Transcranial Focused Ultrasound to the Right Prefrontal Cortex Improves Mood and Alters Functional Connectivity in Humans

Joseph L Sanguinetti, Stuart Hameroff, Ezra E Smith, Tomokazu Sato, Chris M W Daft, William J Tyler, John J B Allen, Joseph L Sanguinetti, Stuart Hameroff, Ezra E Smith, Tomokazu Sato, Chris M W Daft, William J Tyler, John J B Allen

Abstract

Transcranial focused ultrasound (tFUS) is an emerging method for non-invasive neuromodulation akin to transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS). tFUS offers several advantages over electromagnetic methods including high spatial resolution and the ability to reach deep brain targets. Here we describe two experiments assessing whether tFUS could modulate mood in healthy human volunteers by targeting the right inferior frontal gyrus (rIFG), an area implicated in mood and emotional regulation. In a randomized, placebo-controlled, double-blind study, participants received 30 s of 500 kHz tFUS or a placebo control. Visual Analog Mood Scales (VAMS) assessed mood four times within an hour (baseline and three times after tFUS). Participants who received tFUS reported an overall increase in Global Affect (GA), an aggregate score from the VAMS scale, indicating a positive shift in mood. Experiment 2 examined resting-state functional (FC) connectivity using functional magnetic resonance imaging (fMRI) following 2 min of 500 kHz tFUS at the rIFG. As in Experiment 1, tFUS enhanced self-reported mood states and also decreased FC in resting state networks related to emotion and mood regulation. These results suggest that tFUS can be used to modulate mood and emotional regulation networks in the prefrontal cortex.

Keywords: brain stimulation; functional connectivity; mood; neuromodulation; transcranial focused ultrasound.

Copyright © 2020 Sanguinetti, Hameroff, Smith, Sato, Daft, Tyler and Allen.

Figures

FIGURE 1
FIGURE 1
Acoustic simulation model on a representative CT scan of a male patient. The transducer was positioned over the F8 EEG electrode location on the scalp which centers over the rIFG. Hotter colors (red, yellow) indicate more intense sonication, cooler colors (blue, green) indicate less intense sonication.
FIGURE 2
FIGURE 2
Significant clusters for the rIFG seed-to-voxel analysis. Increased connectivity with rIFG is shown in red and decreased connectivity with rIFG in blue in the Post-scan relative to Baseline.
FIGURE 3
FIGURE 3
Significant clusters for the medial prefrontal cortex (MPFC) seed-to-voxel analysis. Increased connectivity with MPFC is shown in red and decreased connectivity with MPFC in blue in the Post-scan relative to Baseline.
FIGURE 4
FIGURE 4
Significant clusters for the medial posterior cingulate gyrus seed-to-voxel analysis. Increased connectivity with posterior cingulate gyrus is shown in red and decreased connectivity with posterior cingulate gyrus in blue in the Post-scan relative to Baseline.

