Direct, intraoperative observation of ~0.1Hz hemodynamic oscillations in awake human cortex: Implications for fMRI

NeuroImage

Volumn 87, Issue , 2014, Pages 323-331

  Rayshubskiy, Aleksandr ^a   Wojtasiewicz, Teresa J ^b   Mikell, Charles B ^b   Bouchard, Matthew B ^a   Timerman, Dmitriy ^a   Youngerman, Brett E ^b   McGovern, Robert A ^b   Otten, Marc L ^b   Canoll, Peter ^b   McKhann, Guy M ^b   Hillman, Elizabeth M C ^a,b  

^a Fu Foundation School of Engineering and Applied Science   (United States)

^b Howard Hughes Medical Institute   (United States)

Author keywords

0.1Hz oscillation; Cerebral hemodynamics; FMRI; Intraoperative optical imaging; Resting state; Vasomotion

Indexed keywords

ARTERIOLE; ARTICLE; BLOOD PRESSURE; BRAIN BLOOD VESSEL; BRAIN CORTEX; BRAIN REGION; BRAIN SURGERY; BRAIN TUMOR; CASE REPORT; CONTROLLED STUDY; EPILEPSY SURGERY; FLUORESCENCE IMAGING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; HUMAN; INTRAOPERATIVE PERIOD; MULTISPECTRAL OPTICAL INTRINSIC SIGNAL IMAGING; NEUROIMAGING; OSCILLATION; PRIORITY JOURNAL; SLOW SINUSOIDAL HEMODYNAMIC OSCILLATION; WAKEFULNESS;

0.1HZ OSCILLATION; CEREBRAL HEMODYNAMICS; FMRI; INTRAOPERATIVE OPTICAL IMAGING; RESTING STATE; VASOMOTION;

ADULT; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; FEMALE; HEMODYNAMICS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INTRAOPERATIVE NEUROPHYSIOLOGICAL MONITORING; MAGNETIC RESONANCE IMAGING; MALE; OPTICAL IMAGING; WAKEFULNESS;

EID: 84890848182     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.10.044     Document Type: Article

References (79)

