Neurovascular coupling: In vivo optical techniques for functional brain imaging

BioMedical Engineering Online

Volumn 12, Issue 1, 2013, Pages

  Liao, Lun De ^a   Tsytsarev, Vassiliy ^b   Delgado Martínez, Ignacio ^a   Li, Meng Lin ^c   Erzurumlu, Reha ^b   Vipin, Ashwati ^a   Orellana, Josue ^a   Lin, Yan Ren ^d   Lai, Hsin Yi ^e   Chen, You Yin ^f   Thakor, Nitish V ^a,g  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^d CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

^e CHANG GUNG UNIVERSITY   (Taiwan)

^f NATIONAL YANG MING UNIVERSITY   (Taiwan)

^g Johns Hopkins University   (United States)

Author keywords

2 photon microscopy; Cerebral neuroimaging; Functional near infrared spectroscopy; Functional photoacoustic microscopy; Laser speckle contrast imaging; Neurovascular coupling; Voltage sensitive dye imaging

Indexed keywords

CLINICAL INVESTIGATION; FUNCTIONAL BRAIN IMAGING; FUNCTIONAL NEAR-INFRARED SPECTROSCOPIES; LASER SPECKLE CONTRAST IMAGING; NEURO-VASCULAR COUPLING; OPTICAL IMAGING TECHNIQUE; OPTICAL IMAGING TECHNOLOGY; VOLTAGE-SENSITIVE DYE IMAGING;

BLOOD VESSELS; IMAGING TECHNIQUES; NEURONS; OPTICAL IMAGE STORAGE; PHOTOACOUSTIC MICROSCOPY; PHOTONS;

FUNCTIONAL NEUROIMAGING;

ANIMALIA;

ANIMAL; BRAIN; BRAIN MAPPING; FLUORESCENCE IMAGING; HUMAN; MULTIMODAL IMAGING; PHYSIOLOGY; PROCEDURES; TRANSLATIONAL RESEARCH; VASCULARIZATION; METHODOLOGY; REVIEW;

ANIMALS; BRAIN; BRAIN MAPPING; HUMANS; MULTIMODAL IMAGING; OPTICAL IMAGING; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84876811672     PISSN: None     EISSN: 1475925X     Source Type: Journal    
DOI: 10.1186/1475-925X-12-38     Document Type: Review

References (122)

1. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 2004, 5:347-360. 10.1038/nrn1387, 15100718.
2. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 2001, 21:1133-1145.
3. Klein B, Kuschinsky W, Schrock H, Vetterlein F. Interdependency of local capillary density, blood flow, and metabolism in rat brains. Am J Physiol 1986, 251:H1333-H1340.
4. Faraci FM, Heistad DD. Regulation of large cerebral arteries and cerebral microvascular pressure. Circ Res 1990, 66:8-17. 10.1161/01.RES.66.1.8, 2403863.
5. Orozco-Cabal L, Pollandt S, Liu J, Shinnick-Gallagher P, Gallagher JP. Regulation of synaptic transmission by CRF receptors. Rev Neuroscience 2006, 17:279-307.
6. Rossi DJ. Another BOLD role for astrocytes: coupling blood flow to neural activity. Nat Neurosci 2006, 9:159-161. 10.1038/nn0206-159, 16439980.
7. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA. Glial and neuronal control of brain blood flow. Nature 2010, 468:232-243. 10.1038/nature09613, 3206737, 21068832.
8. Zhang X, Toronov VY, Fabiani M, Gratton G, Webb AG. The study of cerebral hemodynamic and neuronal response to visual stimulation using simultaneous NIR optical tomography and BOLD fMRI in humans. Proc Soc Photo Opt Instrum Eng 2005, 5686:566-572. 3138137, 21776185.
9. Hudetz AG. Blood flow in the cerebral capillary network: A review emphasizing observations with intravital microscopy. Microcirculation 1997, 4:233-252. 10.3109/10739689709146787, 9219216.
10. Tsytsarev V, Premachandra K, Takeshita D, Bahar S. Imaging cortical electrical stimulation in vivo: fast intrinsic optical signal versus voltage-sensitive dyes. Opt Lett 2008, 33:1032-1034. 10.1364/OL.33.001032, 18451977.
11. Ohki K, Chung S, Ch'ng YH, Kara P, Reid RC. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 2005, 433:597-603. 10.1038/nature03274, 15660108.
12. Stosiek C, Garaschuk O, Holthoff K, Konnerth A. In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci USA 2003, 100:7319-7324. 10.1073/pnas.1232232100, 165873, 12777621.
13. Kucheryavykh LY, Kucheryavykh YV, Rolon-Reyes K, Skatchkov SN, Eaton MJ, Cubano LA, Inyushin M. Visualization of implanted GL261 glioma cells in living mouse brain slices using fluorescent 4-(4-(dimethylamino)-styryl)-N-methylpyridinium iodide (ASP+). Biotechniques 2012, 0:1-4.
14. Inyushin M, Kucheryavykh LY, Kucheryavykh YV, Nichols CG, Buono RJ, Ferraro TN, Skatchkov SN, Eaton MJ. Potassium channel activity and glutamate uptake are impaired in astrocytes of seizure-susceptible DBA/2 mice. Epilepsia 2010, 51:1707-1713. 10.1111/j.1528-1167.2010.02592.x, 3225007, 20831751.
15. Benedikt J, Inyushin M, Kucheryavykh YV, Rivera Y, Kucheryavykh LY, Nichols CG, Eaton MJ, Skatchkov SN. Intracellular polyamines enhance astrocytic coupling. Neuroreport 2012, 23:1021-1025. 10.1097/WNR.0b013e32835aa04b, 23076119.
16. Boas DA, Jones SR, Devor A, Huppert TJ, Dale AM. A vascular anatomical network model of the spatio-temporal response to brain activation. Neuroimage 2008, 40:1116-1129. 10.1016/j.neuroimage.2007.12.061, 2577617, 18289880.
17. Huppert TJ, Allen MS, Benav H, Jones PB, Boas DA. A multicompartment vascular model for inferring baseline and functional changes in cerebral oxygen metabolism and arterial dilation. J Cereb Blood Flow Metab 2007, 27:1262-1279. 10.1038/sj.jcbfm.9600435, 2586902, 17200678.
