Abstract

We report on a miniature label-free imaging system for monitoring brain blood flow and blood oxygenation changes in awake, freely behaving rats. The device, weighing 15 grams, enables imaging in a ∼ 2 × 2 mm field of view with 4.4 μm lateral resolution and 1 − 8 Hz temporal sampling rate. The imaging is performed through a chronically-implanted cranial window that remains optically clear between 2 to > 6 weeks after the craniotomy. This imaging method is well suited for longitudinal studies of chronic models of brain diseases and disorders. In this work, it is applied to monitoring neurovascular coupling during drug-induced absence-like seizures 6 weeks following the craniotomy.

© 2016 Optical Society of America

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref]

2015 (2)

H. Yu, J. Senarathna, B. M. Tyler, N. V. Thakor, and A. P. Pathak, “Miniaturized optical neuroimaging in unrestrained animals,” NeuroImage 113, 397–406 (2015).
[Crossref] [PubMed]

M. A. Cortez, G. K. Kostopoulos, and O. C. Snead, “Acute and chronic pharmacological models of generalized absence seizures,” J. Neurosci. Methods 260, 175–184 (2015).
[Crossref] [PubMed]

2014 (4)

T. Zhang, J. Zhou, R. Jiang, H. Yang, P. R. Carney, and H. Jiang, “Pre-seizure state identified by diffuse optical tomography,” Scientific Reports 4, 3789 (2014).

B. Wang, J. Xiao, and H. Jiang, “Simultaneous real-time 3d photoacoustic tomography and eeg for neurovascular coupling study in an animal model of epilepsy,” J. Neural Eng. 11, 046013 (2014).
[Crossref] [PubMed]

A. Edelstein, M. Tsuchida, N. Amodaj, H. Pinkard, R. Vale, and N. Stuurman, “Advanced methods of microscope control using μmanager software,” J. Biol. Methods 1, e10 (2014).
[Crossref]

T. Durduran and A. G. Yodh, “Diffuse correlation spectroscopy for non-invasive, micro-vascular cerebral blood flow measurement,” NeuroImage 85, 51–63 (2014).
[Crossref]

2013 (2)

2012 (5)

H. Levy, D. Ringuette, and O. Levi, “Rapid monitoring of cerebral ischemia dynamics using laser-based optical imaging of blood oxygenation and flow,” Biomed. Opt. Express 3, 777–791 (2012).
[Crossref] [PubMed]

A. Y. Shih, J. D. Driscoll, P. J. Drew, N. Nishimura, C. B. Schaffer, and D. Kleinfeld, “Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain,” J. Cereb. Blood Flow Metab. 32, 1277–1309 (2012).
[Crossref] [PubMed]

K. Masamoto and I. Kanno, “Anesthesia and the quantitative evaluation of neurovascular coupling,” J. Cereb. Blood Flow Metab. 32, 1233–1247 (2012).
[Crossref] [PubMed]

J. Senarathna, K. Murari, R. Etienne-Cummings, and N. Thakor, “A miniaturized platform for laser speckle contrast imaging,” IEEE Trans. Biomed. Circuits Syst.,  6, 437–445 (2012).
[Crossref]

A. Osman, J. H. Park, D. Dickensheets, J. Platisa, E. Culurciello, and V. A. Pieribone, “Design constraints for mobile, high-speed fluorescence brain imaging in awake animals,” IEEE Trans. Biomed. Circuits Syst. 6, 446–453 (2012).
[Crossref]

2011 (3)

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8, 871–878 (2011).
[Crossref] [PubMed]

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

J. T. Cole and et al., “Craniotomy: true sham for traumatic brain injury, or a sham of a sham?” J. Neurotrauma 28, 359–369 (2011).
[Crossref]

2010 (1)

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

2009 (4)

W. Ou, I. Nissilä, H. Radhakrishnan, D. A. Boas, M. S. Hämäläinen, and M. A. Franceschini, “Study of neurovascular coupling in humans via simultaneous magnetoencephalography and diffuse optical imaging acquisition,” NeuroImage 46, 624–632 (2009).
[Crossref] [PubMed]

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

W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. 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, 2309–2311 (2009).
[Crossref] [PubMed]

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

2008 (3)

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. 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, 935–938 (2008).
[Crossref] [PubMed]

S. J. Kirkpatrick, D. D. Duncan, and E. M. Wells-Gray, “Detrimental effects of speckle-pixel size matching in laser speckle contrast imaging,” Opt. Lett. 33, 2886–2888 (2008).
[Crossref] [PubMed]

R. Mostany and C. Portera-Cailliau, “A craniotomy surgery procedure for chronic brain imaging,” J. Vis. Exp. 18, e680 (2008).

2007 (3)

T. H. Schwartz, “Neurovascular coupling and epilepsy: hemodynamic markers for localizing and predicting seizure onset,” Epilepsy Currents 7, 91–94 (2007).
[Crossref] [PubMed]

D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice,” Neuron 56, 43–57 (2007).
[Crossref] [PubMed]

M. Murayama, E. Pérez-Garci, H.-R. Lüscher, and M. E. Larkum, “Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats,” J. Neurophysiol. 98, 1791–1805 (2007).
[Crossref] [PubMed]

2006 (3)

M. Suh, H. Ma, M. Zhao, S. Sharif, and T. H. Schwartz, “Neurovascular coupling and oximetry during epileptic events,” Molecular Neurobiology 33, 181–197 (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, 1018–1030 (2006).
[Crossref]

