Abstract

We performed the simultaneous measurement of intrinsic optical signals (IOSs) related to metabolic activity and cellular and subcellular morphological characteristics, i.e., light scattering for a rat global ischemic brain model made by rapidly removing blood by saline infusion. The signals were measured on the basis of multiwavelength diffuse reflectances in which 605 and 830nm were used to detect the IOSs that are thought to be dominantly affected by redox changes of heme aa3 and CuA in cytochrome c oxidase (CcO), respectively. For measuring the scattering signal, the wavelength that was found to be most insensitive to the absorption changes, e.g., 620nm, was used. The measurements suggested that an increase in the absorption due to reduction of heme aa3 occurred soon after blood clearance, and this was followed by a large triphasic change in light scattering, during which time a decrease in the absorption due to reduction of CuA occurred. Through the triphasic scattering change, scattering signals increased by 5.2±1.5% (n=5), and the increase in light scattering showed significant correlation with both the reflectance intensity changes at 605 and 830nm. This suggests that morphological changes in cells correlate with reductions of heme aa3 and CuA. Histological analysis of tissue after the triphasic scattering change showed no alteration in either the nuclei or the cytoskeleton, but electron microscopic observation revealed deformed, enlarged mitochondria and expanded dendrites. These findings suggest that the simultaneous measurement of absorption signals related to the redox changes in the CcO and the scattering signal is useful for monitoring tissue viability in the brain.

© 2008 Optical Society of America

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2008 (1)

T. H. Murphy, P. Li, K. Betts, and R. Liu, “Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines,” J. Neurosci. 28, 1756-1772 (2008).
[CrossRef]

2007 (5)

S. Kawauchi, S. Sato, H. Ooigawa, H. Nawashiro, and M. Kikuchi, “Changes in intrinsic optical signals during loss of tissue viability of brains in rats: effect of brain temperature,” Proc. SPIE 6434, 64341O-1-64341O-4 (2007).

I. Belevich, D. A. Bloch, N. Belevich, M. Wikstrom, and M. I. Verkhovsky, “Exploring the proton pump mechanism of cytochrome c oxidase in real time,” Proc. Natl. Acad. Sci. USA 104, 2685-2690 (2007).
[CrossRef]

T. Takano, G. F. Tian, W. Peng, N. Lou, D. Lovatt, A. J. Hansen, K. A. Kasischke, and M. Nedergaard, “Cortical spreading depression causes and coincides with tissue hypoxia,” Nat. Neurosci. 10, 754-762 (2007).
[CrossRef]

M. M. Tisdall, I. Tachtsidis, T. S. Leung, C. E. Elwell, and M. Smith, “Near-infrared spectroscopic quantification of changes in the concentration of oxidized cytochrome c oxidase in the healthy human brain during hypoxemia,” J. Biomed. Opt. 12, 024002 (2007).
[CrossRef]

I. Tachtsidis, M. Tisdall, T. S. Leung, C. E. Cooper, D. T. Delpy, M. Smith, and C. E. Elwell, “Investigation of in vivo measurement of cerebral cytochrome-c-oxidase redox changes using near-infrared spectroscopy in patients with orthostatic hypotension,” Physiol. Meas. 28, 199-211 (2007).
[CrossRef]

2006 (2)

M. Bartek, X. Wang, W. Wells, K. D. Paulsen, and B. W. Pogue, “Estimation of subcellular particle size histograms with electron microscopy for prediction of optical scattering in breast tissue,” J. Biomed. Opt. 11, 064007 (2006).
[CrossRef]

I. Belevich, M. I. Verkhovsky, and M. Wikstrom, “Proton-coupled electron transfer drives the proton pump of cytochrome c oxidase,” Nature 440, 829-832 (2006).
[CrossRef]

2005 (2)

X. Wang, B. W. Pogue, S. Jiang, X. Song, K. D. Paulsen, C. Kogel, S. P. Poplack, and W. A. Wells, “Approximation of Mie scattering parameters in near-infrared tomography of normal breast tissue in vivo,” J. Biomed. Opt. 10, 051704(2005).
[CrossRef]

N. J. Allen, R. Karadottir, and D. Attwell, “A preferential role for glycolysis in preventing the anoxic depolarization of rat hippocampal area CA1 pyramidal cells,” J. Neurosci. 25, 848-859 (2005).
[CrossRef]

2004 (1)

F. Fujii, Y. Nodasaka, G. Nishimura, and M. Tamura, “Anoxia induces matrix shrinkage accompanied by an increase in light scattering in isolated brain mitochondria,” Brain Res. 999, 29-39 (2004).
[CrossRef]

2002 (6)

Y. Kakihana, A. Matsunaga, K. Tobo, S. Isowaki, M. Kawakami, I. Tsuneyoshi, Y. Kanmura, and M. Tamura, “Redox behavior of cytochrome oxidase and neurological prognosis in 66 patients who underwent thoracic aortic surgery,” Eur. J. Cardio-Thorac. Surg. 21, 434-439 (2002).
[CrossRef]

N. N. Boustany, R. Drezek, and N. V. Thakor, “Calcium-induced alterations in mitochondrial morphology quantified in situ with optical scatter imaging,” Biophys. J. 83, 1691-1700 (2002).

D. Fayuk, P. G. Aitken, G. G. Somjen, and D. A. Turner, “Two different mechanisms underlie reversible, intrinsic optical signals in rat hippocampal slices,” J. Neurophysiol. 87, 1924-1937 (2002).

