Intra- and inter-subject variability of high field fMRI digit maps in somatosensory area 3b of new world monkeys

Neuroscience

Volumn 165, Issue 1, 2010, Pages 252-264

  Zhang, N ^a,b   Wang, F ^a   Turner, G H ^a   Gore, J C ^a,c,d   Avison, M J ^a   Chen, L M ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b Clarkson University   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

digits; high field functional MRI; primates; somatosensory cortex; topography

Indexed keywords

ANESTHESIA INDUCTION; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; IMAGE ANALYSIS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REPRODUCIBILITY; SIGNAL PROCESSING; SOMATOSENSORY CORTEX; SQUIRREL MONKEY; STATISTICAL ANALYSIS;

ANIMALS; BRAIN MAPPING; MAGNETIC RESONANCE IMAGING; PLATYRRHINI; SOMATOSENSORY CORTEX; TIME FACTORS;

EID: 70449687843     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.09.066     Document Type: Article

References (97)

1. Chen L.M., Friedman R.M., Ramsden B.M., LaMotte R.H., and Roe A.W. Fine-scale organization of SI (area 3b) in the squirrel monkey revealed with intrinsic optical imaging. J Neurophysiol 86 (2001) 3011-3029
2. Chen L.M., Friedman R.M., and Roe A.W. Optical imaging of a tactile illusion in area 3b of the primary somatosensory cortex. Science 302 (2003) 881-885
3. Chen L.M., Friedman R.M., and Roe A.W. Optical imaging of SI topography in anesthetized and awake squirrel monkeys. J Neurosci 25 (2005) 7648-7659
4. Chen L.M., Friedman R.M., and Roe A.W. Optical imaging of digit topography in individual awake and anesthetized squirrel monkeys. Exp Brain Res 196 (2009) 393-401
5. Chen L.M., Heider B., Williams G.V., Healy F.L., Ramsden B.M., and Roe A.W. A chamber and artificial dura method for long-term optical imaging in the monkey. J Neurosci Methods 113 (2002) 41-49
6. Chen L.M., Turner G.H., Friedman R.M., Zhang N., Gore J.C., Roe A.W., and Avison M.J. High-resolution maps of real and illusory tactile activation in primary somatosensory cortex in individual monkeys with functional magnetic resonance imaging and optical imaging. J Neurosci 27 (2007) 9181-9191
7. Cohen E.R., Ugurbil K., and Kim S.G. Effect of basal conditions on the magnitude and dynamics of the blood oxygenation level-dependent fMRI response. J Cereb Blood Flow Metab 22 (2002) 1042-1053
8. Costafreda S.G., Brammer M.J., Vencio R.Z., Mourao M.L., Portela L.A., de Castro C.C., Giampietro V.P., and Amaro Jr. E. Multisite fMRI reproducibility of a motor task using identical MR systems. J Magn Reson Imaging 26 (2007) 1122-1126
9. Courtine G., Bunge M.B., Fawcett J.W., Grossman R.G., Kaas J.H., Lemon R., Maier I., Martin J., Nudo R.J., Ramon-Cueto A., Rouiller E.M., Schnell L., Wannier T., Schwab M.E., and Edgerton V.R. Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans?. Nat Med 13 (2007) 561-566
10. Dagli M.S., Ingeholm J.E., and Haxby J.V. Localization of cardiac-induced signal change in fMRI. Neuroimage 9 (1999) 407-415
11. DiCarlo J.J., and Johnson K.O. Receptive field structure in cortical area 3b of the alert monkey. Behav Brain Res 135 (2002) 167-178
12. Disbrow E., Roberts T.P., Slutsky D., and Krubitzer L. The use of fMRI for determining the topographic organization of cortical fields in human and nonhuman primates. Brain Res 829 (1999) 167-173
13. Disbrow E.A., Slutsky D.A., Roberts T.P., and Krubitzer L.A. Functional MRI at 1.5 tesla: a comparison of the blood oxygenation level-dependent signal and electrophysiology. Proc Natl Acad Sci U S A 97 (2000) 9718-9723
14. Duncan R.O., and Boynton G.M. Tactile hyperacuity thresholds correlate with finger maps in primary somatosensory cortex (S1). Cereb Cortex 17 (2007) 2878-2891
