Abstract

Observation of brain activities in freely moving animals has become an important approach for neuroscientists to understand the correlation between brain function and behavior. We describe an extendable fiber-optic-based multi-modal imaging system that can concurrently carry out laser speckle contrast imaging (LSCI) of blood flow and optical intrinsic signal (OIS) imaging in freely moving animals, and it could be extended to fluorescence imaging. Our imaging system consists of a multi-source illuminator, a fiber multi-channel optical imaging unit, and a head-mounted microscope. The imaging fiber bundle delivers optical images from the head-mounted microscope to the multi-channel optical imaging unit. Illuminating multi-mode fiber bundles transmit light to the head-mounted microscope which has a mass of less than 1.5 g and includes a gradient index lens, giving the animal maximum movement capability. The internal optical components are adjustable, allowing for a change in magnification and field of view. We test the system by observing hemodynamic changes during cortical spreading depression (CSD) in freely moving and anesthetized animals by simultaneous LSCI and dual-wavelength OIS imaging. Hemodynamic parameters were calculated. Significant differences in CSD propagation durations between the two states were observed. Furthermore, it is capable of performing fluorescence imaging to explore animal behavior and the underlying brain functional activity further.

© 2013 OSA

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References

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    [Crossref] [PubMed]
  2. B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in Light Microscopy for Neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
    [Crossref] [PubMed]
  3. B. A. Flusberg, J. C. Jung, E. D. Cocker, E. P. Anderson, and M. J. Schnitzer, “In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope,” Opt. Lett. 30(17), 2272–2274 (2005).
    [Crossref] [PubMed]
  4. F. Helmchen, M. S. Fee, D. W. Tank, and W. Denk, “A miniature head-mounted two-photon microscope. High-resolution brain imaging in freely moving animals,” Neuron 31(6), 903–912 (2001).
    [Crossref] [PubMed]
  5. W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. J. Barretto, J. C. Jung, H. Ra, O. Solgaard, and M. J. Schnitzer, “In vivo brain imaging using a portable 2.9 g two-photon microscope based on a microelectromechanical systems scanning mirror,” Opt. Lett. 34(15), 2309–2311 (2009).
    [Crossref] [PubMed]
  6. W. Göbel, J. N. D. Kerr, A. Nimmerjahn, and F. Helmchen, “Miniaturized two-photon microscope based on a flexible coherent fiber bundle and a gradient-index lens objective,” Opt. Lett. 29(21), 2521–2523 (2004).
    [Crossref] [PubMed]
  7. C. J. Engelbrecht, R. S. Johnston, E. J. Seibel, and F. Helmchen, “Ultra-compact fiber-optic two-photon microscope for functional fluorescence imaging in vivo,” Opt. Express 16(8), 5556–5564 (2008).
    [Crossref] [PubMed]
  8. B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. J. Barretto, T. H. Ko, L. D. Burns, J. C. Jung, and M. J. Schnitzer, “High-speed, miniaturized fluorescence microscopy in freely moving mice,” Nat. Methods 5(11), 935–938 (2008).
    [Crossref] [PubMed]
  9. J. C. Jung and M. J. Schnitzer, “Multiphoton endoscopy,” Opt. Lett. 28(11), 902–904 (2003).
    [Crossref] [PubMed]
  10. J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. D. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. U.S.A. 106(46), 19557–19562 (2009).
    [Crossref] [PubMed]
  11. I. Ferezou, S. Bolea, and C. C. H. Petersen, “Visualizing the cortical representation of whisker touch: Voltage-sensitive dye imaging in freely moving mice,” Neuron 50(4), 617–629 (2006).
    [Crossref] [PubMed]
  12. P. Miao, H. Y. Lu, Q. Liu, Y. Li, and S. B. Tong, “Laser speckle contrast imaging of cerebral blood flow in freely moving animals,” J. Biomed. Opt. 16(9), 090502 (2011).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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  15. H. Bolay, U. Reuter, A. K. Dunn, Z. H. Huang, D. A. Boas, and M. A. Moskowitz, “Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model,” Nat. Med. 8(2), 136–142 (2002).
    [Crossref] [PubMed]
  16. D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo Large-Scale Cortical Mapping Using Channelrhodopsin-2 Stimulation in Transgenic Mice Reveals Asymmetric and Reciprocal Relationships between Cortical Areas,” Front Neural Circuits 6, 11 (2012), doi:.
    [Crossref] [PubMed]
  17. P. J. Drew and D. E. Feldman, “Intrinsic Signal Imaging of Deprivation-Induced Contraction of Whisker Representations in Rat Somatosensory Cortex,” Cereb. Cortex 19(2), 331–348 (2008).
    [Crossref] [PubMed]
  18. C. C. H. Petersen, “The functional organization of the barrel cortex,” Neuron 56(2), 339–355 (2007).
    [Crossref] [PubMed]
  19. C. C. H. Petersen and B. Sakmann, “Functionally independent columns of rat somatosensory barrel cortex revealed with voltage-sensitive dye imaging,” J. Neurosci. 21(21), 8435–8446 (2001).
    [PubMed]
  20. D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt. 15(1), 011109 (2010).
    [Crossref] [PubMed]
  21. A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. Cereb. Blood Flow Metab. 21(3), 195–201 (2001).
    [Crossref] [PubMed]
  22. Z. C. Luo, Z. J. Yuan, Y. T. Pan, and C. W. Du, “Simultaneous imaging of cortical hemodynamics and blood oxygenation change during cerebral ischemia using dual-wavelength laser speckle contrast imaging,” Opt. Lett. 34(9), 1480–1482 (2009).
    [Crossref] [PubMed]
  23. A. Grinvald, E. Lieke, R. D. Frostig, C. D. Gilbert, and T. N. Wiesel, “Functional architecture of cortex revealed by optical imaging of intrinsic signals,” Nature 324(6095), 361–364 (1986).
    [Crossref] [PubMed]
  24. C. H. Chen-Bee, T. Agoncillo, C. C. Lay, and R. D. Frostig, “Intrinsic signal optical imaging of brain function using short stimulus delivery intervals,” J. Neurosci. Methods 187(2), 171–182 (2010).
    [Crossref] [PubMed]
  25. A. K. Dunn, A. Devor, H. Bolay, M. L. Andermann, M. A. Moskowitz, A. M. Dale, and D. A. Boas, “Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation,” Opt. Lett. 28(1), 28–30 (2003).
    [Crossref] [PubMed]
  26. E. Farkas, F. Bari, and T. P. Obrenovitch, “Multi-modal imaging of anoxic depolarization and hemodynamic changes induced by cardiac arrest in the rat cerebral cortex,” Neuroimage 51(2), 734–742 (2010).
    [Crossref] [PubMed]
  27. T. P. Obrenovitch, S. B. Chen, and E. Farkas, “Simultaneous, live imaging of cortical spreading depression and associated cerebral blood flow changes, by combining voltage-sensitive dye and laser speckle contrast methods,” Neuroimage 45(1), 68–74 (2009).
    [Crossref] [PubMed]
  28. X. L. Sun, Y. R. Wang, S. B. Chen, W. H. Luo, P. C. Li, and Q. M. Luo, “Simultaneous monitoring of intracellular pH changes and hemodynamic response during cortical spreading depression by fluorescence-corrected multimodal optical imaging,” Neuroimage 57(3), 873–884 (2011).
    [Crossref] [PubMed]
  29. A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
    [Crossref] [PubMed]
  30. M. Lauritzen, “Cortical spreading depression in migraine,” Cephalalgia 21(7), 757–760 (2001).
    [Crossref] [PubMed]
  31. H. Martins-Ferreira, M. Nedergaard, and C. Nicholson, “Perspectives on spreading depression,” Brain Res. Brain Res. Rev. 32(1), 215–234 (2000).
    [Crossref] [PubMed]
  32. R. C. Bray, K. R. Forrester, J. Reed, C. Leonard, and J. Tulip, “Endoscopic laser speckle imaging of tissue blood flow: Applications in the human knee,” J. Orthop. Res. 24(8), 1650–1659 (2006).
    [Crossref] [PubMed]
  33. K. R. Forrester, C. Stewart, C. Leonard, J. Tulip, and R. C. Bray, “Endoscopic laser imaging of tissue perfusion: New instrumentation and technique,” Lasers Surg. Med. 33(3), 151–157 (2003).
    [Crossref] [PubMed]
  34. H. Y. Zhang, P. C. Li, N. Y. Feng, J. J. Qiu, B. Li, W. H. Luo, and Q. M. Luo, “Correcting the detrimental effects of nonuniform intensity distribution on fiber-transmitting laser speckle imaging of blood flow,” Opt. Express 20(1), 508–517 (2012).
    [Crossref] [PubMed]
  35. T. M. Le, J. S. Paul, H. Al-Nashash, A. Tan, A. R. Luft, F. S. Sheu, and S. H. Ong, “New insights into image processing of cortical blood flow monitors using laser speckle imaging,” IEEE Trans. Med Imaging 26(6), 833–842 (2007).
    [Crossref]
  36. H. Y. Cheng, Y. M. Yan, and T. Q. Duong, “Temporal statistical analysis of laser speckle images and its application to retinal blood-flow imaging,” Opt. Express 16(14), 10214–10219 (2008).
    [Crossref] [PubMed]
  37. 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(12), 3749–3764 (2000).
    [Crossref] [PubMed]
  38. C. Kudo, A. Nozari, M. A. Moskowitz, and C. Ayata, “The impact of anesthetics and hyperoxia on cortical spreading depression,” Exp. Neurol. 212(1), 201–206 (2008).
    [Crossref] [PubMed]
  39. A. Mayevsky, N. Zarchin, and C. M. Friedli, “Factors affecting the oxygen balance in the awake cerebral cortex exposed to spreading depression,” Brain Res. 236(1), 93–105 (1982).
    [Crossref] [PubMed]
  40. I. Yuzawa, S. Sakadžić, V. J. Srinivasan, H. K. Shin, K. Eikermann-Haerter, D. A. Boas, and C. Ayata, “Cortical spreading depression impairs oxygen delivery and metabolism in mice,” J. Cereb. Blood Flow Metab. 32(2), 376–386 (2012).
    [Crossref] [PubMed]
  41. J. M. Smith, D. P. Bradley, M. F. James, and C. L. H. Huang, “Physiological studies of cortical spreading depression,” Biol. Rev. Camb. Philos. Soc. 81(4), 457–481 (2006).
    [Crossref] [PubMed]
  42. G. G. Somjen, “Mechanisms of spreading depression and hypoxic spreading depression-like depolarization,” Physiol. Rev. 81(3), 1065–1096 (2001).
    [PubMed]
  43. F. Matyas, V. Sreenivasan, F. Marbach, C. Wacongne, B. Barsy, C. Mateo, R. Aronoff, and C. C. Petersen, “Motor control by sensory cortex,” Science 330(6008), 1240–1243 (2010).
    [Crossref] [PubMed]
  44. J. Sonn and A. Mayevsky, “Effects of anesthesia on the responses to cortical spreading depression in the rat brain in vivo,” Neurol. Res. 28(2), 206–219 (2006).
    [Crossref] [PubMed]
  45. R. C. Guedes and J. M. Barreto, “Effect of anesthesia on the propagation of cortical spreading depression in rats,” Braz. J. Med. Biol. Res. 25(4), 393–397 (1992).
    [PubMed]
  46. Y. Kitahara, K. Taga, H. Abe, and K. Shimoji, “The effects of anesthetics on cortical spreading depression elicitation and c-fos expression in rats,” J. Neurosurg. Anesthesiol. 13(1), 26–32 (2001).
    [Crossref] [PubMed]
  47. A. Van Harreveld and J. S. Stamm, “Effect of pentobarbital and ether on the spreading cortical depression,” Am. J. Physiol. 173(1), 164–170 (1953).
    [PubMed]