18. Devor A, Dunn AK, Andermann ML, Ulbert I, Boas DA, Dale AM. Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex. Neuron 2003, 39:353-359. 10.1016/S0896-6273(03)00403-3, 12873390.
19. Franceschini MA, Nissila I, Wu WC, Diamond SG, Bonmassar G, Boas DA. Coupling between somatosensory evoked potentials and hemodynamic response in the rat. Neuroimage 2008, 41:189-203. 10.1016/j.neuroimage.2008.02.061, 2486435, 18420425.
20. Huttunen JK, Grohn O, Penttonen M. Coupling between simultaneously recorded BOLD response and neuronal activity in the rat somatosensory cortex. Neuroimage 2008, 39:775-785. 10.1016/j.neuroimage.2007.06.042, 17964186.
21. Fazl M, Houlden DA, Weaver K. Correlation between Cerebral Blood-Flow, Somatosensory Evoked-Potentials, Ct Scan Grade and Neurological Grade in Patients with Subarachnoid Hemorrhage. Can J Neurol Sci 1991, 18:453-457.
22. Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science 1990, 248:73-76. 10.1126/science.2321027, 2321027.
23. Garaschuk O, Milos RI, Konnerth A. Targeted bulk-loading of fluorescent indicators for two-photon brain imaging in vivo. Nat Protoc 2006, 1:380-386. 10.1038/nprot.2006.58, 17406260.
24. Kuhn B, Denk W, Bruno RM. In vivo two-photon voltage-sensitive dye imaging reveals top-down control of cortical layers 1 and 2 during wakefulness. Proc Natl Acad Sci USA 2008, 105:7588-7593. 10.1073/pnas.0802462105, 2396672, 18508976.
25. Shih AY, Driscoll JD, Drew PJ, Nishimura N, Schaffer CB, Kleinfeld D. Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain. J Cereb Blood Flow Metab 2012, 32:1277-1309. 10.1038/jcbfm.2011.196, 22293983.
26. Peng M, Rege A, Nan L, Thakor NV, Shanbao T. High resolution cerebral blood flow imaging by registered laser speckle contrast analysis. IEEE Trans Biomed Eng 2010, 57:1152-1157.
27. Briers JD. Laser speckle contrast imaging for measuring blood flow. Optica Applicata 2007, 37:139-152.
28. Li N, Jia X, Murari K, Parlapalli R, Rege A, Thakor NV. High spatiotemporal resolution imaging of the neurovascular response to electrical stimulation of rat peripheral trigeminal nerve as revealed by in vivo temporal laser speckle contrast. J Neurosci Methods 2009, 176:230-236. 10.1016/j.jneumeth.2008.07.013, 18706442.
29. Miao P, Li N, Thakor NV, Tong S. Random process estimator for laser speckle imaging of cerebral blood flow. Opt Express 2010, 18:218-236. 10.1364/OE.18.000218, 3369537, 20173842.
30. Miao P, Lu H, Liu Q, Li Y, Tong S. Laser speckle contrast imaging of cerebral blood flow in freely moving animals. J Biomed Opt 2011, 16:090502. 10.1117/1.3625231, 21950906.
31. Hecht N, Woitzik J, Dreier JP, Vajkoczy P. Intraoperative monitoring of cerebral blood flow by laser speckle contrast analysis. Neurosurg Focus 2009, 27:E11.
32. Parthasarathy AB, Weber EL, Richards LM, Fox DJ, Dunn AK. Laser speckle contrast imaging of cerebral blood flow in humans during neurosurgery: a pilot clinical study. J Biomed Opt 2010, 15:066030. 10.1117/1.3526368, 21198204.
33. Rege A, Murari K, Seifert A, Pathak AP, Thakor NV. Multiexposure laser speckle contrast imaging of the angiogenic microenvironment. J Biomed Opt 2011, 16.
34. Li N, Downey JE, Bar-Shir A, Gilad AA, Walczak P, Kim H, Joel SE, Pekar JJ, Thakor NV, Pelled G. Optogenetic-guided cortical plasticity after nerve injury. Proc Natl Acad Sci USA 2011, 108:8838-8843. 10.1073/pnas.1100815108, 3102379, 21555573.
35. Zhang HF, Maslov K, Wang LV. In vivo imaging of subcutaneous structures using functional photoacoustic microscopy. Nat Protoc 2007, 2:797-804. 10.1038/nprot.2007.108, 17446879.
