Ultra high-resolution fMRI and electrophysiology of the rat primary somatosensory cortex

NeuroImage

Volumn 73, Issue , 2013, Pages 113-120

  Shih, Yen Yu Ian ^a,b,c   Chen, You Yin ^d   Lai, Hsin Yi ^a   Kao, Yu Chieh Jill ^a   Shyu, Bai Chuang ^e   Duong, Timothy Q ^c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

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

^d NATIONAL YANG MING UNIVERSITY   (Taiwan)

^e INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

Cerebral blood volume; Current source density; FMRI; High resolution; Local field potential; Rat; Somatosensory cortex

Indexed keywords

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ARTICLE; BRAIN BLOOD VOLUME; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; ELECTRODE; ELECTROSTIMULATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; NOCICEPTIVE STIMULATION; NONHUMAN; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; STIMULUS RESPONSE;

ANIMALS; DATA INTERPRETATION, STATISTICAL; ELECTRIC STIMULATION; ELECTROMAGNETIC FIELDS; ELECTROPHYSIOLOGY; FORELIMB; MAGNETIC RESONANCE IMAGING; MALE; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATION, ARTIFICIAL; SOMATOSENSORY CORTEX; STEREOTAXIC TECHNIQUES;

EID: 84874526613     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.01.062     Document Type: Article

References (98)

