Assessment of brain responses to innocuous and noxious electrical forepaw stimulation in mice using BOLD fMRI

Pain

Volumn 151, Issue 3, 2010, Pages 655-663

  Bosshard, Simone C ^a   Baltes, Christof ^a   Wyss, Matthias T ^b,c   Mueggler, Thomas ^a   Weber, Bruno ^b   Rudin, Markus ^a,b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

BOLD signal; Electrical forepaw stimulation; Mouse fMRI; Somatosensory cortex

Indexed keywords

ISOFLURANE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; ECHO PLANAR IMAGING; FEMALE; FOREFOOT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMIC MONITORING; INSULA; MOUSE; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL PROCESSING; SOMATOSENSORY CORTEX; THALAMUS;

ANIMALS; AUTORADIOGRAPHY; BRAIN; BRAIN MAPPING; FEMALE; FORELIMB; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MICE; PAIN; PAIN PERCEPTION; PHYSICAL STIMULATION;

EID: 78049469319     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2010.08.025     Document Type: Article

References (55)

1. J.M. Adamczak, T.D. Farr, J.U. Seehafer, D. Kalthoff, and M. Hoehn High field BOLD response to forepaw stimulation in the mouse NeuroImage 51 2010 704 712
2. E.T. Ahrens, and D.J. Dubowitz Peripheral somatosensory fMRI in mouse at 11.7 T NMR Biomed 14 2001 318 324
3. C. Baltes, N. Radzwill, S. Bosshard, D. Marek, and M. Rudin Micro MRI of the mouse brain using a novel 400 MHz cryogenic quadrature RF probe NMR Biomed 22 2009 834 842
4. R.B. Buxton, K. Uludag, D.J. Dubowitz, and T.T. Liu Modeling the hemodynamic response to brain activation NeuroImage 23 2004 S220 233
5. R.B. Buxton, E.C. Wong, and L.R. Frank Dynamics of blood flow and oxygenation changes during brain activation: the balloon model Magn Reson Med 39 1998 855 864
6. K.L. Casey Forebrain mechanisms of nociception and pain: analysis through imaging Proc Natl Acad Sci USA 96 1999 7668 7674
7. M.J. Caterina, A. Leffler, A.B. Malmberg, W.J. Martin, J. Trafton, K.R. Petersen-Zeitz, M. Koltzenburg, A.I. Basbaum, and D. Julius Impaired nociception and pain sensation in mice lacking the capsaicin receptor Science 288 2000 306 313
8. C. Chang, and B.-C. Shyu A fMRI study of brain activations during non-noxious and noxious electrical stimulation of the sciatic nerve of rats Brain Res 897 2001 71 81
9. Y.R. Cho, C.P. Pawela, R. Li, D. Kao, M.L. Schulte, M.L. Runquist, J.G. Yan, H.S. Matloub, S.S. Jaradeh, A.G. Hudetz, and J.S. Hyde Refining the sensory and motor ratunculus of the rat upper extremity using fMRI and direct nerve stimulation Magn Reson Med 58 2007 901 909
10. D.R. Corfield, K. Murphy, O. Josephs, L. Adams, and R. Turner Does hypercapnia-induced cerebral vasodilation modulate the hemodynamic response to neural activation? NeuroImage 13 6 Pt 1 2001 1207 1211
11. K.D. Davis, S.J. Taylor, A.P. Crawley, M.L. Wood, and D.J. Mikulis Functional MRI of pain- and attention-related activations in the human cingulate cortex J Neurophysiol 77 1997 3370 3380
12. J.E. Deady, D.D. Koblin, E.I. Eger II, J.E. Heavner, and B. D'Aoust Anesthetic potencies and the unitary theory of narcosis Anesth Analg 60 1981 380 384
13. K. Franklin, and G. Paxinos The mouse brain in stereotaxic coordinates 1997 Academic Press San Diego
14. K.J. Friston, A. Mechelli, R. Turner, and C.J. Price Nonlinear responses in fMRI: the balloon model, volterra kernels, and other hemodynamics NeuroImage 12 2000 466 477
15. A.G. Goloshevsky, A.C. Silva, S.J. Dodd, and A.P. Koretsky BOLD fMRI and somatosensory evoked potentials are well correlated over a broad range of frequency content of somatosensory stimulation of the rat forepaw Brain Res 1195 2008 67 76
16. T.D. Hansen, D.S. Warner, M.M. Todd, and L.J. Vust The role of cerebral metabolism in determining the local cerebral blood flow effects of volatile anesthetics: evidence for persistent flow-metabolism coupling J Cereb Blood Flow Metab 9 1989 323 328
