Pulsed Ultrasound Differentially Stimulates Somatosensory Circuits in Humans as Indicated by EEG and fMRI

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Legon, Wynn ^a   Rowlands, Abby ^a   Opitz, Alexander ^a   Sato, Tomokazu F ^a   Tyler, William J ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANTERIOR MEDULLA CINGULATE CORTEX; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; EVOKED SOMATOSENSORY RESPONSE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INSULA; MALE; NERVE STIMULATION; PARIETAL OPERCULUM; PRIMARY SOMATOSENSORY CORTEX; PULSED ULTRASONIC NEUROSTIMULATION; SENSATION; SOMATOSENSORY STIMULATION; SUPRAMARGINAL GYRUS; VIBRATION SENSE; WAVEFORM;

ADULT; ELECTROENCEPHALOGRAPHY; FEMALE; FINGERS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; OXYGEN; PHYSICAL STIMULATION; SOMATOSENSORY CORTEX; TOUCH; VIBRATION; YOUNG ADULT;

EID: 84870752721     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051177     Document Type: Article

References (60)

1. Rolke R, Magerl W, Campbell KA, Schalber C, Caspari S, et al. (2006) Quantitative sensory testing: a comprehensive protocol for clinical trials. Eur J Pain 10: 77-88.
2. Lumpkin EA, Caterina MJ, (2007) Mechanisms of sensory transduction in the skin. Nature 445: 858-865.
3. Tsunozaki M, Bautista DM, (2009) Mammalian somatosensory mechanotransduction. Curr Opin Neurobiol 19: 362-369.
4. Delmas P, Hao J, Rodat-Despoix L, (2011) Molecular mechanisms of mechanotransduction in mammalian sensory neurons. Nat Rev Neurosci 12: 139-153.
5. Cruccu G, Aminoff MJ, Curio G, Guerit JM, Kakigi R, et al. (2008) Recommendations for the clinical use of somatosensory-evoked potentials. Clin Neurophysiol 119: 1705-1719.
6. Granovsky Y, Matre D, Sokolik A, Lorenz J, Casey KL, (2005) Thermoreceptive innervation of human glabrous and hairy skin: a contact heat evoked potential analysis. PAIN 115: 238-247.
7. Iannetti GD, Zambreanu L, Tracey I, (2006) Similar nociceptive afferents mediate psychophysical and electrophysiological responses to heat stimulation of glabrous and hairy skin in humans. J Physiol 577: 235-248.
8. Tolle TR, Kaufmann T, Siessmeier T, Lautenbacher S, Berthele A, et al. (1999) Region-specific encoding of sensory and affective components of pain in the human brain: a positron emission tomography correlation analysis. Ann Neurol 45: 40-47.
9. Craig AD, (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10: 59-70.
10. Peltz E, Seifert F, DeCol R, Dorfler A, Schwab S, et al. (2011) Functional connectivity of the human insular cortex during noxious and innocuous thermal stimulation. NeuroImage 54: 1324-1335.
11. Gavrilov LR, Gersuni GV, Ilyinsky OB, Sirotyuk MG, Tsirulnikov EM, et al. (1976) The effect of focused ultrasound on the skin and deep nerve structures of man and animal. Prog Brain Res 43: 279-292.
12. Gavrilov LR, Tsirulnikov EM, Davies IA, (1996) Application of focused ultrasound for the stimulation of neural structures. Ultrasound Med Biol 22: 179-192.
13. Dickey TC, Tych R, Kliot M, Loeser JD, Pederson K, et al. (2012) Intense Focused Ultrasound Can Reliably Induce Sensations in Human Test Subjects in a Manner Correlated with the Density of Their Mechanoreceptors. Ultrasound in Medicine and Biology 38: 85-90.
14. Wright A, Davies IA, (1989) The Recording of Brain Evoked-Potentials Resulting from Intra-Articular Focused Ultrasonic Stimulation - a New Experimental-Model for Investigating Joint Pain in Humans. Neurosci Lett 97: 145-150.
15. Wright A, Davies IA, Riddell JG, (1993) Intraarticular Ultrasonic Stimulation and Intracutaneous Electrical-Stimulation - Evoked-Potential and Visual Analog Scale Data. PAIN 52: 149-155.
