monitoring of neural responses in vivo. Approach:The AOW was fabricated by the serial deposition of transparent acoustic stacks on a circular glass coverslip, comprising a piezoelectric material, polyvinylidene fluoride-trifluoroethylene, and indium-tin-oxide electrodes. The fabricated AOW was implanted into a transgenic neural-activity reporter mouse after open craniotomy. Two-photon microscopy was used to observe neuronal activity in response to ultrasonic stimulation through the AOW.Results: The AOW allowed microscopic imaging of calcium activity in cortical neurons in response to ultrasound stimulation. The optical transparency was ∼40% over the visible and near-infrared spectra, and the ultrasonic pressure was 0.035 MPa at 10 MHz corresponding to 10 mW∕cm 2 . In anesthetized Gad2-GCaMP6-tdTomato mice, we observed robust ultrasoundevoked activation of inhibitory cortical neurons at depths up to 200 μm. Conclusions:The AOW is an implantable ultrasonic transducer that is broadly compatible with optical imaging modalities. The AOW will facilitate our understanding of ultrasound neuromodulation in vivo.

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Long term study of motivational and cognitive effects of low-intensity focused ultrasound neuromodulation in the dorsal striatum of nonhuman primates

et al. 2022

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Noninvasive brain stimulation using transcranial focused ultrasound (FUS) has many potential applications as a research and clinical tool, including incorporation into neural prosthetics for cognitive rehabilitation. To develop this technology, it is necessary to evaluate the safety and efficacy of FUS neuromodulation for specific brain targets and cognitive functions. It is also important to test whether repeated long-term application of FUS to deep brain targets improves or degrades behavioral and cognitive function. To this end, we investigated the effects of FUS in the dorsal striatum of nonhuman primates (NHP) performing a visual-motor decision-making task for small or large rewards. Over the course of 2 years, we performed 129 and 147 FUS applications, respectively, in two NHP. FUS (0.5 MHz @ 0.2e0.8 MPa) was applied to the putamen and caudate in both hemispheres to evaluate the effects on movement accuracy, motivation, decision accuracy, and response time. Sonicating the caudate or the putamen unilaterally resulted in modest but statistically significant improvements in motivation and decision accuracy, but at the cost of slower reaction times. The effects were dose (i.e., FUS pressure) and reward dependent. There was no effect on reaching accuracy, nor was there long-term behavioral impairment or neurological trauma evident on T1-weighted, T2-weighted, or susceptibility-weighted MRI scans. Sonication also resulted in significant changes in resting state functional connectivity between the caudate and multiple cortical regions. The results indicate that applying FUS to the dorsal striatum can positively impact the motivational and cognitive aspects of decision making. The capability of FUS to improve motivation and cognition in NHPs points to its therapeutic potential in treating a wide variety of human neural diseases, and warrants further development as a novel technique for noninvasive deep brain stimulation.

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Visuomotor Transformations Are Modulated by Focused Ultrasound over Frontal Eye Field

Cited by 4 publications

References 33 publications

Long Term Study of Motivational and Cognitive Effects of Low-intensity Focused Ultrasound Neuromodulation in the Dorsal Striatum of Nonhuman Primates

Long Term Study of Motivational and Cognitive Effects of Low-intensity Focused Ultrasound Neuromodulation in the Dorsal Striatum of Nonhuman Primates

Implantable acousto-optic window for monitoring ultrasound-mediated neuromodulation in vivo

Long term study of motivational and cognitive effects of low-intensity focused ultrasound neuromodulation in the dorsal striatum of nonhuman primates

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