2012 (3)

D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo Large-Scale Cortical Mapping Using Channelrhodopsin-2 Stimulation in Transgenic Mice Reveals Asymmetric and Reciprocal Relationships between Cortical Areas,” Front Neural Circuits 6, 11 (2012), doi:.
[Crossref] [PubMed]

H. Y. Zhang, P. C. Li, N. Y. Feng, J. J. Qiu, B. Li, W. H. Luo, and Q. M. Luo, “Correcting the detrimental effects of nonuniform intensity distribution on fiber-transmitting laser speckle imaging of blood flow,” Opt. Express 20(1), 508–517 (2012).
[Crossref] [PubMed]

I. Yuzawa, S. Sakadžić, V. J. Srinivasan, H. K. Shin, K. Eikermann-Haerter, D. A. Boas, and C. Ayata, “Cortical spreading depression impairs oxygen delivery and metabolism in mice,” J. Cereb. Blood Flow Metab. 32(2), 376–386 (2012).
[Crossref] [PubMed]

2011 (2)

X. L. Sun, Y. R. Wang, S. B. Chen, W. H. Luo, P. C. Li, and Q. M. Luo, “Simultaneous monitoring of intracellular pH changes and hemodynamic response during cortical spreading depression by fluorescence-corrected multimodal optical imaging,” Neuroimage 57(3), 873–884 (2011).
[Crossref] [PubMed]

