In vivo Near Infrared Spectroscopy: a novel approach for simultaneously estimating molecules and hemodynamic parameters in the human and rat brain: a review

Main Article Content

José Luis González-Mora Estefanía Hernández-Martín Francisco Marcano Pedro Salazar Sergio Elías Hernández Vicente D. Rodríguez

Abstract

There have been great advances in optical brain imaging over the last 50 years and the technique has grown into a richly diverse field. In vivo recording and imaging using light provides extraordinary sensitivity to functional changes through intrinsic contrast, blood, and can even exploit the growing availability of exogenous optical contrast agents. Light can be used to analyze microscopic structures and function in vivo in the exposed animal brain, while also allowing noninvasive imaging of hemodynamics and metabolism in a clinical setting. This review is an overview of approaches that have been applied in vivo optical brain recording, in both animals and humans. The basic principles of each technique are described, emphasizing the techniques used in our laboratory.


Techniques include imaging of exposed cortex, in vivo functional spectroscopy of the living brain using optic fibers, and the broad range of noninvasive topography and tomography approaches to near-infrared imaging of the human brain. The basic principles of each technique are described, followed by examples of current applications to cutting-edge neuroscience research. In summary, it is shown that optical brain recording continues to grow and evolve, embracing new technologies and advancing to address ever more complex and important neuroscientific questions.

Article Details

How to Cite
GONZÁLEZ-MORA, José Luis et al. In vivo Near Infrared Spectroscopy: a novel approach for simultaneously estimating molecules and hemodynamic parameters in the human and rat brain: a review. Medical Research Archives, [S.l.], v. 6, n. 2, feb. 2018. ISSN 2375-1924. Available at: <https://journals.ke-i.org/index.php/mra/article/view/1696>. Date accessed: 18 june 2018. doi: https://doi.org/10.18103/mra.v6i2.1696.
Section
Review Articles