17. R.J. Harvey, U.B. Depner, H. Wassle, S. Ahmadi, C. Heindl, H. Reinold, T.G. Smart, K. Harvey, B. Schutz, O.M. Abo-Salem, A. Zimmer, P. Poisbeau, H. Welzl, D.P. Wolfer, H. Betz, H.U. Zeilhofer, and U. Muller GlyRα3: an essential target for spinal PGE2-mediated inflammatory pain sensitization Science 304 2004 884 887
18. E.W. Hsu, L.W. Hedlund, and J.R. MacFall Functional MRI of the rat somatosensory cortex: effects of hyperventilation Magn Reson Med 40 1998 421 426
19. L.J. Kemna, and S. Posse Effect of respiratory CO(2) changes on the temporal dynamics of the hemodynamic response in functional MR imaging NeuroImage 14 2001 642 649
20. I. Kida, and T. Yamamoto Stimulus frequency dependence of blood oxygenation level-dependent functional magnetic resonance imaging signals in the somatosensory cortex of rats Neurosci Res 62 2008 25 31
21. C. Ledent, O. Valverde, G. Cossu, F. Petitet, Ccedil, ois, J-F. Aubert, F. Beslot, oise, ouml, G.A. hme, A. Imperato, T. Pedrazzini, B.P. Roques, G. Vassart, W. Fratta, and M. Parmentier Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice Science 283 1999 401 404
22. C. Lenz, A. Rebel, K. van Ackern, W. Kuschinsky, and K.F. Waschke Local cerebral blood flow, local cerebral glucose utilization, and flow-metabolism coupling during sevoflurane versus isoflurane anesthesia in rats Anesthesiology 89 1998 1480 1488
23. J. Lilja, T. Endo, C. Hofstetter, E. Westman, J. Young, L. Olson, and C. Spenger Blood oxygenation level-dependent visualization of synaptic relay stations of sensory pathways along the neuroaxis in response to graded sensory stimulation of a limb J Neurosci 26 2006 6330 6336
24. Linden Avd, Camp Nv, P. Ramos-Cabrer, and M. Hoehn Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition NMR Biomed 20 2007 522 545
25. N.J. Maandag, D. Coman, B.G. Sanganahalli, P. Herman, A.J. Smith, H. Blumenfeld, R.G. Shulman, and F. Hyder Energetics of neuronal signaling and fMRI activity Proc Natl Acad Sci USA 104 2007 20546 20551
26. B.H. Manning, M.J. Morgan, and K.B. Franklin Morphine analgesia in the formalin test: evidence for forebrain and midbrain sites of action Neuroscience 63 1994 289 294
27. B.F. Matta, K.J. Heath, K. Tipping, and A.C. Summors Direct cerebral vasodilatory effects of sevoflurane and isoflurane Anesthesiology 91 1999 677 680
28. M.J. Millan The induction of pain: an integrative review Prog Neurobiol 57 1999 1 164
29. M.H. Mohajerani, D.A. McVea, M. Fingas, and T.H. Murphy Mirrored bilateral slow-wave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice J Neurosci 30 2010 3745 3751
30. T.J. Morrow, P.E. Paulson, P.J. Danneman, and K.L. Casey Regional changes in forebrain activation during the early and late phase of formalin nociception: analysis using cerebral blood flow in the rat Pain 75 1998 355 365
31. T. Mueggler, D. Baumann, M. Rausch, M. Staufenbiel, and M. Rudin Age-dependent impairment of somatosensory response in the amyloid precursor protein 23 transgenic mouse model of alzheimer's disease J Neurosci 23 2003 8231 8236
32. T. Mueggler, C. Sturchler-Pierrat, D. Baumann, M. Rausch, M. Staufenbiel, and M. Rudin Compromised hemodynamic response in amyloid precursor protein transgenic mice J Neurosci 22 2002 7218 7224
33. G. Nair, and T.Q. Duong Echo-planar BOLD fMRI of mice on a narrow-bore 9.4 T magnet Magn Reson Med 52 2004 430 434
34. M.A. Nassar, L.C. Stirling, G. Forlani, M.D. Baker, E.A. Matthews, A.H. Dickenson, and J.N. Wood Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain Proc Natl Acad Sci USA 101 2004 12706 12711
35. D. Ratering, C. Baltes, J. Nordmeyer-Massner, D. Marek, and M. Rudin Performance of a 200-MHz cryogenic RF probe designed for MRI and MRS of the murine brain Magn Reson Med 59 2008 1440 1447
36. T. Reese, B. Bjelke, R. Porszasz, D. Baumann, D. Bochelen, A. Sauter, and M. Rudin Regional brain activation by bicuculline visualized by functional magnetic resonance imaging. Time-resolved assessment of bicuculline-induced changes in local cerebral blood volume using an intravascular contrast agent NMR Biomed 13 2000 43 49