P. Miao, H. Y. Lu, Q. Liu, Y. Li, and S. B. Tong, “Laser speckle contrast imaging of cerebral blood flow in freely moving animals,” J. Biomed. Opt. 16(9), 090502 (2011).
[Crossref] [PubMed]

2010 (4)

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt. 15(1), 011109 (2010).
[Crossref] [PubMed]

C. H. Chen-Bee, T. Agoncillo, C. C. Lay, and R. D. Frostig, “Intrinsic signal optical imaging of brain function using short stimulus delivery intervals,” J. Neurosci. Methods 187(2), 171–182 (2010).
[Crossref] [PubMed]

E. Farkas, F. Bari, and T. P. Obrenovitch, “Multi-modal imaging of anoxic depolarization and hemodynamic changes induced by cardiac arrest in the rat cerebral cortex,” Neuroimage 51(2), 734–742 (2010).
[Crossref] [PubMed]

F. Matyas, V. Sreenivasan, F. Marbach, C. Wacongne, B. Barsy, C. Mateo, R. Aronoff, and C. C. Petersen, “Motor control by sensory cortex,” Science 330(6008), 1240–1243 (2010).
[Crossref] [PubMed]

2009 (5)

T. P. Obrenovitch, S. B. Chen, and E. Farkas, “Simultaneous, live imaging of cortical spreading depression and associated cerebral blood flow changes, by combining voltage-sensitive dye and laser speckle contrast methods,” Neuroimage 45(1), 68–74 (2009).
[Crossref] [PubMed]

Z. C. Luo, Z. J. Yuan, Y. T. Pan, and C. W. Du, “Simultaneous imaging of cortical hemodynamics and blood oxygenation change during cerebral ischemia using dual-wavelength laser speckle contrast imaging,” Opt. Lett. 34(9), 1480–1482 (2009).
[Crossref] [PubMed]

B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in Light Microscopy for Neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
[Crossref] [PubMed]

W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. J. Barretto, J. C. Jung, H. Ra, O. Solgaard, and M. J. Schnitzer, “In vivo brain imaging using a portable 2.9 g two-photon microscope based on a microelectromechanical systems scanning mirror,” Opt. Lett. 34(15), 2309–2311 (2009).
[Crossref] [PubMed]

J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. D. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. U.S.A. 106(46), 19557–19562 (2009).
[Crossref] [PubMed]

2008 (6)

C. J. Engelbrecht, R. S. Johnston, E. J. Seibel, and F. Helmchen, “Ultra-compact fiber-optic two-photon microscope for functional fluorescence imaging in vivo,” Opt. Express 16(8), 5556–5564 (2008).
[Crossref] [PubMed]

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. J. Barretto, T. H. Ko, L. D. Burns, J. C. Jung, and M. J. Schnitzer, “High-speed, miniaturized fluorescence microscopy in freely moving mice,” Nat. Methods 5(11), 935–938 (2008).
[Crossref] [PubMed]

P. J. Drew and D. E. Feldman, “Intrinsic Signal Imaging of Deprivation-Induced Contraction of Whisker Representations in Rat Somatosensory Cortex,” Cereb. Cortex 19(2), 331–348 (2008).
[Crossref] [PubMed]

H. Y. Cheng, Y. M. Yan, and T. Q. Duong, “Temporal statistical analysis of laser speckle images and its application to retinal blood-flow imaging,” Opt. Express 16(14), 10214–10219 (2008).
[Crossref] [PubMed]

C. Kudo, A. Nozari, M. A. Moskowitz, and C. Ayata, “The impact of anesthetics and hyperoxia on cortical spreading depression,” Exp. Neurol. 212(1), 201–206 (2008).
[Crossref] [PubMed]

F. Helmchen and C. C. H. Petersen, “New views into the brain of mice on the move,” Nat. Methods 5(11), 925–926 (2008).
[Crossref] [PubMed]

2007 (2)

C. C. H. Petersen, “The functional organization of the barrel cortex,” Neuron 56(2), 339–355 (2007).
[Crossref] [PubMed]

T. M. Le, J. S. Paul, H. Al-Nashash, A. Tan, A. R. Luft, F. S. Sheu, and S. H. Ong, “New insights into image processing of cortical blood flow monitors using laser speckle imaging,” IEEE Trans. Med Imaging 26(6), 833–842 (2007).
[Crossref]

2006 (5)

R. C. Bray, K. R. Forrester, J. Reed, C. Leonard, and J. Tulip, “Endoscopic laser speckle imaging of tissue blood flow: Applications in the human knee,” J. Orthop. Res. 24(8), 1650–1659 (2006).
[Crossref] [PubMed]

H. K. Shin, A. K. Dunn, P. B. Jones, D. A. Boas, M. A. Moskowitz, and C. Ayata, “Vasoconstrictive neurovascular coupling during focal ischemic depolarizations,” J. Cereb. Blood Flow Metab. 26(8), 1018–1030 (2006).
[Crossref] [PubMed]

I. Ferezou, S. Bolea, and C. C. H. Petersen, “Visualizing the cortical representation of whisker touch: Voltage-sensitive dye imaging in freely moving mice,” Neuron 50(4), 617–629 (2006).
[Crossref] [PubMed]

J. Sonn and A. Mayevsky, “Effects of anesthesia on the responses to cortical spreading depression in the rat brain in vivo,” Neurol. Res. 28(2), 206–219 (2006).
[Crossref] [PubMed]

J. M. Smith, D. P. Bradley, M. F. James, and C. L. H. Huang, “Physiological studies of cortical spreading depression,” Biol. Rev. Camb. Philos. Soc. 81(4), 457–481 (2006).
[Crossref] [PubMed]

2005 (2)

B. A. Flusberg, J. C. Jung, E. D. Cocker, E. P. Anderson, and M. J. Schnitzer, “In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope,” Opt. Lett. 30(17), 2272–2274 (2005).
[Crossref] [PubMed]

A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
[Crossref] [PubMed]

2004 (1)

2003 (4)

J. C. Jung and M. J. Schnitzer, “Multiphoton endoscopy,” Opt. Lett. 28(11), 902–904 (2003).
[Crossref] [PubMed]

A. Devor, A. K. Dunn, M. L. Andermann, I. Ulbert, D. A. Boas, and A. M. Dale, “Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex,” Neuron 39(2), 353–359 (2003).
[Crossref] [PubMed]

K. R. Forrester, C. Stewart, C. Leonard, J. Tulip, and R. C. Bray, “Endoscopic laser imaging of tissue perfusion: New instrumentation and technique,” Lasers Surg. Med. 33(3), 151–157 (2003).
[Crossref] [PubMed]