References

1. Jöbsis FF. Spectrophotometric Studies on Intact Muscle : II. Recovery from contractile activity. J Gen Physiol [Internet]. 1963 May;46(5):929–69. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2195306/
2. Jobsis FF. Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science (80- ). 1977;198(4323):1264–7.
3. Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, Nguyen PT, et al. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci. 2005;25(31):7278–87.
4. Ayata C, Dunn AK, Gursoy-Özdemir Y, Huang Z, Boas DA, Moskowitz MA. Laser speckle flowmetry for the study of cerebrovascular physiology in normal and ischemic mouse cortex. J Cereb Blood Flow Metab. 2004;24(7):744–55.
5. Bahar S, Suh M, Zhao M, Schwartz TH. Intrinsic optical signal imaging of neocortical seizures: the “epileptic dip.” Neuroreport. 2006;17(5):499–503.
6. Roche R, Salazar P, Martín M, Marcano F, González-Mora JL. Simultaneous measurements of glucose, oxyhemoglobin and deoxyhemoglobin in exposed rat cortex. J Neurosci Methods. 2011;202(2):192–8.
7. Pouratian N, Cannestra AF, Martin NA, Toga AW. Intraoperative optical intrinsic signal imaging: a clinical tool for functional brain mapping. Neurosurg Focus. 2002;13(4):1–9.
8. Cannestra AF, Pouratian N, Bookheimer SY, Martin NA, Becker DP, Toga AW. Temporal spatial differences observed by functional MRI and human intraoperative optical imaging. Cereb Cortex. 2001;11(8):773–82.
9. Kleinfeld D, Delaney KR. Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltage‐sensitive dyes. J Comp Neurol. 1996;375(1):89–108.
10. Maheswari RU, Takaoka H, Kadono H, Homma R, Tanifuji M. Novel functional imaging technique from brain surface with optical coherence tomography enabling visualization of depth resolved functional structure in vivo. J Neurosci Methods. 2003;124(1):83–92.
11. Hillman EMC, Boas DA, Dale AM, Dunn AK. Laminar optical tomography: demonstration of millimeter-scale depth-resolved imaging in turbid media. Opt Lett. 2004;29(14):1650–2.
12. Bacskai BJ Hickey GA, Allen R, Hyman BT SJ. Fluorescence resonance energy transfer determinations using multiphoton fluorescence lifetime imaging microscopy to characterize amyloid-beta plaques. J Biomed Opt. 2003;8:368–75.
13. 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(7026):597–603.
14. Chaigneau E, Oheim M, Audinat E, Charpak S. Two-photon imaging of capillary blood flow in olfactory bulb glomeruli. Proc Natl Acad Sci. 2003;100(22):13081–6.
15. Hernández SE, Rodríguez VD, Pérez J, Martín FA, Castellano MA, Gonzalez-Mora JL. Diffuse reflectance spectroscopy characterization of hemoglobin and intralipid solutions: in vitro measurements with continuous variation of absorption and scattering. J Biomed Opt. 2009;14(3):34026.
16. González-Mora JL, Martı́n FA, Rojas-Dı́az D, Hernández S, Ramos-Pérez I, Rodrı́guez VD, et al. In vivo spectroscopy: a novel approach for simultaneously estimating nitric oxide and hemodynamic parameters in the rat brain. J Neurosci Methods. 2002;119(2):151–61.
17. Martín FA, Rojas-Díaz D, Morales CA, Camacho J, González–Mora JL, Castellano MA. Simultaneous In Vivo Measurements of Methemoglobin and Other Endogenous Chromophores by Visible Spectroscopy.
18. Del Arco A, González-Mora JL, Armas VR, Mora F. Amphetamine increases the extracellular concentration of glutamate in striatum of the awake rat: involvement of high affinity transporter mechanisms. Neuropharmacology. 1999;38(7):943–54.
19. Kharitonov VG Sharma VS BJ. Interactions of nitric oxide with heme proteins using UV_/VIS spectroscopy. In: Methods in nitric oxide research. 1996. p. 39–45.
20. Felipe A. Martin Simeona J. Alonso, Eduardo Navarro, Miguel A JLG-M. Fiber optic spectroscopy to study neurovascular coupling in small areas of the rat brain. In: Progress in Optical Fibers Research. 2007. p. 369–89.
21. Feelisch M Werringloer J KD. The oxyhemoglobin assay. In: Methods in nitric oxide research. 1996. p. 455–78.
22. Martín FA, Rojas-Díaz D, Luis-García ML, González-Mora JL, Castellano MA. Simultaneous monitoring of nitric oxide, oxyhemoglobin and deoxyhemoglobin from small areas of the rat brain by in vivo visible spectroscopy and a least-square approach. J Neurosci Methods. 2004;140(1):75–80.
23. Espinosa N, Cudeiro J, Mariño J. Spectroscopic measurement of cortical nitric oxide release induced by ascending activation. Neuroscience. 2015;285:303–11.
24. de Labra C. Different sources of nitric oxide mediate neurovascular coupling in the lateral geniculate nucleus of the cat. Front Syst Neurosci [Internet]. 2009;3(September):2–3. Available from: http://journal.frontiersin.org/article/10.3389/neuro.06.009.2009/abstract