H. Girouard and C. Iadecola, “Neurovascular coupling in the normal brain and in hypertension, stroke, and alzheimer disease,” J. Appl. Physiol. 100, 328–335 (2006).
[Crossref]

2005 (3)

A. Devor, I. Ulbert, A. K. Dunn, S. N. Narayanan, S. R. Jones, M. L. Andermann, D. A. Boas, and A. M. Dale, “Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity,” Proc. Natl. Acad. Sci. U.S.A. 102, 3822–3827 (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, 279–290 (2005).
[Crossref] [PubMed]

B. Keogh, D. Cordes, L. Stanberry, B. Figler, C. Robbins, B. Tempel, C. Green, A. Emmi, K. Maravilla, and P. Schwartzkroin, “BOLD-fMRI of PTZ-induced seizures in rats,” Epilepsy Research 66, 75–90 (2005).
[Crossref] [PubMed]

2003 (3)

D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48, 2405–2418 (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, 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, 353–359 (2003).
[Crossref] [PubMed]

2002 (1)

N. Harel, S.-P. Lee, T. Nagaoka, D.-S. Kim, and S.-G. Kim, “Origin of negative blood oxygenation level–dependent fMRI signals,” J. Cereb. Blood Flow Metab. 22, 908–917 (2002).
[Crossref] [PubMed]

2001 (1)

R.-Q. Huang, C. L. Bell-Horner, M. I. Dibas, D. F. Covey, J. A. Drewe, and G. H. Dillon, “Pentylenetetrazole-induced inhibition of recombinant γ-aminobutyric acid type a (gabaa) receptors: mechanism and site of action,” J. Pharm. Exp. Ther. 298, 986–995 (2001).

1988 (1)

R. P. Shockley and J. C. LaManna, “Determination of rat cerebral cortical blood volume changes by capillary mean transit time analysis during hypoxia, hypercapnia and hyperventilation,” Brain Research 454, 170–178 (1988).
[Crossref] [PubMed]

Adelman, T. L.

D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice,” Neuron 56, 43–57 (2007).
[Crossref] [PubMed]

Amodaj, N.

A. Edelstein, M. Tsuchida, N. Amodaj, H. Pinkard, R. Vale, and N. Stuurman, “Advanced methods of microscope control using μmanager software,” J. Biol. Methods 1, e10 (2014).
[Crossref]

Andermann, M. L.

A. Devor, I. Ulbert, A. K. Dunn, S. N. Narayanan, S. R. Jones, M. L. Andermann, D. A. Boas, and A. M. Dale, “Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity,” Proc. Natl. Acad. Sci. U.S.A. 102, 3822–3827 (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, 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, 28–30 (2003).
[Crossref] [PubMed]

Ayata, C.

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, 1018–1030 (2006).
[Crossref]

Barretto, R. P.

W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. 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, 2309–2311 (2009).
[Crossref] [PubMed]

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. 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, 935–938 (2008).
[Crossref] [PubMed]

Bell-Horner, C. L.

R.-Q. Huang, C. L. Bell-Horner, M. I. Dibas, D. F. Covey, J. A. Drewe, and G. H. Dillon, “Pentylenetetrazole-induced inhibition of recombinant γ-aminobutyric acid type a (gabaa) receptors: mechanism and site of action,” J. Pharm. Exp. Ther. 298, 986–995 (2001).

Berger, R. L.

G. Casella and R. L. Berger, Statistical Inference, 2nd ed. (Duxbury Press, Pacific Grove, CA, USA, 2002).

Boas, D. A.

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

W. Ou, I. Nissilä, H. Radhakrishnan, D. A. Boas, M. S. Hämäläinen, and M. A. Franceschini, “Study of neurovascular coupling in humans via simultaneous magnetoencephalography and diffuse optical imaging acquisition,” NeuroImage 46, 624–632 (2009).
[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, 1018–1030 (2006).
[Crossref]

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, 279–290 (2005).
[Crossref] [PubMed]

A. Devor, I. Ulbert, A. K. Dunn, S. N. Narayanan, S. R. Jones, M. L. Andermann, D. A. Boas, and A. M. Dale, “Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity,” Proc. Natl. Acad. Sci. U.S.A. 102, 3822–3827 (2005).
[Crossref] [PubMed]

D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48, 2405–2418 (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, 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, 28–30 (2003).
[Crossref] [PubMed]

Bolay, H.

Brody, C. D.

B. B. Scott, C. D. Brody, and D. W. Tank, “Cellular resolution functional imaging in behaving rats using voluntary head restraint,” Neuron 80, 371–384 (2013).
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W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. 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, 2309–2311 (2009).
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B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. 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, 935–938 (2008).
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T. Zhang, J. Zhou, R. Jiang, H. Yang, P. R. Carney, and H. Jiang, “Pre-seizure state identified by diffuse optical tomography,” Scientific Reports 4, 3789 (2014).

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K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8, 871–878 (2011).
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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, 279–290 (2005).
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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, 353–359 (2003).
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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, 28–30 (2003).
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J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. U.S.A. 106, 19557–19562 (2009).
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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, 279–290 (2005).
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A. Devor, I. Ulbert, A. K. Dunn, S. N. Narayanan, S. R. Jones, M. L. Andermann, D. A. Boas, and A. M. Dale, “Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity,” Proc. Natl. Acad. Sci. U.S.A. 102, 3822–3827 (2005).
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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, 353–359 (2003).
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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, 28–30 (2003).
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R.-Q. Huang, C. L. Bell-Horner, M. I. Dibas, D. F. Covey, J. A. Drewe, and G. H. Dillon, “Pentylenetetrazole-induced inhibition of recombinant γ-aminobutyric acid type a (gabaa) receptors: mechanism and site of action,” J. Pharm. Exp. Ther. 298, 986–995 (2001).

