Mapping iso-orientation columns by contrast agent-enhanced functional magnetic resonance imaging: Reproducibility, specificity, and evaluation by optical imaging of intrinsic signal

Journal of Neuroscience

Volumn 26, Issue 46, 2006, Pages 11821-11832

  Fukuda, Mitsuhiro ^a   Moon, Chan Hong ^a   Wang, Ping ^a   Kim, Seong Gi ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

BOLD; Capillary; CBF; Cerebral blood flow; Hemodynamic response; Visual cortex

Indexed keywords

CONTRAST MEDIUM; MONOCRYSTALLINE IRON OXIDE NANOPARTICLE;

ANIMAL EXPERIMENT; ARTICLE; BLOOD OXYGENATION; BRAIN BLOOD FLOW; BRAIN NERVE CELL; CAT; CELL ACTIVITY; CONTRAST ENHANCEMENT; CONTROLLED STUDY; EVALUATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; IMAGE ANALYSIS; METABOLIC RATE; NANOPARTICLE; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; VISUAL CORTEX;

ANIMALS; BRAIN MAPPING; CATS; CEREBROVASCULAR CIRCULATION; CONTRAST MEDIA; DOMINANCE, OCULAR; FERRIC COMPOUNDS; MAGNETIC RESONANCE IMAGING; METAL NANOPARTICLES; OPTICS; ORIENTATION; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; REPRODUCIBILITY OF RESULTS; SIGNAL PROCESSING, COMPUTER-ASSISTED; SYNAPTIC TRANSMISSION; TIME FACTORS; VISUAL CORTEX;

EID: 33751077496     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3098-06.2006     Document Type: Article

References (69)