References

    1. Ahearn E. P. E. (1997). The use of visual analog scales in mood disorders: a critical review. J. Psychiatr. Res. 31 569–579. 10.1016/S0022-3956(97)00029-0
    1. Andrews-hanna J. R., Reidler J. S., Sepulcre J., Poulin R., Buckner R. L. (2010). Functional-anatomic fractionation of the brain’s default network. Neuron 65 550–562. 10.1016/j.neuron.2010.02.005
    1. Aron A. R., Robbins T. W., Poldrack R. A. (2014). Inhibition and the right inferior frontal cortex: one decade on. Trends Cogn. Sci. 18 177–185. 10.1016/j.tics.2013.12.003
    1. Barnett S. B., Ter Haar G. R., Ziskin M. C., Rott H. D., Duck F. A., Maeda K. (2000). International recommendations and guidelines for the safe use of diagnostic ultrasound in medicine. Ultrasound Med. Biol. 26 355–366. 10.1016/S0301-5629(00)00204-0
    1. Behzadi Y., Restom K., Liau J., Liu T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37 90–101. 10.1016/j.neuroimage.2007.04.042
    1. Berkman E. T., Lieberman M. D. (2009). Using neuroscience to broaden emotion regulation: theoretical and methodological considerations. Soc. Pers. Psychol. Compass 3 475–493. 10.1111/j.1751-9004.2009.00186.x
    1. Bystritsky A., Korb A. S. (2015). A review of low-intensity transcranial focused ultrasound for clinical applications. Curr. Behav. Neurosci. Rep. 2 60–66. 10.1007/s40473-015-0039-0
    1. Chapman I. V., MacNally N. A., Tucker S. (1980). Ultrasound-induced changes in rates of influx and efflux of potassium ions in rat thymocytes in vitro. Ultrasound Med. Biol. 6 47–49. 10.1016/0301-5629(80)90063-0
    1. Chatrian G. E., Lettich E., Nelson P. L. (2018). Ten percent electrode system for topographic studies of spontaneous and evoked EEG activities. Am. J. EEG Technol. 25 83–92. 10.1080/00029238.1985.11080163
    1. Chen Y., Wang C., Zhu X., Tan Y., Zhong Y. (2015). Aberrant connectivity within the default mode network in first-episode, treatment-naïve major depressive disorder. J. Affect. Disord. 183 49–56. 10.1016/j.jad.2015.04.052
    1. Chiu P. H., Holmes A. J., Pizzagalli D. A. (2008). Dissociable recruitment of rostral anterior cingulate and inferior frontal cortex in emotional response inhibition. Neuroimage 42 988–997. 10.1016/j.neuroimage.2008.04.248
    1. Church C. C., Carstensen E. L., Nyborg W. L., Carson P. L., Frizzell L. A., Bailey M. R. (2008). The risk of exposure to diagnostic ultrasound in postnatal subjects: nonthermal mechanisms. J. Ultrasound Med. 27 565–592. 10.7863/jum.2008.27.4.565
    1. Clasen P. C., Beevers C. G., Mumford J. A., Schnyer D. M. (2014). Cognitive control network connectivity in adolescent women with and without a parental history of depression. Dev. Cogn. Neurosci. 7 13–22. 10.1016/j.dcn.2013.10.008
    1. Coan J. A., Allen J. J. (2004). Frontal EEG asymmetry as a moderator and mediator of emotion. Biol. Psychol. 67 7–50. 10.1016/j.biopsycho.2004.03.002
    1. Craig A. D. (2005). Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn. Sci. 9 566–571. 10.1016/j.tics.2005.10.005
    1. Dalecki D. (2004). Mechanical bioeffects of ultrasound. Ann. Rev. Biomed. Eng. 6 229–248. 10.1146/annurev.bioeng.6.040803.140126
    1. Dallapiazza R. F., Timbie K. F., Holmberg S., Gatesman J., Lopes M. B., Price R. J., et al. (2017). Noninvasive neuromodulation and thalamic mapping with low-intensity focused ultrasound. J. Neurosurg. 128 875–884. 10.3171/2016.11.JNS16976
    1. Davidson R. J. (2004). What does the prefrontal cortex “do” in affect: perspectives on frontal EEG asymmetry research. Biol. Psychol. 67 219–233. 10.1016/j.biopsycho.2004.03.008
    1. Downs M. E., Buch A., Karakatsani M. E., Teichert T., Sierra C., Chen S., et al. (2016). Focused ultrasound enhances decision-making in monkeys. BioRxiv [Preprint], 10.1101/041152