L. J. Johnson, W. Chung, D. F. Hanley, and N. V. Thakor, “Optical scatter imaging detects mitochondrial swelling in living tissue slices,” NeuroImage 17, 1649-1657 (2002).
[CrossRef]

L. Tao, D. Masri, S. Hrabetova, and C. Nicholson, “Light scattering in rat neocortical slices differs during spreading depression and ischemia,” Brain Res. 952, 290-300 (2002).
[CrossRef]

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88, 2726-2735 (2002).
[CrossRef]

2001 (1)

M. Haller, S. L. Mironov, and D. W. Richter, “Intrinsic optical signals in respiratory brain stem regions of mice: neurotransmitters, neuromodulators, and metabolic stress,” J. Neurophysiol. 86, 412-421 (2001).

2000 (4)

S. Bahar, D. Fayuk, G. G. Somjen, P. G. Aitken, and D. A. Turner, “Mitochondrial and intrinsic optical signals imaged during hypoxia and spreading depression in rat hippocampal slices,” J. Neurophysiol. 84, 311-324 (2000).

D. L. Nelson and M. M. Cox, “Oxidative phosphorylation and photophosphorylation,” in Lehninger Principles of Biochemistry, D. L. Nelson and M. M. Cox, eds. (Worth Publishers, 2000), pp. 659-673.

M. Kohl, U. Lindauer, G. Royl, M. Kuhl, L. Gold, A. Villringer, and U. Dirnagl, “Physical model for the spectroscopic analysis of cortical intrinsic optical signals,” Phys. Med. Biol. 45, 3749-3764 (2000).
[CrossRef]

R. Springett, J. Newman, M. Cope, and D. T. Delpy, “Oxygen dependency and precision of cytochrome oxidase signal from full spectral NIRS of the piglet brain,” Am. J. Physiol. Heart Circ. Physiol. 279, H2202-2209 (2000).

1999 (7)

C. E. Cooper, M. Cope, R. Springett, P. N. Amess, J. Penrice, L. Tyszczuk, S. Punwani, R. Ordidge, J. Wyatt, and D. T. Delpy, “Use of mitochondrial inhibitors to demonstrate that cytochrome oxidase near-infrared spectroscopy can measure mitochondrial dysfunction noninvasively in the brain,” J. Cereb. Blood Flow Metab. 19, 27-38 (1999).
[CrossRef]

P. Hellwig, S. Grzybek, J. Behr, B. Ludwig, H. Michel, and W. Mantele, “Electrochemical and ultraviolet/visible/infrared spectroscopic analysis of heme a and a3 redox reactions in the cytochrome c oxidase from Paracoccus denitrificans: separation of heme a and a3 contributions and assignment of vibrational modes,” Biochemistry 38, 1685-1694 (1999).
[CrossRef]

A. J. de Crespigny, J. Rother, C. Beaulieu, M. E. Moseley, and M. Hoehn, “Rapid monitoring of diffusion, DC potential, and blood oxygenation changes during global ischemia. Effects of hypoglycemia, hyperglycemia, and TTX,” Stroke 30, 2212-2222 (1999).

P. G. Aitken, D. Fayuk, G. G. Somjen, and D. A. Turner, “Use of intrinsic optical signals to monitor physiological changes in brain tissue slices,” Methods Enzymol. 18, 91-103 (1999).
[CrossRef]

M. Müller and G. G. Somjen, “Intrinsic optical signals in rat hippocampal slices during hypoxia-induced spreading depression-like depolarization,” J. Neurophysiol. 82, 1818-1831 (1999).

R. D. Andrew, C. R. Jarvis, and A. S. Obeidat, “Potential sources of intrinsic optical signals imaged in live brain slices,” Methods Enzymol. 18, 185-196 (1999).
[CrossRef]

C. R. Jarvis, L. Lilge, G. J. Vipond, and R. D. Andrew, “Interpretation of intrinsic optical signals and calcein fluorescence during acute excitotoxic insult in the hippocampal slice,” NeuroImage 10, 357-372 (1999).
[CrossRef]

1998 (5)

S. Charpak and E. Audinat, “Cardiac arrest in rodents: maximal duration compatible with a recovery of neuronal activity,” Proc. Natl. Acad. Sci. USA 95, 4748-4753 (1998).
[CrossRef]

A. Matsunaga, Y. Nomura, S. Kuroda, M. Tamura, J. Nishihira, and N. Yoshimura, “Energy-dependent redox state of heme a+a3 and copper of cytochrome oxidase in perfused rat brain in situ,” Am. J. Physiol. 275, C1022-C1030 (1998).

G. Nollert, T. Shin'oka, and R. A. Jonas, “Near-infrared spectrophotometry of the brain in cardiovascular surgery,” Thorac. Cardiovasc. Surg. 46, 167-175 (1998).

T. M. Polischuk, C. R. Jarvis, and R. D. Andrew, “Intrinsic optical signaling denoting neuronal damage in response to acute excitotoxic insult by domoic acid in the hippocampal slice,” Neurobiol. Dis. 4, 423-437 (1998).
[CrossRef]

M. Kohl, U. Lindauer, U. Dirnagl, and A. Villringer, “Separation of changes in light scattering and chromophore concentrations during cortical spreading depression in rats,” Opt. Lett. 23, 555-557 (1998).
[CrossRef]

1997 (6)

E. Gratton, S. Fantini, M. A. Franceschini, G. Gratton, and M. Fabiani, “Measurements of scattering and absorption changes in muscle and brain,” Philos. Trans. R. Soc. Lond. B 352, 727-735 (1997).
[CrossRef]

A. Villringer and B. Chance, “Non-invasive optical spectroscopy and imaging of human brain function,” Trends Neurosci. 20, 435-442 (1997).
[CrossRef]

B. Chance, Q. Luo, S. Nioka, D. C. Alsop, and J. A. Detre, “Optical investigations of physiology: a study of intrinsic and extrinsic biomedical contrast,” Philos. Trans. R. Soc. Lond. B 352, 707-716 (1997).
[CrossRef]

B. Chance, A. Mayevsky, B. Guan, and Y. Zhang, “Hypoxia/ischemia triggers a light scattering event in rat brain,” in Oxygen Transport to Tissue XIX, D. K. Harrison and D. T. Delpy, eds. (Plenum, 1997), pp. 457-467.