36. Wang LV. Multiscale photoacoustic microscopy and computed tomography. Nat Photonics 2009, 3:503-509. 10.1038/nphoton.2009.157, 2802217, 20161535.
37. Liao LD, Lin CT, Shih YYI, Duong TQ, Lai HY, Wang PH, Wu R, Tsang S, Chang JY, Li ML. Transcranial imaging of functional cerebral hemodynamic changes in single blood vessels using in vivo photoacoustic microscopy. J Cereb Blood Flow Metab 2012, 32:938-951. 10.1038/jcbfm.2012.42, 22472612.
38. Liao LD, Lin CT, Shih YYI, Lai HY, Zhao WT, Duong TQ, Chang JY, Chen YY, Li ML. Investigation of the cerebral hemodynamic response function in single blood vessels by functional photoacoustic microscopy. J Biomed Opt 2012, 17:061210-1-061210-10.
39. Thakor NV. Highlights: Transcranial imaging of functional cerebral hemodynamic changes in single blood vessels. J Cereb Blood Flow Metab 2012, 32:936-937. 10.1038/jcbfm.2012.41, 22472610.
40. Liao LD, Li ML, Lai HY, Shih YYI, Lo YC, Tsang S, Chao PCP, Lin CT, Jaw FS, Chen YY. Imaging brain hemodynamic changes during rat forepaw electrical stimulation using functional photoacoustic microscopy. Neuroimage 2010, 52:562-570. 10.1016/j.neuroimage.2010.03.065, 20362680.
41. Wang LHV, Hu S. Photoacoustic tomography: in vivo imaging from organelles to organs. Science 2012, 335:1458-1462. 10.1126/science.1216210, 3322413, 22442475.
42. Yao J, Wang LV. Transverse flow imaging based on photoacoustic Doppler bandwidth broadening. J Biomed Opt 2010, 15:021304-021305. 10.1117/1.3339953, 2857455, 20459226.
43. Mesquita RC, Franceschini MA, Boas DA. Resting state functional connectivity of the whole head with near-infrared spectroscopy. Biomed Opt Express 2010, 1:324-336. 10.1364/BOE.1.000324, 3005169, 21258470.
44. Bunce SC, Izzetoglu M, Izzetoglu K, Onaral B, Pourrezaei K. Functional near-infrared spectroscopy - An emerging neuroimaging modality. IEEE Eng Med Biol Mag 2006, 25:54-62.
45. Izzetoglu M, Izzetoglu K, Bunce S, Ayaz H, Devaraj A, Onaral B, Pourrezaei K. Functional near-infrared neuroimaging. IEEE Trans Neural Syst Rehabil Eng 2005, 13:153-159. 10.1109/TNSRE.2005.847377, 16003893.
46. Hoshi Y. Functional near-infrared spectroscopy: potential and limitations in neuroimaging studies. Int Rev Neurobiol 2005, 66:237.
47. Suzurikawa J, Tani T, Nakao M, Tanaka S, Takahashi H. Voltage-sensitive-dye imaging of microstimulation-evoked neural activity through intracortical horizontal and callosal connections in cat visual cortex. J Neural Eng 2009, 6:066002. 10.1088/1741-2560/6/6/066002, 19794238.
48. Tsytsarev V, Pope D, Pumbo E, Yablonskii A, Hofmann M. Study of the cortical representation of whisker directional deflection using voltage-sensitive dye optical imaging. Neuroimage 2010, 53:233-238. 10.1016/j.neuroimage.2010.06.022, 20558304.
49. Wayland H, Johnson PC. Erythrocyte velocity measurement in microvessels by a two-slit photometric method. J Appl Physiol 1967, 22:333-337.
50. Dirnagl U, Villringer A, Gebhardt R, Haberl RL, Schmiedek P, Einhaupl KM. Three-dimensional reconstruction of the rat brain cortical microcirculation in vivo. J Cereb Blood Flow Metab 1991, 11:353-360. 10.1038/jcbfm.1991.74, 2016343.
51. Villringer A, Them A, Lindauer U, Einhaupl K, Dirnagl U. Capillary perfusion of the rat brain cortex. An in vivo confocal microscopy study. Circ Res 1994, 75:55-62. 10.1161/01.RES.75.1.55, 8013082.