Dickensheets, D.

A. Osman, J. H. Park, D. Dickensheets, J. Platisa, E. Culurciello, and V. A. Pieribone, “Design constraints for mobile, high-speed fluorescence brain imaging in awake animals,” IEEE Trans. Biomed. Circuits Syst. 6, 446–453 (2012).
[Crossref]

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R.-Q. Huang, C. L. Bell-Horner, M. I. Dibas, D. F. Covey, J. A. Drewe, and G. H. Dillon, “Pentylenetetrazole-induced inhibition of recombinant γ-aminobutyric acid type a (gabaa) receptors: mechanism and site of action,” J. Pharm. Exp. Ther. 298, 986–995 (2001).

Dombeck, D. A.

D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice,” Neuron 56, 43–57 (2007).
[Crossref] [PubMed]

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A. Y. Shih, J. D. Driscoll, P. J. Drew, N. Nishimura, C. B. Schaffer, and D. Kleinfeld, “Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain,” J. Cereb. Blood Flow Metab. 32, 1277–1309 (2012).
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R.-Q. Huang, C. L. Bell-Horner, M. I. Dibas, D. F. Covey, J. A. Drewe, and G. H. Dillon, “Pentylenetetrazole-induced inhibition of recombinant γ-aminobutyric acid type a (gabaa) receptors: mechanism and site of action,” J. Pharm. Exp. Ther. 298, 986–995 (2001).

Driscoll, J. D.

A. Y. Shih, J. D. Driscoll, P. J. Drew, N. Nishimura, C. B. Schaffer, and D. Kleinfeld, “Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain,” J. Cereb. Blood Flow Metab. 32, 1277–1309 (2012).
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Duncan, D. D.

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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, 1018–1030 (2006).
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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, 279–290 (2005).
[Crossref] [PubMed]

A. Devor, I. Ulbert, A. K. Dunn, S. N. Narayanan, S. R. Jones, M. L. Andermann, D. A. Boas, and A. M. Dale, “Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity,” Proc. Natl. Acad. Sci. U.S.A. 102, 3822–3827 (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, 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, 28–30 (2003).
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K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8, 871–878 (2011).
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B. Keogh, D. Cordes, L. Stanberry, B. Figler, C. Robbins, B. Tempel, C. Green, A. Emmi, K. Maravilla, and P. Schwartzkroin, “BOLD-fMRI of PTZ-induced seizures in rats,” Epilepsy Research 66, 75–90 (2005).
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B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. 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, 935–938 (2008).
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K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8, 871–878 (2011).
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J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. U.S.A. 106, 19557–19562 (2009).
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J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. U.S.A. 106, 19557–19562 (2009).
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D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48, 2405–2418 (2003).
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H. Girouard and C. Iadecola, “Neurovascular coupling in the normal brain and in hypertension, stroke, and alzheimer disease,” J. Appl. Physiol. 100, 328–335 (2006).
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D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48, 2405–2418 (2003).
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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, 1018–1030 (2006).
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A. Devor, I. Ulbert, A. K. Dunn, S. N. Narayanan, S. R. Jones, M. L. Andermann, D. A. Boas, and A. M. Dale, “Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity,” Proc. Natl. Acad. Sci. U.S.A. 102, 3822–3827 (2005).
[Crossref] [PubMed]

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W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. 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, 2309–2311 (2009).
[Crossref] [PubMed]

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. 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, 935–938 (2008).
[Crossref] [PubMed]

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K. Masamoto and I. Kanno, “Anesthesia and the quantitative evaluation of neurovascular coupling,” J. Cereb. Blood Flow Metab. 32, 1233–1247 (2012).
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B. Keogh, D. Cordes, L. Stanberry, B. Figler, C. Robbins, B. Tempel, C. Green, A. Emmi, K. Maravilla, and P. Schwartzkroin, “BOLD-fMRI of PTZ-induced seizures in rats,” Epilepsy Research 66, 75–90 (2005).
[Crossref] [PubMed]

Kerr, J. N.

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

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D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice,” Neuron 56, 43–57 (2007).
[Crossref] [PubMed]

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N. Harel, S.-P. Lee, T. Nagaoka, D.-S. Kim, and S.-G. Kim, “Origin of negative blood oxygenation level–dependent fMRI signals,” J. Cereb. Blood Flow Metab. 22, 908–917 (2002).
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N. Harel, S.-P. Lee, T. Nagaoka, D.-S. Kim, and S.-G. Kim, “Origin of negative blood oxygenation level–dependent fMRI signals,” J. Cereb. Blood Flow Metab. 22, 908–917 (2002).
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Kleinfeld, D.

A. Y. Shih, J. D. Driscoll, P. J. Drew, N. Nishimura, C. B. Schaffer, and D. Kleinfeld, “Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain,” J. Cereb. Blood Flow Metab. 32, 1277–1309 (2012).
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B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. 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, 935–938 (2008).
[Crossref] [PubMed]

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M. A. Cortez, G. K. Kostopoulos, and O. C. Snead, “Acute and chronic pharmacological models of generalized absence seizures,” J. Neurosci. Methods 260, 175–184 (2015).
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N. Harel, S.-P. Lee, T. Nagaoka, D.-S. Kim, and S.-G. Kim, “Origin of negative blood oxygenation level–dependent fMRI signals,” J. Cereb. Blood Flow Metab. 22, 908–917 (2002).
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Levy, H.

Li, B.

