Abstract
A theoretical framework is presented for converting Blood Oxygenation Level Dependent (BOLD) images to brain temperature maps, based on the idea that disproportional local changes in cerebral blood flow (CBF) as compared with cerebral metabolic rate of oxygen consumption (CMRO 2) during functional brain activity, lead to both brain temperature changes and the BOLD effect. Using an oxygen limitation model and a BOLD signal model, we obtain a transcendental equation relating CBF and CMRO 2 changes with the corresponding BOLD signal, which is solved in terms of the Lambert W function. Inserting this result in the dynamic bioheat equation describing the rate of temperature changes in the brain, we obtain a nonautonomous ordinary differential equation that depends on the BOLD response, which is solved numerically for each brain voxel. Temperature maps obtained from a real BOLD dataset registered in an attention to visual motion experiment were calculated, obtaining temperature variations in the range: (−0.15, 0.1) which is consistent with experimental results. The statistical analysis revealed that significant temperature activations have a similar distribution pattern than BOLD activations. An interesting difference was the activation of the precuneus in temperature maps, a region involved in visuospatial processing, an effect that was not observed on BOLD maps. Furthermore, temperature maps were more localized to gray matter regions than the original BOLD maps, showing less activated voxels in white matter and cerebrospinal fluid.
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Abeles, M. (1991). Corticonics: neural circuits of the cerebral cortex. Cambridge: Cambridge University Press.
Attwell, D., & Iadecola, C. (2002). The neural basis of functional brain imaging signals. Trends Neurosci., 25, 621–625.
Babajani, A., & Soltanian-Zadeh, H. (2006). Integrated MEG/EEG and fMRI model based on neural masses. IEEE Trans. Biomed. Eng., 53, 1794–1801.
Babajani, A., Soltanian-Zadeh, H., & Moran, J. E. (2008). Integrated MEG/fMRI model validated using real auditory data. Brain Topogr., 21, 61–74.
Bandettini, P. A., Wong, E. C., Hinks, R. S., Tikofsky, R. S., & Hyde, J. S. (1992). Time course EPI of human brain function during task activation. Magn. Reson. Med., 25, 390–397.
Biswal, B., Yetkin, F. Z., Haughton, V. M., & Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med., 34, 537–541.
Blockley, N. P., Francis, S. T., & Gowland, P. A. (2009). Perturbation of the BOLD response by a contrast agent and interpretation through a modified balloon model. NeuroImage, 48, 84–93.
Büchel, C., & Friston, K. (1997). Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. Cereb. Cortex, 7, 768–778.
Buxton, R. B., & Frank, L. R. (1997). A model for the coupling between cerebral blood flow and oxygen metabolism during neural stimulation. J. Cereb. Blood Flow Metab., 17, 64–72.
Buxton, R. B., Wong, E. C., & Frank, L. R. (1998). Dynamics of blood flow and oxygenation changes during brain activation: the Balloon model. Magn. Reson. Med., 39, 855–864.
Buxton, R. B., Uludag, K., Dubowitz, D. J., & Liu, T. T. (2004). Modeling the hemodynamic response to brain activation. NeuroImage, 23, S220–S223.
Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain, 129, 564–583.
Chen, W., Zhu, X. H., Gruetter, R., Seaquist, E. R., Adriany, G., & Ugurbil, K. (2001). Study of tricarboxylic acid cycle flux changes in human visual cortex during hemifield visual stimulation using 1H-[13C] MRS and fMRI. Magn. Reson. Med., 45, 34–55.
Chhina, N., Kuestermann, E., Halliday, J., Simpson, L. J., Macdonald, I. A., Bachelard, H. S., & Morris, P. G. (2001). Measurement of human tricarboxylic acid cycle rates during visual activation by 13C magnetic resonance spectroscopy. J. Neurosci. Res., 66, 737–746.
Collins, C. M., Smith, M. B., & Turner, R. (2004). Model of local temperature changes in brain upon functional activation. J. Appl. Physiol., 97, 2051–2055.
Corless, R. M., Gonnet, G. H., Hare, D. E. G., Jeffrey, D. J., & Knuth, D. E. (1996). On the Lambert W function. Adv. Comput. Math., 5, 329–359.
Davis, T., Kwong, K., Weisskoff, R., & Rosen, B. (1998). Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc. Natl. Acad. Sci. USA, 95, 1834–1839.
Dunn, A. K., Devor, A., Dale, A. M., & Boas, D. A. (2005). Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex. NeuroImage, 27, 279–290.
Fox, P. T., & Raichle, M. E. (1986). Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl. Acad. Sci. USA, 83, 1140–1144.
Fox, P. T., Raichle, M. E., Mintun, M. A., & Dence, C. (1988). Nonoxidative glucose consumption during focal physiologic neural activity. Science, 241, 462–464.