C. E. Cooper and R. Springett, “Measurement of cytochrome oxidase and mitochondrial energetics by near-infrared spectroscopy,” Philos. Trans. R. Soc. Lond. B 352, 669-676 (1997).
[CrossRef]

Y. Hoshi, O. Hazeki, Y. Kakihana, and M. Tamura, “Redox behavior of cytochrome oxidase in the rat brain measured by near-infrared spectroscopy,” J. Appl. Physiol. 83, 1842-1848 (1997).

1996 (2)

Y. Yamashita, M. Oda, H. Naruse, and M. Tamura, “In vivo measurement of reduced scattering and absorption coefficients of living tissue using time-resolved spectroscopy,” OSA Trends Optics Photonics 2, 387-390 (1996).

D. Malonek and A. Grinvald, “Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping,” Science 272, 551-554 (1996).
[CrossRef]

1995 (1)

M. Tsuji, H. Naruse, J. Volpe, and D. Holtzman, “Reduction of cytochrome aa3 measured by near-infrared spectroscopy predicts cerebral energy loss in hypoxic piglets,” Pediatr. Res. 37, 253-259 (1995).

1994 (3)

C. E. Cooper, S. J. Matcher, J. S. Wyatt, M. Cope, G. C. Brown, E. M. Nemoto, and D. T. Delpy, “Near-infrared spectroscopy of the brain: relevance to cytochrome oxidase bioenergetics,” Biochem. Soc. Trans. 22, 974-980 (1994).

K. A. Hossmann, “Viability thresholds and the penumbra of focal ischemia,” Ann. Neurol. 36, 557-565 (1994).
[CrossRef]

R. D. Andrew and B. A. MacVicar, “Imaging cell volume changes and neuronal excitation in the hippocampal slice,” Neuroscience 62, 371-383 (1994).
[CrossRef]

1993 (2)

P. Lappalainen, R. Aasa, B. G. Malmstrom, and M. Saraste, “Soluble CuA-binding domain from the Paracoccus cytochrome c oxidase,” J. Biol. Chem. 268, 26416-26421 (1993).

P. van der Zee, M. Essenpreis, and D. T. Delpy, “Optical properties of brain tissue,” Proc. SPIE 1888, 454-465 (1993).
[CrossRef]

1992 (1)

P. van der Zee, “Measurement and modelling of the optical properties of human tissue in the near infrared,” Ph.D. thesis (University College London, 1992), pp. 266-269.

1991 (2)

H. Miyake, S. Nioka, A. Zaman, D. S. Smith, and B. Chance, “The detection of cytochrome oxidase heme iron and copper absorption in the blood-perfused and blood-free brain in normoxia and hypoxia,” Anal. Biochem. 192, 149-155 (1991).
[CrossRef]

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. USA 88, 9382-9386(1991).
[CrossRef]

1990 (1)

M. Ferrari, D. F. Hanley, D. A. Wilson, and R. J. Traystman, “Redox changes in cat brain cytochrome-c oxidase after blood-fluorocarbon exchange,” Am. J. Physiol. 258, H1706-H1713(1990).

1989 (1)

K. Kitagawa, M. Matsumoto, M. Niinobe, K. Mikoshiba, R. Hata, H. Ueda, N. Handa, R. Fukunaga, Y. Isaka, K. Kimura, and T. Kamada, “Microtubule-associated protein 2 as a sensitive marker for cerebral ischemic damage-immunohistochemical investigation of dendritic damage,” Neuroscience 31, 401-411 (1989).
[CrossRef]

1988 (1)

S. Wray, M. Cope, D. T. Delpy, J. S. Wyatt, and E. O. Reynolds, “Characterization of the near infrared absorption spectra of cytochrome aa3 and haemoglobin for the non-invasive monitoring of cerebral oxygenation,” Biochim. Biophys. Acta 933, 184-192 (1988).
[CrossRef]

1987 (1)

U. Heinrich, J. Hoffmann, and D. W. Lubbers, “Quantitative evaluation of optical reflection spectra of blood-free perfused guinea pig brain using a nonlinear multicomponent analysis,” Pflugers Arch. 409, 152-157 (1987).
[CrossRef]

1985 (2)

B. M. Salzberg, A. L. Obaid, and H. Gainer, “Large and rapid changes in light scattering accompany secretion by nerve terminals in the mammalian neurohypophysis,” J. Gen. Physiol. 86, 395-411 (1985).
[CrossRef]

A. J. Hansen, “Effect of anoxia on ion distribution in the brain,” Physiol. Rev. 65, 101-148 (1985).

1984 (1)

C. A. Piantadosi and F. F. Jobsis-Vandervliet, “Spectrophotometry of cerebral cytochrome a, a3 in bloodless rats,” Brain Res. 305, 89-94 (1984).
[CrossRef]

1981 (1)

N. R. Kreisman, T. J. Sick, J. C. LaManna, and M. Rosenthal, “Local tissue oxygen tension-cytochrome a, a3 redox relationships in rat cerebral cortex in vivo,” Brain Res. 218, 161-174(1981).
[CrossRef]

1980 (1)

A. J. Hansen and C. E. Olsen, “Brain extracellular space during spreading depression and ischemia,” Acta Physiol. Scand. 108, 355-365 (1980).