Li, P.

Li, Y.

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

Lu, H.

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

Luo, Q.

Luo, Z.

Lüscher, H.-R.

M. Murayama, E. Pérez-Garci, H.-R. Lüscher, and M. E. Larkum, “Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats,” J. Neurophysiol. 98, 1791–1805 (2007).
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B. Keogh, D. Cordes, L. Stanberry, B. Figler, C. Robbins, B. Tempel, C. Green, A. Emmi, K. Maravilla, and P. Schwartzkroin, “BOLD-fMRI of PTZ-induced seizures in rats,” Epilepsy Research 66, 75–90 (2005).
[Crossref] [PubMed]

Masamoto, K.

K. Masamoto and I. Kanno, “Anesthesia and the quantitative evaluation of neurovascular coupling,” J. Cereb. Blood Flow Metab. 32, 1233–1247 (2012).
[Crossref] [PubMed]

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P. Miao, H. Lu, Q. Liu, Y. Li, and S. Tong, “Laser speckle contrast imaging of cerebral blood flow in freely moving animals,” J. Biomed. Opt. 16, 090502 (2011).
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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, 1018–1030 (2006).
[Crossref]

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, 28–30 (2003).
[Crossref] [PubMed]

Mostany, R.

R. Mostany and C. Portera-Cailliau, “A craniotomy surgery procedure for chronic brain imaging,” J. Vis. Exp. 18, e680 (2008).

Mukamel, E. A.

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. 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, 935–938 (2008).
[Crossref] [PubMed]

Murari, K.

J. Senarathna, K. Murari, R. Etienne-Cummings, and N. Thakor, “A miniaturized platform for laser speckle contrast imaging,” IEEE Trans. Biomed. Circuits Syst.,  6, 437–445 (2012).
[Crossref]

Murayama, M.

M. Murayama, E. Pérez-Garci, H.-R. Lüscher, and M. E. Larkum, “Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats,” J. Neurophysiol. 98, 1791–1805 (2007).
[Crossref] [PubMed]

Nagaoka, T.

N. Harel, S.-P. Lee, T. Nagaoka, D.-S. Kim, and S.-G. Kim, “Origin of negative blood oxygenation level–dependent fMRI signals,” J. Cereb. Blood Flow Metab. 22, 908–917 (2002).
[Crossref] [PubMed]

Narayanan, S. N.

A. Devor, I. Ulbert, A. K. Dunn, S. N. Narayanan, S. R. Jones, M. L. Andermann, D. A. Boas, and A. M. Dale, “Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity,” Proc. Natl. Acad. Sci. U.S.A. 102, 3822–3827 (2005).
[Crossref] [PubMed]

Nimmerjahn, A.

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8, 871–878 (2011).
[Crossref] [PubMed]

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. 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, 935–938 (2008).
[Crossref] [PubMed]

Nishimura, N.

A. Y. Shih, J. D. Driscoll, P. J. Drew, N. Nishimura, C. B. Schaffer, and D. Kleinfeld, “Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain,” J. Cereb. Blood Flow Metab. 32, 1277–1309 (2012).
[Crossref] [PubMed]

Nissilä, I.

W. Ou, I. Nissilä, H. Radhakrishnan, D. A. Boas, M. S. Hämäläinen, and M. A. Franceschini, “Study of neurovascular coupling in humans via simultaneous magnetoencephalography and diffuse optical imaging acquisition,” NeuroImage 46, 624–632 (2009).
[Crossref] [PubMed]

Osman, A.

A. Osman, J. H. Park, D. Dickensheets, J. Platisa, E. Culurciello, and V. A. Pieribone, “Design constraints for mobile, high-speed fluorescence brain imaging in awake animals,” IEEE Trans. Biomed. Circuits Syst. 6, 446–453 (2012).
[Crossref]

Ou, W.

W. Ou, I. Nissilä, H. Radhakrishnan, D. A. Boas, M. S. Hämäläinen, and M. A. Franceschini, “Study of neurovascular coupling in humans via simultaneous magnetoencephalography and diffuse optical imaging acquisition,” NeuroImage 46, 624–632 (2009).
[Crossref] [PubMed]

Pan, Y.

Park, J. H.

A. Osman, J. H. Park, D. Dickensheets, J. Platisa, E. Culurciello, and V. A. Pieribone, “Design constraints for mobile, high-speed fluorescence brain imaging in awake animals,” IEEE Trans. Biomed. Circuits Syst. 6, 446–453 (2012).
[Crossref]

Pathak, A. P.

H. Yu, J. Senarathna, B. M. Tyler, N. V. Thakor, and A. P. Pathak, “Miniaturized optical neuroimaging in unrestrained animals,” NeuroImage 113, 397–406 (2015).
[Crossref] [PubMed]

Pérez-Garci, E.

M. Murayama, E. Pérez-Garci, H.-R. Lüscher, and M. E. Larkum, “Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats,” J. Neurophysiol. 98, 1791–1805 (2007).
[Crossref] [PubMed]

Pieribone, V. A.

A. Osman, J. H. Park, D. Dickensheets, J. Platisa, E. Culurciello, and V. A. Pieribone, “Design constraints for mobile, high-speed fluorescence brain imaging in awake animals,” IEEE Trans. Biomed. Circuits Syst. 6, 446–453 (2012).
[Crossref]

Pinkard, H.

A. Edelstein, M. Tsuchida, N. Amodaj, H. Pinkard, R. Vale, and N. Stuurman, “Advanced methods of microscope control using μmanager software,” J. Biol. Methods 1, e10 (2014).
[Crossref]

Pitkänen, A.