A. K. Dunn, A. Devor, H. Bolay, M. L. Andermann, M. A. Moskowitz, A. M. Dale, and D. A. Boas, “Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation,” Opt. Lett. 28(1), 28–30 (2003).
[Crossref] [PubMed]

2002 (1)

H. Bolay, U. Reuter, A. K. Dunn, Z. H. Huang, D. A. Boas, and M. A. Moskowitz, “Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model,” Nat. Med. 8(2), 136–142 (2002).
[Crossref] [PubMed]

2001 (6)

C. C. H. Petersen and B. Sakmann, “Functionally independent columns of rat somatosensory barrel cortex revealed with voltage-sensitive dye imaging,” J. Neurosci. 21(21), 8435–8446 (2001).
[PubMed]

F. Helmchen, M. S. Fee, D. W. Tank, and W. Denk, “A miniature head-mounted two-photon microscope. High-resolution brain imaging in freely moving animals,” Neuron 31(6), 903–912 (2001).
[Crossref] [PubMed]

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. Cereb. Blood Flow Metab. 21(3), 195–201 (2001).
[Crossref] [PubMed]

M. Lauritzen, “Cortical spreading depression in migraine,” Cephalalgia 21(7), 757–760 (2001).
[Crossref] [PubMed]

G. G. Somjen, “Mechanisms of spreading depression and hypoxic spreading depression-like depolarization,” Physiol. Rev. 81(3), 1065–1096 (2001).
[PubMed]

Y. Kitahara, K. Taga, H. Abe, and K. Shimoji, “The effects of anesthetics on cortical spreading depression elicitation and c-fos expression in rats,” J. Neurosurg. Anesthesiol. 13(1), 26–32 (2001).
[Crossref] [PubMed]

2000 (2)

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(12), 3749–3764 (2000).
[Crossref] [PubMed]

H. Martins-Ferreira, M. Nedergaard, and C. Nicholson, “Perspectives on spreading depression,” Brain Res. Brain Res. Rev. 32(1), 215–234 (2000).
[Crossref] [PubMed]

1992 (1)

R. C. Guedes and J. M. Barreto, “Effect of anesthesia on the propagation of cortical spreading depression in rats,” Braz. J. Med. Biol. Res. 25(4), 393–397 (1992).
[PubMed]

1986 (1)

A. Grinvald, E. Lieke, R. D. Frostig, C. D. Gilbert, and T. N. Wiesel, “Functional architecture of cortex revealed by optical imaging of intrinsic signals,” Nature 324(6095), 361–364 (1986).
[Crossref] [PubMed]

1982 (1)

A. Mayevsky, N. Zarchin, and C. M. Friedli, “Factors affecting the oxygen balance in the awake cerebral cortex exposed to spreading depression,” Brain Res. 236(1), 93–105 (1982).
[Crossref] [PubMed]

1953 (1)

A. Van Harreveld and J. S. Stamm, “Effect of pentobarbital and ether on the spreading cortical depression,” Am. J. Physiol. 173(1), 164–170 (1953).
[PubMed]

Abe, H.

Y. Kitahara, K. Taga, H. Abe, and K. Shimoji, “The effects of anesthetics on cortical spreading depression elicitation and c-fos expression in rats,” J. Neurosurg. Anesthesiol. 13(1), 26–32 (2001).
[Crossref] [PubMed]

Agoncillo, T.

C. H. Chen-Bee, T. Agoncillo, C. C. Lay, and R. D. Frostig, “Intrinsic signal optical imaging of brain function using short stimulus delivery intervals,” J. Neurosci. Methods 187(2), 171–182 (2010).
[Crossref] [PubMed]

Al-Nashash, H.

T. M. Le, J. S. Paul, H. Al-Nashash, A. Tan, A. R. Luft, F. S. Sheu, and S. H. Ong, “New insights into image processing of cortical blood flow monitors using laser speckle imaging,” IEEE Trans. Med Imaging 26(6), 833–842 (2007).
[Crossref]

Andermann, M. L.

A. K. Dunn, A. Devor, H. Bolay, M. L. Andermann, M. A. Moskowitz, A. M. Dale, and D. A. Boas, “Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation,” Opt. Lett. 28(1), 28–30 (2003).
[Crossref] [PubMed]

A. Devor, A. K. Dunn, M. L. Andermann, I. Ulbert, D. A. Boas, and A. M. Dale, “Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex,” Neuron 39(2), 353–359 (2003).
[Crossref] [PubMed]

Anderson, E. P.

Aronoff, R.

F. Matyas, V. Sreenivasan, F. Marbach, C. Wacongne, B. Barsy, C. Mateo, R. Aronoff, and C. C. Petersen, “Motor control by sensory cortex,” Science 330(6008), 1240–1243 (2010).
[Crossref] [PubMed]

Ayata, C.

I. Yuzawa, S. Sakadžić, V. J. Srinivasan, H. K. Shin, K. Eikermann-Haerter, D. A. Boas, and C. Ayata, “Cortical spreading depression impairs oxygen delivery and metabolism in mice,” J. Cereb. Blood Flow Metab. 32(2), 376–386 (2012).
[Crossref] [PubMed]

C. Kudo, A. Nozari, M. A. Moskowitz, and C. Ayata, “The impact of anesthetics and hyperoxia on cortical spreading depression,” Exp. Neurol. 212(1), 201–206 (2008).
[Crossref] [PubMed]

H. K. Shin, A. K. Dunn, P. B. Jones, D. A. Boas, M. A. Moskowitz, and C. Ayata, “Vasoconstrictive neurovascular coupling during focal ischemic depolarizations,” J. Cereb. Blood Flow Metab. 26(8), 1018–1030 (2006).
[Crossref] [PubMed]

Bari, F.

E. Farkas, F. Bari, and T. P. Obrenovitch, “Multi-modal imaging of anoxic depolarization and hemodynamic changes induced by cardiac arrest in the rat cerebral cortex,” Neuroimage 51(2), 734–742 (2010).
[Crossref] [PubMed]

Barreto, J. M.

R. C. Guedes and J. M. Barreto, “Effect of anesthesia on the propagation of cortical spreading depression in rats,” Braz. J. Med. Biol. Res. 25(4), 393–397 (1992).
[PubMed]

Barretto, R. P. J.