1978 (1)

B. K. Siesjo, “Brain metabolism and anaesthesia,” Acta Anaesthesiologica Scandinavica Supplement 70, 56-59 (1978).

1977 (1)

F. F. Jöbsis, J. H. Keizer, J. C. LaManna, and M. Rosenthal, “Reflectance spectrophotometry of cytochrome aa3in vivo,” J. Appl. Physiol. 43, 858-872 (1977).

1972 (1)

M. K. Wikstrom, “Energy-linked change in the redox state and absorption spectrum of cytochrome a in situ,” Biochim. Biophys. Acta 283, 385-390 (1972).
[CrossRef]

1966 (2)

D. C. Wharton and Q. H. Gibson, “Spectrophotometric characterization and function of copper in cytochrome c oxidase,” in Biochemistry of Copper, J. Peisach, ed. (Academic, 1966), pp. 235-244.

D. Keilin, “Indophenol oxidase, cytochrome oxidase and cytochrome a3,” in The History of Cell Respiration and Cytochrome, J. Keilin, ed. (Cambridge University, 1966), pp. 224-251.

1961 (1)

D. E. Griffiths and D. C. Wharton, “Studies of the electron transport system. XXXV. Purification and properties of cytochrome oxidase,” J. Biol. Chem. 236, 1850-1856 (1961).

1956 (1)

J. R. Platt, “Electronic structure and excitation of polyenes and porphyrins,” in Radiation Biology, A. Hollander, ed. (McGraw-Hill, 1956), pp. 71-123.

1955 (1)

B. Chance and G. R. Williams, “A method for the localization of sites for oxidative phosphorylation,” Nature 176, 250-254(1955).
[CrossRef]

Aasa, R.

P. Lappalainen, R. Aasa, B. G. Malmstrom, and M. Saraste, “Soluble CuA-binding domain from the Paracoccus cytochrome c oxidase,” J. Biol. Chem. 268, 26416-26421 (1993).

Aitken, P. G.

D. Fayuk, P. G. Aitken, G. G. Somjen, and D. A. Turner, “Two different mechanisms underlie reversible, intrinsic optical signals in rat hippocampal slices,” J. Neurophysiol. 87, 1924-1937 (2002).

S. Bahar, D. Fayuk, G. G. Somjen, P. G. Aitken, and D. A. Turner, “Mitochondrial and intrinsic optical signals imaged during hypoxia and spreading depression in rat hippocampal slices,” J. Neurophysiol. 84, 311-324 (2000).

P. G. Aitken, D. Fayuk, G. G. Somjen, and D. A. Turner, “Use of intrinsic optical signals to monitor physiological changes in brain tissue slices,” Methods Enzymol. 18, 91-103 (1999).
[CrossRef]

Allen, N. J.

N. J. Allen, R. Karadottir, and D. Attwell, “A preferential role for glycolysis in preventing the anoxic depolarization of rat hippocampal area CA1 pyramidal cells,” J. Neurosci. 25, 848-859 (2005).
[CrossRef]

Alsop, D. C.

B. Chance, Q. Luo, S. Nioka, D. C. Alsop, and J. A. Detre, “Optical investigations of physiology: a study of intrinsic and extrinsic biomedical contrast,” Philos. Trans. R. Soc. Lond. B 352, 707-716 (1997).
[CrossRef]

Amess, P. N.

C. E. Cooper, M. Cope, R. Springett, P. N. Amess, J. Penrice, L. Tyszczuk, S. Punwani, R. Ordidge, J. Wyatt, and D. T. Delpy, “Use of mitochondrial inhibitors to demonstrate that cytochrome oxidase near-infrared spectroscopy can measure mitochondrial dysfunction noninvasively in the brain,” J. Cereb. Blood Flow Metab. 19, 27-38 (1999).
[CrossRef]

Andrew, R. D.

R. D. Andrew, C. R. Jarvis, and A. S. Obeidat, “Potential sources of intrinsic optical signals imaged in live brain slices,” Methods Enzymol. 18, 185-196 (1999).
[CrossRef]

C. R. Jarvis, L. Lilge, G. J. Vipond, and R. D. Andrew, “Interpretation of intrinsic optical signals and calcein fluorescence during acute excitotoxic insult in the hippocampal slice,” NeuroImage 10, 357-372 (1999).
[CrossRef]

T. M. Polischuk, C. R. Jarvis, and R. D. Andrew, “Intrinsic optical signaling denoting neuronal damage in response to acute excitotoxic insult by domoic acid in the hippocampal slice,” Neurobiol. Dis. 4, 423-437 (1998).
[CrossRef]

R. D. Andrew and B. A. MacVicar, “Imaging cell volume changes and neuronal excitation in the hippocampal slice,” Neuroscience 62, 371-383 (1994).
[CrossRef]

Attwell, D.

N. J. Allen, R. Karadottir, and D. Attwell, “A preferential role for glycolysis in preventing the anoxic depolarization of rat hippocampal area CA1 pyramidal cells,” J. Neurosci. 25, 848-859 (2005).
[CrossRef]

Audinat, E.

S. Charpak and E. Audinat, “Cardiac arrest in rodents: maximal duration compatible with a recovery of neuronal activity,” Proc. Natl. Acad. Sci. USA 95, 4748-4753 (1998).
[CrossRef]

Ba, A. M.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88, 2726-2735 (2002).
[CrossRef]

Bahar, S.