A. Pitkänen, P. A. Schwartzkroin, and S. L. Moshé, Models of seizures and epilepsy (Academic Press, Burlington, MA, USA, 2005).

Piyawattanametha, W.

Platisa, J.

A. Osman, J. H. Park, D. Dickensheets, J. Platisa, E. Culurciello, and V. A. Pieribone, “Design constraints for mobile, high-speed fluorescence brain imaging in awake animals,” IEEE Trans. Biomed. Circuits Syst. 6, 446–453 (2012).
[Crossref]

Poldrack, R. A.

D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48, 2405–2418 (2003).
[Crossref] [PubMed]

Portera-Cailliau, C.

R. Mostany and C. Portera-Cailliau, “A craniotomy surgery procedure for chronic brain imaging,” J. Vis. Exp. 18, e680 (2008).

Ra, H.

Radhakrishnan, H.

W. Ou, I. Nissilä, H. Radhakrishnan, D. A. Boas, M. S. Hämäläinen, and M. A. Franceschini, “Study of neurovascular coupling in humans via simultaneous magnetoencephalography and diffuse optical imaging acquisition,” NeuroImage 46, 624–632 (2009).
[Crossref] [PubMed]

Ringuette, D.

Robbins, C.

B. Keogh, D. Cordes, L. Stanberry, B. Figler, C. Robbins, B. Tempel, C. Green, A. Emmi, K. Maravilla, and P. Schwartzkroin, “BOLD-fMRI of PTZ-induced seizures in rats,” Epilepsy Research 66, 75–90 (2005).
[Crossref] [PubMed]

Rosen, B. R.

D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48, 2405–2418 (2003).
[Crossref] [PubMed]

Sawinski, J.

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

Schaffer, C. B.

A. Y. Shih, J. D. Driscoll, P. J. Drew, N. Nishimura, C. B. Schaffer, and D. Kleinfeld, “Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain,” J. Cereb. Blood Flow Metab. 32, 1277–1309 (2012).
[Crossref] [PubMed]

Schnitzer, M. J.

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8, 871–878 (2011).
[Crossref] [PubMed]

W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. 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, 2309–2311 (2009).
[Crossref] [PubMed]

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. 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, 935–938 (2008).
[Crossref] [PubMed]

Schwartz, T. H.

T. H. Schwartz, “Neurovascular coupling and epilepsy: hemodynamic markers for localizing and predicting seizure onset,” Epilepsy Currents 7, 91–94 (2007).
[Crossref] [PubMed]

M. Suh, H. Ma, M. Zhao, S. Sharif, and T. H. Schwartz, “Neurovascular coupling and oximetry during epileptic events,” Molecular Neurobiology 33, 181–197 (2006).
[Crossref] [PubMed]

Schwartzkroin, P.

B. Keogh, D. Cordes, L. Stanberry, B. Figler, C. Robbins, B. Tempel, C. Green, A. Emmi, K. Maravilla, and P. Schwartzkroin, “BOLD-fMRI of PTZ-induced seizures in rats,” Epilepsy Research 66, 75–90 (2005).
[Crossref] [PubMed]

Schwartzkroin, P. A.

A. Pitkänen, P. A. Schwartzkroin, and S. L. Moshé, Models of seizures and epilepsy (Academic Press, Burlington, MA, USA, 2005).

Scott, B. B.

B. B. Scott, C. D. Brody, and D. W. Tank, “Cellular resolution functional imaging in behaving rats using voluntary head restraint,” Neuron 80, 371–384 (2013).
[Crossref] [PubMed]

Senarathna, J.

H. Yu, J. Senarathna, B. M. Tyler, N. V. Thakor, and A. P. Pathak, “Miniaturized optical neuroimaging in unrestrained animals,” NeuroImage 113, 397–406 (2015).
[Crossref] [PubMed]

J. Senarathna, K. Murari, R. Etienne-Cummings, and N. Thakor, “A miniaturized platform for laser speckle contrast imaging,” IEEE Trans. Biomed. Circuits Syst.,  6, 437–445 (2012).
[Crossref]

Sharif, S.

M. Suh, H. Ma, M. Zhao, S. Sharif, and T. H. Schwartz, “Neurovascular coupling and oximetry during epileptic events,” Molecular Neurobiology 33, 181–197 (2006).
[Crossref] [PubMed]

Shih, A. Y.

A. Y. Shih, J. D. Driscoll, P. J. Drew, N. Nishimura, C. B. Schaffer, and D. Kleinfeld, “Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain,” J. Cereb. Blood Flow Metab. 32, 1277–1309 (2012).
[Crossref] [PubMed]

Shin, H. K.

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, 1018–1030 (2006).
[Crossref]

Shockley, R. P.

R. P. Shockley and J. C. LaManna, “Determination of rat cerebral cortical blood volume changes by capillary mean transit time analysis during hypoxia, hypercapnia and hyperventilation,” Brain Research 454, 170–178 (1988).
[Crossref] [PubMed]

Snead, O. C.

M. A. Cortez, G. K. Kostopoulos, and O. C. Snead, “Acute and chronic pharmacological models of generalized absence seizures,” J. Neurosci. Methods 260, 175–184 (2015).
[Crossref] [PubMed]

Solgaard, O.

Stanberry, L.

B. Keogh, D. Cordes, L. Stanberry, B. Figler, C. Robbins, B. Tempel, C. Green, A. Emmi, K. Maravilla, and P. Schwartzkroin, “BOLD-fMRI of PTZ-induced seizures in rats,” Epilepsy Research 66, 75–90 (2005).
[Crossref] [PubMed]

Strangman, G.