25. Hyde DC, Boas DA, Blair C, Carey S. Near-infrared spectroscopy shows right parietal specialization for number in pre-verbal infants. Neuroimage [Internet]. 2010;53(2):647–52. Available from: http://www.sciencedirect.com/science/article/pii/S1053811910008748
26. Okada F, Tokumitsu Y, Hoshi Y, Tamura M. Impaired interhemispheric integration in brain oxygenation and hemodynamics in schizophrenia. Eur Arch Psychiatry Clin Neurosci [Internet]. 1994;244(1):17–25. Available from: http://dx.doi.org/10.1007/BF02279807
27. 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(2):921–35.
28. Afergan DA. Implicit Brain-Computer Interfaces for Adaptive Systems: Improving Performance through Physiological Sensing. Tufts University; 2015.
29. Kirilina E, Jelzow A, Heine A, Niessing M, Wabnitz H, Brühl R, et al. The physiological origin of task-evoked systemic artefacts in functional near infrared spectroscopy. Neuroimage. 2012;61(1):70–81.
30. Saager R, Berger A. Measurement of layer-like hemodynamic trends in scalp and cortex: implications for physiological baseline suppression in functional near-infrared spectroscopy. J Biomed Opt. 2008;13(3):10.
31. Turkeltaub PE, Coslett HB. Localization of sublexical speech perception components. Brain Lang. 2010;114(1):1–15.
32. Yang J, Andric M, Mathew MM. The neural basis of hand gesture comprehension: a meta-analysis of functional magnetic resonance imaging studies. Neurosci Biobehav Rev. 2015;57:88–104.
33. Samara Z, Evers EAT, Goulas A, Uylings HBM, Rajkowska G, Ramaekers JG, et al. Human orbital and anterior medial prefrontal cortex: Intrinsic connectivity parcellation and functional organization. Brain Struct Funct. 2017;1–20.
34. Toronov V, Webb A, Choi JH, Wolf M, Safonova L, Wolf U, et al. Study of local cerebral hemodynamics by frequency-domain near-infrared spectroscopy and correlation with simultaneously acquired functional magnetic resonance imaging. Opt Express. 2001;9(8):417–27.
35. Toronov VY, Zhang X, Webb AG. A spatial and temporal comparison of hemodynamic signals measured using optical and functional magnetic resonance imaging during activation in the human primary visual cortex. Neuroimage [Internet]. 2007;34(3):1136–48. Available from: http://www.sciencedirect.com/science/article/pii/S105381190600841X
36. Eggebrecht AT, White BR, Ferradal SL, Chen C, Zhan Y, Snyder AZ, et al. A quantitative spatial comparison of high-density diffuse optical tomography and fMRI cortical mapping. Neuroimage. 2012;61(4):1120–8.
37. Bailey DL, Townsend DW, Valk PE, Maisey MN. Positron emission tomography. Springer; 2005.
38. Kalender WA. X-ray computed tomography. Phys Med Biol. 2006;51(13):R29–R29.
39. Schmitz CH, Löcker M, Lasker JM, Hielscher AH, Barbour RL. Instrumentation for fast functional optical tomography. Rev Sci Instrum. 2002;73(2):429–39.
40. Joseph DK, Huppert TJ, Franceschini MA, Boas DA. Diffuse optical tomography system to image brain activation with improved spatial resolution and validation with functional magnetic resonance imaging. Appl Opt. 2006;45(31):8142–51.
41. Steinbrink J, Wabnitz H, Obrig H, Villringer A, Rinneberg H. Determining changes in NIR absorption using a layered model of the human head. Phys Med Biol. 2001;46(3):879.
42. Liebert A, Wabnitz H, Steinbrink J, Obrig H, Möller M, Macdonald R, et al. Time-resolved multidistance near-infrared spectroscopy of the adult head: intracerebral and extracerebral absorption changes from moments of distribution of times of flight of photons. Appl Opt. 2004;43(15):3037–47.
43. Hielscher AH, Bluestone AY, Abdoulaev GS, Klose AD, Lasker J, Stewart M, et al. Near-infrared diffuse optical tomography. Dis Markers. 2002;18(5–6):313–37.
44. Hueber DM, Franceschini MA, Ma HY, Zhang Q, Ballesteros JR, Fantini S, et al. Non-invasive and quantitative near-infrared haemoglobin spectrometry in the piglet brain during hypoxic stress, using a frequency-domain multidistance instrument. Phys Med Biol. 2001;46(1):41.
45. Culver JP, Choe R, Holboke MJ, Zubkov L, Durduran T, Slemp A, et al. Three‐dimensional diffuse optical tomography in the parallel plane transmission geometry: Evaluation of a hybrid frequency domain/continuous wave clinical system for breast imaging. Med Phys. 2003;30(2):235–47.
46. Singer JR, Grunbaum FA, Kohn P, Zubelli JP. Image reconstruction of the interior of bodies that diffuse radiation. Science (80- ). 1990;248(4958):990–3.
47. Arridge SR, Schweiger M, Delpy DT. Iterative reconstruction of near infrared absorption images. In: Proc SPIE. 1992. p. 372–83.
