Functional neuroimaging of the baboon during concurrent image-guided transcranial magnetic stimulation

NeuroImage

Volumn 57, Issue 4, 2011, Pages 1393-1401

  Salinas, Felipe S ^a   Szabó, C Ákos ^a,b   Zhang, Wei ^a   Jones, Lisa ^a   Leland, M Michelle ^a   Wey, Hsiao Ying ^a   Duong, Timothy Q ^a   Fox, Peter T ^a   Narayana, Shalini ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Animal models; FMRI; Motor cortex; PET; TMS

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BABOON; BOLD SIGNAL; BRAIN BLOOD FLOW; BRAIN REGION; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; EXPERIMENTAL MODEL; FEMALE; FUNCTIONAL ANATOMY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; IMAGE PROCESSING; MALE; NEUROIMAGING; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; TRANSCRANIAL MAGNETIC STIMULATION;

ANIMALS; BRAIN; BRAIN MAPPING; ELECTROENCEPHALOGRAPHY; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; PAPIO; POSITRON-EMISSION TOMOGRAPHY; SIGNAL PROCESSING, COMPUTER-ASSISTED; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 79960216908     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.05.065     Document Type: Article

References (72)

1. Ákeson J., Björkman S., Messeter K., Rosen I., Helfer M. Cerebral pharmacodynamics of anaesthetic and subanaesthetic doses of ketamine in the normoventilated pig. Acta Anaesthesiol. Scand. 1993, 37:211-218.
2. Amassian V.E., Eberle L., Maccabee P.J., Cracco R.Q. Modeling magnetic coil excitation of human cerebral cortex with a peripheral nerve immersed in a brain-shaped volume conductor: the significance of fiber bending in excitation. Electroencephalogr. Clin. Neurophysiol. 1992, 85:291-301.
3. Ameli M., Grefkes C., Kemper F., Riegg F.P., Rehme A.K., Karbe H., Fink G.R., Nowak D.A. Differential effects of high-frequency repetitive transcranial magnetic stimulation over ipsilesional primary motor cortex in cortical and subcortical middle cerebral artery stroke. Ann. Neurol. 2009, 66:298-309.
4. Bestmann S., Baudewig J., Siebner H.R., Rothwell J.C., Frahm J. Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS. Neuroimage 2003, 20:1685-1696.
5. Black K.J., Snyder A.Z., Koller J.M., Gado M.H., Perlmutter J.S. Template images for nonhuman primate neuroimaging: 1. Baboon. NeuroImage 2001, 14:736-743.
6. Black K.J., Koller J.M., Snyder A.Z., Perlmutter J.S. Template images for nonhuman primate neuroimaging: 2. Macaque. NeuroImage 2001, 14:744-748.
7. Brasil-Neto J.P., Cohen L.G., Panizza M., Nilsson J., Roth B.J., Hallett M. Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J. Clin. Neurophysiol. 1992, 9:132-136.
8. Brown T.G., Sherrington C.S. Observations on the localisation in the motor cortex of the baboon ("Papio anubis"). J. Physiol. 1911, 43:209-218.
9. Cavada C., Compañy T., Tejedor J., Cruz-Rizzolo R.J., Reinoso-Suárez F. The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb. Cortex 2000, 10:220-242.
10. Cavazzuti M., Porro C.A., Biral G.P., Benassi C., Barbieri G.C. Ketamine effects on local cerebral blood flow and metabolism in the rat. J. Cereb. Blood Flow Metab. 1987, 7:806-811.
11. Chen R., Gerloff C., Classen J., Wassermann E.M., Hallett M., Cohen L.G. Safety of different inter-train intervals for repetitive transcranial magnetic stimulation and recommendations for safe ranges of stimulation parameters. Electroencephalogr. Clin. Neurophysiol. 1997, 105:415-421.
12. Chen R., Tam A., Butefisch C., Corwell B., Ziemann U., Rothwell J.C., Cohen L.G. Intracortical inhibition and facilitation in different representations of the human motor cortex. J. Neurophysiol. 1998, 80:2870-2881.
13. Day B.L., Dressler D., Maertens de Noordhout A., Marsden C.D., Nakashima K., Rothwell J.C., Thompson P.D. Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. J. Physiol. 1989, 412:449-473.