    1. Drevets W. C., Price J. L., Furey M. L. (2008). Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct. Funct. 213 93–118. 10.1007/s00429-008-0189-x
    1. Fini M., Tyler W. J. (2017). Transcranial focused ultrasound: a new tool for non-invasive neuromodulation. Intern. Rev. Psychiat. 29 168–177. 10.1080/09540261.2017.1302924
    1. Fitzgerald P. B., Laird A. R., Maller J., Daskalakis Z. J. (2008). A meta-analytic study of changes in brain activation in depression. Hum. Brain Mapp. 29 683–695. 10.1002/hbm.20426.A
    1. Folloni D., Verhagen L., Mars R. B., Fouragnan E., Constans C., Aubry J. F., et al. (2019). Manipulation of subcortical and deep cortical activity in the primate brain using transcranial focused ultrasound stimulation. Neuron 101 1109–1116.e5. 10.1016/j.neuron.2019.01.019
    1. Fry W. (1957). Use of intense ultrasound in neurological research. Am. J. Phys. Med. 37 143–147.r
    1. George M. S., Nahas Z., Molloy M., Speer A. M., Oliver N. C., Li X. B., et al. (2000). A controlled trial of daily left prefrontal cortex TMS for treating depression. Biol. Psychiatr. 48 962–970. 10.1016/S0006-3223(00)01048-9
    1. Goldin P. R., McRae K., Ramel W., Gross J. J. (2008). The neural bases of emotion regulation: reappraisal and suppression of negative emotion. Biol. Psychiatr. 63 577–586. 10.1016/j.biopsych.2007.05.031
    1. Golkar A., Lonsdorf T. B., Olsson A., Lindstrom K. M., Berrebi J., Fransson P., et al. (2012). Distinct contributions of the dorsolateral prefrontal and orbitofrontal cortex during emotion regulation. PLoS One 7:48107. 10.1371/journal.pone.0048107
    1. Greicius M. D., Krasnow B., Reiss A. L., Menon V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U.S.A. 100 253–258. 10.1073/pnas.0135058100
    1. Guo H., Hamilton M., Offutt S. J., Gloeckner C. D., Li T., Kim Y., et al. (2018). Ultrasound produces extensive brain activation via a cochlear pathway. Neuron 98 1020–1030.e4. 10.1016/j.neuron.2018.04.036
    1. Gusnard D. A., Akbudak E., Shulman G. L., Raichle M. E. (2001). Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98 4259–4264. 10.1073/pnas.071043098
    1. Hameroff S., Penrose R. (2014). Consciousness in the universe a review of the ‘ Orch OR ’ theory. Phys. Life Rev. 11 39–78. 10.1016/j.plrev.2013.08.002
    1. Hameroff S., Trakas M., Duffield C., Annabi E., Gerace M. B., Boyle P., et al. (2013). Transcranial ultrasound (TUS) effects on mental states: a pilot study. Brain Stimul. 6 409–415. 10.1016/j.brs.2012.05.002
    1. Hauptman J. S., DeSalles A. A., Espinoza R., Sedrak M., Ishida W. (2008). Potential surgical targets for deep brain stimulation in treatment-resistant depression. Neurosurg. Focus 25:E3. 10.3171/FOC/2008/25/7/E3
    1. Kaiser R. H., Andrews-Hanna J. R., Wager T. D., Pizzagalli D. A. (2015). Large-scale network dysfunction in major depressive disorder: a meta-analysis of resting-state functional connectivity. JAMA Psychiatry 72 603–611. 10.1001/jamapsychiatry.2015.0071
    1. Kaiser R. H., Whitfield-Gabrieli S., Dillon D. G., Goer F., Beltzer M., Minkel J., et al. (2016). Dynamic resting-state functional connectivity in major depression. Neuropsychopharmacology 41 1822–1830. 10.1038/npp.2015.352
    1. Kalisch R. (2009). The functional neuroanatomy of reappraisal: time matters. Neurosci. Biobehav. Rev. 33 1215–1226. 10.1016/j.neubiorev.2009.06.003
    1. Keng S. L., Smoski M. J., Robins C. J. (2011). Effects of mindfulness on psychological health: a review of empirical studies. Clin. Psychol. Rev. 31 1041–1056. 10.1016/j.cpr.2011.04.006