S. Bahar, D. Fayuk, G. G. Somjen, P. G. Aitken, and D. A. Turner, “Mitochondrial and intrinsic optical signals imaged during hypoxia and spreading depression in rat hippocampal slices,” J. Neurophysiol. 84, 311-324 (2000).

Bartek, M.

M. Bartek, X. Wang, W. Wells, K. D. Paulsen, and B. W. Pogue, “Estimation of subcellular particle size histograms with electron microscopy for prediction of optical scattering in breast tissue,” J. Biomed. Opt. 11, 064007 (2006).
[CrossRef]

Beaulieu, C.

A. J. de Crespigny, J. Rother, C. Beaulieu, M. E. Moseley, and M. Hoehn, “Rapid monitoring of diffusion, DC potential, and blood oxygenation changes during global ischemia. Effects of hypoglycemia, hyperglycemia, and TTX,” Stroke 30, 2212-2222 (1999).

Behr, J.

P. Hellwig, S. Grzybek, J. Behr, B. Ludwig, H. Michel, and W. Mantele, “Electrochemical and ultraviolet/visible/infrared spectroscopic analysis of heme a and a3 redox reactions in the cytochrome c oxidase from Paracoccus denitrificans: separation of heme a and a3 contributions and assignment of vibrational modes,” Biochemistry 38, 1685-1694 (1999).
[CrossRef]

Belevich, I.

I. Belevich, D. A. Bloch, N. Belevich, M. Wikstrom, and M. I. Verkhovsky, “Exploring the proton pump mechanism of cytochrome c oxidase in real time,” Proc. Natl. Acad. Sci. USA 104, 2685-2690 (2007).
[CrossRef]

I. Belevich, M. I. Verkhovsky, and M. Wikstrom, “Proton-coupled electron transfer drives the proton pump of cytochrome c oxidase,” Nature 440, 829-832 (2006).
[CrossRef]

Belevich, N.

I. Belevich, D. A. Bloch, N. Belevich, M. Wikstrom, and M. I. Verkhovsky, “Exploring the proton pump mechanism of cytochrome c oxidase in real time,” Proc. Natl. Acad. Sci. USA 104, 2685-2690 (2007).
[CrossRef]

Betts, K.

T. H. Murphy, P. Li, K. Betts, and R. Liu, “Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines,” J. Neurosci. 28, 1756-1772 (2008).
[CrossRef]

Bloch, D. A.

I. Belevich, D. A. Bloch, N. Belevich, M. Wikstrom, and M. I. Verkhovsky, “Exploring the proton pump mechanism of cytochrome c oxidase in real time,” Proc. Natl. Acad. Sci. USA 104, 2685-2690 (2007).
[CrossRef]

Blonder, G. E.

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. USA 88, 9382-9386(1991).
[CrossRef]

Boustany, N. N.

N. N. Boustany, R. Drezek, and N. V. Thakor, “Calcium-induced alterations in mitochondrial morphology quantified in situ with optical scatter imaging,” Biophys. J. 83, 1691-1700 (2002).

Brown, G. C.

C. E. Cooper, S. J. Matcher, J. S. Wyatt, M. Cope, G. C. Brown, E. M. Nemoto, and D. T. Delpy, “Near-infrared spectroscopy of the brain: relevance to cytochrome oxidase bioenergetics,” Biochem. Soc. Trans. 22, 974-980 (1994).

Cannestra, A. F.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88, 2726-2735 (2002).
[CrossRef]

Chance, B.

A. Villringer and B. Chance, “Non-invasive optical spectroscopy and imaging of human brain function,” Trends Neurosci. 20, 435-442 (1997).
[CrossRef]

B. Chance, Q. Luo, S. Nioka, D. C. Alsop, and J. A. Detre, “Optical investigations of physiology: a study of intrinsic and extrinsic biomedical contrast,” Philos. Trans. R. Soc. Lond. B 352, 707-716 (1997).
[CrossRef]

B. Chance, A. Mayevsky, B. Guan, and Y. Zhang, “Hypoxia/ischemia triggers a light scattering event in rat brain,” in Oxygen Transport to Tissue XIX, D. K. Harrison and D. T. Delpy, eds. (Plenum, 1997), pp. 457-467.

H. Miyake, S. Nioka, A. Zaman, D. S. Smith, and B. Chance, “The detection of cytochrome oxidase heme iron and copper absorption in the blood-perfused and blood-free brain in normoxia and hypoxia,” Anal. Biochem. 192, 149-155 (1991).
[CrossRef]

B. Chance and G. R. Williams, “A method for the localization of sites for oxidative phosphorylation,” Nature 176, 250-254(1955).
[CrossRef]

Charpak, S.

S. Charpak and E. Audinat, “Cardiac arrest in rodents: maximal duration compatible with a recovery of neuronal activity,” Proc. Natl. Acad. Sci. USA 95, 4748-4753 (1998).
[CrossRef]

Chen, J. W.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88, 2726-2735 (2002).
[CrossRef]

Chung, W.

L. J. Johnson, W. Chung, D. F. Hanley, and N. V. Thakor, “Optical scatter imaging detects mitochondrial swelling in living tissue slices,” NeuroImage 17, 1649-1657 (2002).
[CrossRef]

Cooper, C. E.