1. Bannister A.P. Inter- and intra-laminar connections of pyramidal cells in the neocortex. Neurosci. Res. 2005, 53:95-103.
2. Bédard C., Destexhe A. Generalized theory for current-source-density analysis in brain tissue. Phys. Rev. E 2011, 84:041909.
3. Bernardo K.L., Woolsey T.A. Axonal trajectories between mouse somatosensory thalamus and cortex. J. Comp. Neurol. 1987, 258:542-564.
4. Brinker G., Bock C., Busch E., Krep H., Hossmann K.A., Hoehn-Berlage M. Simultaneous recording of evoked potentials and T2*-weighted MR images during somatosensory stimulation of rat. Magn. Reson. Med. 1999, 41:469-473.
5. Buzsaki G., Anastassiou C.A., Koch C. The origin of extracellular fields and currents-EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 2012, 13:407-420.
6. Chang C., Shyu B.C. A fMRI study of brain activations during non-noxious and noxious electrical stimulation of the sciatic nerve of rats. Brain Res. 2001, 897:71-81.
7. Chapman C.A., Trepel C., Ivanco T.L., Froc D.J., Wilson K., Racine R.J. Changes in field potentials and membrane currents in rat sensorimotor cortex following repeated tetanization of the corpus callosum in vivo. Cereb. Cortex 1998, 8:730-742.
8. Chen Y.Y., Lai H.Y., Lin S.H., Cho C.W., Chao W.H., Liao C.H., Tsang S., Chen Y.F., Lin S.Y. Design and fabrication of a polyimide-based microelectrode array: application in neural recording and repeatable electrolytic lesion in rat brain. J. Neurosci. Methods 2009, 182:6-16.
9. Croze S., Duclaux R., Kenshalo D.R. The thermal sensitivity of the polymodal nociceptors in the monkey. J. Physiol. 1976, 263:539-562.
10. Csicsvari J., Henze D.A., Jamieson B., Harris K.D., Sirota A., Barthó P., Wise K.D., Buzsáki G. Massively parallel recording of unit and local field potentials with silicon-based electrodes. J. Neurophysiol. 2003, 90:1314-1323.
11. de Kock C.P., Bruno R.M., Spors H., Sakmann B. Layer- and cell-type-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J. Physiol. 2007, 581:139-154.
12. Devor A., Dunn A.K., Andermann M.L., Ulbert I., Boas D.A., Dale A.M. Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex. Neuron 2003, 39:353-359.
13. Disbrow E.A., Slutsky D.A., Roberts T.P., 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. 2000, 97:9718-9723.
14. Djouhri L., Bleazard L., Lawson S.N. Association of somatic action potential shape with sensory receptive properties in guinea-pig dorsal root ganglion neurones. J. Physiol. 1998, 513(Pt. 3):857-872.
15. Duong T.Q., Muir E.R. Magnetic resonance imaging of the retina. Jpn. J. Ophthalmol. 2009, 53:352-367.
16. Duong T.Q., Silva A.C., Lee S.P., Kim S.G. Functional MRI of calcium-dependent synaptic activity: cross correlation with CBF and BOLD measurements. Magn. Reson. Med. 2000, 43:383-392.
17. Duong T.Q., Kim D.S., Ugurbil K., Kim S.G. Localized cerebral blood flow response at submillimeter columnar resolution. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:10904-10909.
18. Duong T.Q., Yacoub E., Adriany G., Hu X., Ugurbil K., Kim S.G. Microvascular BOLD contribution at 4 and 7T in the human brain: gradient-echo and spin-echo fMRI with suppression of blood effects. Magn. Reson. Med. 2003, 49:1019-1027.
19. Duvernoy H.M., Delon S., Vannson J.L. Cortical blood vessels of the human brain. Brain Res. Bull. 1981, 7:519-579.
20. Einevoll G.T., Pettersen K.H., Devor A., Ulbert I., Halgren E., Dale A.M. Laminar population analysis: estimating firing rates and evoked synaptic activity from multielectrode recordings in rat barrel cortex. J. Neurophysiol. 2007, 97:2174-2190.
21. Feldmeyer D. Excitatory neuronal connectivity in the barrel cortex. Front. Neuroanat. 2012, 6:24.
22. Fonta C., Imbert M. Vascularization in the primate visual cortex during development. Cereb. Cortex 2002, 12:199-211.
23. Freeman J.A., Nicholson C. Experimental optimization of current source-density technique for anuran cerebellum. J. Neurophysiol. 1975, 38:369-382.
24. Fukuda M., Moon C.H., Wang P., 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. 2006, 26:11821-11832.
25. Goldenholz D.M., Ahlfors S.P., Hämäläinen M.S., Sharon D., Ishitobi M., Vaina L.M., Stufflebeam S.M. Mapping the signal-to-noise-ratios of cortical sources in magnetoencephalography and electroencephalography. Hum. Brain Mapp. 2009, 30:1077-1086.