48. Bluestone AY, Abdoulaev G, Schmitz CH, Barbour RL, Hielscher AH. Three-dimensional optical tomography of hemodynamics in the human head. Opt Express. 2001;9(6):272–86.
49. Barbour RL, Graber HL, Pei Y, Zhong S, Schmitz CH. Optical tomographic imaging of dynamic features of dense-scattering media. JOSA A. 2001;18(12):3018–36.
50. Tanosaki M, Hoshi Y, Iguchi Y, Oikawa Y, Oda I, Oda M. Variation of temporal characteristics in human cerebral hemodynamic responses to electric median nerve stimulation: a near-infrared spectroscopic study. Neurosci Lett. 2001;316(2):75–8.
51. O’Leary MA, Boas DA, Chance B, Yodh AG. Experimental images of heterogeneous turbid media by frequency-domain diffusing-photon tomography. Opt Lett. 1995;20(5):426–8.
52. Boas DA, Culver JP, Stott JJ, Dunn AK. Three dimensional Monte Carlo code for photon migration through complex heterogeneous media including the adult human head. Opt Express [Internet]. 2002 Feb;10(3):159–70. Available from: http://www.opticsexpress.org/abstract.cfm?URI=oe-10-3-159
53. Eggebrecht AT, Ferradal SL, Robichaux-Viehoever A, Hassanpour MS, Dehghani H, Snyder AZ, et al. Mapping distributed brain function and networks with diffuse optical tomography. Nat Photonics. 2014;8(6):448–54.
54. Arridge SR, Schweiger M. Photon-measurement density functions. Part 2: Finite-element-method calculations. Appl Opt. 1995;34(34):8026–37.
55. Hielscher AH, Klose AD, Hanson KM. Gradient-based iterative image reconstruction scheme for time-resolved optical tomography. IEEE Trans Med Imaging. 1999;18(3):262–71.
56. Habermehl C, Steinbrink J, Müller K-R, Haufe S. Optimizing the regularization for image reconstruction of cerebral diffuse optical tomography. J Biomed Opt. 2014;19(9):96006.
57. Yamashita O, Shimokawa T, Aisu R, Amita T, Inoue Y, Sato M. Multi-subject and multi-task experimental validation of the hierarchical Bayesian diffuse optical tomography algorithm. Neuroimage. 2016;135:287–99.
58. Hernandez-Martin E, Marcano F, Casanova O, Modrono C, Plata-Bello J, Gonzalez-Mora JL. Comparing diffuse optical tomography and functional magnetic resonance imaging signals during a cognitive task: pilot study. Neurophotonics. 2017 Jan;4(1):15003.
59. Custo A, Boas DA, Tsuzuki D, Dan I, Mesquita R, Fischl B, et al. Anatomical atlas-guided diffuse optical tomography of brain activation. Neuroimage. 2010;49(1):561–7.
60. Habermehl C, Holtze S, Steinbrink J, Koch SP, Obrig H, Mehnert J, et al. Somatosensory activation of two fingers can be discriminated with ultrahigh-density diffuse optical tomography. Neuroimage. 2012;59(4):3201–11.
61. Yuan Z, Zhang Q, Sobel ES, Jiang H. Tomographic x-ray–guided three-dimensional diffuse optical tomography of osteoarthritis in the finger joints. J Biomed Opt. 2008;13(4):44006.
62. Kavuri VC, Liu H. Hierarchical clustering method to improve transrectal ultrasound-guided diffuse optical tomography for prostate cancer imaging. Acad Radiol. 2014;21(2):250–62.
63. Siegel AM, Culver JP, Mandeville JB, Boas DA. Temporal comparison of functional brain imaging with diffuse optical tomography and fMRI during rat forepaw stimulation. Phys Med Biol. 2003;48(10):1391.
64. Franceschini MA, Joseph DK, Huppert TJ, Diamond SG, Boas DA. Diffuse optical imaging of the whole head. J Biomed Opt. 2006;11(5):54007.
65. Boecker M, Buecheler MM, Schroeter ML, Gauggel S. Prefrontal brain activation during stop-signal response inhibition: an event-related functional near-infrared spectroscopy study. Behav Brain Res. 2007;176(2):259–66.
66. Power SD, Kushki A, Chau T. Towards a system-paced near-infrared spectroscopy brain–computer interface: differentiating prefrontal activity due to mental arithmetic and mental singing from the no-control state. J Neural Eng. 2011;8(6):66004.
67. Huppert TJ, Hoge RD, Diamond SG, Franceschini MA, Boas DA. A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans. Neuroimage [Internet]. 2006 Jan;29(2):368–82. Available from: http://www.sciencedirect.com/science/article/pii/S1053811905005823
68. Becerra L, Harris W, Joseph D, Huppert T, Boas DA, Borsook D. Diffuse optical tomography of pain and tactile stimulation: Activation in cortical sensory and emotional systems. Neuroimage [Internet]. 2008 Jun;41(2):252–9. Available from: http://www.sciencedirect.com/science/article/pii/S1053811908001006
69. Strangman G, Culver JP, Thompson JH, Boas DA. A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage. 2002;17(2):719–31.
70. Gagnon L, Yücel MA, Boas DA, Cooper RJ. Further improvement in reducing superficial contamination in NIRS using double short separation measurements. Neuroimage [Internet]. 2014 Jan;85:127–35. Available from: http://www.sciencedirect.com/science/article/pii/S1053811913001201
