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• W2806795384 abstract "Many neuroscientists are excited regarding the potential of ultrasound to yield spatiotemporally precise and noninvasive modulation of arbitrary brain regions. Here, Guo et al., 2018Guo H. Hamilton M. Offutt S.J. Gloeckner C.D. Li T. Kim Y. Legon W. Alford J.K. Lim H.H. Ultrasound produces extensive brain activation via a cochlear pathway.Neuron. 2018; 98 (this issue): 1020-1030Abstract Full Text Full Text PDF PubMed Scopus (118) Google Scholar and Sato et al., 2018Sato T. Shapiro M. Tsao D. Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism.Neuron. 2018; 98 (this issue): 1031-1041Abstract Full Text Full Text PDF PubMed Scopus (145) Google Scholar show that applying ultrasound to rodent brains activates acoustic responses more prominently than eliciting neuromodulation directly, suggesting potential confounds of ultrasound neuromodulation experiments. Many neuroscientists are excited regarding the potential of ultrasound to yield spatiotemporally precise and noninvasive modulation of arbitrary brain regions. Here, Guo et al., 2018Guo H. Hamilton M. Offutt S.J. Gloeckner C.D. Li T. Kim Y. Legon W. Alford J.K. Lim H.H. Ultrasound produces extensive brain activation via a cochlear pathway.Neuron. 2018; 98 (this issue): 1020-1030Abstract Full Text Full Text PDF PubMed Scopus (118) Google Scholar and Sato et al., 2018Sato T. Shapiro M. Tsao D. Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism.Neuron. 2018; 98 (this issue): 1031-1041Abstract Full Text Full Text PDF PubMed Scopus (145) Google Scholar show that applying ultrasound to rodent brains activates acoustic responses more prominently than eliciting neuromodulation directly, suggesting potential confounds of ultrasound neuromodulation experiments. Current techniques for noninvasive neuromodulation, such as transcranial magnetic stimulation (TMS) or either transcranial alternating or direct current stimulation (tcACS or tcDCS), show a limiting trade-off between the spatial resolution and depth of penetration of the intervention (Deng et al., 2013Deng Z.-D. Lisanby S.H. Peterchev A.V. Electric field depth-focality tradeoff in transcranial magnetic stimulation: simulation comparison of 50 coil designs.Brain Stimulat. 2013; 6: 1-13Abstract Full Text Full Text PDF PubMed Scopus (555) Google Scholar). In contrast, focused ultrasound can deliver energy with millimeter-scale spatial resolution to any point of the brain, with guidance and real-time visualization of the ultrasound focus with MRI, using hardware that is already clinically available (Elias et al., 2016Elias W.J. Lipsman N. Ondo W.G. Ghanouni P. Kim Y.G. Lee W. Schwartz M. Hynynen K. Lozano A.M. Shah B.B. et al.A Randomized Trial of Focused Ultrasound Thalamotomy for Essential Tremor.N. Engl. J. Med. 2016; 375: 730-739Crossref PubMed Scopus (576) Google Scholar, Hynynen and Clement, 2007Hynynen K. Clement G. Clinical applications of focused ultrasound-the brain.Int. J. Hyperthermia. 2007; 23: 193-202Crossref PubMed Scopus (101) Google Scholar). Since as early as the 1950’s, electrophysiological, functional neuroimaging, and behavioral effects have been reported after applying focused ultrasound to the mammalian brain across a range of species, including mice, rats, cats, monkeys, and humans (reviewed in depth in Tyler et al., 2018Tyler W.J. Lani S.W. Hwang G.M. Ultrasonic modulation of neural circuit activity.Curr. Opin. Neurobiol. 2018; 50: 222-231Crossref PubMed Scopus (106) Google Scholar). These features and data have led to a surge of recent interest in developing focused ultrasound as a tool for noninvasive neuromodulation. However, the mechanism by which ultrasound may interact with neural tissue to drive these effects, as well as the robustness of this mechanism, has been unsettled and to some a matter of controversy. Additionally, there have been some reports of acoustic responses to ultrasound application to the brain (Foster and Wiederhold, 1978Foster K.R. Wiederhold M.L. Auditory responses in cats produced by pulsed ultrasound.J. Acoust. Soc. Am. 1978; 63: 1199-1205Crossref PubMed Scopus (50) Google Scholar), despite the applied ultrasound fundamental frequency being in a frequency band well beyond the accepted hearing sensitivity range for the animal. In this issue of Neuron, an important pair of studies in rodents (Guo et al., 2018Guo H. Hamilton M. Offutt S.J. Gloeckner C.D. Li T. Kim Y. Legon W. Alford J.K. Lim H.H. Ultrasound produces extensive brain activation via a cochlear pathway.Neuron. 