52. Helmchen F, Denk W. Deep tissue two-photon microscopy. Nat Methods 2005, 2:932-940. 10.1038/nmeth818, 16299478.
53. Svoboda K, Yasuda R. Principles of two-photon excitation microscopy and its applications to neuroscience. Neuron 2006, 50:823-839. 10.1016/j.neuron.2006.05.019, 16772166.
54. Cauli B, Tong XK, Rancillac A, Serluca N, Lambolez B, Rossier J, Hamel E. Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J Neurosci 2004, 24:8940-8949. 10.1523/JNEUROSCI.3065-04.2004, 15483113.
55. Filosa JA, Bonev AD, Straub SV, Meredith AL, Wilkerson MK, Aldrich RW, Nelson MT. Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci 2006, 9:1397-1403. 10.1038/nn1779, 17013381.
56. Mulligan SJ, MacVicar BA. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 2004, 431:195-199. 10.1038/nature02827, 15356633.
57. Rancillac A, Rossier J, Guille M, Tong XK, Geoffroy H, Amatore C, Arbault S, Hamel E, Cauli B. Glutamatergic Control of Microvascular Tone by Distinct GABA Neurons in the Cerebellum. J Neurosci 2006, 26:6997-7006. 10.1523/JNEUROSCI.5515-05.2006, 16807329.
58. Simard M, Arcuino G, Takano T, Liu QS, Nedergaard M. Signaling at the gliovascular interface. J Neurosci 2003, 23:9254-9262.
59. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 2003, 6:43-50. 10.1038/nn980, 12469126.
60. Devor A, Tian PF, Nishimura N, Teng IC, Hillman EMC, Narayanan SN, Ulbert I, Boas DA, Kleinfeld D, Dale AM. Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J Neurosci 2007, 27:4452-4459. 10.1523/JNEUROSCI.0134-07.2007, 2680207, 17442830.
61. Faraci FM, Breese KR. Nitric oxide mediates vasodilatation in response to activation of N-methyl-D-aspartate receptors in brain. Circ Res 1993, 72:476-480. 10.1161/01.RES.72.2.476, 8380361.
62. Kleinfeld D, Mitra PP, Helmchen F, Denk W. Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc Natl Acad Sci USA 1998, 95:15741-15746. 10.1073/pnas.95.26.15741, 28114, 9861040.
63. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 2006, 9:260-267. 10.1038/nn1623, 16388306.
64. Zhang SX, Murphy TH. Imaging the impact of cortical microcirculation on synaptic structure and sensory-evoked hemodynamic responses in vivo. PLoS Biol 2007, 5:1152-1167.
65. Chaigneau E, Tiret P, Lecoq J, Ducros M, Knopfel T, Charpak S. The relationship between blood flow and neuronal activity in the rodent olfactory bulb. J Neurosci 2007, 27:6452-6460. 10.1523/JNEUROSCI.3141-06.2007, 17567806.
66. Chuquet J, Hollender L, Nimchinsky EA. High-resolution in vivo imaging of the neurovascular unit during spreading depression. J Neurosci 2007, 27:4036-4044. 10.1523/JNEUROSCI.0721-07.2007, 17428981.
67. Filosa JA, Bonev AD, Nelson MT. Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ Res 2004, 95:E73-E81. 10.1161/01.RES.0000148636.60732.2e, 15499024.
68. Theer P, Hasan MT, Denk W. Two-photon imaging to a depth of 1000 microm in living brains by use of a Ti:Al2O3 regenerative amplifier. Opt Lett 2003, 28:1022-1024. 10.1364/OL.28.001022, 12836766.
69. Helmchen F. Two-Photon Functional Imaging of Neuronal Activity 2009, 37-58. ed: CRC Press.
70. Smith LE, Wesolowski E, McLellan A, Kostyk SK, D'Amato R, Sullivan R, D'Amore PA. Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 1994, 35:101-111.
71. Devor A, Shih A, Tsai P, Blinder P, Tian P, Teng I, Kleinfeld D. Two-Photon Laser Scanning Microscopy as a Tool to Study Cortical Vasodynamics Under Normal and Ischemic Conditions. Imaging the Brain with Optical Methods 2010, 245-261. Springer New York: LA - English, Roe AW.