I. Tachtsidis, M. Tisdall, T. S. Leung, C. E. Cooper, D. T. Delpy, M. Smith, and C. E. Elwell, “Investigation of in vivo measurement of cerebral cytochrome-c-oxidase redox changes using near-infrared spectroscopy in patients with orthostatic hypotension,” Physiol. Meas. 28, 199-211 (2007).
[CrossRef]

C. E. Cooper, M. Cope, R. Springett, P. N. Amess, J. Penrice, L. Tyszczuk, S. Punwani, R. Ordidge, J. Wyatt, and D. T. Delpy, “Use of mitochondrial inhibitors to demonstrate that cytochrome oxidase near-infrared spectroscopy can measure mitochondrial dysfunction noninvasively in the brain,” J. Cereb. Blood Flow Metab. 19, 27-38 (1999).
[CrossRef]

C. E. Cooper and R. Springett, “Measurement of cytochrome oxidase and mitochondrial energetics by near-infrared spectroscopy,” Philos. Trans. R. Soc. Lond. B 352, 669-676 (1997).
[CrossRef]

C. E. Cooper, S. J. Matcher, J. S. Wyatt, M. Cope, G. C. Brown, E. M. Nemoto, and D. T. Delpy, “Near-infrared spectroscopy of the brain: relevance to cytochrome oxidase bioenergetics,” Biochem. Soc. Trans. 22, 974-980 (1994).

Cope, M.

R. Springett, J. Newman, M. Cope, and D. T. Delpy, “Oxygen dependency and precision of cytochrome oxidase signal from full spectral NIRS of the piglet brain,” Am. J. Physiol. Heart Circ. Physiol. 279, H2202-2209 (2000).

C. E. Cooper, M. Cope, R. Springett, P. N. Amess, J. Penrice, L. Tyszczuk, S. Punwani, R. Ordidge, J. Wyatt, and D. T. Delpy, “Use of mitochondrial inhibitors to demonstrate that cytochrome oxidase near-infrared spectroscopy can measure mitochondrial dysfunction noninvasively in the brain,” J. Cereb. Blood Flow Metab. 19, 27-38 (1999).
[CrossRef]

C. E. Cooper, S. J. Matcher, J. S. Wyatt, M. Cope, G. C. Brown, E. M. Nemoto, and D. T. Delpy, “Near-infrared spectroscopy of the brain: relevance to cytochrome oxidase bioenergetics,” Biochem. Soc. Trans. 22, 974-980 (1994).

S. Wray, M. Cope, D. T. Delpy, J. S. Wyatt, and E. O. Reynolds, “Characterization of the near infrared absorption spectra of cytochrome aa3 and haemoglobin for the non-invasive monitoring of cerebral oxygenation,” Biochim. Biophys. Acta 933, 184-192 (1988).
[CrossRef]

Cox, M. M.

D. L. Nelson and M. M. Cox, “Oxidative phosphorylation and photophosphorylation,” in Lehninger Principles of Biochemistry, D. L. Nelson and M. M. Cox, eds. (Worth Publishers, 2000), pp. 659-673.

de Crespigny, A. J.

A. J. de Crespigny, J. Rother, C. Beaulieu, M. E. Moseley, and M. Hoehn, “Rapid monitoring of diffusion, DC potential, and blood oxygenation changes during global ischemia. Effects of hypoglycemia, hyperglycemia, and TTX,” Stroke 30, 2212-2222 (1999).

Delpy, D. T.

I. Tachtsidis, M. Tisdall, T. S. Leung, C. E. Cooper, D. T. Delpy, M. Smith, and C. E. Elwell, “Investigation of in vivo measurement of cerebral cytochrome-c-oxidase redox changes using near-infrared spectroscopy in patients with orthostatic hypotension,” Physiol. Meas. 28, 199-211 (2007).
[CrossRef]

R. Springett, J. Newman, M. Cope, and D. T. Delpy, “Oxygen dependency and precision of cytochrome oxidase signal from full spectral NIRS of the piglet brain,” Am. J. Physiol. Heart Circ. Physiol. 279, H2202-2209 (2000).

C. E. Cooper, M. Cope, R. Springett, P. N. Amess, J. Penrice, L. Tyszczuk, S. Punwani, R. Ordidge, J. Wyatt, and D. T. Delpy, “Use of mitochondrial inhibitors to demonstrate that cytochrome oxidase near-infrared spectroscopy can measure mitochondrial dysfunction noninvasively in the brain,” J. Cereb. Blood Flow Metab. 19, 27-38 (1999).
[CrossRef]

C. E. Cooper, S. J. Matcher, J. S. Wyatt, M. Cope, G. C. Brown, E. M. Nemoto, and D. T. Delpy, “Near-infrared spectroscopy of the brain: relevance to cytochrome oxidase bioenergetics,” Biochem. Soc. Trans. 22, 974-980 (1994).

P. van der Zee, M. Essenpreis, and D. T. Delpy, “Optical properties of brain tissue,” Proc. SPIE 1888, 454-465 (1993).
[CrossRef]

S. Wray, M. Cope, D. T. Delpy, J. S. Wyatt, and E. O. Reynolds, “Characterization of the near infrared absorption spectra of cytochrome aa3 and haemoglobin for the non-invasive monitoring of cerebral oxygenation,” Biochim. Biophys. Acta 933, 184-192 (1988).
[CrossRef]

Detre, J. A.

B. Chance, Q. Luo, S. Nioka, D. C. Alsop, and J. A. Detre, “Optical investigations of physiology: a study of intrinsic and extrinsic biomedical contrast,” Philos. Trans. R. Soc. Lond. B 352, 707-716 (1997).
[CrossRef]

Dirnagl, U.