D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48, 2405–2418 (2003).
[Crossref] [PubMed]

Stuurman, N.

A. Edelstein, M. Tsuchida, N. Amodaj, H. Pinkard, R. Vale, and N. Stuurman, “Advanced methods of microscope control using μmanager software,” J. Biol. Methods 1, e10 (2014).
[Crossref]

Suh, M.

M. Suh, H. Ma, M. Zhao, S. Sharif, and T. H. Schwartz, “Neurovascular coupling and oximetry during epileptic events,” Molecular Neurobiology 33, 181–197 (2006).
[Crossref] [PubMed]

Tank, D. W.

B. B. Scott, C. D. Brody, and D. W. Tank, “Cellular resolution functional imaging in behaving rats using voluntary head restraint,” Neuron 80, 371–384 (2013).
[Crossref] [PubMed]

D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice,” Neuron 56, 43–57 (2007).
[Crossref] [PubMed]

Tempel, B.

B. Keogh, D. Cordes, L. Stanberry, B. Figler, C. Robbins, B. Tempel, C. Green, A. Emmi, K. Maravilla, and P. Schwartzkroin, “BOLD-fMRI of PTZ-induced seizures in rats,” Epilepsy Research 66, 75–90 (2005).
[Crossref] [PubMed]

Thakor, N.

J. Senarathna, K. Murari, R. Etienne-Cummings, and N. Thakor, “A miniaturized platform for laser speckle contrast imaging,” IEEE Trans. Biomed. Circuits Syst.,  6, 437–445 (2012).
[Crossref]

Thakor, N. V.

H. Yu, J. Senarathna, B. M. Tyler, N. V. Thakor, and A. P. Pathak, “Miniaturized optical neuroimaging in unrestrained animals,” NeuroImage 113, 397–406 (2015).
[Crossref] [PubMed]

Tong, S.

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

H. Lu, P. Miao, Q. Liu, Y. Li, and S. Tong, “Dual-modal (OIS/LSCI) imager of cerebral cortex in freely moving animals,” in “Photonics and Optoelectronics Meetings 2011,” (SPIE, 2012), p. 83290P.

Tsuchida, M.

A. Edelstein, M. Tsuchida, N. Amodaj, H. Pinkard, R. Vale, and N. Stuurman, “Advanced methods of microscope control using μmanager software,” J. Biol. Methods 1, e10 (2014).
[Crossref]

Tyler, B. M.

H. Yu, J. Senarathna, B. M. Tyler, N. V. Thakor, and A. P. Pathak, “Miniaturized optical neuroimaging in unrestrained animals,” NeuroImage 113, 397–406 (2015).
[Crossref] [PubMed]

Ulbert, I.

A. Devor, I. Ulbert, A. K. Dunn, S. N. Narayanan, S. R. Jones, M. L. Andermann, D. A. Boas, and A. M. Dale, “Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity,” Proc. Natl. Acad. Sci. U.S.A. 102, 3822–3827 (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, 353–359 (2003).
[Crossref] [PubMed]

Vale, R.

A. Edelstein, M. Tsuchida, N. Amodaj, H. Pinkard, R. Vale, and N. Stuurman, “Advanced methods of microscope control using μmanager software,” J. Biol. Methods 1, e10 (2014).
[Crossref]

Wallace, D. J.

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

Wang, B.

B. Wang, J. Xiao, and H. Jiang, “Simultaneous real-time 3d photoacoustic tomography and eeg for neurovascular coupling study in an animal model of epilepsy,” J. Neural Eng. 11, 046013 (2014).
[Crossref] [PubMed]

Wang, J.

Wells-Gray, E. M.

Xiao, J.

B. Wang, J. Xiao, and H. Jiang, “Simultaneous real-time 3d photoacoustic tomography and eeg for neurovascular coupling study in an animal model of epilepsy,” J. Neural Eng. 11, 046013 (2014).
[Crossref] [PubMed]

Yang, H.

T. Zhang, J. Zhou, R. Jiang, H. Yang, P. R. Carney, and H. Jiang, “Pre-seizure state identified by diffuse optical tomography,” Scientific Reports 4, 3789 (2014).

Yin, C.

Yodh, A. G.

T. Durduran and A. G. Yodh, “Diffuse correlation spectroscopy for non-invasive, micro-vascular cerebral blood flow measurement,” NeuroImage 85, 51–63 (2014).
[Crossref]

Yu, H.

H. Yu, J. Senarathna, B. M. Tyler, N. V. Thakor, and A. P. Pathak, “Miniaturized optical neuroimaging in unrestrained animals,” NeuroImage 113, 397–406 (2015).
[Crossref] [PubMed]

Yuan, Z.

Zhang, T.

T. Zhang, J. Zhou, R. Jiang, H. Yang, P. R. Carney, and H. Jiang, “Pre-seizure state identified by diffuse optical tomography,” Scientific Reports 4, 3789 (2014).

Zhao, M.

M. Suh, H. Ma, M. Zhao, S. Sharif, and T. H. Schwartz, “Neurovascular coupling and oximetry during epileptic events,” Molecular Neurobiology 33, 181–197 (2006).
[Crossref] [PubMed]

Zhou, J.

T. Zhang, J. Zhou, R. Jiang, H. Yang, P. R. Carney, and H. Jiang, “Pre-seizure state identified by diffuse optical tomography,” Scientific Reports 4, 3789 (2014).

Ziv, Y.