1. Aalkjær C., Nilsson H. Vasomotion: cellular background for the oscillator and for the synchronization of smooth muscle cells. Br. J. Pharmacol. 2005, 144:605-616.
2. Aalkjær C., Boedtkjer D., Matchkov V. Vasomotion - what is currently thought?. Acta Physiol. 2011, 202:253-269.
3. Ances B.M., Greenberg J.H., Detre J.A. Interaction between nitric oxide synthase inhibitor induced oscillations and the activation flow coupling response. Brain Res. 2010, 1309:19-28.
4. Anis N.A., Berry S.C., Burton N.R., Lodge D. The dissociative anaesthetics, ketamine and phencyclidine, selectively reduce excitation of central mammalian neurones by N-methyl-aspartate. Br. J. Pharmacol. 1983, 79:565-575.
5. Attwell D., Buchan A.M., Charpak S., Lauritzen M., MacVicar B.A., Newman E.A. Glial and neuronal control of brain blood flow. Nature 2010, 468:232-243.
6. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
7. Bouchard M.B., Chen B.R., Burgess S.A., Hillman E.M.C. Ultra-fast multispectral optical imaging of cortical oxygenation, blood flow, and intracellular calcium dynamics. Opt. Express 2009, 17:15670-15678.
8. Bouskela E., Grampp W. Spontaneous vasomotion in hamster cheek pouch arterioles in varying experimental conditions. Am. J. Physiol. Heart Circ. Physiol. 1992, 262:H478-H485.
9. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network. Ann. N. Y. Acad. Sci. 2008, 1124:1-38.
10. Buckner R.L., Sepulcre J., Talukdar T., Krienen F.M., Liu H., Hedden T., Andrews-Hanna J.R., Sperling R.A., Johnson K.A. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J. Neurosci. 2009, 29:1860-1873.
11. Dirnagl U., Lindauer U., Villringer A. Nitric oxide synthase blockade enhances vasomotion in the cerebral microcirculation of anesthetized rats. Microvasc. Res. 1993, 45:318-323.
12. Drew P.J., Duyn J.H., Golanov E., Kleinfeld D. Finding coherence in spontaneous oscillations. Nat. Neurosci. 2008, 11:991-993.
13. Elwell C.E., Springett R., Hillman E., Delpy D.T. Oscillations in cerebral haemodynamics. Implications for functional activation studies. Adv. Exp. Med. Biol. 1999, 471:57-65.
14. Farin A., Suzuki S.O., Weiker M., Goldman J.E., Bruce J.N., Canoll P. Transplanted glioma cells migrate and proliferate on host brain vasculature: a dynamic analysis. Glia 2006, 53:799-808.
15. Ferguson A. A review of the physiology of cranial osteopathy. J. Osteopath. Med. 2003, 6:74-84.
16. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8:700-711.
17. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9673-9678.
18. Fujii K., Heistad D.D., Faraci F.M. Vasomotion of basilar arteries in vivo. Am. J. Physiol. Heart Circ. Physiol. 1990, 258:H1829-H1834.
19. Garrity A.G., Pearlson G.D., McKiernan K., Lloyd D., Kiehl K.A., Calhoun V.D. Aberrant "default mode" functional connectivity in schizophrenia. Am. J. Psychiatr. 2007, 164:450-457.
20. Golanov E.V., Yamamoto S., Reis D.J. Spontaneous waves of cerebral blood flow associated with a pattern of electrocortical activity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1994, 266:R204-R214.
21. Grefkes C., Fink G.R. Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches. Brain 2011, 134:1264-1276.
22. Grosberg L.E., Chen B.R., Hillman E.M.C. Simultaneous multiplane in vivo nonlinear microscopy using spectral encoding. Opt. Lett. 2012, 37:2967-2969.
23. Haddock R.E., Hill C.E. Rhythmicity in arterial smooth muscle. J. Physiol. 2005, 566:645-656.
24. Haddock R.E., Hirst G.D.S., Hill C.E. Voltage independence of vasomotion in isolated irideal arterioles of the rat. J. Physiol. 2002, 540:219-229.
25. Haglund M.M., Hochman D.W. Optical imaging of epileptiform activity in human neocortex. Epilepsia 2004, 45:43-47.
26. Haglund M.M., Ojemann G.A., Hochman D.W. Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature 1992, 358:668-671.
27. Harrison N.L., Simmonds M.A. Quantitative studies on some antagonists of N-methyl D-aspartate in slices of rat cerebral-cortex. Br. J. Pharmacol. 1985, 84:381-391.
28. Hecht N., Woitzik J., Konig S., Horn P., Vajkoczy P. Laser speckle imaging allows real-time intraoperative blood flow assessment during neurosurgical procedures. J. Cereb. Blood Flow Metab. 2013, 33:1000-1007.
29. Hillman E.M.C. Optical brain imaging in vivo: techniques and applications from animal to man. J. Biomed. Opt. 2007, 12. [051402-051402].
30. Hundley W.G., Renaldo G.J., Levasseur J.E., Kontos H.A. Vasomotion in cerebral microcirculation of awake rabbits. Am. J. Physiol. Heart Circ. Physiol. 1988, 254:H67-H71.