2018; 98 (this issue): 1020-1030Abstract Full Text Full Text PDF PubMed Scopus (118) Google Scholar, Sato et al., 2018Sato T. Shapiro M. Tsao D. Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism.Neuron. 2018; 98 (this issue): 1031-1041Abstract Full Text Full Text PDF PubMed Scopus (145) Google Scholar) uses complementary methods to report that ultrasound protocols that have been described as effective for directly modulating brain activity yield activity patterns that are more consistent with a response to an acoustic stimulus. The study by Guo et al., 2018Guo H. Hamilton M. Offutt S.J. Gloeckner C.D. Li T. Kim Y. Legon W. Alford J.K. Lim H.H. Ultrasound produces extensive brain activation via a cochlear pathway.Neuron. 2018; 98 (this issue): 1020-1030Abstract Full Text Full Text PDF PubMed Scopus (118) Google Scholar first used multi-electrode recording arrays in guinea pig primary auditory cortex (A1) to assess the electrophysiological responses to focused ultrasound directed to A1. They observed that the responses to ultrasound directed to A1 were highly similar to responses to a broadband acoustic noise stimulus, including having similar timing to the acoustic stimulus; this suggested an indirect polysynaptic activation mechanism, consistent with a cochlear source of the ultrasound-induced response. They then proceeded on a truly comprehensive set of experiments varying the trajectory, target, and timing parameters of the applied ultrasound (including insonation of not the brain, but the eye) and saw responses in A1 that were relatively invariant to these variations in where and how ultrasound was applied. Additionally, they observed an activation of somatosensory cortex (SC1) in response to ultrasound that was similarly invariant to the specific trajectory and target of ultrasound application, and they likewise showed timing characteristics suggesting a polysynaptic pathway to the cortex instead of a direct manipulation of the tissue by ultrasound. Critically, they observed that transection of the auditory nerves eliminated the A1 responses and that removal of cochlear fluid to render the cochleae insensate eliminated both the A1 and SC1 responses. They further showed that the A1 and SC1 responses to ultrasound depended mainly on there being a continuous transduction path for the ultrasound from the transducer to the brain via gel, soft tissue, or fluid—including a somewhat macabre experiment in which a dead guinea pig brain served as part of the conduction medium. In a complementary set of experiments, Sato et al., 2018Sato T. Shapiro M. Tsao D. Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism.Neuron. 2018; 98 (this issue): 1031-1041Abstract Full Text Full Text PDF PubMed Scopus (145) Google Scholar used calcium imaging in mice to image dorsal cortical responses to ultrasound directed to visual cortex. Similar to the results of Guo et al., 2018Guo H. Hamilton M. Offutt S.J. Gloeckner C.D. Li T. Kim Y. Legon W. Alford J.K. Lim H.H. Ultrasound produces extensive brain activation via a cochlear pathway.Neuron. 2018; 98 (this issue): 1020-1030Abstract Full Text Full Text PDF PubMed Scopus (118) Google Scholar, despite directing the sonication field to visual cortex, Sato et al., 2018Sato T. Shapiro M. Tsao D. Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism.Neuron. 