W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. J. Barretto, J. C. Jung, H. Ra, O. Solgaard, and M. J. Schnitzer, “In vivo brain imaging using a portable 2.9 g two-photon microscope based on a microelectromechanical systems scanning mirror,” Opt. Lett. 34(15), 2309–2311 (2009).
[Crossref] [PubMed]

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. J. Barretto, T. H. Ko, L. D. Burns, J. C. Jung, and M. J. Schnitzer, “High-speed, miniaturized fluorescence microscopy in freely moving mice,” Nat. Methods 5(11), 935–938 (2008).
[Crossref] [PubMed]

Barsy, B.

F. Matyas, V. Sreenivasan, F. Marbach, C. Wacongne, B. Barsy, C. Mateo, R. Aronoff, and C. C. Petersen, “Motor control by sensory cortex,” Science 330(6008), 1240–1243 (2010).
[Crossref] [PubMed]

Boas, D. A.

I. Yuzawa, S. Sakadžić, V. J. Srinivasan, H. K. Shin, K. Eikermann-Haerter, D. A. Boas, and C. Ayata, “Cortical spreading depression impairs oxygen delivery and metabolism in mice,” J. Cereb. Blood Flow Metab. 32(2), 376–386 (2012).
[Crossref] [PubMed]

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt. 15(1), 011109 (2010).
[Crossref] [PubMed]

H. K. Shin, A. K. Dunn, P. B. Jones, D. A. Boas, M. A. Moskowitz, and C. Ayata, “Vasoconstrictive neurovascular coupling during focal ischemic depolarizations,” J. Cereb. Blood Flow Metab. 26(8), 1018–1030 (2006).
[Crossref] [PubMed]

A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
[Crossref] [PubMed]

A. Devor, A. K. Dunn, M. L. Andermann, I. Ulbert, D. A. Boas, and A. M. Dale, “Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex,” Neuron 39(2), 353–359 (2003).
[Crossref] [PubMed]

A. K. Dunn, A. Devor, H. Bolay, M. L. Andermann, M. A. Moskowitz, A. M. Dale, and D. A. Boas, “Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation,” Opt. Lett. 28(1), 28–30 (2003).
[Crossref] [PubMed]

H. Bolay, U. Reuter, A. K. Dunn, Z. H. Huang, D. A. Boas, and M. A. Moskowitz, “Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model,” Nat. Med. 8(2), 136–142 (2002).
[Crossref] [PubMed]

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. Cereb. Blood Flow Metab. 21(3), 195–201 (2001).
[Crossref] [PubMed]

Bolay, H.

A. K. Dunn, A. Devor, H. Bolay, M. L. Andermann, M. A. Moskowitz, A. M. Dale, and D. A. Boas, “Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation,” Opt. Lett. 28(1), 28–30 (2003).
[Crossref] [PubMed]

H. Bolay, U. Reuter, A. K. Dunn, Z. H. Huang, D. A. Boas, and M. A. Moskowitz, “Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model,” Nat. Med. 8(2), 136–142 (2002).
[Crossref] [PubMed]

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. Cereb. Blood Flow Metab. 21(3), 195–201 (2001).
[Crossref] [PubMed]

Bolea, S.

I. Ferezou, S. Bolea, and C. C. H. Petersen, “Visualizing the cortical representation of whisker touch: Voltage-sensitive dye imaging in freely moving mice,” Neuron 50(4), 617–629 (2006).
[Crossref] [PubMed]

Boyd, J.

D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo Large-Scale Cortical Mapping Using Channelrhodopsin-2 Stimulation in Transgenic Mice Reveals Asymmetric and Reciprocal Relationships between Cortical Areas,” Front Neural Circuits 6, 11 (2012), doi:.
[Crossref] [PubMed]

Bradley, D. P.

J. M. Smith, D. P. Bradley, M. F. James, and C. L. H. Huang, “Physiological studies of cortical spreading depression,” Biol. Rev. Camb. Philos. Soc. 81(4), 457–481 (2006).
[Crossref] [PubMed]

Bray, R. C.

R. C. Bray, K. R. Forrester, J. Reed, C. Leonard, and J. Tulip, “Endoscopic laser speckle imaging of tissue blood flow: Applications in the human knee,” J. Orthop. Res. 24(8), 1650–1659 (2006).
[Crossref] [PubMed]

K. R. Forrester, C. Stewart, C. Leonard, J. Tulip, and R. C. Bray, “Endoscopic laser imaging of tissue perfusion: New instrumentation and technique,” Lasers Surg. Med. 33(3), 151–157 (2003).
[Crossref] [PubMed]

Burns, L. D.

B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in Light Microscopy for Neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
[Crossref] [PubMed]

W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. J. Barretto, J. C. Jung, H. Ra, O. Solgaard, and M. J. Schnitzer, “In vivo brain imaging using a portable 2.9 g two-photon microscope based on a microelectromechanical systems scanning mirror,” Opt. Lett. 34(15), 2309–2311 (2009).
[Crossref] [PubMed]

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. J. Barretto, T. H. Ko, L. D. Burns, J. C. Jung, and M. J. Schnitzer, “High-speed, miniaturized fluorescence microscopy in freely moving mice,” Nat. Methods 5(11), 935–938 (2008).
[Crossref] [PubMed]

Chen, S.

D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo Large-Scale Cortical Mapping Using Channelrhodopsin-2 Stimulation in Transgenic Mice Reveals Asymmetric and Reciprocal Relationships between Cortical Areas,” Front Neural Circuits 6, 11 (2012), doi:.
[Crossref] [PubMed]

Chen, S. B.

X. L. Sun, Y. R. Wang, S. B. Chen, W. H. Luo, P. C. Li, and Q. M. Luo, “Simultaneous monitoring of intracellular pH changes and hemodynamic response during cortical spreading depression by fluorescence-corrected multimodal optical imaging,” Neuroimage 57(3), 873–884 (2011).
[Crossref] [PubMed]

T. P. Obrenovitch, S. B. Chen, and E. Farkas, “Simultaneous, live imaging of cortical spreading depression and associated cerebral blood flow changes, by combining voltage-sensitive dye and laser speckle contrast methods,” Neuroimage 45(1), 68–74 (2009).
[Crossref] [PubMed]

Chen-Bee, C. H.

C. H. Chen-Bee, T. Agoncillo, C. C. Lay, and R. D. Frostig, “Intrinsic signal optical imaging of brain function using short stimulus delivery intervals,” J. Neurosci. Methods 187(2), 171–182 (2010).
[Crossref] [PubMed]

Cheng, H. Y.

Cocker, E. D.

Dale, A. M.

A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
[Crossref] [PubMed]

A. Devor, A. K. Dunn, M. L. Andermann, I. Ulbert, D. A. Boas, and A. M. Dale, “Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex,” Neuron 39(2), 353–359 (2003).
[Crossref] [PubMed]

A. K. Dunn, A. Devor, H. Bolay, M. L. Andermann, M. A. Moskowitz, A. M. Dale, and D. A. Boas, “Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation,” Opt. Lett. 28(1), 28–30 (2003).
[Crossref] [PubMed]

Denk, W.