26. Goloshevsky A.G., Silva A.C., Dodd S.J., Koretsky A.P. 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. 2008, 1195:67-76.
27. Guilbaud G., Peschanski M., Gautron M., Binder D. Neurones responding to noxious stimulation in VB complex and caudal adjacent regions in the thalamus of the rat. Pain 1980, 8:303-318.
28. Harel N., Lin J., Moeller S., Ugurbil K., Yacoub E. Combined imaging-histological study of cortical laminar specificity of fMRI signals. NeuroImage 2006, 29:879-887.
29. Harel N., Bolan P.J., Turner R., Ugurbil K., Yacoub E. Recent advances in high-resolution MR application and its implications for neurovascular coupling research. Front. Neuroenerg. 2010, 2:130.
30. Helmstaedter M., de Kock C.P., Feldmeyer D., Bruno R.M., Sakmann B. Reconstruction of an average cortical column in silico. Brain Res. Rev. 2007, 55:193-203.
31. Herkenham M. Laminar organization of thalamic projections to the rat neocortex. Science 1980, 207:532-535.
32. Hewson-Stoate N., Jones M., Martindale J., Berwick J., Mayhew J. Further nonlinearities in neurovascular coupling in rodent barrel cortex. NeuroImage 2005, 24:565-574.
33. Huttunen J.K., Grohn O., Penttonen M. Coupling between simultaneously recorded BOLD response and neuronal activity in the rat somatosensory cortex. NeuroImage 2008, 39:775-785.
34. Jellema T., Brunia C.H., Wadman W.J. Sequential activation of microcircuits underlying somatosensory-evoked potentials in rat neocortex. Neuroscience 2004, 129:283-295.
35. Jin T., Kim S.G. Cortical layer-dependent dynamic blood oxygenation, cerebral blood flow and cerebral blood volume responses during visual stimulation. NeuroImage 2008, 43:1-9.
36. Jones M., Hewson-Stoate N., Martindale J., Redgrave P., Mayhew J. Nonlinear coupling of neural activity and CBF in rodent barrel cortex. NeuroImage 2004, 22:956-965.
37. Julius D., Basbaum A.I. Molecular mechanisms of nociception. Nature 2001, 413:203-210.
38. Kalliomaki J., Weng H.R., Nilsson H.J., Schouenborg J. Nociceptive C fibre input to the primary somatosensory cortex (SI). A field potential study in the rat. Brain Res. 1993, 622:262-270.
39. Kajikawa Y., Schroeder C.E. How local is the local field potential?. Neuron 2011, 72:847-858.
40. Keller A., White E.L., Cipolloni P.B. The identification of thalamocortical axon terminals in barrels of mouse Sml cortex using immunohistochemistry of anterogradely transported lectin (Phaseolus vulgaris-leucoagglutinin). Brain Res. 1985, 343:159-165.
41. Kennedy C., Des Rosiers M.H., Sakurada O., Shinohara M., Reivich M., Jehle J.W., Sokoloff L. Metabolic mapping of the primary visual system of the monkey by means of the autoradiographic [14C]deoxyglucose technique. Proc. Natl. Acad. Sci. U. S. A. 1976, 73:4230-4234.
42. Kim S.G., Fukuda M. Lessons from fMRI about mapping cortical columns. Neuroscientist 2008, 14:287-299.
43. Kim D.S., Duong T.Q., Kim S.G. High-resolution mapping of iso-orientation columns by fMRI. Nat. Neurosci. 2000, 3:164-169.
44. Koopmans P.J., Barth M., Norris D.G. Layer-specific BOLD activation in human V1. Hum. Brain Mapp. 2010, 31:1297-1304.
45. Kossut M., Hand P.J., Greenberg J., Hand C.L. Single vibrissal cortical column in SI cortex of rat and its alterations in neonatal and adult vibrissa-deafferented animals: a quantitative 2DG study. J. Neurophysiol. 1988, 60:829-852.
46. Krupa D.J., Wiest M.C., Shuler M.G., Laubach M., Nicolelis M.A. Layer-specific somatosensory cortical activation during active tactile discrimination. Science 2004, 304:1989-1992.
47. Lamour Y., Guilbaud G., Willer J.C. Rat somatosensory (SmI) cortex: II. Laminar and columnar organization of noxious and non-noxious inputs. Exp. Brain Res. 1983, 49:46-54.
48. Lamour Y., Willer J.C., Guilbaud G. Rat somatosensory (SmI) cortex: I. Characteristics of neuronal responses to noxious stimulation and comparison with responses to non-noxious stimulation. Exp. Brain Res. 1983, 49:35-45.
49. Lauwers F., Cassot F., Lauwers-Cances V., Puwanarajah P., Duvernoy H. Morphometry of the human cerebral cortex microcirculation: general characteristics and space-related profiles. NeuroImage 2008, 39:936-948.
50. Lee S.P., Silva A.C., Ugurbil K., Kim S.G. Diffusion-weighted spin-echo fMRI at 9.4T: microvascular/tissue contribution to BOLD signal changes. Magn. Reson. Med. 1999, 42:919-928.