M. Kohl, U. Lindauer, G. Royl, M. Kuhl, L. Gold, A. Villringer, and U. Dirnagl, “Physical model for the spectroscopic analysis of cortical intrinsic optical signals,” Phys. Med. Biol. 45, 3749-3764 (2000).
[CrossRef]

M. Kohl, U. Lindauer, U. Dirnagl, and A. Villringer, “Separation of changes in light scattering and chromophore concentrations during cortical spreading depression in rats,” Opt. Lett. 23, 555-557 (1998).
[CrossRef]

Drezek, R.

N. N. Boustany, R. Drezek, and N. V. Thakor, “Calcium-induced alterations in mitochondrial morphology quantified in situ with optical scatter imaging,” Biophys. J. 83, 1691-1700 (2002).

Elwell, C. E.

I. Tachtsidis, M. Tisdall, T. S. Leung, C. E. Cooper, D. T. Delpy, M. Smith, and C. E. Elwell, “Investigation of in vivo measurement of cerebral cytochrome-c-oxidase redox changes using near-infrared spectroscopy in patients with orthostatic hypotension,” Physiol. Meas. 28, 199-211 (2007).
[CrossRef]

M. M. Tisdall, I. Tachtsidis, T. S. Leung, C. E. Elwell, and M. Smith, “Near-infrared spectroscopic quantification of changes in the concentration of oxidized cytochrome c oxidase in the healthy human brain during hypoxemia,” J. Biomed. Opt. 12, 024002 (2007).
[CrossRef]

Essenpreis, M.

P. van der Zee, M. Essenpreis, and D. T. Delpy, “Optical properties of brain tissue,” Proc. SPIE 1888, 454-465 (1993).
[CrossRef]

Fabiani, M.

E. Gratton, S. Fantini, M. A. Franceschini, G. Gratton, and M. Fabiani, “Measurements of scattering and absorption changes in muscle and brain,” Philos. Trans. R. Soc. Lond. B 352, 727-735 (1997).
[CrossRef]

Fantini, S.

E. Gratton, S. Fantini, M. A. Franceschini, G. Gratton, and M. Fabiani, “Measurements of scattering and absorption changes in muscle and brain,” Philos. Trans. R. Soc. Lond. B 352, 727-735 (1997).
[CrossRef]

Fayuk, D.

D. Fayuk, P. G. Aitken, G. G. Somjen, and D. A. Turner, “Two different mechanisms underlie reversible, intrinsic optical signals in rat hippocampal slices,” J. Neurophysiol. 87, 1924-1937 (2002).

S. Bahar, D. Fayuk, G. G. Somjen, P. G. Aitken, and D. A. Turner, “Mitochondrial and intrinsic optical signals imaged during hypoxia and spreading depression in rat hippocampal slices,” J. Neurophysiol. 84, 311-324 (2000).

P. G. Aitken, D. Fayuk, G. G. Somjen, and D. A. Turner, “Use of intrinsic optical signals to monitor physiological changes in brain tissue slices,” Methods Enzymol. 18, 91-103 (1999).
[CrossRef]

Ferrari, M.

M. Ferrari, D. F. Hanley, D. A. Wilson, and R. J. Traystman, “Redox changes in cat brain cytochrome-c oxidase after blood-fluorocarbon exchange,” Am. J. Physiol. 258, H1706-H1713(1990).

Franceschini, M. A.

E. Gratton, S. Fantini, M. A. Franceschini, G. Gratton, and M. Fabiani, “Measurements of scattering and absorption changes in muscle and brain,” Philos. Trans. R. Soc. Lond. B 352, 727-735 (1997).
[CrossRef]

Fujii, F.

F. Fujii, Y. Nodasaka, G. Nishimura, and M. Tamura, “Anoxia induces matrix shrinkage accompanied by an increase in light scattering in isolated brain mitochondria,” Brain Res. 999, 29-39 (2004).
[CrossRef]

Fukunaga, R.

K. Kitagawa, M. Matsumoto, M. Niinobe, K. Mikoshiba, R. Hata, H. Ueda, N. Handa, R. Fukunaga, Y. Isaka, K. Kimura, and T. Kamada, “Microtubule-associated protein 2 as a sensitive marker for cerebral ischemic damage-immunohistochemical investigation of dendritic damage,” Neuroscience 31, 401-411 (1989).
[CrossRef]

Gainer, H.

B. M. Salzberg, A. L. Obaid, and H. Gainer, “Large and rapid changes in light scattering accompany secretion by nerve terminals in the mammalian neurohypophysis,” J. Gen. Physiol. 86, 395-411 (1985).
[CrossRef]

Gibson, Q. H.

D. C. Wharton and Q. H. Gibson, “Spectrophotometric characterization and function of copper in cytochrome c oxidase,” in Biochemistry of Copper, J. Peisach, ed. (Academic, 1966), pp. 235-244.

Gold, L.

M. Kohl, U. Lindauer, G. Royl, M. Kuhl, L. Gold, A. Villringer, and U. Dirnagl, “Physical model for the spectroscopic analysis of cortical intrinsic optical signals,” Phys. Med. Biol. 45, 3749-3764 (2000).
[CrossRef]

Gratton, E.

E. Gratton, S. Fantini, M. A. Franceschini, G. Gratton, and M. Fabiani, “Measurements of scattering and absorption changes in muscle and brain,” Philos. Trans. R. Soc. Lond. B 352, 727-735 (1997).
[CrossRef]

Gratton, G.

E. Gratton, S. Fantini, M. A. Franceschini, G. Gratton, and M. Fabiani, “Measurements of scattering and absorption changes in muscle and brain,” Philos. Trans. R. Soc. Lond. B 352, 727-735 (1997).
[CrossRef]

Griffiths, D. E.