J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. D. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. U.S.A. 106(46), 19557–19562 (2009).
[Crossref] [PubMed]

F. Helmchen, M. S. Fee, D. W. Tank, and W. Denk, “A miniature head-mounted two-photon microscope. High-resolution brain imaging in freely moving animals,” Neuron 31(6), 903–912 (2001).
[Crossref] [PubMed]

Devor, A.

A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
[Crossref] [PubMed]

A. Devor, A. K. Dunn, M. L. Andermann, I. Ulbert, D. A. Boas, and A. M. Dale, “Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex,” Neuron 39(2), 353–359 (2003).
[Crossref] [PubMed]

A. K. Dunn, A. Devor, H. Bolay, M. L. Andermann, M. A. Moskowitz, A. M. Dale, and D. A. Boas, “Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation,” Opt. Lett. 28(1), 28–30 (2003).
[Crossref] [PubMed]

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(12), 3749–3764 (2000).
[Crossref] [PubMed]

Drew, P. J.

P. J. Drew and D. E. Feldman, “Intrinsic Signal Imaging of Deprivation-Induced Contraction of Whisker Representations in Rat Somatosensory Cortex,” Cereb. Cortex 19(2), 331–348 (2008).
[Crossref] [PubMed]

Du, C. W.

Dunn, A. K.

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt. 15(1), 011109 (2010).
[Crossref] [PubMed]

H. K. Shin, A. K. Dunn, P. B. Jones, D. A. Boas, M. A. Moskowitz, and C. Ayata, “Vasoconstrictive neurovascular coupling during focal ischemic depolarizations,” J. Cereb. Blood Flow Metab. 26(8), 1018–1030 (2006).
[Crossref] [PubMed]

A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
[Crossref] [PubMed]

A. Devor, A. K. Dunn, M. L. Andermann, I. Ulbert, D. A. Boas, and A. M. Dale, “Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex,” Neuron 39(2), 353–359 (2003).
[Crossref] [PubMed]

A. K. Dunn, A. Devor, H. Bolay, M. L. Andermann, M. A. Moskowitz, A. M. Dale, and D. A. Boas, “Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation,” Opt. Lett. 28(1), 28–30 (2003).
[Crossref] [PubMed]

H. Bolay, U. Reuter, A. K. Dunn, Z. H. Huang, D. A. Boas, and M. A. Moskowitz, “Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model,” Nat. Med. 8(2), 136–142 (2002).
[Crossref] [PubMed]

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. Cereb. Blood Flow Metab. 21(3), 195–201 (2001).
[Crossref] [PubMed]

Duong, T. Q.

Eikermann-Haerter, K.

I. Yuzawa, S. Sakadžić, V. J. Srinivasan, H. K. Shin, K. Eikermann-Haerter, D. A. Boas, and C. Ayata, “Cortical spreading depression impairs oxygen delivery and metabolism in mice,” J. Cereb. Blood Flow Metab. 32(2), 376–386 (2012).
[Crossref] [PubMed]

Engelbrecht, C. J.

Farkas, E.

E. Farkas, F. Bari, and T. P. Obrenovitch, “Multi-modal imaging of anoxic depolarization and hemodynamic changes induced by cardiac arrest in the rat cerebral cortex,” Neuroimage 51(2), 734–742 (2010).
[Crossref] [PubMed]

T. P. Obrenovitch, S. B. Chen, and E. Farkas, “Simultaneous, live imaging of cortical spreading depression and associated cerebral blood flow changes, by combining voltage-sensitive dye and laser speckle contrast methods,” Neuroimage 45(1), 68–74 (2009).
[Crossref] [PubMed]

Fee, M. S.

F. Helmchen, M. S. Fee, D. W. Tank, and W. Denk, “A miniature head-mounted two-photon microscope. High-resolution brain imaging in freely moving animals,” Neuron 31(6), 903–912 (2001).
[Crossref] [PubMed]

Feldman, D. E.

P. J. Drew and D. E. Feldman, “Intrinsic Signal Imaging of Deprivation-Induced Contraction of Whisker Representations in Rat Somatosensory Cortex,” Cereb. Cortex 19(2), 331–348 (2008).
[Crossref] [PubMed]

Feng, N. Y.

Ferezou, I.

I. Ferezou, S. Bolea, and C. C. H. Petersen, “Visualizing the cortical representation of whisker touch: Voltage-sensitive dye imaging in freely moving mice,” Neuron 50(4), 617–629 (2006).
[Crossref] [PubMed]

Flusberg, B. A.

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. J. Barretto, T. H. Ko, L. D. Burns, J. C. Jung, and M. J. Schnitzer, “High-speed, miniaturized fluorescence microscopy in freely moving mice,” Nat. Methods 5(11), 935–938 (2008).
[Crossref] [PubMed]

B. A. Flusberg, J. C. Jung, E. D. Cocker, E. P. Anderson, and M. J. Schnitzer, “In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope,” Opt. Lett. 30(17), 2272–2274 (2005).
[Crossref] [PubMed]

Forrester, K. R.

R. C. Bray, K. R. Forrester, J. Reed, C. Leonard, and J. Tulip, “Endoscopic laser speckle imaging of tissue blood flow: Applications in the human knee,” J. Orthop. Res. 24(8), 1650–1659 (2006).
[Crossref] [PubMed]

K. R. Forrester, C. Stewart, C. Leonard, J. Tulip, and R. C. Bray, “Endoscopic laser imaging of tissue perfusion: New instrumentation and technique,” Lasers Surg. Med. 33(3), 151–157 (2003).
[Crossref] [PubMed]

Friedli, C. M.

A. Mayevsky, N. Zarchin, and C. M. Friedli, “Factors affecting the oxygen balance in the awake cerebral cortex exposed to spreading depression,” Brain Res. 236(1), 93–105 (1982).
[Crossref] [PubMed]

Frostig, R. D.

C. H. Chen-Bee, T. Agoncillo, C. C. Lay, and R. D. Frostig, “Intrinsic signal optical imaging of brain function using short stimulus delivery intervals,” J. Neurosci. Methods 187(2), 171–182 (2010).
[Crossref] [PubMed]

A. Grinvald, E. Lieke, R. D. Frostig, C. D. Gilbert, and T. N. Wiesel, “Functional architecture of cortex revealed by optical imaging of intrinsic signals,” Nature 324(6095), 361–364 (1986).
[Crossref] [PubMed]

Ghosh, K. K.