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8, 871–878 (2011).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

Brain Research (1)

R. P. Shockley and J. C. LaManna, “Determination of rat cerebral cortical blood volume changes by capillary mean transit time analysis during hypoxia, hypercapnia and hyperventilation,” Brain Research 454, 170–178 (1988).
[Crossref] [PubMed]

Epilepsy Currents (1)

T. H. Schwartz, “Neurovascular coupling and epilepsy: hemodynamic markers for localizing and predicting seizure onset,” Epilepsy Currents 7, 91–94 (2007).
[Crossref] [PubMed]

Epilepsy Research (1)

B. Keogh, D. Cordes, L. Stanberry, B. Figler, C. Robbins, B. Tempel, C. Green, A. Emmi, K. Maravilla, and P. Schwartzkroin, “BOLD-fMRI of PTZ-induced seizures in rats,” Epilepsy Research 66, 75–90 (2005).
[Crossref] [PubMed]

IEEE Trans. Biomed. Circuits Syst. (2)

J. Senarathna, K. Murari, R. Etienne-Cummings, and N. Thakor, “A miniaturized platform for laser speckle contrast imaging,” IEEE Trans. Biomed. Circuits Syst.,  6, 437–445 (2012).
[Crossref]

A. Osman, J. H. Park, D. Dickensheets, J. Platisa, E. Culurciello, and V. A. Pieribone, “Design constraints for mobile, high-speed fluorescence brain imaging in awake animals,” IEEE Trans. Biomed. Circuits Syst. 6, 446–453 (2012).
[Crossref]

J. Appl. Physiol. (1)

H. Girouard and C. Iadecola, “Neurovascular coupling in the normal brain and in hypertension, stroke, and alzheimer disease,” J. Appl. Physiol. 100, 328–335 (2006).
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J. Biol. Methods (1)

A. Edelstein, M. Tsuchida, N. Amodaj, H. Pinkard, R. Vale, and N. Stuurman, “Advanced methods of microscope control using μmanager software,” J. Biol. Methods 1, e10 (2014).
[Crossref]

J. Biomed. Opt. (2)

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

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt. 15, 011109 (2010).
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J. Cereb. Blood Flow Metab. (4)

K. Masamoto and I. Kanno, “Anesthesia and the quantitative evaluation of neurovascular coupling,” J. Cereb. Blood Flow Metab. 32, 1233–1247 (2012).
[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, 1018–1030 (2006).
[Crossref]

A. Y. Shih, J. D. Driscoll, P. J. Drew, N. Nishimura, C. B. Schaffer, and D. Kleinfeld, “Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain,” J. Cereb. Blood Flow Metab. 32, 1277–1309 (2012).
[Crossref] [PubMed]

N. Harel, S.-P. Lee, T. Nagaoka, D.-S. Kim, and S.-G. Kim, “Origin of negative blood oxygenation level–dependent fMRI signals,” J. Cereb. Blood Flow Metab. 22, 908–917 (2002).
[Crossref] [PubMed]

J. Neural Eng. (1)

B. Wang, J. Xiao, and H. Jiang, “Simultaneous real-time 3d photoacoustic tomography and eeg for neurovascular coupling study in an animal model of epilepsy,” J. Neural Eng. 11, 046013 (2014).
[Crossref] [PubMed]

J. Neurophysiol. (1)

M. Murayama, E. Pérez-Garci, H.-R. Lüscher, and M. E. Larkum, “Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats,” J. Neurophysiol. 98, 1791–1805 (2007).
[Crossref] [PubMed]

J. Neurosci. Methods (1)

M. A. Cortez, G. K. Kostopoulos, and O. C. Snead, “Acute and chronic pharmacological models of generalized absence seizures,” J. Neurosci. Methods 260, 175–184 (2015).
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J. Neurotrauma (1)

J. T. Cole and et al., “Craniotomy: true sham for traumatic brain injury, or a sham of a sham?” J. Neurotrauma 28, 359–369 (2011).
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J. Pharm. Exp. Ther. (1)

R.-Q. Huang, C. L. Bell-Horner, M. I. Dibas, D. F. Covey, J. A. Drewe, and G. H. Dillon, “Pentylenetetrazole-induced inhibition of recombinant γ-aminobutyric acid type a (gabaa) receptors: mechanism and site of action,” J. Pharm. Exp. Ther. 298, 986–995 (2001).

J. Vis. Exp. (1)

R. Mostany and C. Portera-Cailliau, “A craniotomy surgery procedure for chronic brain imaging,” J. Vis. Exp. 18, e680 (2008).

Molecular Neurobiology (1)

M. Suh, H. Ma, M. Zhao, S. Sharif, and T. H. Schwartz, “Neurovascular coupling and oximetry during epileptic events,” Molecular Neurobiology 33, 181–197 (2006).
[Crossref] [PubMed]

Nat. Methods (2)

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. 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, 935–938 (2008).
[Crossref] [PubMed]

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8, 871–878 (2011).
[Crossref] [PubMed]

NeuroImage (4)

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, 279–290 (2005).
[Crossref] [PubMed]

H. Yu, J. Senarathna, B. M. Tyler, N. V. Thakor, and A. P. Pathak, “Miniaturized optical neuroimaging in unrestrained animals,” NeuroImage 113, 397–406 (2015).
[Crossref] [PubMed]

W. Ou, I. Nissilä, H. Radhakrishnan, D. A. Boas, M. S. Hämäläinen, and M. A. Franceschini, “Study of neurovascular coupling in humans via simultaneous magnetoencephalography and diffuse optical imaging acquisition,” NeuroImage 46, 624–632 (2009).
[Crossref] [PubMed]

