Direct visualization of non-human primate subcortical nuclei with contrast-enhanced high field MRI

NeuroImage

Volumn 58, Issue 1, 2011, Pages 60-68

  Tani, Naoki ^a,b,c   Joly, Olivier ^a,b   Iwamuro, Hirokazu ^a,b,c   Uhrig, Lynn ^a,b,d   Wiggins, Christopher J ^b   Poupon, Cyril ^b   Kolster, Hauke ^e   Vanduffel, Wim ^e,f   Le Bihan, Denis ^b   Palfi, Stéphane ^a,b,c   Jarraya, Béchir ^a,b,c  

^a INSERM   (France)

^b CEA SACLAY   (France)

^c FACULTÉ DE MÉDECINE   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e UNIVERSITY OF LEUVEN   (Belgium)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Electrophysiology; High field; Iron oxide; MRI; Non human primate; Subthalamic nucleus

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; BASAL GANGLION; BRAIN MAPPING; CAUDATE NUCLEUS; CONTRAST ENHANCEMENT; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; GRAY MATTER; IMAGE ANALYSIS; IMAGE PROCESSING; IMAGE QUALITY; LATERAL GENICULATE NUCLEUS; MALE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROBABILITY; PUTAMEN; SIGNAL NOISE RATIO; SUBTHALAMIC NUCLEUS;

AGING; ALGORITHMS; ANIMALS; BASAL GANGLIA; BRAIN MAPPING; BRAIN STEM; ELECTROPHYSIOLOGICAL PHENOMENA; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; INDIVIDUALITY; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; MICROELECTRODES; PROBABILITY; SIGNAL-TO-NOISE RATIO; SUBTHALAMIC NUCLEUS;

EID: 79960634107     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.06.019     Document Type: Article

References (61)