31. 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.
32. Jones M., Berwick J., Hewson-Stoate N., Gias C., Mayhew J. The effect of hypercapnia on the neural and hemodynamic responses to somatosensory stimulation. NeuroImage 2005, 27:609-623.
33. Julien C. The enigma of Mayer waves: facts and models. Cardiovasc. Res. 2006, 70:12-21.
34. Kapela A., Parikh J., Tsoukias Nikolaos M. Multiple factors influence calcium synchronization in arterial vasomotion. Biophys. J. 2012, 102:211-220.
35. Kiviniemi V., Jauhiainen J., Tervonen O., Pääkkö E., Oikarinen J., Vainionpää V., Rantala H., Biswal B. Slow vasomotor fluctuation in fMRI of anesthetized child brain. Magn. Reson. Med. 2000, 44:373-378.
36. Klein S., Staring M., Murphy K., Viergever M.A., Pluim J.P.W. elastix: a toolbox for intensity-based medical image registration. IEEE Trans. Med. Imaging 2010, 29:196-205.
37. Kolyva C., Kingston H., Tachtsidis I., Mohanty S., Mishra S., Patnaik R., Maude R., Dondorp A., Elwell C. Oscillations in cerebral haemodynamics in patients with falciparum malaria. Oxygen Transport to Tissue XXXIV 2013, 101-107. Springer, New York. W.J. Welch, F. Palm, D.F. Bruley, D.K. Harrison (Eds.).
38. Kruggel F., von Cramon D.Y. Temporal properties of the hemodynamic response in functional MRI. Hum. Brain Mapp. 1999, 8:259-271.
39. Kvernmo H.D., Stefanovska A., Bracic M., Kirkebøen K.A., Kvernebo K. Spectral analysis of the laser Doppler perfusion signal in human skin before and after exercise. Microvasc. Res. 1998, 56:173-182.
40. Lavine M., Haglund M.M., Hochman D.W. Dynamic linear model analysis of optical imaging data acquired from the human neocortex. J. Neurosci. Methods 2011, 199:346-362.
41. Leopold D.A., Murayama Y., Logothetis N.K. Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. Cereb. Cortex 2003, 13:422-433.
42. Lorincz M.L., Geall F., Bao Y., Crunelli V., Hughes S.W. ATP-dependent infra-slow (<0.1Hz) oscillations in thalamic networks. PLoS ONE 2009, 4:e4447.
43. Majeed W., Magnuson M., Keilholz S.D. Spatiotemporal dynamics of low frequency fluctuations in BOLD fMRI of the rat. J. Magn. Reson. Imaging 2009, 30:384-393.
44. Mantini D., Gerits A., Nelissen K., Durand J.-B., Joly O., Simone L., Sawamura H., Wardak C., Orban G.A., Buckner R.L., Vanduffel W. Default mode of brain function in monkeys. J. Neurosci. 2011, 31:12954-12962.
45. Mayer S. Studien zur physiologie des herzens und blutgeflaesse V. Ueber spontane blutdruckschwankungen. Akademie der Wissenschaften in Wien. Math. Naturwiss. Cl. 1876, 74:281-307.
46. Mayer A.R., Mannell M.V., Ling J., Gasparovic C., Yeo R.A. Functional connectivity in mild traumatic brain injury. Hum. Brain Mapp. 2011, 32:1825-1835.
47. Mayhew J.E.W., Askew S., Zheng Y., Porrill J., Westby G.W.M., Redgrave P., Rector D.M., Harper R.M. Cerebral vasomotion: a 0.1-Hz oscillation in reflected light imaging of neural activity. NeuroImage 1996, 4:183-193.
48. Mitra P.P., Ogawa S., Hu X., Uǧurbil K. The nature of spatiotemporal changes in cerebral hemodynamics as manifested in functional magnetic resonance imaging. Magn. Reson. Med. 1997, 37:511-518.
49. Murphy K., Birn R.M., Bandettini P.A. Resting-state fMRI confounds and cleanup. NeuroImage 2013, 80:349-359.
50. Nakai M., Maeda M. Scopolamine-sensitive and resistant components of increase in cerebral cortical blood flow elicited by periaqueductal gray matter of rats. Neurosci. Lett. 1999, 270:173-176.
51. Näsi T., Virtanen J., Noponen T., Toppila J., Salmi T., Ilmoniemi R.J. Spontaneous hemodynamic oscillations during human sleep and sleep stage transitions characterized with near-infrared spectroscopy. PLoS ONE 2011, 6:e25415.
52. Negishi M., Martuzzi R., Novotny E.J., Spencer D.D., Constable R.T. Functional MRI connectivity as a predictor of the surgical outcome of epilepsy. Epilepsia 2011, 52:1733-1740.
53. Nir Y., Mukamel R., Dinstein I., Privman E., Harel M., Fisch L., Gelbard-Sagiv H., Kipervasser S., Andelman F., Neufeld M.Y., Kramer U., Arieli A., Fried I., Malach R. Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat. Neurosci. 2008, 11:1100-1108.
54. Obrig H., Neufang M., Wenzel R., Kohl M., Steinbrink J., Einhäupl K., Villringer A. Spontaneous low frequency oscillations of cerebral hemodynamics and metabolism in human adults. NeuroImage 2000, 12:623-639.
55. Oishi H., Schuster A., Lamboley M., Stergiopulos N., Meister J.-J., Bény J.-L. Role of membrane potential in vasomotion of isolated pressurized rat arteries. Life Sci. 2002, 71:2239-2248.