15. Favorov O., and Whitsel B.L. Spatial organization of the peripheral input to area 1 cell columns: part II. The forelimb representation achieved by a mosaic of segregates. Brain Res 472 (1988) 43-56
16. Favorov O., and Whitsel B.L. Spatial organization of the peripheral input to area 1 cell columns: part I. The detection of "segregates". Brain Res 472 (1988) 25-42
17. Favorov O.V., Diamond M.E., and Whitsel B.L. Evidence for a mosaic representation of the body surface in area 3b of the somatic cortex of cat. Proc Natl Acad Sci U S A 84 (1987) 6606-6610
18. Feldman D.E., and Brecht M. Map plasticity in somatosensory cortex. Science 310 (2005) 810-815
19. Fernandez G., Specht K., Weis S., Tendolkar I., Reuber M., Fell J., Klaver P., Ruhlmann J., Reul J., and Elger C.E. Intrasubject reproducibility of presurgical language lateralization and mapping using fMRI. Neurology 60 (2003) 969-975
20. Fitzpatrick J.M., and West J.B. The distribution of target registration error in rigid-body point-based registration. IEEE Trans Med Imaging 20 (2001) 917-927
21. Fox K., Glazewski S., and Schulze S. Plasticity and stability of somatosensory maps in thalamus and cortex. Curr Opin Neurobiol 10 (2000) 494-497
22. Friedman R.M., Chen L.M., and Roe A.W. Modality maps within primate somatosensory cortex. Proc Natl Acad Sci U S A 101 (2004) 12724-12729
23. Friedman R.M., Chen L.M., and Roe A.W. Responses of areas: 3b and 1 in anesthetized squirrel monkeys to single and dual site stimulation of the digits. J Neurophysiol 100 (2008) 3185-3196
24. Fukuda M., Moon C.H., Wang P., and Kim S.G. Mapping iso-orientation columns by contrast agent-enhanced functional magnetic resonance imaging: reproducibility, specificity, and evaluation by optical imaging of intrinsic signal. J Neurosci 26 (2006) 11821-11832
25. Fukuda M., Rajagopalan U.M., Homma R., Matsumoto M., Nishizaki M., and Tanifuji M. Localization of activity-dependent changes in blood volume to submillimeter-scale functional domains in cat visual cortex. Cereb Cortex 15 (2005) 823-833
26. Garraghty P.E., Pons T.P., Sur M., and Kaas J.H. The arbors of axons terminating in middle cortical layers of somatosensory area 3b in owl monkeys. Somatosens Mot Res 6 (1989) 401-411
27. Gelnar P.A., Krauss B.R., Szeverenyi N.M., and Apkarian A.V. Fingertip representation in the human somatosensory cortex: an fMRI study. Neuroimage 7 (1998) 261-283
28. Godde B., Ehrhardt J., and Braun C. Behavioral significance of input-dependent plasticity of human somatosensory cortex. Neuroreport 14 (2003) 543-546
29. Goense J.B., and Logothetis N.K. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr Biol 18 (2008) 631-640
30. Grinvald A., Frostig R.D., Siegel R.M., and Bartfeld E. High-resolution optical imaging of functional brain architecture in the awake monkey. Proc Natl Acad Sci U S A 88 (1991) 11559-11563
31. Grinvald A., Lieke E., Frostig R.D., Gilbert C.D., and Wiesel T.N. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324 (1986) 361-364
32. Harper R.M., Gozal D., Bandler R., Spriggs D., Lee J., and Alger J. Regional brain activation in humans during respiratory and blood pressure challenges. Clin Exp Pharmacol Physiol 25 (1998) 483-486
33. Harrington G.S., Tomaszewski Farias S., Buonocore M.H., and Yonelinas A.P. The intersubject and intrasubject reproducibility of FMRI activation during three encoding tasks: implications for clinical applications. Neuroradiology 48 (2006) 495-505
34. Hill D.L., Hawkes D.J., Crossman J.E., Gleeson M.J., Cox T.C., Bracey E.E., Strong A.J., and Graves P. Registration of MR and CT images for skull base surgery using point-like anatomical features. Br J Radiol 64 (1991) 1030-1035
35. Jones E.G. Cortical and subcortical contributions to activity-dependent plasticity in primate somatosensory cortex. Annu Rev Neurosci 23 (2000) 1-37