1. Airan R.D., Thompson K.R., Fenno L.E., Bernstein H., Deisseroth K. Temporally precise in vivo control of intracellular signalling. Nature 2009, 458:1025-1029.
2. Bernd H., De Kerviler E., Gaillard S., Bonnemain B. Safety and tolerability of ultrasmall superparamagnetic iron oxide contrast agent: comprehensive analysis of a clinical development program. Invest. Radiol. 2009, 44:336-342.
3. Bolan P.J., Yacoub E., Garwood M., Ugurbil K., Harel N. In vivo micro-MRI of intracortical neurovasculature. Neuroimage 2006, 32:62-69.
4. Breit S., LeBas J.F., Koudsie A., Schulz J., Benazzouz A., Pollak P., Benabid A.L. Pretargeting for the implantation of stimulation electrodes into the subthalamic nucleus: a comparative study of magnetic resonance imaging and ventriculography. Neurosurgery 2006, 58. (ONS83-95).
5. Chakravarty M., Frey S., Collins D. 'Digital Atlas of the Monkey Brain in Stereotactic Co-ordinates' in The Rhesus Monkey Brain in Stereotactic Coordinate, G Paxinos, XF Huang, M Petrides 2008, AW Toga, Elesevier.
6. Cho Z.H., Min H.K., Oh S.H., Han J.Y., Park C.W., Chi J.G., Kim Y.B., Paek S.H., Lozano A.M., Lee K.H. Direct visualization of deep brain stimulation targets in Parkinson disease with the use of 7-tesla magnetic resonance imaging. J. Neurosurg. 2010, 113:639-647.
7. Corot C., Port M., Guilbert I., Robert P., Raynal I., Robic C., Raynaud J.S., Prigent P., Dencausse A., Idee J.M. Superparamagnetic contrast agents. Molecular and Cellular MR Imaging 2007, 59-83. FL:CRC Press, Boca Raton. M.M.J. Modo, J.W.M. Bulte (Eds.).
8. Daniluk S., K.G.D., Ellias S.A., Novak P., Nazzaro J.M. Assessment of the variability in the anatomical position and size of the subthalamic nucleus among patients with advanced Parkinson's disease using magnetic resonance imaging. Acta Neurochir. (Wien) 2010, 152:201-210. (discussion 210).
9. Daniluk, S., K, G.D., Ellias, S.A., Novak, P., Nazzaro, J.M., Assessment of the variability in the anatomical position and size of the subthalamic nucleus among patients with advanced Parkinson's disease using magnetic resonance imaging. Acta Neurochir (Wien) 152, 201-210; discussion 210.
10. Danish S.F., Jaggi J.L., Moyer J.T., Finkel L., Baltuch G.H. Conventional MRI is inadequate to delineate the relationship between the red nucleus and subthalamic nucleus in Parkinson's disease. Stereotact. Funct. Neurosurg. 2006, 84:12-18.
11. DeLong M.R. Putamen: activity of single units during slow and rapid arm movements. Science 1973, 179:1240-1242.
12. DeLong M.R., Crutcher M.D., Georgopoulos A.P. Relations between movement and single cell discharge in the substantia nigra of the behaving monkey. J. Neurosci. 1983, 3:1599-1606.
13. DeLong M.R., Crutcher M.D., Georgopoulos A.P. Primate globus pallidus and subthalamic nucleus: functional organization. J. Neurophysiol. 1985, 53:530-543.
14. Dormont D., Ricciardi K.G., Tande D., Parain K., Menuel C., Galanaud D., Navarro S., Cornu P., Agid Y., Yelnik J. Is the subthalamic nucleus hypointense on T2-weighted images? A correlation study using MR imaging and stereotactic atlas data. AJNR Am. J. Neuroradiol. 2004, 25:1516-1523.
15. Ekstrom L.B., Roelfsema P.R., Arsenault J.T., Bonmassar G., Vanduffel W. Bottom-up dependent gating of frontal signals in early visual cortex. Science 2008, 321:414-417.
16. Elolf E., Bockermann V., Gringel T., Knauth M., Dechent P., Helms G. Improved visibility of the subthalamic nucleus on high-resolution stereotactic MR imaging by added susceptibility (T2*) contrast using multiple gradient echoes. AJNR Am. J. Neuroradiol. 2007, 28:1093-1094.
17. Fisel C.R., Ackerman J.L., Buxton R.B., Garrido L., Belliveau J.W., Rosen B.R., Brady T.J. MR contrast due to microscopically heterogeneous magnetic susceptibility: numerical simulations and applications to cerebral physiology. Magn. Reson. Med. 1991, 17:336-347.
18. Francois C., Nguyen-Legros J., Percheron G. Topographical and cytological localization of iron in rat and monkey brains. Brain Res. 1981, 215:317-322.
19. Francois C., Percheron G., Yelnik J., Heyner S. A histological atlas of the macaque (Macaca mulatta) substantia nigra in ventricular coordinates. Brain Res. Bull. 1985, 14:349-367.