    1. Kerestes R., Bhagwagar Z., Nathan P. J., Meda S. A., Ladouceur C. D., Maloney K., et al. (2012). Prefrontal cortical response to emotional faces in individuals with major depressive disorder in remission. Psychiatry Res. Neuroimag. 202 30–37. 10.1016/j.pscychresns.2011.11.004
    1. Killingsworth M. A., Gilbert D. T. (2010). A wandering mind is an unhappy mind. Science 12:932. 10.1126/science.1192439
    1. Kim H., Lee S. D., Chiu A., Yoo S. S., Park S. (2014). Estimation of the spatial profile of neuromodulation and the temporal latency in motor responses induced by focused ultrasound brain stimulation. Neuroreport 25 475–479. 10.1097/WNR.0000000000000118
    1. Klem G. H., Lüders H. O., Jasper H. H., Elger C. (1999). The ten-twenty electrode system of the international federation. Electroencephalogr. Clin. Neurophysiol. 52 3–6.r
    1. Koessler L., Maillard L., Benhadid A., Vignal J. P., Felblinger J., Vespignani H., et al. (2009). Automated cortical projection of EEG sensors: anatomical correlation via the international 10-10 system. Neuroimage 46 64–72. 10.1016/j.neuroimage.2009.02.006
    1. Krasovitski B., Frenkel V., Shoham S., Kimmel E. (2011). Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects. Proc. Natl. Acad. Sci. U.S.A. 108 3258–3263. 10.1073/pnas.1015771108
    1. Kubanek J. (2018). Neuromodulation with transcranial focused ultrasound. Neurosurg. Focus 44:E14. 10.3171/2017.11.FOCUS17621
    1. Kubanek J., Shi J., Marsh J., Chen D., Deng C., Cui J. (2016). Ultrasound modulates ion channel currents. Sci. Rep. 6 1–14. 10.1038/srep24170
    1. Lee W., Chung Y. A., Jung Y., Song I.-U., Yoo S.-S. (2016a). Simultaneous acoustic stimulation of human primary and secondary somatosensory cortices using transcranial focused ultrasound. BMC Neurosci. 17:68. 10.1186/s12868-016-0303-6
    1. Lee W., Kim H.-C., Jung Y., Chung Y. A., Song I.-U., Lee J.-H., et al. (2016b). Transcranial focused ultrasound stimulation of human primary visual cortex. Sci. Rep. 6:34026. 10.1038/srep34026
    1. Lee W., Kim H., Jung Y., Song I.-U., Chung Y. A., Yoo S.-S. (2015). Image-guided transcranial focused ultrasound stimulates human primary somatosensory cortex. Sci. Rep. 5:8743. 10.1038/srep08743
    1. Lee W., Lee S. D., Park M. Y., Foley L., Purcell-Estabrook E., Kim H., et al. (2016c). Image-guided focused ultrasound-mediated regional brain stimulation in sheep. Ultrasound Med. Biol. 42 459–470. 10.1016/j.ultrasmedbio.2015.10.001
    1. Legon W., Ai L., Bansal P., Mueller J. K. (2018). Neuromodulation with single-element transcranial focused ultrasound in human thalamus. Hum. Brain Mapp 39 1995–2006. 10.1002/hbm.23981
    1. Legon W., Rowlands A., Opitz A., Sato T. F., Tyler W. J. (2012). Pulsed ultrasound differentially stimulates somatosensory circuits in humans as indicated by EEG and fMRI. PLoS One 7:e51177. 10.1371/journal.pone.0051177
    1. Legon W., Sato T. F., Opitz A., Mueller J., Barbour A., Williams A., et al. (2014). Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans. Nat. Neurosci. 17 322–329. 10.1038/nn.3620
    1. Lindquist K. A., Satpute A. B., Wager T. D., Weber J., Barrett L. F. (2016). The brain basis of positive and negative affect: evidence from a meta-analysis of the human neuroimaging literature. Cereb. Cortex 26 1910–1922. 10.1093/cercor/bhv001
    1. Lozano A. M., Mayberg H. S., Craddock R. C., Kennedy S. H. (2010). Stimulation for treatment- resistant depression. J. Am. Psychiatry 8 583–591.
    1. Marsh-Richard D. M., Hatzis E. S., Mathias C. W., Venditti N., Dougherty D. M. (2009). Adaptive Visual analog scales (AVAS): a modifiable software program for the creation, administration, and scoring of visual analog scales. Behav. Res. Methods 41 99–106. 10.3758/BRM.41.1.99
    1. Michael N., Erfurth A. (2004). Treatment of bipolar mania with right prefrontal rapid transcranial magnetic stimulation. J. Affect. Disord. 78 253–257. 10.1016/S0165-0327(02)00308-7