36. Juliano S.L., and Whitsel B.L. Metabolic labeling associated with index finger stimulation in monkey SI: between animal variability. Brain Res 342 (1985) 242-251
37. Kaas J.H. Plasticity of sensory and motor maps in adult mammals. Annu Rev Neurosci 14 (1991) 137-167
38. Kaas J.H. The reorganization of somatosensory and motor cortex after peripheral nerve or spinal cord injury in primates. Prog Brain Res 128 (2000) 173-179
39. Kaas J.H., Qi H.X., Burish M.J., Gharbawie O.A., Onifer S.M., and Massey J.M. Cortical and subcortical plasticity in the brains of humans, primates, and rats after damage to sensory afferents in the dorsal columns of the spinal cord. Exp Neurol 209 (2008) 407-416
40. Kannurpatti S.S., and Biswal B.B. Effect of anesthesia on CBF, MAP and fMRI-BOLD signal in response to apnea. Brain Res 1011 (2004) 141-147
41. Kannurpatti S.S., Biswal B.B., and Hudetz A.G. Baseline physiological state and the fMRI-BOLD signal response to apnea in anesthetized rats. NMR Biomed 16 (2003) 261-268
42. Kida I., Xu F., Shulman R.G., and Hyder F. Mapping at glomerular resolution: fMRI of rat olfactory bulb. Magn Reson Med 48 (2002) 570-576
43. Kim D.S., Duong T.Q., and Kim S.G. High-resolution mapping of iso-orientation columns by fMRI. Nat Neurosci 3 (2000) 164-169
44. Kohn A., Pinheiro A., Tommerdahl M.A., and Whitsel B.L. Optical imaging in vitro provides evidence for the minicolumnar nature of cortical response. Neuroreport 8 (1997) 3513-3518
45. Krause T., Kurth R., Ruben J., Schwiemann J., Villringer K., Deuchert M., Moosmann M., Brandt S., Wolf K., Curio G., and Villringer A. Representational overlap of adjacent fingers in multiple areas of human primary somatosensory cortex depends on electrical stimulus intensity: an fMRI study. Brain Res 899 (2001) 36-46
46. Landuyt W., Hermans R., Bosmans H., Sunaert S., Beatse E., Farina D., Meijerink M., Zhang H., Van Den Bogaert W., Lambin P., and Marchal G. BOLD contrast fMRI of whole rodent tumour during air or carbogen breathing using echo-planar imaging at 1.5 T. Eur Radiol 11 (2001) 2332-2340
47. Lauritzen M., and Gold L. Brain function and neurophysiological correlates of signals used in functional neuroimaging. J Neurosci 23 (2003) 3972-3980
48. Lee S.P., Silva A.C., Ugurbil K., and Kim S.G. Diffusion-weighted spin-echo fMRI at 9.4 T: microvascular/tissue contribution to BOLD signal changes. Magn Reson Med 42 (1999) 919-928
49. Leontiev O., and Buxton R.B. Reproducibility of BOLD, perfusion, and CMRO2 measurements with calibrated-BOLD fMRI. Neuroimage 35 (2007) 175-184
50. Logothetis N.K., Pauls J., Augath M., Trinath T., and Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 412 (2001) 150-157
51. Macey K.E., Macey P.M., Woo M.A., Harper R.K., Alger J.R., Keens T.G., and Harper R.M. fMRI signal changes in response to forced expiratory loading in congenital central hypoventilation syndrome. J Appl Physiol 97 (2004) 1897-1907
52. Maldjian J.A., Gottschalk A., Patel R.S., Detre J.A., and Alsop D.C. The sensory somatotopic map of the human hand demonstrated at 4 Tesla. Neuroimage 10 (1999) 55-62
53. Meier J.D., Aflalo T.N., Kastner S., and Graziano M.S. Complex organization of human primary motor cortex: a high-resolution fMRI study. J Neurophysiol 100 (2008) 1800-1812
54. Menon R.S., and Goodyear B.G. Submillimeter functional localization in human striate cortex using BOLD contrast at 4 Tesla: implications for the vascular point-spread function. Magn Reson Med 41 (1999) 230-235
55. Menz M.M., Neumann J., Muller K., and Zysset S. Variability of the BOLD response over time: an examination of within-session differences. Neuroimage 32 (2006) 1185-1194
56. Merzenich M.M., Nelson R.J., Kaas J.H., Stryker M.P., Jenkins W.M., Zook J.M., Cynader M.S., and Schoppmann A. Variability in hand surface representations in areas 3b and 1 in adult owl and squirrel monkeys. J Comp Neurol 258 (1987) 281-296