16. Tyler WJ, Tufail Y, Finsterwald M, Tauchmann ML, Olson EJ, et al. (2008) Remote excitation of neuronal circuits using low-intensity, low-frequency ultrasound. PLoS One 3: e3511.
17. Tufail Y, Matyushov A, Baldwin N, Tauchmann ML, Georges J, et al. (2010) Transcranial pulsed ultrasound stimulates intact brain circuits. Neuron 66: 681-694.
18. Tyler WJ, (2011) Noninvasive Neuromodulation with Ultrasound? A Continuum Mechanics Hypothesis. Neuroscientist 17: 25-36.
19. Oldfield RC, (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9: 97-113.
20. Tufail Y, Yoshihiro A, Pati S, Li MM, Tyler WJ, (2011) Ultrasonic neuromodulation by brain stimulation with transcranial ultrasound. Nat Protoc 6: 1453-1470.
21. Eickhoff S, Walters NB, Schleicher A, Kril J, Egan GF, et al. (2005) High-resolution MRI reflects myeloarchitecture and cytoarchitecture of human cerebral cortex. Hum Brain Mapp 24: 206-215.
22. Delorme A, Makeig S, (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134: 9-21.
23. Gevins A, Le J, Martin NK, Brickett P, Desmond J, et al. (1994) High resolution EEG: 124-channel recording, spatial deblurring and MRI integration methods. Electroencephalogr Clin Neurophysiol 90: 337-358.
24. Perrin F, Bertrand O, Pernier J, (1987) Scalp current density mapping: value and estimation from potential data. IEEE Trans Biomed Eng 34: 283-288.
25. Perrin F, Pernier J, Bertrand O, Echallier JF, (1989) Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neurophysiol 72: 184-187.
26. Dalecki D, (2004) Mechanical bioeffects of ultrasound. Annu Rev Biomed Eng 6: 229-248.
27. O'Brien WD Jr, (2007) Ultrasound-biophysics mechanisms. Prog Biophys Mol Biol 93: 212-255.
28. Gavrilov LR, Gersuni GV, Ilyinski OB, Tsirulnikov EM, Shchekanov EE, (1977) A study of reception with the use of focused ultrasound. I. Effects on the skin and deep receptor structures in man. Brain Res 135: 265-277.
29. Treede RD, Kief S, Holzer T, Bromm B, (1988) Late somatosensory evoked cerebral potentials in response to cutaneous heat stimuli. Electroencephalogr Clin Neurophysiol 70: 429-441.
30. Chen AC, Niddam DM, Arendt-Nielsen L, (2001) Contact heat evoked potentials as a valid means to study nociceptive pathways in human subjects. Neurosci Lett 316: 79-82.
31. Allison T, Mccarthy G, Wood CC, Darcey TM, Spencer DD, et al. (1989) Human Cortical Potentials-Evoked by Stimulation of the Median Nerve. 1. Cytoarchitectonic Areas Generating Short-Latency Activity. Journal of Neurophysiology 62: 694-710.
32. Allison T, Mccarthy G, Wood CC, (1992) The Relationship between Human Long-Latency Somatosensory Evoked-Potentials Recorded from the Cortical Surface and from the Scalp. Electroencephalogr Clin Neurophysiol 84: 301-314.
33. Frot M, Garcia-Larrea L, Guenot M, Mauguiere F, (2001) Responses of the supra-sylvian (SII) cortex in humans to painful and innocuous stimuli. A study using intra-cerebral recordings. PAIN 94: 65-73.
34. Iannetti GD, Truini A, Romaniello A, Galeotti F, Rizzo C, et al. (2003) Evidence of a specific spinal pathway for the sense of warmth in humans. J Neurophysiol 89: 562-570.
35. Treede RD, (2003) Neurophysiological studies of pain pathways in peripheral and central nervous system disorders. J Neurol 250: 1152-1161.
36. Valentini E, Hu L, Chakrabarti B, Hu Y, Aglioti SM, et al. (2012) The primary somatosensory cortex largely contributes to the early part of the cortical response elicited by nociceptive stimuli. NeuroImage 59: 1571-1581.
37. Eickhoff SB, Grefkes C, Zilles K, Fink GR, (2007) The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. Cereb Cortex 17: 1800-1811.