56. Otten M.L., Mikell C.B., Youngerman B.E., Liston C., Sisti M.B., Bruce J.N., Small S.A., McKhann G.M. Motor deficits correlate with resting state motor network connectivity in patients with brain tumours. Brain 2012, 135:1017-1026.
57. Pawela C.P., Biswal B.B., Cho Y.R., Kao D.S., Li R., Jones S.R., Schulte M.L., Matloub H.S., Hudetz A.G., Hyde J.S. Resting-state functional connectivity of the rat brain. Magn. Reson. Med. 2008, 59:1021-1029.
58. Pekanmäki K., Kolari P.J., Kiistala U. Laser Doppler vasomotion among patients with post-thrombotic venous insufficiency: effect of intermittent pneumatic compression. VASA 1991, 20:394-397.
59. Peng H., Matchkov V., Ivarsen A., Aalkjær C., Nilsson H. Hypothesis for the initiation of vasomotion. Circ. Res. 2001, 88:810-815.
60. Prahl S.A. Online resource http://omlc.ogi.edu/spectra/hemoglobin/summary.html.
61. Prakash N., Uhlemann F., Sheth S.A., Bookheimer S., Martin N., Toga A.W. Current trends in intraoperative optical imaging for functional brain mapping and delineation of lesions of language cortex. NeuroImage 2009, 47(Supplement 2):T116-T126.
62. Ren T.-Y., Brown J.N., Nuttall A.L., Miller J.M. Cochlear flux motion and arterial pressure reduction in guinea pig. Acta Otolaryngol. 1994, 114:254-258.
63. Rivadulla C., de Labra C., Grieve K.L., Cudeiro J. Vasomotion and neurovascular coupling in the visual thalamus in vivo. PLoS ONE 2011, 6:e28746.
64. Saka M., Berwick J., Jones M. Linear superposition of sensory-evoked and ongoing cortical hemodynamics. Front. Neuroenerg. 2010, 2.
65. Sakurai T., Terui N. Effects of sympathetically induced vasomotion on tissue-capillary fluid exchange. Am. J. Physiol. Heart Circ. Physiol. 2006, 291:H1761-H1767.
66. Sassaroli A., Pierro M., Bergethon P.R., Fantini S. Low-frequency spontaneous oscillations of cerebral hemodynamics investigated with near-infrared spectroscopy: a review. IEEE J. Sel. Top. Quantum Electron. 2012, 18:1478-1492.
67. Schmidt J.A., Intaglietta M., Borgstrom P. Periodic hemodynamics in skeletal muscle during local arterial pressure reduction. J. Appl. Physiol. 1992, 73:1077-1083.
68. Schmidt J.A., Borgström P., Firestone G.P., von Wichert P., Intaglietta M., Fronek A. Periodic hemodynamics (flow motion) in peripheral arterial occlusive disease. J. Vasc. Surg. 1993, 18:207-215.
69. Schroeter M.L., Bucheler M.M., Preul C., Scheid R., Schmiedel O., Guthke T., von Cramon D.Y. Spontaneous slow hemodynamic oscillations are impaired in cerebral microangiopathy. J. Cereb. Blood Flow Metab. 2005, 25:1675-1684.
70. Setchell B.P., Bergh A., Widmark A., Damber J.E. Effect of testicular temperature on vasomotion and blood flow. Int. J. Androl. 1995, 18:120-126.
71. Sheline Y.I., Raichle M.E. Resting state functional connectivity in preclinical Alzheimer's disease. Biol. Psychiatry 2013, 74:340-347.
72. Spitzer M.W., Calford M.B., Clarey J.C., Pettigrew J.D., Roe A.W. Spontaneous and stimulus-evoked intrinsic optical signals in primary auditory cortex of the cat. J. Neurophysiol. 2001, 85:1283-1298.
73. Stefanovska A. Coupled oscillatros: complex but not complicated cardiovascular and brain interactions. IEEE Eng. Med. Biol. Mag. 2007, 26:25-29.
74. Suh M., Ma H., Zhao M., Geneslaw A., Schwartz T. Intraoperative optical imaging of human cortex. Imaging the Brain With Optical Methods 2010, 135-157. Springer, New York. A.W. Roe (Ed.).
75. Sun R., Bouchard M.B., Hillman E.M.C. SPLASSH: open source software for camera-based high-speed, multispectral in-vivo optical image acquisition. Biomed. Opt. Express 2010, 1:385-397.
76. Tian P., Devor A., Sakadžić S., Dale A.M., Boas D.A. Monte Carlo simulation of the spatial resolution and depth sensitivity of two-dimensional optical imaging of the brain. J. Biomed. Opt. 2011, 16. (016006-016006-016013).
77. Wang H.H., Menezes N.M., Zhu M.W., Ay H., Koroshetz W.J., Aronen H.J., Karonen J.O., Liu Y., Nuutinen J., Wald L.L., Sorensen A.G. Physiological noise in MR images: an indicator of the tissue response to ischemia?. J. Magn. Reson. Imaging 2008, 27:866-871.
78. White B.R., Bauer A.Q., Snyder A.Z., Schlaggar B.L., Lee J.-M., Culver J.P. Imaging of functional connectivity in the mouse brain. PLoS ONE 2011, 6:e16322.
79. Zhao M., Suh M., Ma H., Perry C., Geneslaw A., Schwartz T.H. Focal increases in perfusion and decreases in hemoglobin oxygenation precede seizure onset in spontaneous human epilepsy. Epilepsia 2007, 48:2059-2067.