71. Hisakata R, Nishida S, Johnston A. An Adaptable Metric Shapes Perceptual Space. Curr Biol [Internet]. 2016 Jul;26(14):1911–5. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4963211/
72. Plichta MM, Heinzel S, Ehlis A-C, Pauli P, Fallgatter AJ. Model-based analysis of rapid event-related functional near-infrared spectroscopy (NIRS) data: a parametric validation study. Neuroimage. 2007;35(2):625–34.
73. Plata-Bello J, Modroño C, Hernández-Martín E, Pérez-Martín Y, Fariña H, Castañón-Pérez A, et al. The mirror neuron system also rests. Brain Struct Funct. 2017;222(5):2193–202.
74. Sasai S, Homae F, Watanabe H, Taga G. Frequency-specific functional connectivity in the brain during resting state revealed by NIRS. Neuroimage. 2011;56(1):252–7.
75. Grant PE, Roche-Labarbe N, Surova A, Themelis G, Selb J, Warren EK, et al. Increased cerebral blood volume and oxygen consumption in neonatal brain injury. J Cereb Blood Flow Metab. 2009;29(10):1704–13.
76. Hebden JC, Gibson A, Yusof RM, Everdell N, Hillman EMC, Delpy DT, et al. Three-dimensional optical tomography of the premature infant brain. Phys Med Biol. 2002;47(23):4155.
77. Maidan I, Bernad-Elazari H, Gazit E, Giladi N, Hausdorff JM, Mirelman A. Changes in oxygenated hemoglobin link freezing of gait to frontal activation in patients with Parkinson disease: an fNIRS study of transient motor-cognitive failures. J Neurol. 2015;262(4):899–908.
78. Hock C, Villringer K, Müller-Spahn F, Wenzel R, Heekeren H, Schuh-Hofer S, et al. Decrease in parietal cerebral hemoglobin oxygenation during performance of a verbal fluency task in patients with Alzheimer’s disease monitored by means of near-infrared spectroscopy (NIRS) - Correlation with simultaneous rCBF-PET measurements. Brain Res [Internet]. 1997 May;755(2):293–303. Available from: http://www.sciencedirect.com/science/article/pii/S0006899397001224
79. Sokol DK, Markand ON, Daly EC, Luerssen TG, Malkoff MD. Near infrared spectroscopy (NIRS) distinguishes seizure types. Seizure. 2000;9(5):323–7.
80. Shidoh S, Akiyama T, Horiguchi T, Ohira T, Yoshida K. The process of change in hemodynamics after revascularization in the ischemic brain. Neuroreport. 2015;26(11):629–33.
81. Herrmann MJ, Walter A, Ehlis A-C, Fallgatter AJ. Cerebral oxygenation changes in the prefrontal cortex: effects of age and gender. Neurobiol Aging. 2006;27(6):888–94.
82. Koike S, Nishimura Y, Takizawa R, Yahata N, Kasai K. Near-infrared spectroscopy in schizophrenia: a possible biomarker for predicting clinical outcome and treatment response. Front psychiatry. 2013;4.
83. Tuscan L-A, Herbert JD, Forman EM, Juarascio AS, Izzetoglu M, Schultheis M. Exploring frontal asymmetry using functional near-infrared spectroscopy: a preliminary study of the effects of social anxiety during interaction and performance tasks. Brain Imaging Behav. 2013;7(2):140–53.
84. Zhang Q, Brukilacchio TJ, Li A, Stott JJ, Chaves T, Hillman E, et al. Coregistered tomographic x-ray and optical breast imaging: initial results. J Biomed Opt. 2005;10(2):24033–240339.
85. Taroni P, Torricelli A, Spinelli L, Pifferi A, Arpaia F, Danesini G, et al. Time-resolved optical mammography between 637 and 985 nm: clinical study on the detection and identification of breast lesions. Phys Med Biol. 2005;50(11):2469.
86. Arenth PM, Ricker JH, Schultheis MT. Applications of functional near-infrared spectroscopy (fNIRS) to neurorehabilitation of cognitive disabilities. Clin Neuropsychol. 2007;21(1):38–57.
87. Suzuki M, Miyai I, Ono T, Oda I, Konishi I, Kochiyama T, et al. Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: An optical imaging study. Neuroimage [Internet]. 2004 Nov;23(3):1020–6. Available from: http://www.sciencedirect.com/science/article/pii/S1053811904003672?via%3Dihub
88. Pedersen PM, Stig Jørgensen H, Nakayama H, Raaschou HO, Olsen TS. Aphasia in acute stroke: incidence, determinants, and recovery. Ann Neurol. 1995;38(4):659–66.
89. Bonato C, Miniussi C, Rossini PM. Transcranial magnetic stimulation and cortical evoked potentials: a TMS/EEG co-registration study. Clin Neurophysiol. 2006;117(8):1699–707.
90. Bohning DE, Shastri A, Nahas Z, Lorberbaum JP, Andersen SW, Dannels WR, et al. Echoplanar BOLD fMRI of brain activation induced by concurrent transcranial magnetic stimulation. Invest Radiol. 1998;33(6):336–40.

Most read articles by the same author(s)

Obs.: This plugin requires at least one statistics/report plugin to be enabled. If your statistics plugins provide more than one metric then please also select a main metric on the admin's site settings page and/or on the journal manager's settings pages.