72. Murari K, Li N, Rege A, Jia X, All A, Thakor N. Contrast-enhanced imaging of cerebral vasculature with laser speckle. Appl Opt 2007, 46:5340-5346. 10.1364/AO.46.005340, 17676149.
73. Murari K, Greenwald E, Etienne-Cummings R, Cauwenberghs G, Thakor N. Design and characterization of a miniaturized epi-illuminated microscope. Conf Proc IEEE Eng Med Biol Soc 2009, 2009:5369-5372.
74. Arulmozhi DK, Veeranjaneyulu A, Bodhankar SL. Migraine: current concepts and emerging therapies. Vascul Pharmacol 2005, 43:176-187. 10.1016/j.vph.2005.07.001, 16099727.
75. Bouchard MB, Chen BR, Burgess SA, Hillman EMC. Ultra-fast multispectral optical imaging of cortical oxygenation, blood flow, and intracellular calcium dynamics. Opt Express 2009, 17:15670-15678. 10.1364/OE.17.015670, 2760073, 19724566.
76. Grinvald A, Hildesheim R. VSDI: a new era in functional imaging of cortical dynamics. Nat Rev Neurosci 2004, 5:874-885. 10.1038/nrn1536, 15496865.
77. Chemla S, Chavane F. Voltage-sensitive dye imaging: Technique review and models. J Physiol Paris 2010, 104:40-50. 10.1016/j.jphysparis.2009.11.009, 19909809.
78. Tsytsarev V, Bernardelli C, Maslov KI. Living brain optical imaging: technology, methods and applications. J Neurosci Neuroeng 2012, 1.
79. Shoham D, Glaser DE, Arieli A, Kenet T, Wijnbergen C, Toledo Y, Hildesheim R, Grinvald A. Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron 1999, 24:791-802. 10.1016/S0896-6273(00)81027-2, 10624943.
80. Tsytsarev V, Fukuyama H, Pope D, Pumbo E, Kimura M. Optical imaging of interaural time difference representation in rat auditory cortex. Front Neuroeng 2009, 2:2. 2654020, 19277218.
81. Devor A, Sakadzic S, Srinivasan VJ, Yaseen MA, Nizar K, Saisan PA, Tian P, Dale AM, Vinogradov SA, Franceschini MA, Boas DA. Frontiers in optical imaging of cerebral blood flow and metabolism. J Cereb Blood Flow Metab 2012, 32:1259-1276. 10.1038/jcbfm.2011.195, 22252238.
82. Barnett L, Platisa J, Popovic M, Pieribone VA, Hughes T. A fluorescent, genetically-encoded voltage probe capable of resolving action potentials. PLoS One 2012, 7:e43454. 10.1371/journal.pone.0043454, 3435330, 22970127.
83. Wang LV. Tutorial on photoacoustic microscopy and computed tomography. IEEE J Sel Top Quantum Electronics 2008, 14:171-179.
84. Maslov K, Stoica G, Wang LV. In vivo dark-field reflection-mode photoacoustic microscopy. Opt Lett 2005, 30:625-627. 10.1364/OL.30.000625, 15791997.
85. Zhang HF, Maslov K, Stoica G, Wang LV. Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging. Nat Biotechnol 2006, 24:848-851. 10.1038/nbt1220, 16823374.
86. Tsytsarev V, Hu S, Yao JJ, Maslov K, Barbour DL, Wang LV. Photoacoustic microscopy of microvascular responses to cortical electrical stimulation. J Biomed Opt 2011, 16.
87. Yao J, Maslov KI, Shi Y, Taber LA, Wang LV. In vivo photoacoustic imaging of transverse blood flow by using Doppler broadening of bandwidth. Opt Lett 2010, 35:1419-1421. 10.1364/OL.35.001419, 2916025, 20436589.
88. Stein EW, Maslov K, Wang LV. Noninvasive, in vivo imaging of blood-oxygenation dynamics within the mouse brain using photoacoustic microscopy. J Biomed Opt 2009, 14:020502. 10.1117/1.3095799, 2676448, 19405708.
89. Ermilov SA, Khamapirad T, Conjusteau A, Leonard MH, Lacewell R, Mehta K, Miller T, Oraevsky AA. Laser optoacoustic imaging system for detection of breast cancer. J Biomed Opt 2009, 14:024007. 10.1117/1.3086616, 19405737.