B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in Light Microscopy for Neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
[Crossref] [PubMed]

Gilbert, C. D.

A. Grinvald, E. Lieke, R. D. Frostig, C. D. Gilbert, and T. N. Wiesel, “Functional architecture of cortex revealed by optical imaging of intrinsic signals,” Nature 324(6095), 361–364 (1986).
[Crossref] [PubMed]

Göbel, W.

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(12), 3749–3764 (2000).
[Crossref] [PubMed]

Greenberg, D. S.

J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. D. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. U.S.A. 106(46), 19557–19562 (2009).
[Crossref] [PubMed]

Grinvald, A.

A. Grinvald, E. Lieke, R. D. Frostig, C. D. Gilbert, and T. N. Wiesel, “Functional architecture of cortex revealed by optical imaging of intrinsic signals,” Nature 324(6095), 361–364 (1986).
[Crossref] [PubMed]

Grossmann, S.

J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. D. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. U.S.A. 106(46), 19557–19562 (2009).
[Crossref] [PubMed]

Guedes, R. C.

R. C. Guedes and J. M. Barreto, “Effect of anesthesia on the propagation of cortical spreading depression in rats,” Braz. J. Med. Biol. Res. 25(4), 393–397 (1992).
[PubMed]

Helmchen, F.

Huang, C. L. H.

J. M. Smith, D. P. Bradley, M. F. James, and C. L. H. Huang, “Physiological studies of cortical spreading depression,” Biol. Rev. Camb. Philos. Soc. 81(4), 457–481 (2006).
[Crossref] [PubMed]

Huang, Z. H.

H. Bolay, U. Reuter, A. K. Dunn, Z. H. Huang, D. A. Boas, and M. A. Moskowitz, “Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model,” Nat. Med. 8(2), 136–142 (2002).
[Crossref] [PubMed]

James, M. F.

J. M. Smith, D. P. Bradley, M. F. James, and C. L. H. Huang, “Physiological studies of cortical spreading depression,” Biol. Rev. Camb. Philos. Soc. 81(4), 457–481 (2006).
[Crossref] [PubMed]

Johnston, R. S.

Jones, P. B.

H. K. Shin, A. K. Dunn, P. B. Jones, D. A. Boas, M. A. Moskowitz, and C. Ayata, “Vasoconstrictive neurovascular coupling during focal ischemic depolarizations,” J. Cereb. Blood Flow Metab. 26(8), 1018–1030 (2006).
[Crossref] [PubMed]

Jung, J. C.

Kerr, J. N. D.

J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. D. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. U.S.A. 106(46), 19557–19562 (2009).
[Crossref] [PubMed]

W. Göbel, J. N. D. Kerr, A. Nimmerjahn, and F. Helmchen, “Miniaturized two-photon microscope based on a flexible coherent fiber bundle and a gradient-index lens objective,” Opt. Lett. 29(21), 2521–2523 (2004).
[Crossref] [PubMed]

Kitahara, Y.

Y. Kitahara, K. Taga, H. Abe, and K. Shimoji, “The effects of anesthetics on cortical spreading depression elicitation and c-fos expression in rats,” J. Neurosurg. Anesthesiol. 13(1), 26–32 (2001).
[Crossref] [PubMed]

Ko, T. H.

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. J. Barretto, T. H. Ko, L. D. Burns, J. C. Jung, and M. J. Schnitzer, “High-speed, miniaturized fluorescence microscopy in freely moving mice,” Nat. Methods 5(11), 935–938 (2008).
[Crossref] [PubMed]

Kohl, M.

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(12), 3749–3764 (2000).
[Crossref] [PubMed]

Kudo, C.

C. Kudo, A. Nozari, M. A. Moskowitz, and C. Ayata, “The impact of anesthetics and hyperoxia on cortical spreading depression,” Exp. Neurol. 212(1), 201–206 (2008).
[Crossref] [PubMed]

Kuhl, M.

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(12), 3749–3764 (2000).
[Crossref] [PubMed]

Lauritzen, M.

M. Lauritzen, “Cortical spreading depression in migraine,” Cephalalgia 21(7), 757–760 (2001).
[Crossref] [PubMed]

Lay, C. C.

C. H. Chen-Bee, T. Agoncillo, C. C. Lay, and R. D. Frostig, “Intrinsic signal optical imaging of brain function using short stimulus delivery intervals,” J. Neurosci. Methods 187(2), 171–182 (2010).
[Crossref] [PubMed]

Le, T. M.

T. M. Le, J. S. Paul, H. Al-Nashash, A. Tan, A. R. Luft, F. S. Sheu, and S. H. Ong, “New insights into image processing of cortical blood flow monitors using laser speckle imaging,” IEEE Trans. Med Imaging 26(6), 833–842 (2007).
[Crossref]

Ledue, J.

D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo Large-Scale Cortical Mapping Using Channelrhodopsin-2 Stimulation in Transgenic Mice Reveals Asymmetric and Reciprocal Relationships between Cortical Areas,” Front Neural Circuits 6, 11 (2012), doi:.
[Crossref] [PubMed]

Leonard, C.

R. C. Bray, K. R. Forrester, J. Reed, C. Leonard, and J. Tulip, “Endoscopic laser speckle imaging of tissue blood flow: Applications in the human knee,” J. Orthop. Res. 24(8), 1650–1659 (2006).
[Crossref] [PubMed]

K. R. Forrester, C. Stewart, C. Leonard, J. Tulip, and R. C. Bray, “Endoscopic laser imaging of tissue perfusion: New instrumentation and technique,” Lasers Surg. Med. 33(3), 151–157 (2003).
[Crossref] [PubMed]

Li, B.

Li, P. C.

H. Y. Zhang, P. C. Li, N. Y. Feng, J. J. Qiu, B. Li, W. H. Luo, and Q. M. Luo, “Correcting the detrimental effects of nonuniform intensity distribution on fiber-transmitting laser speckle imaging of blood flow,” Opt. Express 20(1), 508–517 (2012).
[Crossref] [PubMed]

X. L. Sun, Y. R. Wang, S. B. Chen, W. H. Luo, P. C. Li, and Q. M. Luo, “Simultaneous monitoring of intracellular pH changes and hemodynamic response during cortical spreading depression by fluorescence-corrected multimodal optical imaging,” Neuroimage 57(3), 873–884 (2011).
[Crossref] [PubMed]

Li, Y.

P. Miao, H. Y. Lu, Q. Liu, Y. Li, and S. B. Tong, “Laser speckle contrast imaging of cerebral blood flow in freely moving animals,” J. Biomed. Opt. 16(9), 090502 (2011).
[Crossref] [PubMed]

Lieke, E.