51. 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.
52. Logothetis N., Merkle H., Augath M., Trinath T., Ugurbil K. Ultra high-resolution fMRI in monkeys with implanted RF coils. Neuron 2002, 35:227-242.
53. Lowe A.S., Beech J.S., Williams S.C. Small animal, whole brain fMRI: innocuous and nociceptive forepaw stimulation. Neuroimage 2007, 35:719-728.
54. Lu H., Patel S., Luo F., Li S.J., Hillard C.J., Ward B.D., Hyde J.S. Spatial correlations of laminar BOLD and CBV responses to rat whisker stimulation with neuronal activity localized by Fos expression. Magn. Reson. Med. 2004, 52:1060-1068.
55. Lubke J., Feldmeyer D. Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain Struct. Funct. 2007, 212:3-17.
56. Lynn B., Carpenter S.E. Primary afferent units from the hairy skin of the rat hind limb. Brain Res. 1982, 238:29-43.
57. Mandeville J.B., Marota J.J., Kosofsky B.E., Keltner J.R., Weissleder R., Rosen B.R., Weisskoff R.M. Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation. Magn. Reson. Med. 1998, 39:615-624.
58. Masamoto K., Kim T., Fukuda M., Wang P., Kim S.G. Relationship between neural, vascular, and BOLD signals in isoflurane-anesthetized rat somatosensory cortex. Cereb. Cortex 2007, 17:942-950.
59. McAllister J.P., Wells J. The structural organization of the ventral posterolateral nucleus in the rat. J. Comp. Neurol. 1981, 197:271-301.
60. Meyer H.S., Wimmer V.C., Oberlaender M., de Kock C.P., Sakmann B., Helmstaedter M. Number and laminar distribution of neurons in a thalamocortical projection column of rat vibrissal cortex. Cereb. Cortex 2010, 20:2277-2286.
61. Mitzdorf U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 1985, 65:37-100.
62. Mitzdorf U. Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex. Int. J. Neurosci. 1987, 33:33-59.
63. Muir E.R., Duong T.Q. MRI of retinal and choroidal blood flow with laminar resolution. NMR Biomed. 2011, 24:216-223.
64. Nielsen A.N., Lauritzen M. Coupling and uncoupling of activity-dependent increases of neuronal activity and blood flow in rat somatosensory cortex. J. Physiol. 2001, 533:773-785.
65. Ogawa S., Lee T.M., Stepnoski R., Chen W., Zhu X.H., Ugurbil K. An approach to probe some neural systems interaction by functional MRI at neural time scale down to milliseconds. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11026-11031.
66. Olman C.A., Harel N., Feinberg D.A., He S., Zhang P., Ugurbil K., Yacoub E. Layer-specific fMRI reflects different neuronal computations at different depths in human V1. PLoS One 2012, 7:e32536.
67. Patel U. Non-random distribution of blood vessels in the posterior region of the rat somatosensory cortex. Brain Res. 1983, 289:65-70.
68. Pettersen K.H., Devor A., Ulbert I., Dale A.M., Einevoll G.T. Current-source density estimation based on inversion of electrostatic forward solution: effects of finite extent of neuronal activity and conductivity discontinuities. J. Neurosci. Methods 2006, 154:116-133.
69. Polimeni J.R., Fischl B., Greve D.N., Wald L.L. Laminar analysis of 7T BOLD using an imposed spatial activation pattern in human V1. NeuroImage 2010, 52:1334-1346.
70. Sakata S., Harris K.D. Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 2009, 64:404-418.
71. Schouenborg J., Kalliomaki J., Gustavsson P., Rosen I. Field potentials evoked in rat primary somatosensory cortex (SI) by impulses in cutaneous A beta- and C-fibres. Brain Res. 1986, 397:86-92.
72. Schubert D., Kotter R., Staiger J.F. Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits. Brain Struct. Funct. 2007, 212:107-119.
73. Shen Q., Ren H., Duong T.Q. CBF, BOLD, CBV, and CMRO(2) fMRI signal temporal dynamics at 500-msec resolution. J. Magn. Reson. Imaging 2008, 27:599-606.
74. Sheth S.A., Nemoto M., Guiou M., Walker M., Pouratian N., Toga A.W. Linear and nonlinear relationships between neuronal activity, oxygen metabolism, and hemodynamic responses. Neuron 2004, 42:347-355.
75. Shih Y.Y., Chen C.C., Shyu B.C., Lin Z.J., Chiang Y.C., Jaw F.S., Chen Y.Y., Chang C. A new scenario for negative functional magnetic resonance imaging signals: endogenous neurotransmission. J. Neurosci. 2009, 29:3036-3044.
76. Shih Y.Y., Wey H.Y., De La Garza B.H., Duong T.Q. Striatal and cortical BOLD, blood flow, blood volume, oxygen consumption, and glucose consumption changes in noxious forepaw electrical stimulation. J. Cereb. Blood Flow Metab. 2011, 31:832-841.
