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Noninvasive Neuromodulation and Thalamic Mapping with Low-Intensity Focused Ultrasound

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Noninvasive Neuromodulation and Thalamic Mapping with Low-Intensity Focused Ultrasound LABORATORY INVESTIGATION J Neurosurg 128:875–884, 2018 Noninvasive neuromodulation and thalamic mapping with low-intensity focused ultrasound Robert F. Dallapiazza, MD, PhD,1 Kelsie F. Timbie, PhD,2 Stephen Holmberg, CINM,6 Jeremy Gatesman, BA, LVT,3 M. Beatriz Lopes, MD, PhD,4 Richard J. Price, PhD,2 G. Wilson Miller, PhD,5 and W. Jeffrey Elias, MD1 Departments of 1Neurosurgery, 2Biomedical Engineering, 3Comparative Medicine, 4Pathology (Neuropathology), and 5Radiology, and 6Impulse Monitoring, University of Virginia, Charlottesville, Virginia OBJECTIVE Ultrasound can be precisely focused through the intact human skull to target deep regions of the brain for stereotactic ablations. Acoustic energy at much lower intensities is capable of both exciting and inhibiting neural tissues without causing tissue heating or damage. The objective of this study was to demonstrate the effects of low-intensity focused ultrasound (LIFU) for neuromodulation and selective mapping in the thalamus of a large-brain animal. METHODS Ten Yorkshire swine (Sus scrofa domesticus) were used in this study. In the first neuromodulation experi- ment, the lemniscal sensory thalamus was stereotactically targeted with LIFU, and somatosensory evoked potentials (SSEPs) were monitored. In a second mapping experiment, the ventromedial and ventroposterolateral sensory thalamic nuclei were alternately targeted with LIFU, while both trigeminal and tibial evoked SSEPs were recorded. Temperature at the acoustic focus was assessed using MR thermography. At the end of the experiments, all tissues were assessed histologically for damage. RESULTS LIFU targeted to the ventroposterolateral thalamic nucleus suppressed SSEP amplitude to 71.6% ± 11.4% (mean ± SD) compared with baseline recordings. Second, we found a similar degree of inhibition with a high spatial res- olution (~ 2 mm) since adjacent thalamic nuclei could be selectively inhibited. The ventromedial thalamic nucleus could be inhibited without affecting the ventrolateral nucleus. During MR thermography imaging, there was no observed tissue heating during LIFU sonications and no histological evidence of tissue damage. CONCLUSIONS These results suggest that LIFU can be safely used to modulate neuronal circuits in the central ner- vous system and that noninvasive brain mapping with focused ultrasound may be feasible in humans. https://thejns.org/doi/abs/10.3171/2016.11.JNS16976 KEY WORDS neuromodulation; noninvasive; brain mapping; low intensity focused ultrasound; thalamus; somatosensory evoked potentials; functional neurosurgery COUSTIC energy has long been known to influence Advances in noninvasive, transcranial delivery of ultra- the activity of electrically excitable tissues, in- sound over the past 15 years have renewed an interest in cluding muscle, peripheral nerves, and the central its use for neurosurgical applications.3–6,18,19,28 Transcranial nervousA system.1,13,15,16 During the 1950s, high-intensity HIFU can be delivered in a precise, highly localized man- focused ultrasound (HIFU) was used experimentally to ner with millimeter accuracy to induce tissue ablation in reversibly inhibit neuronal activity through moderate heat- deep cerebral structures in the human brain. The clinical ing below the threshold for tissue ablation,14 and it was effects of HIFU therapy have been highlighted in several used clinically to treat patients with movement disorders recent clinical trials involving patients with movement dis- and brain tumors.17,27 orders and psychiatric diseases.2,9,11,20,25,26 ABBREVIATIONS FUS = focused ultrasound; H & E = hematoxylin and eosin; HIFU = high-intensity focused ultrasound; ISA = spatial average intensity; LFB = Luxol fast blue; LIFU = low-intensity focused ultrasound; PRFS = proton resonance frequency shift; SSEP = somatosensory evoked potential; VPL = ventroposterolateral thalamic nucleus; VPM = ventroposteromedial thalamic nucleus. SUBMITTED April 16, 2016. ACCEPTED November 17, 2016. INCLUDE WHEN CITING Published online April 21, 2017; DOI: 10.3171/2016.11.JNS16976. ©AANS 2018, except where prohibited by US copyright law J Neurosurg Volume 128 • March 2018 875 Unauthenticated | Downloaded 10/04/21 01:36 PM UTC R. F. Dallapiazza et al. Perhaps the most exciting, yet largely unharnessed, Upon completion of electrophysiological recordings in potential for transcranial ultrasound is for neuromodula- all 8 animals, the contralateral (left) thalamus was target- tion and noninvasive brain mapping with low-intensity ed first with LIFU and subsequently with HIFU sonica- focused ultrasound (LIFU). The mechanisms of LIFU are tions during real-time MR thermography. Two