1. Blasdel GG (1992) Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex. J Neurosci 12:3115-3138.
2. Blasdel GG, Salama G (1986) Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321:579-585.
3. Bonhoeffer T, Grinvald A (1993) The layout of iso-orientation domains in area 18 of cat visual cortex: optical imaging reveals a pinwheel-like organization. J Neurosci 13:4157-4180.
4. Bonhoeffer T, Kim DS, Malonek D, Shoham D, Grinvald A (1995) Optical imaging of the layout of functional domains in area 17 and across the area 17/18 border in cat visual cortex. Eur J Neurosci 7:1973-1988.
5. Bosking WH, Crowley JC, Fitzpatrick D (2002) Spatial coding of position and orientation in primary visual cortex. Nat Neurosci 5:874-882.
6. Boynton GM, Engel SA, Glover GH, Heeger DJ (1996) Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci 16:4207-4221.
7. Cheng K, Waggoner RA, Tanaka K (2001) Human ocular dominance columns as revealed by high-field functional magnetic resonance imaging. Neuron 32:359-374.
8. Dechent P, Frahm J (2000) Direct mapping of ocular dominance columns in human primary visual cortex. NeuroReport 11:3247-3249.
9. Dubowitz DJ, Bernheim KA, Chen DY, Bradley Jr WG, Andersen RA (2001) Enhancing fMRI contrast in awake-behaving primates using intravascular magnetite dextran nanopartieles. NeuroReport 12:2335-2340.
10. Duong TQ, Kim DS, Ugurbil K, Kim SG (2000) Spatiotemporal dynamics of the BOLD fMRI signals: toward mapping submillimeter cortical columns using the early negative response. Magn Reson Med 44:231-242.
11. Duong TQ, Kim DS, Ugurbil K, Kim SG (2001) Localized cerebral blood flow response at submillimeter columnar resolution. Proc Natl Acad Sci USA 98:10904-10909.
12. Engel SA, Rumelhart DE, Wandell BA, Lee AT, Glover GH, Chichilnisky EJ, Shadlen MN (1994) fMRI of human visual cortex. Nature 369:525.
13. Engel SA, Glover GH, Wandell BA (1997) Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex 7:181-192.
14. Fize D, Vanduffel W, Nelissen K, Denys K, Chef d'Hotel C, Faugeras O, Orban GA (2003) The retinotopic organization of primate dorsal V4 and surrounding areas: a functional magnetic resonance imaging study in awake monkeys. J Neurosci 23:7395-7406.
15. Frostig RD, Lieke EE, Ts'o DY, Grinvald A (1990) Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sci USA 87:6082-6086.
16. Fukuda M, Rajagopalan UM, Homma R, Matsumoto M, Nishizaki M, Tanifuji M (2005) Localization of activity-dependent changes in blood volume to submillimeter-scale functional domains in cat visual cortex. Cereb Cortex 15:823-833.
17. Fukuda M, Wang P, Moon CH, Tanifuji M, Kim SG (2006) Spatial specificity of the enhanced dip inherently induced by prolonged oxygen consumption in cat visual cortex: implication for columnar resolution functional MRI. NeuroImage 30:70-87.
18. Goodyear BG, Menon RS (2001) Brief visual stimulation allows mapping of ocular dominance in visual cortex using fMRI. Hum Brain Mapp 14:210-217.
19. Grinvald A, Lieke E, Frostig RD, Gilbert CD, Wiesel TN (1986) Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324:361-364.
20. Heeger DJ, Huk AC, Geisler WS, Albrecht DG (2000) Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? Nat Neurosci 3:631-633.
21. Howarth C, Peppiatt CM, Mobbs P, Attwell D (2005) Pericytes can regulate capillary diameter in rat retina and cerebellum. Soc Neurosci Abstr 31:407.9.
22. Hudetz AG (1997) Blood flow in the cerebral capillary network: a review emphasizing observations with intravital microscopy. Microcirculation 4:233-252.
23. Kalatsky VA, StrykerMP (2003) New paradigm for optical imaging: temporally encoded maps of intrinsic signal. Neuron 38:529-545.
24. Kennan RP, Scanley BE, Innis RB, Gore JC (1998) Physiological basis for BOLD MR signal changes due to neuronal stimulation: separation of blood volume and magnetic susceptibility effects. Magn Reson Med 40:840-846.
25. Kennerley AJ, Berwick J, Martindale J, Johnston D, Papadakis N, Mayhew JE (2005) Concurrent fMRI and optical measures for the investigation of the hemodynamic response function. Magn Reson Med 54:354-365.
26. Kim DS, Duong TQ, Kim SG (2000) High-resolution mapping of iso-orientation columns by fMRI. Nat Neurosci 3:164-169.
27. Kim SG, Ugurbil K (2003) High-resolution functional magnetic resonance imaging of the animal brain. Methods 30:28-41.
28. Leite FP, Tsao D, Vanduffel W, Fize D, Sasaki Y, Wald LL, Dale AM, Kwong KK, Orban GA, Rosen BR, Tootell RB, Mandeville JB (2002) Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla. NeuroImage 16:283-294.
29. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150-157.
30. Lowel S, Freeman B, Singer W (1987) Topographic organization of the orientation column system in large flat-mounts of the cat visual cortex: a 2-deoxyglucose study. J Comp Neurol 255:401-415.
31. Lu H, Golay X, Pekar JJ, Van Zijl PC (2003) Functional magnetic resonance imaging based on changes in vascular space occupancy. Magn Reson Med 50:263-274.
32. Lu H, van Zijl PC, Hendrikse J, Golay X (2004) Multiple acquisitions with global inversion cycling (MAGIC): a multislice technique for vascular-space-occupancy dependent fMRI. Magn Reson Med 51:9-15.
33. Maldonado PE, Godecke I, Gray CM, Bonhoeffer T (1997) Orientation selectivity in pinwheel centers in cat striate cortex. Science 276:1551-1555.
34. Malonek D, Grinvald A (1996) Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science 272:551-554.
35. Malonek D, Dirnagl U, Lindauer U, Yamada K, Kanno I, Grinvald A (1997) Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc Natl Acad Sci USA 94:14826-14831.
36. Mandeville JB, Marota JJ (1999) Vascular filters of functional MRI: spatial localization using BOLD and CBV contrast. Magn Reson Med 42:591-598.