77. Shih Y.Y., Chiang Y.C., Shyu B.C., Jaw F.S., Duong T.Q., Chang C. Endogenous opioid-dopamine neurotransmission underlie negative CBV fMRI signals. Exp. Neurol. 2012, 234:382-388.
78. Shih Y.Y., Li G., Muir E.R., De La Garza B.H., Kiel J.W., Duong T.Q. Pharmacological MRI of the choroid and retina: Blood flow and BOLD responses during nitroprusside infusion. Magn. Reson. Med. 2012, 68:1273-1278.
79. Shih Y.Y., Muir E.R., Li G., De La Garza B.H., Duong T.Q. High-resolution 3D MR microangiography of the rat ocular circulation. Radiology 2012, 264:234-241.
80. Siero J.C., Petridou N., Hoogduin H., Luijten P.R., Ramsey N.F. Cortical depth-dependent temporal dynamics of the BOLD response in the human brain. J. Cereb. Blood Flow Metab. 2011, 31:1999-2008.
81. Silva A.C., Koretsky A.P. Laminar specificity of functional MRI onset times during somatosensory stimulation in rat. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15182-15187.
82. Silva A.C., Lee S.P., Iadecola C., Kim S.G. Early temporal characteristics of cerebral blood flow and deoxyhemoglobin changes during somatosensory stimulation. J. Cereb. Blood Flow Metab. 2000, 20:201-206.
83. Silva A.C., Koretsky A.P., Duyn J.H. Functional MRI impulse response for BOLD and CBV contrast in rat somatosensory cortex. Magn. Reson. Med. 2007, 57:1110-1118.
84. Smirnakis S.M., Schmid M.C., Weber B., Tolias A.S., Augath M., Logothetis N.K. Spatial specificity of BOLD versus cerebral blood volume fMRI for mapping cortical organization. J. Cereb. Blood Flow Metab. 2007, 27:1248-1261.
85. Sun J.J., Yang J.W., Shyu B.C. Current source density analysis of laser heat-evoked intra-cortical field potentials in the primary somatosensory cortex of rats. Neuroscience 2006, 140:1321-1336.
86. Tenke C.E., Schroeder C.E., Arezzo J.C., Vaughan H.G. Interpretation of high-resolution current source density profiles: a simulation of sublaminar contributions to the visual evoked potential. Exp. Brain Res. 1993, 94:183-192.
87. Tian P., Teng I.C., May L.D., Kurz R., Lu K., Scadeng M., Hillman E.M., De Crespigny A.J., D'Arceuil H.E., Mandeville J.B., Marota J.J., Rosen B.R., Liu T.T., Boas D.A., Buxton R.B., Dale A.M., Devor A. Cortical depth-specific microvascular dilation underlies laminar differences in blood oxygenation level-dependent functional MRI signal. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15246-15251.
88. Torebjork H.E. Afferent C units responding to mechanical, thermal and chemical stimuli in human non-glabrous skin. Acta Physiol. Scand. 1974, 92:374-390.
89. Van Hees J., Gybels J.M. Pain related to single afferent C fibers from human skin. Brain Res. 1972, 48:397-400.
90. Van C.N., Verhoye M., Van der L.A. Stimulation of the rat somatosensory cortex at different frequencies and pulse widths. NMR Biomed. 2006, 19:10-17.
91. Viswanathan A., Freeman R.D. Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity. Nat. Neurosci. 2007, 10:1308-1312.
92. White E.L. Thalamocortical synaptic relations: a review with emphasis on the projections of specific thalamic nuclei to the primary sensory areas of the neocortex. Brain Res. 1979, 180:275-311.
93. Wojcik D.K., Leski S. Current source density reconstruction from incomplete data. Neural Comput. 2010, 22:48-60.
94. Woolsey T.A., Rovainen C.M., Cox S.B., Henegar M.H., Liang G.E., Liu D., Moskalenko Y.E., Sui J., Wei L. Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain. Cereb. Cortex 1996, 6:647-660.
95. Yu X., Glen D., Wang S., Dodd S., Hirano Y., Saad Z., Reynolds R., Silva A.C., Koretsky A.P. Direct imaging of macrovascular and microvascular contributions to BOLD fMRI in layers IV-V of the rat whisker-barrel cortex. NeuroImage 2012, 59:1451-1460.
96. Zhao F., Wang P., Kim S.G. Cortical depth-dependent gradient-echo and spin-echo BOLD fMRI at 9.4T. Magn. Reson. Med. 2004, 51:518-524.
97. Zhao F., Wang P., Hendrich K., Ugurbil K., Kim S.G. Cortical layer-dependent BOLD and CBV responses measured by spin-echo and gradient-echo fMRI: insights into hemodynamic regulation. NeuroImage 2006, 30:1149-1160.
98. Zheng D., LaMantia A.S., Purves D. Specialized vascularization of the primate visual cortex. J. Neurosci. 1991, 11:2622-2629.