2018; 98 (this issue): 1031-1041Abstract Full Text Full Text PDF PubMed Scopus (145) Google Scholar observed imaging activation patterns of greatest strength in the primary auditory and somatosensory cortices, with no or minimal changes in the visual cortex, to the resolution of their assay. They showed that the imaging activation patterns they saw in response to focused ultrasound directed to visual cortex were more similar to activation patterns seen in response to auditory tones than to light flashes. They then showed that focused ultrasound directed to the visual cortex was able to induce motor activity and showed that this motor behavior was similar to that observed in response to aversive air puffs or loud sounds. Finally, they demonstrated that partial chemical deafening of the animal blunted these motor responses and that, on a per animal basis, the degree of retained motor responses to ultrasound correlated well with the degree of retained motor responses to sound. Taken together, these studies are a warning to neuroscientists looking to utilize ultrasound as a neuromodulatory tool, particularly in rodents. The potential for results of these experiments to be biased by an acoustic or other cross-modal sensory response will need to be controlled for and directly addressed. It does remain a somewhat open question what the exact mechanism is for transduction of higher frequency ultrasound into the lower frequencies that could stimulate cochlear afferents. Sato et al., 2018Sato T. Shapiro M. Tsao D. Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism.Neuron. 2018; 98 (this issue): 1031-1041Abstract Full Text Full Text PDF PubMed Scopus (145) Google Scholar used a 1.5 kHz pulse repetition frequency and showed that there was indeed broadband acoustic power at the cochlea, with a peak at 1.5 kHz. Guo et al., 2018Guo H. Hamilton M. Offutt S.J. Gloeckner C.D. Li T. Kim Y. Legon W. Alford J.K. Lim H.H. Ultrasound produces extensive brain activation via a cochlear pathway.Neuron. 2018; 98 (this issue): 1020-1030Abstract Full Text Full Text PDF PubMed Scopus (118) Google Scholar likewise saw peaks of acoustic power at the pulse repetition frequency (and its harmonics) at the animal cochlea. However, Guo et al., 2018Guo H. Hamilton M. Offutt S.J. Gloeckner C.D. Li T. Kim Y. Legon W. Alford J.K. Lim H.H. Ultrasound produces extensive brain activation via a cochlear pathway.Neuron. 2018; 98 (this issue): 1020-1030Abstract Full Text Full Text PDF PubMed Scopus (118) Google Scholar also tested timing protocols in which there was no (i.e., single pulse) or low (10 to 50 Hz) pulse repetition frequency and they still saw neural activations to ultrasound that were nearly or completely eliminated following cochlear nerve transection. Notably, the sharp onset and offset of each rectangular ultrasound pulse will itself contain frequencies across a broad range. In smaller rodent skulls, it is entirely likely that frequency components that overlap with the cochlear sensitivity range could propagate to the cochleae. Additionally, it is in principle possible that a radiation-force-type mechanism or nonlinear propagation via bone could transduce the ultrasound energy into direct mechanical action on the ossicles or cochlear hair cells. Furthermore, it is unclear how relevant these findings are for ultrasound neuromodulation experiments in larger animals and humans. Lower frequency, 650 kHz ultrasound is routinely used in clinical transcranial focused ultrasound treatments (Elias et al., 2016Elias W.J. Lipsman N. Ondo W.G. Ghanouni P. Kim Y.G. Lee W. Schwartz M. Hynynen K. Lozano A.M. Shah B.B. et al.A Randomized Trial of Focused Ultrasound Thalamotomy for Essential Tremor.N. Engl. J. Med. 2016; 375: 730-739Crossref PubMed Scopus (576) Google Scholar) with intensities that are orders of magnitude higher than those used in these studies, and these patients—who are awake during these procedures—do not report hearing a loud sound during sonication. Likewise, ultrasound with pulse repetition frequencies similar to some of the protocols in these papers is used routinely for human transcranial Doppler ultrasound studies and for ultrasound imaging of the body more generally, and neither patients nor ultrasonographers report a significant acoustic stimulus accompanying the examination. Conversely, even if there was a significant acoustic stimulus associated with ultrasound application, humans and primates can easily adapt to and ignore that stimulus, as occurs routinely with acoustic stimuli associated with TMS treatments and functional MRI studies. Importantly, these results do not invalidate the observations of neural activity changes seen with focused ultrasound applied in relatively reduced systems like C. elegans, tissue culture, retinae (Menz et al., 2013Menz M.D. Oralkan O. Khuri-Yakub P.T. Baccus S.A. Precise neural stimulation in the retina using focused ultrasound.J. Neurosci. 