Frahm, J., Bruhn, H., Merboldt, K. D., & Hanicke, W. (1992). Dynamic MR imaging of human brain oxygenation during rest and photic stimulation. J. Magn. Reson. Imaging, 2, 501–505.
Friston, K. J., Mechelli, A., Turner, R., & Price, C. J. (2000). Nonlinear responses in fMRI: the Balloon model, Volterra kernels, and other hemodynamics. NeuroImage, 12, 466–477.
Friston, K. J., Harrison, L., & Penny, W. (2003). Dynamic causal modeling. NeuroImage, 19, 1273–1302.
Gorbach, A. M. (1993). Infrared imaging of brain function. Adv. Exp. Med. Biol., 333, 95–123.
Gorbach, A. M., Heiss, J., Kufta, C., Sato, S., Fedio, P., Kammerer, W. A., Solomon, J., & Oldfield, E. H. (2003). Intraoperative infrared functional imaging of human brain. Ann. Neurol., 54, 297–309.
Gusnard, D. A., & Raichle, M. E. (2001). Searching for a baseline: functional imaging and the resting human brain. Nat. Rev., Neurosci., 2, 685–694.
Hayward, J. N., & Baker, M. A. (1968). Role of cerebral arterial blood in the regulation of brain temperature in the monkey. Am. J. Physiol., 215, 389–402.
Hindman, J. C. (1966). Proton resonance shift of water in the gas and liquid states. J. Chem. Phys., 44, 4582–4592.
Hoge, R. D., Atkinson, J., Gill, B., Crelier, G. R., Marrett, S., & Pike, G. B. (1999). Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. Proc. Natl. Acad. Sci. USA, 96, 9403–9408.
Hyder, F., Shulman, R. G., & Rothman, D. L. (1998). A model for the regulation of cerebral oxygen delivery. J. Appl. Physiol., 85, 554–564.
Kwong, K. K., Belliveau, J. W., Chesler, D. A., Goldberg, I. E., Weisskoff, R. M., Poncelet, B. P., Kennedy, D. N., Hoppel, B. E., Cohen, M. S., & Turner, R. (1992). Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc. Natl. Acad. Sci. USA, 89, 5675–5679.
Krüger, G., & Glover, G. H. (2001). Physiological noise in oxygenation-sensitive magnetic resonance imaging. Magn. Reson. Med., 46, 631–637.
Kuroda, K., Suzuki, Y., Ishihara, Y., & Okamoto, K. (1996). Temperature mapping using water proton chemical shift obtained with 3D-MRSI: feasibility in vivo. Magn. Reson. Med., 35, 20–29.
LaManna, J. C., McCracken, K. A., Patil, M., & Prohaska, O. J. (1989). Stimulus-activated changes in brain tissue temperature in the anesthetized rat. Metab. Brain Dis., 4, 225–237.
Le Bihan, D. (Ed.) (1995). Diffusion and perfusion magnetic resonance imaging. New York: Raven Press Ltd.
Leithner, C., Roy, G., Offenhauser, N., Füchtemeier, M., Kohl-Bareis, M., Villringer, A., & Lindauer, U. (2010). Pharmacological uncoupling of activation induced increases in CBF and CMRO2. J. Cereb. Blood Flow Metab., 30, 311–322.
Lin, A. L., Fox, P. T., Hardies, J., Duong, T. Q., & Gao, J. H. (2010). Nonlinear coupling between cerebral blood flow, oxygen consumption, and ATP production in human visual cortex. Proc. Natl. Acad. Sci. USA, 107, 8446–8451.
Madsen, P. L., Hasselbalch, S. G., Hagemann, L. P., Olsen, K. S., Bulow, J., Holm, S., Wildschiodtz, G., Paulson, O. B., & Lassen, N. A. (1995). Persistent resetting of the cerebral oxygen/glucose uptake ratio by brain activation: evidence obtained with the Kety–Schmidt technique. J. Cereb. Blood Flow Metab., 15, 485–91.
Marrett, S., Fujita, H., Meyer, E., Ribeiro, L., Evans, A., Kuwabara, H., & Gjedde, A. (1993). Stimulus specific increase of oxidative metabolism in human visual cortex (pp. 217–224). Amsterdam: Elsevier.
McElligott, J. G., & Melzack, R. (1967). Localized thermal changes evoked in the brain by visual and auditory stimulation. Exp. Neurol., 17, 293–312.
Melzack, R., & Casey, K. L. (1967). Localized temperature changes evoked in the brain by somatic stimulation. Exp. Neurol., 17, 276–292.
Newberg, A. B., Wang, J., Rao, H., Swanson, R. L., Wintering, N., Karp, J. S., Alavi, A., Greenberg, J. H., & Detre, J. A. (2005). Concurrent CBF and CMRGlc changes during human brain activation by combined fMRI–PET scanning. NeuroImage, 28, 500–506.