57. Moon C.H., Fukuda M., Park S.H., and Kim S.G. Neural interpretation of blood oxygenation level-dependent fMRI maps at submillimeter columnar resolution. J Neurosci 27 (2007) 6892-6902
58. Moser E., Teichtmeister C., and Diemling M. Reproducibility and postprocessing of gradient-echo functional MRI to improve localization of brain activity in the human visual cortex. Magn Reson Imaging 14 (1996) 567-579
59. Mountcastle V.B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol 20 (1957) 408-434
60. Mountcastle V.B. The columnar organization of the neocortex. Brain 120 Pt 4 (1997) 701-722
61. Mountcastle V.B. Introduction: computation in cortical columns. Cereb Cortex 13 (2003) 2-4
62. Nelson A.J., and Chen R. Digit somatotopy within cortical areas of the postcentral gyrus in humans. Cereb Cortex 18 (2008) 2341-2351
63. Nelson R.J., Sur M., Felleman D.J., and Kaas J.H. Representations of the body surface in postcentral parietal cortex of Macaca fascicularis. J Comp Neurol 192 (1980) 611-643
64. Neumann J., Lohmann G., Zysset S., and von Cramon D.Y. Within-subject variability of BOLD response dynamics. Neuroimage 19 (2003) 784-796
65. Peeters R.R., Tindemans I., De Schutter E., and Van der Linden A. Comparing BOLD fMRI signal changes in the awake and anesthetized rat during electrical forepaw stimulation. Magn Reson Imaging 19 (2001) 821-826
66. Pons T.P., Garraghty P.E., and Mishkin M. Lesion-induced plasticity in the second somatosensory cortex of adult macaques. Proc Natl Acad Sci U S A 85 (1988) 5279-5281
67. Pons T.P., Wall J.T., Garraghty P.E., Cusick C.G., and Kaas J.H. Consistent features of the representation of the hand in area 3b of macaque monkeys. Somatosens Res 4 (1987) 309-331
68. Reed J.L., Pouget P., Qi H.X., Zhou Z., Bernard M.R., Burish M.J., Haitas J., Bonds A.B., and Kaas J.H. Widespread spatial integration in primary somatosensory cortex. Proc Natl Acad Sci U S A 105 (2008) 10233-10237
69. Rombouts S.A., Barkhof F., Hoogenraad F.G., Sprenger M., and Scheltens P. Within-subject reproducibility of visual activation patterns with functional magnetic resonance imaging using multislice echo planar imaging. Magn Reson Imaging 16 (1998) 105-113
70. Rosso T., Aglioti S.M., Zanette G., Ischia S., Finco G., Farina S., Fiaschi A., and Tinazzi M. Functional plasticity in the human primary somatosensory cortex following acute lesion of the anterior lateral spinal cord: neurophysiological evidence of short-term cross-modal plasticity. Pain 101 (2003) 117-127
71. Salli E., Korvenoja A., Visa A., Katila T., and Aronen H.J. Reproducibility of fMRI: effect of the use of contextual information. Neuroimage 13 (2001) 459-471
72. Schaechter J.D., Moore C.I., Connell B.D., Rosen B.R., and Dijkhuizen R.M. Structural and functional plasticity in the somatosensory cortex of chronic stroke patients. Brain 129 (2006) 2722-2733
73. Schaefer M., Rothemund Y., Heinze H.J., and Rotte M. Short-term plasticity of the primary somatosensory cortex during tool use. Neuroreport 15 (2004) 1293-1297
74. Schafer J.R., Kida I., Xu F., Rothman D.L., and Hyder F. Reproducibility of odor maps by fMRI in rodents. Neuroimage 31 (2006) 1238-1246
75. Schweizer R., Voit D., and Frahm J. Finger representations in human primary somatosensory cortex as revealed by high-resolution functional MRI of tactile stimulation. Neuroimage 42 (2008) 28-35
76. Shmuel A., Yacoub E., Chaimow D., Logothetis N.K., and Ugurbil K. Spatiotemporal point-spread function of fMRI signal in human gray matter at 7 Tesla. Neuroimage 35 (2007) 539-552
77. Sripati A.P., Yoshioka T., Denchev P., Hsiao S.S., and Johnson K.O. Spatiotemporal receptive fields of peripheral afferents and cortical area 3b and 1 neurons in the primate somatosensory system. J Neurosci 26 (2006) 2101-2114