20. Francois C., Yelnik J., Percheron G. A stereotaxic atlas of the basal ganglia in macaques. Brain Res. Bull. 1996, 41:151-158.
21. Frey S., Comeau R., Hynes B., Mackey S., Petrides M. Frameless stereotaxy in the nonhuman primate. Neuroimage 2004, 23:1226-1234.
22. Frey S., Pandya D., Chakravarty M., Petrides M., Collins D. MNI monkey space. Neurosci. Res. 2009, 65:S130.
23. Fried R. Topographic Brain Chemistry 1966, Academic Press Inc, New York.
24. Gradinaru V., Mogri M., Thompson K.R., Henderson J.M., Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science 2009, 324:354-359.
25. Hallgren B., Sourander P. The non-haemin iron in the cerebral cortex in Alzheimer's disease. J. Neurochem. 1960, 5:307-310.
26. Hamada I., DeLong M.R. Excitotoxic acid lesions of the primate subthalamic nucleus result in transient dyskinesias of the contralateral limbs. J. Neurophysiol. 1992, 68:1850-1858.
27. Hamberg L.M., Boccalini P., Stranjalis G., Hunter G.J., Huang Z., Halpern E., Weisskoff R.M., Moskowitz M.A., Rosen B.R. Continuous assessment of relative cerebral blood volume in transient ischemia using steady state susceptibility-contrast MRI. Magn. Reson. Med. 1996, 35:168-173.
28. Helms G., Draganski B., Frackowiak R., Ashburner J., Weiskopf N. Improved segmentation of deep brain grey matter structures using magnetization transfer (MT) parameter maps. Neuroimage 2009, 47:194-198.
29. Jenkinson M., Smith S. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 2001, 5:143-156.
30. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17:825-841.
31. Kalwani R.M., Bloy L., Elliott M.A., Gold J.I. A method for localizing microelectrode trajectories in the macaque brain using MRI. J. Neurosci. Methods 2009, 176:104-111.
32. Kaplitt M.G., Feigin A., Tang C., Fitzsimons H.L., Mattis P., Lawlor P.A., Bland R.J., Young D., Strybing K., Eidelberg D., During M.J. Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 2007, 369:2097-2105.
33. Le Duc G., Peoc'h M., Remy C., Charpy O., Muller R.N., Le Bas J.F., Decorps M. Use of T(2)-weighted susceptibility contrast MRI for mapping the blood volume in the glioma-bearing rat brain. Magn. Reson. Med. 1999, 42:754-761.
34. Leite F.P., Tsao D., Vanduffel W., Fize D., Sasaki Y., Wald L.L., Dale A.M., Kwong K.K., Orban G.A., Rosen B.R., Tootell R.B., Mandeville J.B. Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3Tesla. Neuroimage 2002, 16:283-294.
35. Limousin P., Krack P., Pollak P., Benazzouz A., Ardouin C., Hoffmann D., Benabid A.L. Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N. Engl. J. Med. 1998, 339:1105-1111.
36. Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
37. Mallet L., Schupbach M., N'Diaye K., Remy P., Bardinet E., Czernecki V., Welter M.L., Pelissolo A., Ruberg M., Agid Y., Yelnik J. Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:10661-10666.
38. Mallet L., Polosan M., Jaafari N., Baup N., Welter M.L., Fontaine D., du Montcel S.T., Yelnik J., Chereau I., Arbus C., Raoul S., Aouizerate B., Damier P., Chabardes S., Czernecki V., Ardouin C., Krebs M.O., Bardinet E., Chaynes P., Burbaud P., Cornu P., Derost P., Bougerol T., Bataille B., Mattei V., Dormont D., Devaux B., Verin M., Houeto J.L., Pollak P., Benabid A.L., Agid Y., Krack P., Millet B., Pelissolo A. Subthalamic nucleus stimulation in severe obsessive-compulsive disorder. N. Engl. J. Med. 2008, 359:2121-2134.
39. McLaren D.G., Kosmatka K.J., Oakes T.R., Kroenke C.D., Kohama S.G., Matochik J.A., Ingram D.K., Johnson S.C. A population-average MRI-based atlas collection of the rhesus macaque. Neuroimage 2009, 45:52-59.
40. Nambu A., Takada M., Inase M., Tokuno H. Dual somatotopical representations in the primate subthalamic nucleus: evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area. J. Neurosci. 1996, 16:2671-2683.
41. Neuwelt E.A., Hamilton B.E., Varallyay C.G., Rooney W.R., Edelman R.D., Jacobs P.M., Watnick S.G. Ultrasmall superparamagnetic iron oxides (USPIOs): a future alternative magnetic resonance (MR) contrast agent for patients at risk for nephrogenic systemic fibrosis (NSF)?. Kidney Int. 2009, 75:465-474.