14. Dum R.P., Strick P.L. Motor areas in the frontal lobe of the primate. Physiol. Behav. 2002, 77:677-682.
15. Dum R.P., Strick P.L. Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J. Neurosci. 2005, 25:1375-1386.
16. Fink G.R. Multiple nonprimary motor areas in the human cortex. J. Neurophysiol. 1997, 77:2164-2174.
17. Fox P., Ingham R., George M.S., Mayberg H., Ingham J., Roby J., Martin C., Jerabek P. Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport 1997, 8:2787-2791.
18. Fox P.T., Narayana S., Tandon N., Sandoval H., Fox S.P., Kochunov P., Lancaster J.L. Column-based model of electric field excitation of cerebral cortex. Hum. Brain Mapp. 2004, 22:1-14.
19. Fox P.T., Narayana S., Tandon N., Fox S.P., Sandoval H., Kochunov P., Capaday C., Lancaster J.L. Intensity modulation of TMS-induced cortical excitation: primary motor cortex. Hum. Brain Mapp. 2006, 27:478-487.
20. Fukuda S., del Zoppo G.J. Models of focal cerebral ischemia in the nonhuman primate. ILAR J. 2003, 44:96-104.
21. Geyer S., Matelli M., Luppino G., Zilles K. Functional neuroanatomy of the primate isocortical motor system. Anat. Embryol. 2000, 202:443-474.
22. Guye M., Parker G.J.M., Symms M., Boulby P., Wheeler-Kingshott C.A.M., Salek-Haddadi A., Barker G.J., Duncan J.S. Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo. Neuroimage 2003, 19:1349-1360.
23. Hayashi T., Ohnishi T., Okabe S., Teramoto N., Nonaka Y., Watabe H., Imabayashi E., Ohta Y., Jino H., Ejima N., Sawada T., Iida H., Matsuda H., Ugawa Y. Long-term effect of motor cortical repetitive transcranial magnetic stimulation [correction]. Ann. Neurol. 2004, 56:77-85.
24. 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.
25. Kochunov P., Lancaster J., Thompson P., Toga A.W., Brewer P., Hardies J., Fox P. An optimized individual target brain in the Talairach coordinate system. Neuroimage 2002, 17:922-927.
26. Kujirai T., Caramia M.D., Rothwell J.C., Day B.L., Thompson P.D., Ferbert A., Wroe S., Asselman P., Marsden C.D. Corticocortical inhibition in human motor cortex. J. Physiol. 1993, 471:501-519.
27. Laird A.R., Robbins J.M., Li K., Price L.R., Cykowski M.D., Narayana S., Laird R.W., Franklin C., Fox P.T. Modeling motor connectivity using TMS/PET and structural equation modeling. Neuroimage 2008, 41:424-436.
28. Lancaster J.L., Fox P.T., Downs H., Nickerson D.S., Hander T.A., El Mallah M., Kochunov P.V., Zamarripa F. Global spatial normalization of human brain using convex hulls. J. Nucl. Med. 1999, 40:942-955.
29. Lancaster J.L., Narayana S., Wenzel D., Luckemeyer J., Roby J., Fox P. Evaluation of an image-guided, robotically positioned transcranial magnetic stimulation system. Hum. Brain Mapp. 2004, 22:329-340.
30. Långsjö J.K., Kaisti K.K., Aalto S., Hinkka S., Aantaa R., Oikonen V., Sipilä H., Kurki T., Silvanto M., Scheinin H. Effects of subanesthetic doses of ketamine on regional cerebral blood flow, oxygen consumption, and blood volume in humans. Anesthesiology 2003, 99:614-623.
31. Margulies D.S., Vincent J.L., Kelly C., Lohmann G., Uddin L.Q., Biswal B.B., Villringer A., Castellanos F.X., Milham M.P., Petrides M. Precuneus shares intrinsic functional architecture in humans and monkeys. Proc. Natl Acad. Sci. U. S. A. 2009, 106:20069-20074.
32. Matelli M., Carmada R., Glickstein M., Rizzolatti G. Interconnections within the postarcuate cortex (area 6) of the macaque monkey. Brain Res. 1984, 310:388-392.
33. Mills K.R., Boniface S.J., Schubert M. Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr. Clin. Neurophysiol. 1992, 85:17-21.
34. Nachev P., Kennard C., Husain M. Functional role of the supplementary and pre-supplementary motor areas. Nature reviews. Neuroscience 2008, 9:856-869.