    1. Monk T. H. (1989). A visual analogue scale technique to measure global vigor and affect. Psychiatry Res. 27 89–99. 10.1016/0165-1781(89)90013-9
    1. Monti M. M., Schnakers C., Korb A. S., Bystritsky A., Vespa P. M. (2016). Non-invasive ultrasonic thalamic stimulation in disorders of consciousness after severe brain injury: a first-in-man report. Brain Stimul. 9 940–941. 10.1016/j.brs.2016.07.008
    1. Mueller J., Legon W., Opitz A., Sato T. F., Tyler W. J. (2014). Transcranial focused ultrasound modulates intrinsic and evoked EEG dynamics. Brain Stimul. 7 900–908. 10.1016/j.brs.2014.08.008
    1. Nyenhuis D. L. (1997). Standardization and validation of the standardization and validation of the visual analog mood scales. Clin. Neuropsychol. 11 407–415. 10.1080/13854049708400470
    1. O’Brien W. D. (2007). Ultrasound-biophysics mechanisms. Prog. Biophys. Mol. Biol. 93 212–255. 10.1016/j.pbiomolbio.2006.07.010
    1. Ochsner K. N., Gross J. J. (2005). The cognitive control of emotion. Trends Cogn. Sci. 9 242–249. 10.1016/j.tics.2005.03.010
    1. Parvaz M. A., MacNamara A., Goldstein R. Z., Hajcak G. (2012). Event-related induced frontal alpha as a marker of lateral prefrontal cortex activation during cognitive reappraisal. Cogn. Affect. Behav. Neurosci. 12 730–740. 10.3758/s13415-012-0107-9
    1. Phan K. L., Wager T., Taylor S. F., Liberzon I. (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16 331–348. 10.1006/nimg.2002.1087
    1. Phillips M. L., Drevets W. C., Rauch S. L., Lane R. (2003). Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol. Psychiatry 54 504–514. 10.1016/S0006-3223(03)00168-9
    1. Phillips M. L., Ladouceur C. D., Drevets W. C. (2008). A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol. Psychiatry 13 833–857. 10.1038/mp.2008.65
    1. Price J. L., Drevets W. C. (2012). Neural circuits underlying the pathophysiology of mood disorders. Trends Cogn. Sci. 16 61–71. 10.1016/j.tics.2011.12.011
    1. Ray R. D., Zald D. H. (2012). Anatomical insights into the interaction of emotion and cognition in the prefrontal cortex. Neurosci. Biobehav. Rev. 36 479–501. 10.1016/j.neubiorev.2011.08.005
    1. Rempel-Clower N. L. (2007). Role of orbitofrontal cortex connections in emotion. Ann. N. Y. Acad. Sci. U.S.A. 1121 72–86. 10.1196/annals.1401.026
    1. Renner F., Siep N., Arntz A., van de Ven V., Peeters F. P. M. L., Quaedflieg C. W. E. M., et al. (2017). Negative mood-induction modulates default mode network resting-state functional connectivity in chronic depression. J. Affect. Disord. 208 590–596. 10.1016/j.jad.2016.10.022
    1. Riva P., Romero Lauro L. J., DeWall C. N., Bushman B. J. (2012). Buffer the pain away: stimulating the right ventrolateral prefrontal cortex reduces pain following social exclusion. Psychol. Sci. 23 1473–1475. 10.1177/0956797612450894
    1. Riva P., Romero Lauro L. J., DeWall C. N., Chester D. S., Bushman B. J. (2015a). Reducing aggressive responses to social exclusion using transcranial direct current stimulation. Soc. Cogn. Affect. Neurosci. 10 352–356. 10.1093/scan/nsu053
    1. Riva P., Romero Lauro L. J., Vergallito A., DeWall C. N., Bushman B. J. (2015b). Electrified emotions: modulatory effects of transcranial direct stimulation on negative emotional reactions to social exclusion. Soc. Neurosci. 10 46–54. 10.1080/17470919.2014.946621
    1. Sahu S., Ghosh S., Ghosh B., Aswani K., Hirata K., Fujita D., et al. (2013). Atomic water channel controlling remarkable properties of a single brain microtubule: correlating single protein to its supramolecular assembly. Biosens. Bioelectron. 47 141–148. 10.1016/j.bios.2013.02.050