2013; 33: 4550-4560Crossref PubMed Scopus (129) Google Scholar), and brain slices (reviewed in Tyler et al., 2018Tyler W.J. Lani S.W. Hwang G.M. Ultrasonic modulation of neural circuit activity.Curr. Opin. Neurobiol. 2018; 50: 222-231Crossref PubMed Scopus (106) Google Scholar) in which an auditory apparatus does not exist. The results of this current pair of studies do not invalidate the likelihood that the mechanisms by which neural cells are sensitive to ultrasound in these reduced preparations will be preserved analogously in intact rodent and human brains. Further, it should be noted that these current studies use assays—electrophysiological spiking activity (Guo et al., 2018Guo H. Hamilton M. Offutt S.J. Gloeckner C.D. Li T. Kim Y. Legon W. Alford J.K. Lim H.H. Ultrasound produces extensive brain activation via a cochlear pathway.Neuron. 2018; 98 (this issue): 1020-1030Abstract Full Text Full Text PDF PubMed Scopus (118) Google Scholar) and calcium imaging (Sato et al., 2018Sato T. Shapiro M. Tsao D. Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism.Neuron. 2018; 98 (this issue): 1031-1041Abstract Full Text Full Text PDF PubMed Scopus (145) Google Scholar)—that are potentially insensitive to subthreshold or inhibitory modulations that ultrasound may induce directly in the brain. Moving forward, these studies underscore the need to define and understand the potential mechanisms for transduction of ultrasound into neural activity changes. Experimentalists that wish to use or study endogenous neuromodulatory responses to ultrasound will need to consider the potential for acoustic or other cross-modal sensory responses to bias their results. Indeed, these studies raise a challenge to the field to accomplish ultrasonic neuromodulation of the brain without inducing confounding acoustic, other cross-modal sensory, or peripheral nervous stimuli. Notably, the lack of a noticeable ultrasound-induced electrophysiological response in the sonicated brain following auditory nerve transection or cochlear fluid removal calls into question the robustness of ultrasound by itself as a tool for neuromodulation. This potentially necessitates alternative approaches to neuromodulation (Airan et al., 2017Airan R.D. Meyer R.A. Ellens N.P.K. Rhodes K.R. Farahani K. Pomper M.G. Kadam S.D. Green J.J. Noninvasive targeted transcranial neuromodulation via focused ultrasound gated drug release from nanoemulsions.Nano Lett. 2017; 17: 652-659Crossref PubMed Scopus (96) Google Scholar, McDannold et al., 2015McDannold N. Zhang Y. Power C. Arvanitis C.D. Vykhodtseva N. Livingstone M. Targeted, noninvasive blockade of cortical neuronal activity.Sci. Rep. 2015; 5: 16253Crossref PubMed Scopus (24) Google Scholar) that still capitalize on the ability of ultrasound to efficiently transmit energy to the brain noninvasively, focally, and at depth. Ultrasound Produces Extensive Brain Activation via a Cochlear PathwayGuo et al.NeuronMay 24, 2018In BriefGuo et al. apply ultrasound to the brain and record across cortical and subcortical regions in guinea pigs, revealing that ultrasound-induced activation occurs through a cochlear pathway. These findings challenge the idea that ultrasound directly activates neurons in the brain. Full-Text PDF Open ArchiveUltrasonic Neuromodulation Causes Widespread Cortical Activation via an Indirect Auditory MechanismSato et al.NeuronMay 24, 2018In BriefApplying ultrasound to the brain leads to cortical activity patterns consistent with auditory pathway stimulation rather than direct neuromodulation. These findings reveal an indirect auditory mechanism for ultrasound-induced cortical and motor responses, requiring consideration in future development of ultrasonic neuromodulation. Full-Text PDF Open Archive" @default.
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• W2806795384 title "Hearing out Ultrasound Neuromodulation" @default.
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