90. Jokerst JV, Thangaraj M, Kempen PJ, Sinclair R, Gambhir SS. Photoacoustic imaging of mesenchymal stem cells in living mice via silica-coated gold nanorods. ACS Nano 2012, 6:5920-5930. 10.1021/nn302042y, 3582222, 22681633.
91. Laufer J, Johnson P, Zhang E, Treeby B, Cox B, Pedley B, Beard P. In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy. J Biomed Opt 2012, 17:056016. 10.1117/1.JBO.17.5.056016, 22612139.
92. Prost A, Funke A, Tanter M, Aubry JF, Bossy E. Photoacoustic-guided ultrasound therapy with a dual-mode ultrasound array. J Biomed Opt 2012, 17:061205. 10.1117/1.JBO.17.6.061205, 22734735.
93. Petrov IY, Petrov Y, Prough DS, Cicenaite I, Deyo DJ, Esenaliev RO. Optoacoustic monitoring of cerebral venous blood oxygenation though intact scalp in large animals. Opt Express 2012, 20:4159-4167. 10.1364/OE.20.004159, 3482910, 22418173.
94. Nie L, Cai X, Maslov K, Garcia-Uribe A, Anastasio MA, Wang LV. Photoacoustic tomography through a whole adult human skull with a photon recycler. J Biomed Opt 2012, 17:110506-110506. 10.1117/1.JBO.17.11.110506, 23123972.
95. Hajireza P, Shi W, Zemp RJ. Real-time handheld optical-resolution photoacoustic microscopy. Opt Express 2011, 19:20097-20102. 10.1364/OE.19.020097, 21997020.
96. Khan B, Chand P, Alexandrakis G. Spatiotemporal relations of primary sensorimotor and secondary motor activation patterns mapped by NIR imaging. Biomed Opt Express 2011, 2:3367-3386. 10.1364/BOE.2.003367, 3233255, 22162826.
97. Aletti F, Re R, Pace V, Contini D, Molteni E, Cerutti S, Maria Bianchi A, Torricelli A, Spinelli L, Cubeddu R, Baselli G. Deep and surface hemodynamic signal from functional time resolved transcranial near infrared spectroscopy compared to skin flowmotion. Comput Biol Med 2012, 42:282-289. 10.1016/j.compbiomed.2011.06.001, 21742320.
98. Bozkurt A, Rosen A, Rosen H, Onaral B. A portable near infrared spectroscopy system for bedside monitoring of newborn brain. Biomed Eng Online 2005, 4:29. 10.1186/1475-925X-4-29, 1112605, 15862131.
99. Coyle SM, Ward TE, Markham CM. Brain-computer interface using a simplified functional near-infrared spectroscopy system. J Neural Eng 2007, 4:219-226. 10.1088/1741-2560/4/3/007, 17873424.
100. Wang Y, Hu S, Maslov K, Zhang Y, Xia Y, Wang LV. In vivo integrated photoacoustic and confocal microscopy of hemoglobin oxygen saturation and oxygen partial pressure. Opt Lett 2011, 36:1029-1031. 10.1364/OL.36.001029, 3076119, 21478972.
101. Liu T, Wei Q, Wang J, Jiao SL, Zhang HF. Combined photoacoustic microscopy and optical coherence tomography can measure metabolic rate of oxygen. Biomedical Optics Express 2011, 2:1359-1365. 10.1364/BOE.2.001359, 3087592, 21559147.
102. Yakovlev VV, Zhang HF, Noojin GD, Denton ML, Thomas RJ, Scully MO. Stimulated Raman photoacoustic imaging. Proc Natl Acad Sci USA 2010, 107:20335-20339. 10.1073/pnas.1012432107, 2996670, 21059930.
103. Yao J, Xia J, Maslov KI, Nasiriavanaki M, Tsytsarev V, Demchenko AV, Wang LV. Noninvasive photoacoustic computed tomography of mouse brain metabolism in vivo. Neuroimage 2012,
104. Ma H, Zhao M, Schwartz TH. Dynamic Neurovascular Coupling and Uncoupling during Ictal Onset, Propagation, and Termination Revealed by Simultaneous In Vivo Optical Imaging of Neural Activity and Local Blood Volume. Cereb Cortex 2012,