Ogawa, S., Tank, D. W., Menon, R., Ellermann, J. M., Kim, S., Merkle, H., & Ugurbil, K. (1992). Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc. Natl. Acad. Sci. USA, 89, 5951–5955.
Parker, D. L., Smith, V., Sheldon, P., Crooks, L., & Fussel, L. (1983). Temperature distribution measurements in two-dimensional NMR imaging. Med. Phys., 10, 321–325.
Pennes, H. H. (1948). Analysis of tissue and arterial blood temperature in the resting human forearm. J. Appl. Physiol., 1, 93–122.
Reis, D. J., & Golanov, E. V. (1997). Autonomic and vasomotor regulation. Int. Rev. Neurobiol., 41, 121–149.
Ribeiro, L., Kuwabara, H., Meyer, E., Fujita, H., Marrett, S., Evans, A., & Gjedde, A. (1993). In K. Uemura, N. Lassen, T. Jones, & I. Kanno (Eds.), Quantification of brain function (pp. 229–236). Amsterdam: Elsevier.
Riera, J., Wan, X., Jimenez, J. C., & Kawashima, R. (2006). Nonlinear local electro-vascular coupling. Part I: a theoretical model. Hum. Brain Mapp., 27, 896–914.
Riera, J., Jimenez, J. C., Wan, X., Kawashima, R., & Ozaki, T. (2007). Nonlinear local electro-vascular coupling. Part II: from data to neuronal masses. Hum. Brain Mapp., 28, 335–354.
Seitz, R. J., & Roland, P. E. (1992). Vibratory stimulation increases and decreases the regional cerebral blood flow and oxidative metabolism: a positron emission tomography (PET) study. Acta Neural. Scand., 86, 60–67.
Serota, H. M., & Gerard, R. W. (1938). Localized thermal changes in the cats brain. J. Neurophysiol., 1, 115–24.
Shevelev, I. A. (1998). Functional imaging of the brain by infrared radiation (thermoencephaloscopy). Prog. Neurobiol., 56, 269–305.
Shevelev, I. A., Tsicalov, E. N., Gorbach, A. M., Budko, K. P., & Sharaev, G. A. (1993). Thermoimaging of the brain. J. Neurosci. Methods, 46, 49–57.
Shevelev, I. A., & Tsicalov, E. N. (1997). Fast thermal waves spreading over the cerebral cortex. Neuroscience, 76, 531–540.
Shitzer, A., Stroschein, L. A., Gonzalez, R. R., & Pandol, K. B. (1996). Lumped-parameter tissue temperature-blood perfusion model of a cold-stressed fingertip. J. Appl. Physiol., 80, 1829–1834.
Shmuel, A., Yacoub, E., Pfeuffer, J., Van de Moortele, P., Adriany, G., Hu, X., & Ugurbil, K. (2002). Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron, 36, 1195–1210.
Sotero, R. C., & Trujillo-Barreto, N. J. (2007). Modelling the role of excitatory and inhibitory neuronal activity in the generation of the BOLD signal. NeuroImage, 35, 149–165.
Sukstanskii, A., & Yablonskiy, D. A. (2006). Theoretical model of temperature regulation in the brain during changes in functional activity. PNAS, 103, 12144–12149.
Takuya, H., Watabe, H., Kudomi, N., Kim, K. M., Enmi, J. I., Hayashida, K., & Iida, H. (2003). A theoretical model of oxygen delivery and metabolism for physiological interpretation of quantitative cerebral blood flow and metabolic rate of oxygen. J. Cereb. Blood Flow Metab., 23, 1314–1323.
Trübel, H. K. F., Sacolick, L. I., & Hyder, F. (2006). Regional temperature changes in the brain during somatosensory stimulation. J. Cereb. Blood Flow Metab., 26, 68–78.
Vafaee, M. S., & Gjedde, A. (2000). Model of blood-brain transfer of oxygen explains nonlinear flow- metabolism coupling during stimulation of visual cortex. J. Cereb. Blood Flow Metab., 20, 747–754.
Weber, B., Keller, A. L., Reichold, J., & Logothetis, N. (2008). The microvascular system of the striate and extrastriate visual cortex of the macaque. Cereb. Cortex, 18, 2318–2330.
Yablonskiy, D. A., Ackerman, J. J. H., & Raichle, M. E. (2000). Coupling between changes in human brain temperature and oxidative metabolism during prolonged visual stimulation. PNAS, 97, 7603–7608.
Zheng, Y., Martindale, J., Johnston, D., Jones, M., Berwick, J., & Mayhew, J. (2002). A model of the hemodynamic response and oxygen delivery to brain. NeuroImage, 16, 617–637.
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Sotero, R.C., Iturria-Medina, Y. From Blood Oxygenation Level Dependent (BOLD) Signals to Brain Temperature Maps. Bull Math Biol 73, 2731–2747 (2011). https://doi.org/10.1007/s11538-011-9645-5
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DOI: https://doi.org/10.1007/s11538-011-9645-5