37. Mandeville JB, Marota JJ, Kosofsky BE, Keltner JR, Weissleder R, Rosen BR, Weisskoff RM (1998) Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation. Magn Reson Med 39:615-624.
38. Mandeville JB, Jenkins BG, Chen YC, Choi JK, Kim YR, Belen D, Liu C, Kosofsky BE, Marota JJ (2004) Exogenous contrast agent improves sensitivity of gradient-echo functional magnetic resonance imaging at 9.4 T. Magn Reson Med 52:1272-1281.
39. Mayhew JE, Askew S, Zheng Y, Porrill J, Westby GW, Redgrave P, Rector DM, Harper RM (1996) Cerebral vasomotion: a 0.1-Hz oscillation in reflected light imaging of neural activity. NeuroImage 4:183-193.
40. Menon RS, Goodyear BG (1999) Submillimeter functional localization in human striate cortex using BOLD contrast at 4 Tesla: implications for the vascular point-spread function. Magn Reson Med 41:230-235.
41. Menon RS, Ogawa S, Strupp JP, Ugurbil K (1997) Ocular dominance in human V1 demonstrated by functional magnetic resonance imaging. J Neurophysiol 77:2780-2787.
42. Moon CH, Fukuda M, Kim SG (2004) Analysis of continuous intrinsic optical imaging data. Soc Neurosci Abstr 30:920.13.
43. Movshon JA, Thompson ID, Tolhurst DJ (1978) Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. J Physiol (Lond) 283:101-120.
44. Nagaoka T, Zhao F, Wang P, Harel N, Kennan RP, Ogawa S, Kim SG (2006) Increases in oxygen consumption without cerebral blood volume change during visual stimulation under hypotension condition. J Cereb Blood Flow Metab 26:1043-1051.
45. Narayan SM, Esfahani P, Blood AJ, Sikkens L, Toga AW (1995) Functional increases in cerebral blood volume over somatosensory cortex. J Cereb Blood Flow Metab 15:754-765.
46. Obrig H, Neufang M, Wenzel R, Kohl M, Steinbrink J, Einhaupl K, Villringer A (2000) Spontaneous low frequency oscillations of cerebral hemodynamics and metabolism in human adults. NeuroImage 12:623-639.
47. Park SH, Kim SG (2005) MR venography using BOLD contrast at 9.4T. Proc Intl Soc Mag Reson Med 13:1718.
48. Rao SC, Toth LJ, Sur M (1997) Optically imaged maps of orientation preference in primary visual cortex of cats and ferrets. J Comp Neurol 387:358-370.
49. Ress D, Backus BT, Heeger DJ (2000) Activity in primary visual cortex predicts performance in a visual detection task. Nat Neurosci 3:940-945.
50. Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RB (1995) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268:889-893.
51. Sheth SA, Nemoto M, Guiou M, Walker M, Pouratian N, Hageman N, Toga AW (2004) Columnar specificity of microvascular oxygenation and volume responses: implications for functional brain mapping. J Neurosci 24:634-641.
52. Shmuel A, Grinvald A (1996) Functional organization for direction of motion and its relationship to orientation maps in cat area 18. J Neurosci 16:6945-6964.
53. Suh M, Bahar S, Mehta AD, Schwartz TH (2005) Temporal dependence in uncoupling of blood volume and oxygenation during interictal epileptiform events in rat neocortex. J Neurosci 25:68-77.
54. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M (2006) Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9:260-267.
55. Thompson JK, Peterson MR, Freeman RD (2003) Single-neuron activity and tissue oxygenation in the cerebral cortex. Science 299:1070-1072.
56. Tootell RB, Hadjikhani NK, Vanduffel W, Liu AK, Mendola JD, Sereno MI, Dale AM (1998) Functional analysis of primary visual cortex (V1) in humans. Proc Natl Acad Sci USA 95:811-817.
57. Tsao DY, Freiwald WA, Tootell RB, Livingstone MS (2006) A cortical region consisting entirely of face-selective cells. Science 311:670-674.
58. van Bruggen N, Busch E, Palmer JT, Williams SP, de Crespigny AJ (1998) High-resolution functional magnetic resonance imaging of the rat brain: mapping changes in cerebral blood volume using iron oxide contrast media. J Cereb Blood Flow Metab 18:1178-1183.
59. Vanduffel W, Fize D, Mandeville JB, Nelissen K, Van Hecke P, Rosen BR, Tootell RB, Orban GA (2001) Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys. Neuron 32:565-577.
60. Vanzetta I, Slovin H, Omer DB, Grinvald A (2004) Columnar resolution of blood volume and oximetry functional maps in the behaving monkey; implications for fMRI. Neuron 42:843-854.
61. Vanzetta I, Hildesheim R, Grinvald A (2005) Compartment-resolved imaging of activity-dependent dynamics of cortical blood volume and oximetry. J Neurosci 25:2233-2244.
62. Villringer A, Them A, Lindauer U, Einhaupl K, Dirnagl U (1994) Capillary perfusion of the rat brain cortex. An in vivo confocal microscopy study. Circ Res 75:55-62.
63. Warnking J, Dojat M, Guerin-Dugue A, Delon-Martin C, Olympieff S, Richard N, Chehikian A, Segebarth C (2002) fMRI retinotopic mapping - step by step. NeuroImage 17:1665-1683.
64. Wei L, Otsuka T, Acuff V, Bereczki D, Pettigrew K, Patlak C, Fenstermacher J (1993) The velocities of red cell and plasma flows through parenchymal microvessels of rat brain are decreased by pentobarbital. J Cereb Blood Flow Metab 13:487-497.
65. Womelsdorf T, Eysel UT, Kisvarday ZF (2001) Comparison of orientation maps obtained with different number of stimulus orientations. NeuroImage 13:1131-1139.
66. Zepeda A, Arias C, Sengpiel F (2004) Optical imaging of intrinsic signals: recent developments in the methodology and its applications. J Neurosci Methods 136:1-21.
67. Zhao F, Wang P, Hendrich K, Kim SG (2005) Spatial specificity of cerebral blood volume-weighted fMRI responses at columnar resolution. Neuro-Image 27:416-424.
68. Zhao F, Wang P, Hendrich K, Ugurbil K, Kim SG (2006) Cortical layer-dependent BOLD and CBV responses measured by spin-echo and gradient-echo fMRI: insights into hemodynamic regulation. NeuroImage 30:1149-1160.
69. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6:43-50.