D. E. Griffiths and D. C. Wharton, “Studies of the electron transport system. XXXV. Purification and properties of cytochrome oxidase,” J. Biol. Chem. 236, 1850-1856 (1961).

Grinvald, A.

D. Malonek and A. Grinvald, “Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping,” Science 272, 551-554 (1996).
[CrossRef]

Grzybek, S.

P. Hellwig, S. Grzybek, J. Behr, B. Ludwig, H. Michel, and W. Mantele, “Electrochemical and ultraviolet/visible/infrared spectroscopic analysis of heme a and a3 redox reactions in the cytochrome c oxidase from Paracoccus denitrificans: separation of heme a and a3 contributions and assignment of vibrational modes,” Biochemistry 38, 1685-1694 (1999).
[CrossRef]

Guan, B.

B. Chance, A. Mayevsky, B. Guan, and Y. Zhang, “Hypoxia/ischemia triggers a light scattering event in rat brain,” in Oxygen Transport to Tissue XIX, D. K. Harrison and D. T. Delpy, eds. (Plenum, 1997), pp. 457-467.

Guiou, M.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88, 2726-2735 (2002).
[CrossRef]

Haller, M.

M. Haller, S. L. Mironov, and D. W. Richter, “Intrinsic optical signals in respiratory brain stem regions of mice: neurotransmitters, neuromodulators, and metabolic stress,” J. Neurophysiol. 86, 412-421 (2001).

Handa, N.

K. Kitagawa, M. Matsumoto, M. Niinobe, K. Mikoshiba, R. Hata, H. Ueda, N. Handa, R. Fukunaga, Y. Isaka, K. Kimura, and T. Kamada, “Microtubule-associated protein 2 as a sensitive marker for cerebral ischemic damage-immunohistochemical investigation of dendritic damage,” Neuroscience 31, 401-411 (1989).
[CrossRef]

Hanley, D. F.

L. J. Johnson, W. Chung, D. F. Hanley, and N. V. Thakor, “Optical scatter imaging detects mitochondrial swelling in living tissue slices,” NeuroImage 17, 1649-1657 (2002).
[CrossRef]

M. Ferrari, D. F. Hanley, D. A. Wilson, and R. J. Traystman, “Redox changes in cat brain cytochrome-c oxidase after blood-fluorocarbon exchange,” Am. J. Physiol. 258, H1706-H1713(1990).

Hansen, A. J.

T. Takano, G. F. Tian, W. Peng, N. Lou, D. Lovatt, A. J. Hansen, K. A. Kasischke, and M. Nedergaard, “Cortical spreading depression causes and coincides with tissue hypoxia,” Nat. Neurosci. 10, 754-762 (2007).
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Figures (9)

Fig. 1
Fig. 1

Diagram of the experimental setup for multiwavelength diffuse reflectance measurement in rat brains.

Fig. 2
Fig. 2

Time courses of normalized diffuse reflectance intensities at 540 nm after starting saline infusion for all five rats investigated. The bold line shows the reflectance intensity of Rat 1. Infusion was started at t = 0 and continued for 500 s . The time of completed blood clearance was 157.6 ± 11.4 s for all five rats. Reflectance intensities at 540 nm are normalized by those at the time of blood clearance.

Fig. 3
Fig. 3

Absorption spectra of oxidized and reduced states of purified CcO from Ref. [2].

Fig. 4
Fig. 4

Wavelength dependence of changes in normalized diffuse reflectance intensities in the spectral region of 600 630 nm in the time domain between blood removal completion and start of the triphasic scattering change, i.e., 160 to 210 s , for Rat 1.

Fig. 5
Fig. 5

Time courses of normalized diffuse reflectance intensities at (a) 623, (b) 605, and (c)  830 nm during saline infusion in the brain of Rat 1; reflectance intensity at 623 nm shows the light scattering signal. Infusion was started at t = 0 and continued for 500 s . Reflectance intensities at all of the wavelengths are normalized by those at the time of blood clearance ( 160 s ). The gray line in (b) and (c) shows the light scattering signal shown in (a).

Fig. 6
Fig. 6

Time courses of light absorption signals related to reductions of heme aa 3 and CuA for Rat 1, (a) where relative changes in reflectance intensities at 605 and 830 nm to that of the scattering signal are shown. The gray dotted line shows heme aa 3 -related signal, and the gray line shows CuA-related signal. The time course of the light scattering signal of Rat 1, i.e., reflectance intensity at 623 nm , is shown by a black line. (b) The time courses of light scattering signals for all five rats investigated.

Fig. 7
Fig. 7

Correlations between (a) light scattering signal and absorption signal related to the redox state of heme aa 3 and between (b) light scattering signal and that of CuA in CcO for five rats. The blue plots show the correlation of Rat 1. Open plots represent the data for the triphasic scattering change in Phases II, III, and IV, and solid plots show the data after the triphasic change (Phase V).

Fig. 8
Fig. 8

Histologies with HE staining and immunohistochemical MAP2 staining of the cerebral cortex at different times after the start of saline infusion: (a)  0 s (control) and (b)  350 s for HE staining, and (c)  0 s (control) and (d)  350 s for MAP2 staining. The scale bar in each panel represents 10 μm .

Fig. 9
Fig. 9

TEM images of cortical surface tissues at (a)  50 s and (b)  350 s after starting saline infusion, corresponding to before and after the triphasic scattering change, respectively. (b) shows remarkably enlarged dendrites (arrowheads) and enlarged, deformed mitochondria with irregular cristae (arrows). Scale bar in each panel represents 1 μm .

Tables (1)

Tables Icon

Table 1 Starting Time and Duration of Each Phase (I–IV) for Five Rats a

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