105. Obrenovitch TP, Chen SB, Farkas E. Simultaneous, live imaging of cortical spreading depression and associated cerebral blood flow changes, by combining voltage-sensitive dye and laser speckle contrast methods. Neuroimage 2009, 45:68-74. 10.1016/j.neuroimage.2008.11.025, 19100842.
106. Keller E, Ishihara H, Nadler A, Niederer P, Seifert B, Yonekawa Y, Frei K. Evaluation of brain toxicity following near infrared light exposure after indocyanine green dye injection. J Neurosci Methods 2002, 117:23-31. 10.1016/S0165-0270(02)00044-4, 12084561.
107. Moore GE, Peyton WT, French LA, Walker WW. The Clinical Use of Fluorescein in Neurosurgery - the Localization of Brain Tumors. J Neurosurg 1948, 5:392-398. 10.3171/jns.1948.5.4.0392, 18872412.
108. Kim EH, Cho JM, Chang JH, Kim SH, Lee KS. Application of intraoperative indocyanine green videoangiography to brain tumor surgery. Acta Neurochir 2011, 153:1487-1495. 10.1007/s00701-011-1046-x, 21590519.
109. Tsytsarev V, Maslov KI, Yao J, Parameswar AR, Demchenko AV, Wang LV. In vivo imaging of epileptic activity using 2-NBDG, a fluorescent deoxyglucose analog. J Neurosci Methods 2012, 203:136-140. 10.1016/j.jneumeth.2011.09.005, 3221836, 21939688.
110. Reichold J, Stampanoni M, Lena Keller A, Buck A, Jenny P, Weber B. Vascular graph model to simulate the cerebral blood flow in realistic vascular networks. J Cereb Blood Flow Metab 2009, 29:1429-1443. 10.1038/jcbfm.2009.58, 19436317.
111. Hill DK, Keynes RD. Opacity changes in stimulated nerve. J Physiol 1949, 108:278-281. 1392485, 16991859.
112. Lenkov DN, Volnova AB, Pope A, Tsytsarev V. Advantages and limitations of brain imaging methods in the research of absence epilepsy in humans and animal models. J Neurosci Methods 2012,
113. Ferrari M, Quaresima V. A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application. Neuroimage 2012, 63:921-935. 10.1016/j.neuroimage.2012.03.049, 22510258.
114. Gratton G, Fabiani M. Fast optical imaging of human brain function. Front Hum Neurosci 2010, 4:52. 2903192, 20631845.
115. Haglund MM, Hochman DW. Imaging of intrinsic optical signals in primate cortex during epileptiform activity. Epilepsia 2007, 48 Suppl 4:65-74.
116. Beard P. Biomedical photoacoustic imaging. Interface focus 2011, 1:602-631. 10.1098/rsfs.2011.0028, 3262268, 22866233.
117. Wang L. Photoacoustic Imaging and Spectroscopy vol. 144 2009, CRC Press.
118. Flusberg BA, Nimmerjahn A, Cocker ED, Mukamel EA, Barretto RP, Ko TH, Burns LD, Jung JC, Schnitzer MJ. High-speed, miniaturized fluorescence microscopy in freely moving mice. Nat Methods 2008, 5:935-938. 10.1038/nmeth.1256, 2828344, 18836457.
119. Sanai N, Eschbacher J, Hattendorf G, Coons SW, Preul MC, Smith KA, Nakaji P, Spetzler RF. Intraoperative confocal microscopy for brain tumors: a feasibility analysis in humans. Neurosurgery 2011, 68:282-290. discussion 290.
120. Kozma R, Davis JJJ, Freeman WJ. Synchronized minima in ECoG power at frequencies between beta-gamma oscillations disclose cortical singularities in cognition. J Neurosci Neuroeng 2012, 1.
121. Liao LD, Lin CT. Novel trends in biosensors used for electroencephalography measurements in neurocognitive engineering applications. J Neurosci Neuroeng 2012, 1:32-41.
122. Liao LD, Lin CT, McDowell K, Wickenden AE, Gramann K, Jung TP, Ko LW, Chang JY. Biosensor technologies for augmented brain-computer interfaces in the next decades. Proc IEEE 2012, 100:1553-1566.