    1. Sang H. K., Hamann S. (2007). Neural correlates of positive and negative emotion regulation. J. Cogn. Neurosci. 19 776–798. 10.1162/jocn.2007.19.5.776
    1. Sanguinetti J. L., Smith E. E., Dieckman L., Vanuk J., Hameroff S., Allen J. J. B. (2013). Transcranial ultrasound for brain stimulation: effects on mood. Psychophysiology 50:S46.r
    1. Sassaroli E., Vykhodtseva N. (2016). Acoustic neuromodulation from a basic science prospective. J. Therap. Ultrasound 4 1–14. 10.1186/s40349-016-0061-z
    1. Sato T., Shapiro M. G., Tsao D. Y. (2018). Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism. Neuron 98 1031–1041.e5. 10.1016/j.neuron.2018.05.009
    1. Sheline Y. I., Barch D. M., Price J. L., Rundle M. M., Vaishnavi S. N., Snyder A. Z., et al. (2009). The default mode network and self-referential processes in depression. Proc. Natl. Acad. Sci. U.S.A. 106 1942–1947. 10.1073/pnas.0812686106
    1. Stewart J. L., Coan J. A., Towers D. N., Allen J. J. B. (2014). Resting and task-elicited prefrontal EEG alpha asymmetry in depression: support for the capability model. Psychophysiology 51 446–455. 10.1111/psyp.12191
    1. Taylor V. A., Daneault V., Grant J., Scavone G., Breton E., Roffe-vidal S., et al. (2013). Impact of meditation training on the default mode network during a restful state. Soc. Cogn. Affect. Neurosci. 8 4–14. 10.1093/scan/nsr087
    1. ter Haar G. (2007). Therapeutic applications of ultrasound. Prog. Biophys. Mol. Biol. 93 111–129. 10.1016/j.pbiomolbio.2006.07.005
    1. Touroutoglou A., Lindquist K. A., Dickerson B. C., Barrett L. F. (2014). Intrinsic connectivity in the human brain does not reveal networks for “basic” emotions. Soc. Cogn. Affect. Neurosci. 10 1257–1265. 10.1093/scan/nsv013
    1. Treeby B. E., Cox B. T. (2010). k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields. J. Biomed. Opt. 15:021314. 10.1117/1.3360308
    1. Tufail Y., Matyushov A., Baldwin N., Tauchmann M. L., Georges J., Yoshihiro A., et al. (2010). Transcranial pulsed ultrasound stimulates intact brain circuits. Neuron 66 681–694. 10.1016/j.neuron.2010.05.008
    1. Tyler W. J. (2011). Noninvasive neuromodulation with ultrasound? A continuum mechanics hypothesis. Neuroscientist 17 25–36. 10.1177/1073858409348066
    1. Tyler W. J., Tufail Y., Finsterwald M., Tauchmann M. L., Olson E. J., Majestic C. (2008). Remote excitation of neuronal circuits using low-intensity, low-frequency ultrasound. PLoS One 3:3511. 10.1371/journal.pone.0003511
    1. Vergallito A., Riva P., Pisoni A., Lauro L. J. R. (2018). Modulation of negative emotions through anodal tDCS over the right ventrolateral prefrontal cortex. Neuropsychologia 119 128–135. 10.1016/j.neuropsychologia.2018.07.037
    1. Verhagen L., Gallea C., Folloni D., Constans C., Jensen D. E. A., Ahnine H., et al. (2019). Offline impact of transcranial focused ultrasound on cortical activation in primates. eLife 8:e40541. 10.7554/eLife.40541
    1. Wager T. D., Davidson M. L., Hughes B. L., Lindquist M. A., Ochsner K. N. (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 59 1037–1050. 10.1016/j.neuron.2008.09.006
    1. Whitfield-Gabrieli S., Nieto-Castanon A. (2012). Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2 125–141. 10.1089/brain.2012.0073
    1. Wu J., Nyborg W. L. (2008). Ultrasound, cavitation bubbles and their interaction with cells. Adv. Drug Deliv. Rev. 60 1103–1116. 10.1016/j.addr.2008.03.009
    1. Yoo S.-S., Bystritsky A., Lee J.-H., Zhang Y., Fischer K., Min B.-K., et al. (2011). Focused ultrasound modulates region-specific brain activity. Neuroimage 56 1267–1275. 10.1016/j.neuroimage.2011.02.058

Source: PubMed

Sponsorer och medarbetare

Medicinska tillstånd

Läkemedelsinterventioner

3
Prenumerera