38. Burton H, MacLeod AMK, Videen TO, Raichle ME, (1997) Multiple foci in parietal and frontal cortex activated by rubbing embossed grating patterns across fingerpads: A positron emission tomography study in humans. Cerebral Cortex 7: 3-17.
39. Gelnar PA, Krauss BR, Szeverenyi NM, Apkarian AV, (1998) Fingertip representation in the human somatosensory cortex: an fMRI study. NeuroImage 7: 261-283.
40. Buchel C, Bornhovd K, Quante M, Glauche V, Bromm B, et al. (2002) Dissociable neural responses related to pain intensity, stimulus intensity, and stimulus awareness within the anterior cingulate cortex: a parametric single-trial laser functional magnetic resonance imaging study. J Neurosci 22: 970-976.
41. Ringler R, Greiner M, Kohlloeffel L, Handwerker HO, Forster C, (2003) BOLD effects in different areas of the cerebral cortex during painful mechanical stimulation. PAIN 105: 445-453.
42. Oertel BG, Preibisch C, Martin T, Walter C, Gamer M, et al. (2012) Separating brain processing of pain from that of stimulus intensity. Hum Brain Mapp 33: 883-894.
43. Burton H, Sinclair RJ, (2000) Tactile-spatial and cross-modal attention effects in the primary somatosensory cortical areas 3b and 1-2 of rhesus monkeys. Somatosens Mot Res 17: 213-228.
44. Van de Winckel A, Sunaert S, Wenderoth N, Peeters R, Van Hecke P, et al. (2005) Passive somatosensory discrimination tasks in healthy volunteers: Differential networks involved in familiar versus unfamiliar shape and length discrimination. NeuroImage 26: 441-453.
45. Hegner YL, Lee Y, Grodd W, Braun C, (2010) Comparing Tactile Pattern and Vibrotactile Frequency Discrimination: A Human fMRI Study. Journal of Neurophysiology 103: 3115-3122.
46. Bodegard A, Geyer S, Grefkes C, Zilles K, Roland PE, (2001) Hierarchical processing of tactile shape in the human brain. Neuron 31: 317-328.
47. Peyron R, Laurent B, Garcia-Larrea L, (2000) Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiol Clin 30: 263-288.
48. Tommerdahl M, Favorov OV, Whitsel BL, (2010) Dynamic representations of the somatosensory cortex. Neurosci Biobehav Rev 34: 160-170.
49. Holland CK, Apfel RE, (1990) Thresholds for transient cavitation produced by pulsed ultrasound in a controlled nuclei environment. J Acoust Soc Am 88: 2059-2069.
50. Brotchie A, Grieser F, Ashokkumar M, (2009) Effect of power and frequency on bubble-size distributions in acoustic cavitation. Phys Rev Lett 102: 084302.
51. Sommer FG, Pounds D, (1982) Transient cavitation in tissues during ultrasonically induced hyperthermia. Med Phys 9: 1-3.
52. Hynynen K, (1991) The threshold for thermally significant cavitation in dog's thigh muscle in vivo. Ultrasound Med Biol 17: 157-169.
53. Christensen AP, Corey DP, (2007) TRP channels in mechanosensation: direct or indirect activation? Nat Rev Neurosci 8: 510-521.
54. Arnadottir J, Chalfie M, (2010) Eukaryotic mechanosensitive channels. Annu Rev Biophys 39: 111-137.
55. Hamill OP, (2006) Twenty odd years of stretch-sensitive channels. Pflugers Arch 453: 333-351.
56. Galkin VE, Orlova A, Egelman EH, (2012) Actin filaments as tension sensors. Curr Biol 22: R96-R101.
57. Meng F, Suchyna TM, Lazakovitch E, Gronostajski RM, Sachs F, (2011) Real Time FRET Based Detection of Mechanical Stress in Cytoskeletal and Extracellular Matrix Proteins. Cell Mol Bioeng 4: 148-159.
58. Qin Z, Buehler MJ, Kreplak L, (2010) A multi-scale approach to understand the mechanobiology of intermediate filaments. J Biomech 43: 15-22.
59. Hameroff S, Trakas M, Duffield C, Annabi E, Bagambhrini Gerace M, et al. (2012) Transcranial ultrasound (TUS) effects on mental states: A pilot study. Brain Stimul.
60. Cruccu G, Anand P, Attal N, Garcia-Larrea L, Haanpaa M, et al. (2004) EFNS guidelines on neuropathic pain assessment. Eur J Neurol 11: 153-162.