35. Nagarajan S.S., Durand D.M., Warman E.N. Effects of induced electric fields on finite neuronal structures: a simulation study. IEEE Trans. Biomed. Eng. 1993, 40:1175-1188.
36. Nonaka Y., Hayashi T., Ohnishi T., Okabe S., Teramoto N., Ueno S., Watabe H., Matsuda H., Iida H., Ugawa Y. A coil for magnetic stimulation of the macaque monkey brain. Suppl. Clin. Neurophysiol. 2003, 56:75-80.
37. Nowak D.A., Grefkes C., Ameli M., Fink G. Interhemispheric competition after stroke: brain stimulation to enhance recovery of function of the affected hand. Neurorehabil. Neural Repair 2009, 23:641-656.
38. Ohnishi T., Hayashi T., Okabe S., Nonaka I., Matsuda H., Iida H., Imabayashi E., Watabe H., Miyake Y., Ogawa M., Teramoto N., Ohta Y., Ejima N., Sawada T., Ugawa Y. Endogenous dopamine release induced by repetitive transcranial magnetic stimulation over the primary motor cortex: an [11C]raclopride positron emission tomography study in anesthetized macaque monkeys. Biol. Psychiatry 2004, 55:484-489.
39. Pandya D.N., Hoesen G.W.V., Mesulam M.M. Efferent connections of the cingulate gyrus in the rhesus monkey. Exp. Brain Res. 1981, 42:319-330.
40. Paus T. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nature reviews. Neuroscience 2001, 2:417-424.
41. Paus T., Jech R., Thompson C.J., Comeau R., Peters T., Evans A.C. Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J. Neurosci. 1997, 17:3178-3184.
42. Penfield W., Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 1937, 60:389-443.
43. Rizzolatti G., Luppino G. The cortical motor system. Neuron 2001, 31:889-901.
44. Roth B.J., Basser P.J. A model of the stimulation of a nerve fiber by electromagnetic induction. IEEE Trans. Biomed. Eng. 1990, 37:588-597.
45. Roth B.J., Pascual-Leone A., Cohen L.G., Hallett M. The heating of metal electrodes during rapid-rate magnetic stimulation: a possible safety hazard. Electroencephalogr. Clin. Neurophysiol. 1992, 85:116-123.
46. Saleem K.S., Logothetis N.K. A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates 2007, Academic Press, London.
47. Salinas F.S., Lancaster J.L., Fox P.T. Detailed 3D models of the induced electric field of transcranial magnetic stimulation coils. Phys. Med. Biol. 2007, 52:2879-2892.
48. Salinas F.S., Lancaster J.L., Fox P.T. 3D modeling of the total electric field induced by transcranial magnetic stimulation using the boundary element method. Phys. Med. Biol. 2009, 54:3631-3647.
49. Salinas F.S., Szabó C.Á., Franklin C., Zhang W., Leland M.M., Wey H.-Y., Duong T.Q., Fox P.T., Narayana S. Development of a baboon model using repetitive transcranial magnetic stimulation as evidenced by rate dependent regional brain activations. 16th Annual Meeting of the Organization for Human Brain Mapping, Barcelona, Spain, June 6-10 2010.
50. Salinas F.S., Knape K.D., Franklin C., Narayana S., Leland M.M., Wey H.-Y., Duong T.Q., Fox P.T., Szabó C.Á. Rate dependent brain activation using intermittent light stimulation in a baboon model. 16th Annual Meeting of the Organization for Human Brain Mapping, Barcelona, Spain, June 6-10 2010.
51. Salinas F.S., Narayana S., Knape K.D., Leland M.M., Szabó C.Á. Rate dependent regional brain activations during intermittent light stimulation in photosensitive and control non-human primates. 64th Annual Meeting of the American Epilepsy Society, San Antonio, Texas, December 4-8 2010.
52. Salinas F.S., Narayana S., Zhang W., Jones L., Leland M.M., Lancaster J.L., Fox P.T. Baboon validations of the cortical column cosine aiming model of TMS induced brain activations. 17th Annual Meeting of the Organization for Human Brain Mapping, Quebec City, Canada, June 26-30 2011.