A. Grinvald, E. Lieke, R. D. Frostig, C. D. Gilbert, and T. N. Wiesel, “Functional architecture of cortex revealed by optical imaging of intrinsic signals,” Nature 324(6095), 361–364 (1986).
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Lim, D. H.

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P. Miao, H. Y. Lu, Q. Liu, Y. Li, and S. B. Tong, “Laser speckle contrast imaging of cerebral blood flow in freely moving animals,” J. Biomed. Opt. 16(9), 090502 (2011).
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P. Miao, H. Y. Lu, Q. Liu, Y. Li, and S. B. Tong, “Laser speckle contrast imaging of cerebral blood flow in freely moving animals,” J. Biomed. Opt. 16(9), 090502 (2011).
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T. M. Le, J. S. Paul, H. Al-Nashash, A. Tan, A. R. Luft, F. S. Sheu, and S. H. Ong, “New insights into image processing of cortical blood flow monitors using laser speckle imaging,” IEEE Trans. Med Imaging 26(6), 833–842 (2007).
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F. Matyas, V. Sreenivasan, F. Marbach, C. Wacongne, B. Barsy, C. Mateo, R. Aronoff, and C. C. Petersen, “Motor control by sensory cortex,” Science 330(6008), 1240–1243 (2010).
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F. Matyas, V. Sreenivasan, F. Marbach, C. Wacongne, B. Barsy, C. Mateo, R. Aronoff, and C. C. Petersen, “Motor control by sensory cortex,” Science 330(6008), 1240–1243 (2010).
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P. Miao, H. Y. Lu, Q. Liu, Y. Li, and S. B. Tong, “Laser speckle contrast imaging of cerebral blood flow in freely moving animals,” J. Biomed. Opt. 16(9), 090502 (2011).
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IEEE Trans. Med Imaging (1)

T. M. Le, J. S. Paul, H. Al-Nashash, A. Tan, A. R. Luft, F. S. Sheu, and S. H. Ong, “New insights into image processing of cortical blood flow monitors using laser speckle imaging,” IEEE Trans. Med Imaging 26(6), 833–842 (2007).
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I. Yuzawa, S. Sakadžić, V. J. Srinivasan, H. K. Shin, K. Eikermann-Haerter, D. A. Boas, and C. Ayata, “Cortical spreading depression impairs oxygen delivery and metabolism in mice,” J. Cereb. Blood Flow Metab. 32(2), 376–386 (2012).
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Figures (8)

Fig. 1
Fig. 1

(a) Scheme of the system setup. The mixed light beam transmits down to the cortex through the 1.5-m-long illuminating fiber bundles. The cortex is imaged by the head-mounted microscope, and the image is delivered through an imaging fiber bundle of the same length, the near-end surface of which is coupled to the objective. Multiple images are acquired by the two CCD cameras. (b) A mechanical drawing of the fiber-optic-based head-mounted microscope. (c) GRIN objective lens at working distance. The observation region is coupled to the far-end surface of the fiber bundle. Units are in millimeters.

Fig. 2
Fig. 2

(a) Lin drawing shows the bregma, the location of the craniotomy observation window, and the CSD induction window. (b) (c) (d) are the images of 550-nm OIS, 625-nm OIS and laser speckle blood flow respectively.

Fig. 3
Fig. 3

(a) A 240-g Wistar rat carrying the head-mounted microscope. (b) Resolution test of the head-mounted microscope at high magnification using an Edmund 1951 USAF negative board. The last circle of line-pairs is shown. The line width marked by the arrow is 5.52 µm. (c) Resolution test of the head-mounted microscope at a wide FOV. A 14-line-pairs per millimeter pattern of a positive resolution board was used. The bar represents 1 mm. (d) The cortex is imaged by the head-mounted microscope. (e) The same area imaged by Olympus microscope at the same magnification as (d). (f) Zoom-in images from ROI1 in (d) and ROI2 in (e).

Fig. 4
Fig. 4

(a) Two zoomed-in images of the white boxes show two regions of vessel cross-structures on the cortex: a “V” cross-structure and a “T” cross-structure. Point 1 and point 2 marked by the two white arrows are selected as the measure points of the vessel cross-structures in all the images as the zoomed-in images shown. The geometric center of the image is changeless and is selected as the origin of coordinate. (b) The acceleration of the rat’s head is measured by the accelerometer which is fixed on the rat’s head during the resting and freely moving states. Six time points are pointed out. (c) The relative locations of the two measure points to the origin of coordinate in (a) during the six time points.

Fig. 5
Fig. 5

(a) The fiber bundle (12-µm core, 0.8-mm diameter) is used for illuminating. During resting state the CBF relative change is shown in the left side. During freely moving state it is shown in the right side. (b) A multi-mode fiber (800µm dia.) is used as the illuminating fiber. In resting state the relative change of CBF is shown in the left side. The large artifact of the relative change of CBF caused by the motion of the fiber is shown in the right side. The acceleration is measured by the head fixed accelerometer.

Fig. 6
Fig. 6

Comparison of the time courses of hemodynamic parameters between freely moving and anesthetized states, including 550-nm OIS, 625-nm OIS, CBF, as well as HbO, HbR, and HbT, which were recalculated form dual-wavelength OISs. CSDs were induced at the same time under both freely moving and anesthetized conditions 200 s after signal recording.

Fig. 7
Fig. 7

Spatial spreading patterns of 550-nm OIS, 625-nm OIS, and blood flow signals during CSDs under anesthetized and freely moving states. The upper 2 rows of spreading patterns represent the dual-wavelength OIS changes during CSD at 15-s intervals. The last row shows the CBF spreading patterns in which the time intervals are 30 s and 45 s in freely moving and anesthetized states, respectively. The color bars indicate the relative changes from the baseline. The scale bar represents 1 mm for all images. Note that the CSD wavefronts of the OISs are broader under anesthesia.

Fig. 8
Fig. 8

Statistical analysis of the durations of 550- and 625-nm OISs, CBF, HbO, HbR and HbT related to CSD (n = 8) both in anesthetized and freely moving states. Values are presented as mean ± SD. The vertical axis presents the duration of the CSD (in seconds). The horizontal axis presents the kinds of signals related to CSD. The significance between the groups was *p < 0.05.

Equations (4)

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I n (x,y,i)=I(x,y,i)/ I mean (x,y,i) I mean (x,y,i)= t=i(N1) t=i I(x,y,t) N
log( R 0 / R t )=( ε HbO (λ)Δ c HbO + ε HbR (λ)Δ c HbR )D(λ)
ΔI= ( I t I t+Δt ) / I 0
ΔI= ( I t I 0 ) / I 0

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