78. Sur M., Nelson R.J., and Kaas J.H. Representations of the body surface in cortical areas 3b and 1 of squirrel monkeys: comparisons with other primates. J Comp Neurol 211 (1982) 177-192
79. Sur M., Wall J.T., and Kaas J.H. Modular segregation of functional cell classes within the postcentral somatosensory cortex of monkeys. Science 212 (1981) 1059-1061
80. Sur M., Wall J.T., and Kaas J.H. Modular distribution of neurons with slowly adapting and rapidly adapting responses in area 3b of somatosensory cortex in monkeys. J Neurophysiol 51 (1984) 724-744
81. Tegeler C., Strother S.C., Anderson J.R., and Kim S.G. Reproducibility of BOLD-based functional MRI obtained at 4 T. Hum Brain Mapp 7 (1999) 267-283
82. Thomason M.E., Burrows B.E., Gabrieli J.D., and Glover G.H. Breath holding reveals differences in fMRI BOLD signal in children and adults. Neuroimage 25 (2005) 824-837
83. Tjandra T., Brooks J.C., Figueiredo P., Wise R., Matthews P.M., and Tracey I. Quantitative assessment of the reproducibility of functional activation measured with BOLD and MR perfusion imaging: implications for clinical trial design. Neuroimage 27 (2005) 393-401
84. Tommerdahl M., Delemos K.A., Whitsel B.L., Favorov O.V., and Metz C.B. Response of anterior parietal cortex to cutaneous flutter versus vibration. J Neurophysiol 82 (1999) 16-33
85. Tommerdahl M., Favorov O., and Whitsel B.L. Optical imaging of intrinsic signals in somatosensory cortex. Behav Brain Res 135 (2002) 83-91
86. Ungerleider L.G., Doyon J., and Karni A. Imaging brain plasticity during motor skill learning. Neurobiol Learn Mem 78 (2002) 553-564
87. van Gelderen P., W H Wu C., de Zwart J.A., Cohen L., Hallett M., and Duyn J.H. Resolution and reproducibility of BOLD and perfusion functional MRI at 3.0 Tesla. Magn Reson Med 54 (2005) 569-576
88. Vanzetta I., and Grinvald A. Coupling between neuronal activity and microcirculation: implications for functional brain imaging. HFSP J 2 (2008) 79-98
89. Waldvogel D., van Gelderen P., Immisch I., Pfeiffer C., and Hallett M. The variability of serial fMRI data: correlation between a visual and a motor task. Neuroreport 11 (2000) 3843-3847
90. Wang R., Foniok T., Wamsteeker J.I., Qiao M., Tomanek B., Vivanco R.A., and Tuor U.I. Transient blood pressure changes affect the functional magnetic resonance imaging detection of cerebral activation. Neuroimage 31 (2006) 1-11
91. West J.B., Fitzpatrick J.M., Toms S.A., Maurer Jr. C.R., and Maciunas R.J. Fiducial point placement and the accuracy of point-based, rigid body registration. Neurosurgery 48 (2001) 810-816 discussion: 816-817
92. Whalley H.C., Gountouna V.E., Hall J., McIntosh A.M., Simonotto E., Job D.E., Owens D.G., Johnstone E.C., and Lawrie S.M. fMRI changes over time and reproducibility in unmedicated subjects at high genetic risk of schizophrenia. Psychol Med 39 (2009) 1189-1199
93. Yacoub E., Harel N., and Ugurbil K. High-field fMRI unveils orientation columns in humans. Proc Natl Acad Sci U S A 105 (2008) 10607-10612
94. Yang X., Hyder F., and Shulman R.G. Functional MRI BOLD signal coincides with electrical activity in the rat whisker barrels. Magn Reson Med 38 (1997) 874-877
95. Yoo S.S., O'Leary H.M., Lee J.H., Chen N.K., Panych L.P., and Jolesz F.A. Reproducibility of trial-based functional MRI on motor imagery. Int J Neurosci 117 (2007) 215-227
96. Yoo S.S., Wei X., Dickey C.C., Guttmann C.R., and Panych L.P. Long-term reproducibility analysis of fMRI using hand motor task. Int J Neurosci 115 (2005) 55-77
97. Zhang N., Gore J.C., Chen L.M., and Avison M.J. Dependence of BOLD signal change on tactile stimulus intensity in SI of primates. Magn Reson Imaging 25 (2007) 784-794