53. Siebner H.R., Takano B., Peinemann A., Schwaiger M., Conrad B., Drzezga A. Continuous transcranial magnetic stimulation during positron emission tomography: a suitable tool for imaging regional excitability of the human cortex. Neuroimage 2001, 14:883-890.
54. Siebner H.R., Bergmann T.O., Bestmann S., Massimini M., Johansen-Berg H., Mochizuki H., Bohning D.E., Boorman E.D., Groppa S., Miniussi C., Pascual-Leone A., Huber R., Taylor P.C., Ilmoniemi R.J., De Gennaro L., Strafella A.P., Kahkonen S., Kloppel S., Frisoni G.B., George M.S., Hallett M., Brandt S.A., Rushworth M.F., Ziemann U., Rothwell J.C., Ward N., Cohen L.G., Baudewig J., Paus T., Ugawa Y., Rossini P.M. Consensus paper: combining transcranial stimulation with neuroimaging. Brain Stimul. 2009, 2:58-80.
55. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., Luca M.D., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., Stefano N.D., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23(Suppl. 1):S208-S219.
56. Speer A.M., Willis M.W., Herscovitch P., Daube-Witherspoon M., Shelton J.R., Benson B.E., Post R.M., Wassermann E.M. Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H215O positron emission tomography: I. Effects of primary motor cortex rTMS. Biol. Psychiatry 2003, 54:818-825.
57. Szabó C.A., Leland M.M., Knape K., Elliott J.J., Haines V., Williams J.T. Clinical and EEG phenotypes of epilepsy in the baboon (Papio hamadryas spp.). Epilepsy Res. 2005, 65:71-80.
58. Szabó C.A., Narayana S., Franklin C., Knape K.D., Davis M.D., Fox P.T. "Resting" CBF in the epileptic baboon: correlation with ketamine dose and interictal epileptic discharges. Epilepsy Res. 2008, 82:57-63.
59. Szabó, C.A., Salinas, F.S., Narayana, S., in press. Functional PET evaluation of the photosensitive baboon. OPEN Neurosci. J. Special Issue.
60. Tanji J. The supplementary motor area in the cerebral cortex. Neurosci. Res. 1994, 19:251-268.
61. Tassinari C.A., Cincotta M., Zaccara G., Michelucci R. Transcranial magnetic stimulation and epilepsy. Clin. Neurophysiol. 2003, 114:777-798.
62. Terao Y., Ugawa Y. Basic mechanisms of TMS. J. Clin. Neurophysiol. 2002, 19:322-343.
63. Thielscher A., Kammer T. Electric field properties of two commercial figure-8 coils in TMS: calculation of focality and efficiency. Clin. Neurophysiol. 2004, 115:1697-1708.
64. Tokuno H., Nambu A. Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: an electrophysiological study in the macaque monkey. Cereb. Cortex 2000, 10:58-68.
65. Vincent J.L., Patel G.H., Fox M.D., Snyder A.Z., Baker J.T., Van Essen D.C., Zempel J.M., Snyder L.H., Corbetta M., Raichle M.E. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 2007, 447:83-86.
66. Wassermann E.M. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalogr. Clin. Neurophysiol. 1998, 108:1-16.
67. Wassermann E.M., Fuhr P., Cohen L.G., Hallett M. Effects of transcranial magnetic stimulation on ipsilateral muscles. Neurology 1991, 41:1795-1799.
68. Wey H.-Y., Li J., Szabó C.Á., Fox P.T., Leland M.M., Jones L., Duong T.Q. BOLD fMRI of visual and somatosensory-motor stimulations in baboons. Neuroimage 2010, 52:1420-1427.
69. Wey H.-Y., Wang D.J., Duong T.Q. Baseline CBF, and BOLD, CBF, and CMRO(2) fMRI of visual and vibrotactile stimulations in baboons. J. Cereb. Blood Flow Metab. 2011, 31:715-724.
70. Woolrich M.W., Jbabdi S., Patenaude B., Chappell M., Makni S., Behrens T., Beckmann C., Jenkinson M., Smith S.M. Bayesian analysis of neuroimaging data in FSL. Neuroimage 2009, 45:S173-S186.
71. Wu T., Sommer M., Tergau F., Paulus W. Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci. Lett. 2000, 287:37-40.
72. Yeterian E.H., Pandya D.N. Fiber pathways and cortical connections of preoccipital areas in rhesus monkeys. J. Comp. Neurol. 2010, 518:3725-3751.