additional nonthermal and are thought to be mediated by mechanical animals underwent HIFU ablations only, during electro- forces within the brain tissue.31,32 LIFU shares many of physiological recordings. Tissue from all 10 animals was the appealing characteristics of HIFU. It can be focused submitted for histological analysis. through the human skull to target deep cerebral structures without affecting intervening tissues, while demonstrating Anesthesia and Surgery a high spatial accuracy that is not available with current Anesthesia was induced with a single intramuscular noninvasive neuromodulation methods, such as transcra- injection of tiletamine and zolazepam (Telazol, 6 mg/kg) nial magnetic stimulation or transcranial electrical stimu- and xylazine (2 mg/kg). The animals were moved from the lation. cage area to a surgical preparation room. An intravenous Most current studies of LIFU neuromodulation have catheter was place in the marginal vein of each ear. An en- applied ultrasound to the motor cortex of rodents to elicit 21,29,33,34 dotracheal tube was placed and secured to the mandible. muscle contractions. Limb, tail, whisker, and eye Anesthesia was maintained with a continuous infusion of muscles can be independently activated, depending on the propofol at 10 mg/kg/hr. Animals were placed on a venti- LIFU focus. However, somatotopic mapping is difficult lator (10 ml/kg tidal volume) at a rate of 18 breaths/minute due to the mismatch in size between the acoustic focus of room air. Prior to SSEP testing, an intravenous drip of and the rodent brain.21 More recently, Legon et al.24 and 22 rocuronium (200 mg diluted in a 500-ml bag of normal Lee et al. applied LIFU to the human somatosensory saline) was initiated. The drip rate was set to administer cortex, demonstrating that ultrasound could suppress me- 2.0–2.5 mg/kg/hr. The effects of paralytics were assessed dian nerve evoked potentials on EEG and stimulate sub- using physical indicators such as palpebral reflex, eye po- jective somatosensory phenomena. sition, toe pinch, and jaw tone. Depth of anesthesia and Despite these exciting advances, LIFU neuromodula- analgesia were monitored by continuous measurements of tion needs to be translated and refined in large-brain ani- 8,23 heart rate and oxygen saturation. mal models. Furthermore, prior research has not fully To implant the epidural electrode, the scalp was first highlighted the capabilities of LIFU neuromodulation— infiltrated with 0.25% bupivicaine (Marcaine), and then namely, its ability to noninvasively penetrate deep cortical a U-shaped incision was made to reflect the scalp posteri- structures (beyond the cerebral cortex) with a high spatial orly. A 4 × 4–cm craniectomy centered on the bregma was resolution (millimeter scale). In this article, we describe a performed using a high-speed drill, and the dura mater large-brain animal model that targets LIFU to the somato- was kept intact. A 4-contact epidural recording electrode sensory thalamus, alters somatosensory evoked potentials was placed over the right cerebral hemisphere and tucked (SSEPs) for long durations, is selective and precise within laterally out of the ultrasonic beam path. The electrode 2 mm, and does not result in tissue heating or histological was secured to the dura and tunneled posteriorly for elec- damage. trophysiological recordings. Methods Electrophysiology and SSEPs Animals and Experimental Design A 32-channel recording system with 9 channels for All experiments were approved by the University of stimulation was used to measure SSEPs in swine (Cadwell Virginia Animal Care and Use Committee. Female York- Cascade Pro). MR-compatible platinum electrodes (Gen- shire swine (Sus scrofa domesticus) weighing 25–30 lbs, uine Grass F-E2–24) were used for bipolar stimulation age 6–7 weeks, were used in these experiments. Ten ani- of the trigeminal (snout), median (forelimb), and tibial mals were used in total. (hindlimb) nerves. Recording electrodes were placed mid- LIFU neuromodulation was assessed in the first cohort line at the front of the skull, midline at the back of the of 4 animals. The right thalamus was targeted with LIFU. skull, 4 cm laterally in each direction from midline at the The left forelimb (median nerve) was stimulated, and re- back of the skull, over the cervical spine, and bilaterally cordings were made from an epidural grid placed over over the brachial plexus in the shoulder. A 1 × 4 cortical the right cerebral hemisphere. Control experiments were grid was implanted over the right lateral convexity of the conducted during alternate sonications; the contralateral cortex to optimize recordings. All recordings were refer- (left) thalamus was targeted with LIFU during left median enced to a cephalic recording electrode with the exception nerve stimulation and right cortical monitoring. of recordings from the brachial
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