42. O'Gorman R.L., Shmueli K., Ashkan K., Samuel M., Lythgoe D.J., Shahidiani A., Wastling S.J., Footman M., Selway R.P., Jarosz J. Optimal MRI methods for direct stereotactic targeting of the subthalamic nucleus and globus pallidus. Eur. Radiol. 2011, 21:130-136.
43. Ordidge R.J., Gorell J.M., Deniau J.C., Knight R.A., Helpern J.A. Assessment of relative brain iron concentrations using T2-weighted and T2*-weighted MRI at 3Tesla. Magn. Reson. Med. 1994, 32:335-341.
44. Patel G.H., Shulman G.L., Baker J.T., Akbudak E., Snyder A.Z., Snyder L.H., Corbetta M. Topographic organization of macaque area LIP. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4728-4733.
45. Paxinos G., Huang X.-F., Petrides M., Toga A.W. The Rhesus Monkey Brain in Stereotaxic Coordinates 2009, Academic Press, London. second edition.
46. Perles-Barbacaru T.A., Procissi D., Demyanenko A.V., Hall F.S., Uhl G.R., Jacobs R.E. Quantitative pharmacologic MRI: mapping the cerebral blood volume response to cocaine in dopamine transporter knockout mice. Neuroimage 2011, 55:622-628.
47. Saint-Cyr J.A., Hoque T., Pereira L.C., Dostrovsky J.O., Hutchison W.D., Mikulis D.J., Abosch A., Sime E., Lang A.E., Lozano A.M. Localization of clinically effective stimulating electrodes in the human subthalamic nucleus on magnetic resonance imaging. J. Neurosurg. 2002, 97:1152-1166.
48. Sigovan M., Boussel L., Sulaiman A., Sappey-Marinier D., Alsaid H., Desbleds-Mansard C., Ibarrola D., Gamondes D., Corot C., Lancelot E., Raynaud J.S., Vives V., Lacledere C., Violas X., Douek P.C., Canet-Soulas E. Rapid-clearance iron nanoparticles for inflammation imaging of atherosclerotic plaque: initial experience in animal model. Radiology 2009, 252:401-409.
49. Slavin K.V., Thulborn K.R., Wess C., Nersesyan H. Direct visualization of the human subthalamic nucleus with 3T MR imaging. AJNR Am. J. Neuroradiol. 2006, 27:80-84.
50. Srihasam K., Sullivan K., Savage T., Livingstone M.S. Noninvasive functional MRI in alert monkeys. Neuroimage 2011, 51:267-273.
51. Thomas L.O., Boyko O.B., Anthony D.C., Burger P.C. MR detection of brain iron. AJNR Am. J. Neuroradiol. 1993, 14:1043-1048.
52. Tolias A.S., Sultan F., Augath M., Oeltermann A., Tehovnik E.J., Schiller P.H., Logothetis N.K. Mapping cortical activity elicited with electrical microstimulation using fMRI in the macaque. Neuron 2005, 48:901-911.
53. Tsao D.Y., Freiwald W.A., Tootell R.B., Livingstone M.S. A cortical region consisting entirely of face-selective cells. Science 2006, 311:670-674.
54. Vanduffel W., Fize D., Mandeville J.B., Nelissen K., Van Hecke P., Rosen B.R., Tootell R.B., Orban G.A. Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys. Neuron 2001, 32:565-577.
55. Vanduffel W., Fize D., Peuskens H., Denys K., Sunaert S., Todd J.T., Orban G.A. Extracting 3D from motion: differences in human and monkey intraparietal cortex. Science 2002, 298:413-415.
56. Vertinsky A.T., Coenen V.A., Lang D.J., Kolind S., Honey C.R., Li D., Rauscher A. Localization of the subthalamic nucleus: optimization with susceptibility-weighted phase MR imaging. AJNR Am. J. Neuroradiol. 2009, 30:1717-1724.
57. Villringer A., Rosen B.R., Belliveau J.W., Ackerman J.L., Lauffer R.B., Buxton R.B., Chao Y.S., Wedeen V.J., Brady T.J. Dynamic imaging with lanthanide chelates in normal brain: contrast due to magnetic susceptibility effects. Magn. Reson. Med. 1988, 6:164-174.
58. Wichmann T., Bergman H., DeLong M.R. The primate subthalamic nucleus. I. Functional properties in intact animals. J. Neurophysiol. 1994, 72:494-506.
59. Wu E.X., Wong K.K., Andrassy M., Tang H. High-resolution in vivo CBV mapping with MRI in wild-type mice. Magn. Reson. Med. 2003, 49:765-770.
60. Yushkevich P.A., Piven J., Hazlett H.C., Smith R.G., Ho S., Gee J.C., Gerig G. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 2006, 31:1116-1128.
61. Zonenshayn M., Rezai A.R., Mogilner A.Y., Beric A., Sterio D., Kelly P.J. Comparison of anatomic and neurophysiological methods for subthalamic nucleus targeting. Neurosurgery 2000, 47:282-292. (discussion 292-284).