37. T. Reese, D. Bochelen, D. Baumann, M. Rausch, A. Sauter, and M. Rudin Impaired functionality of reperfused brain tissue following short transient focal ischemia in rats Magn Reson Imaging 20 2002 447 454
38. 2+ waves in rat spinal dorsal horn Eur J NeuroSci 22 2005 1967 1976
39. B.G. Sanganahalli, C.J. Bailey, P. Herman, and F. Hyder Tactile and non-tactile sensory paradigms for fMRI and neurophysiologic studies in rodents Methods Mol Biol 489 2009 213 242
40. A. Sauter, T. Reese, R. Porszasz, D. Baumann, M. Rausch, and M. Rudin Recovery of function in cytoprotected cerebral cortex in rat stroke model assessed by functional MRI Magn Reson Med 47 2002 759 765
41. A.C. Silva, A.P. Koretsky, and J.H. Duyn Functional MRI impulse response for BOLD and CBV contrast in rat somatosensory cortex Magn Reson Med 57 2007 1110 1118
42. A.C. Silva, S.P. Lee, G. Yang, C. Iadecola, and S.G. Kim Simultaneous blood oxygenation level-dependent and cerebral blood flow functional magnetic resonance imaging during forepaw stimulation in the rat J Cereb Blood Flow Metab 19 1999 871 879
43. M.G. Sommers, Jv Egmond, L.H. Booij, and A. Heerschap Isoflurane anesthesia is a valuable alternative for alpha-chloralose anesthesia in the forepaw stimulation model in rats NMR Biomed 22 2009 414 418
44. N. Spaeth, M.T. Wyss, B. Weber, S. Scheidegger, A. Lutz, J. Verwey, I. Radovanovic, J. Pahnke, D. Wild, G. Westera, D. Weishaupt, D.M. Hermann, B. Kaser-Hotz, A. Aguzzi, and A. Buck Uptake of 18F-fluorocholine, 18F-fluoroethyl-L-tyrosine, and 18F-FDG in acute cerebral radiation injury in the rat: implications for separation of radiation necrosis from tumor recurrence J Nucl Med 45 2004 1931 1938
45. A. Stancák, J. Svoboda, R. Rachmanová, J. Vrána, J. Králík, and J. Tintera Desynchronization of cortical rhythms following cutaneous stimulation: effects of stimulus repetition and intensity, and of the size of corpus callosum Clin Neurophysiol 114 2003 1936 1947
46. R. Staud, J.G. Craggs, M.E. Robinson, W.M. Perlstein, and D.D. Price Brain activity related to temporal summation of C-fiber evoked pain Pain 129 2007 130 142
47. M.T. Sutherland, and A.C. Tang Reliable detection of bilateral activation in human primary somatosensory cortex by unilateral median nerve stimulation NeuroImage 33 2006 1042 1054
48. E. Sydekum, C. Baltes, A. Ghosh, T. Mueggler, M.E. Schwab, and M. Rudin Functional reorganization in rat somatosensory cortex assessed by fMRI: elastic image registration based on structural landmarks in fMRI images and application to spinal cord injured rats NeuroImage 44 2009 1345 1354
49. P. Terekhin, and C. Forster Hypocapnia related changes in pain-induced brain activation as measured by functional MRI Neurosci Lett 400 2006 110 114
50. 2 during surgical anesthesia in mice J Neurosci Methods 159 2007 261 267
51. H.E. Torebjork, R.H. LaMotte, and C.J. Robinson Peripheral neural correlates of magnitude of cutaneous pain and hyperalgesia: simultaneous recordings in humans of sensory judgments of pain and evoked responses in nociceptors with C-fibers J Neurophysiol 51 1984 325 339
52. K. Torquati, V. Pizzella, C. Babiloni, C.D. Gratta, S.D. Penna, A. Ferretti, R. Franciotti, P.M. Rossini, and G.L. Romani Nociceptive and non-nociceptive sub-regions in the human secondary somatosensory cortex: an MEG study using fMRI constraints NeuroImage 26 2005 48 56
53. U.I. Tuor, K. Malisza, T. Foniok, R. Papadimitropoulos, M. Jarmasz, R. Somorjai, and P. Kozlowski Functional magnetic resonance imaging in rats subjected to intense electrical and noxious chemical stimulation of the forepaw Pain 87 2000 315 324
54. S.G. Wilson, and J.S. Mogil Measuring pain in the (knockout) mouse: big challenges in a small mammal Behav Brain Res 125 2001 65 73
55. M.T. Wyss, N.M. Obrist, F. Haiss, R. Eckert, R. Stanley, C. Burger, A. Buck, and B. Weber A beta-scintillator for surface measurements of radiotracer kinetics in the intact rodent cortex NeuroImage 48 2009 339 347