T. Durduran and A. G. Yodh, “Diffuse correlation spectroscopy for non-invasive, micro-vascular cerebral blood flow measurement,” NeuroImage 85, 51–63 (2014).
[Crossref]

Neuron (3)

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, 353–359 (2003).
[Crossref] [PubMed]

D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice,” Neuron 56, 43–57 (2007).
[Crossref] [PubMed]

B. B. Scott, C. D. Brody, and D. W. Tank, “Cellular resolution functional imaging in behaving rats using voluntary head restraint,” Neuron 80, 371–384 (2013).
[Crossref] [PubMed]

Opt. Express (1)

Opt. Lett. (4)

Phys. Med. Biol. (1)

D. A. Boas, G. Strangman, J. P. Culver, R. D. Hoge, G. Jasdzewski, R. A. Poldrack, B. R. Rosen, and J. B. Mandeville, “Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy?” Phys. Med. Biol. 48, 2405–2418 (2003).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (2)

A. Devor, I. Ulbert, A. K. Dunn, S. N. Narayanan, S. R. Jones, M. L. Andermann, D. A. Boas, and A. M. Dale, “Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity,” Proc. Natl. Acad. Sci. U.S.A. 102, 3822–3827 (2005).
[Crossref] [PubMed]

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

Scientific Reports (1)

T. Zhang, J. Zhou, R. Jiang, H. Yang, P. R. Carney, and H. Jiang, “Pre-seizure state identified by diffuse optical tomography,” Scientific Reports 4, 3789 (2014).

Other (3)

A. Pitkänen, P. A. Schwartzkroin, and S. L. Moshé, Models of seizures and epilepsy (Academic Press, Burlington, MA, USA, 2005).

G. Casella and R. L. Berger, Statistical Inference, 2nd ed. (Duxbury Press, Pacific Grove, CA, USA, 2002).

H. Lu, P. Miao, Q. Liu, Y. Li, and S. Tong, “Dual-modal (OIS/LSCI) imager of cerebral cortex in freely moving animals,” in “Photonics and Optoelectronics Meetings 2011,” (SPIE, 2012), p. 83290P.

Supplementary Material (2)

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Figures (7)

Fig. 1
Fig. 1 Miniature head-mounted imaging system for monitoring rat brain hemodynamics. a) Device schematic. Insets: the imaging tube (top left), skull adapter plate (bottom left), and the light source module (bottom right). b) System diagram. c) Image of a USAF resolution target: computed contrast values are 11.5% at 161 lp/mm, 15% at 144 lp/mm, 19% at 128 lp/mm. d) Brain imaged through the chronic cranial window.
Fig. 2
Fig. 2 LSCI-derived relative flow speed maps in a rat, imaged through a chronic cranial window. Each tile depicts a flow speed map imaged weekly, from 2nd to 6th week following a craniotomy. The flow speeds in the arterial and parenchymal regions vary within ±10% across 5 weeks of measurement. Scale bar is 0.5 mm.
Fig. 3
Fig. 3 a) A photograph of the rat exploring the imaging chamber with the skull-mounted imaging system. b) An LSCI-derived blood flow map. Inset: flow speed intensity scale, in arbitrary units. Highlighted are three areas used for generating the time courses for subsequent vascular analysis: vein (blue), artery (red), and the parenchymal region (yellow). c) Time course of the normalized blood flow speeds in the artery (red) and vein (blue). d) Time course of changes in HbO (cyan) and HbR (magenta) in the vein. Two time points are marked with vertical dashed lines: t = −1.8 min marks the time when the animal was picked up from the imaging chamber, and t = 0 min marks the time of PTZ injection.
Fig. 4
Fig. 4 Time courses of hemodynamic response between 8 and 20 minutes following PTZ injection. a) Changes in normalized blood flow speeds in artery (red), vein (blue), and parenchymal region (dark green). b) Changes in HbO in the artery (black), vein, (green) and parenchymal region (brown). c) Changes in HbR in the artery (cyan), vein (magenta), and parenchymal region (dark blue).
Fig. 5
Fig. 5 Mean Changes in hemodynamic activity prior to, and immediately after, onset of motor arrest. All curves represent average time courses of 39 seizures during a single imaging session in a single animal, superimposed on a time scale where T = 0 sec is the seizure onset, characterized by motor arrest. Error bars represent 95% confidence bounds on the mean standard error. a) arterial flow speed, b) venous flow speed, c) parenchymal flow speed, d) arterial HbO concentration, e) venous HbO concentration, f) parenchymal HbO concentration, g) arterial HbR concentration, h) venous HbR concentration, i) parenchymal HbR concentration
Fig. 6
Fig. 6 Mean changes in the flow speeds (top two rows), HbO (middle two rows), and HbR (bottom two rows) across the full ROI. Each tile corresponds to a time point on the horizontal axis in Fig. 5, in seconds. t = 0 s correspond to onset of motor arrest, coinciding with the shaded gray region in Fig. 5. The first and last tiles, at t = −10 s and t = 9 s, respectively, were removed to improve visual clarity in print. The figure represents a single imaging session in a single animal
Fig. 7
Fig. 7 Hemodynamic response of a rat to handling and IP bolus injection. t = 0: isoflurance was turned off and the rat was allowed to recover. There are 4 vertical dashed lines that mark time points of interest: 4:20 min: rat regained consciousness, 5:15 min: rat was transferred to the imaging chamber, 15:45 min: the animal was picked up, removed from the chamber, and placed on its side. No injection took place. 22:50 min: 1 mL bolous saline was delivered via an IP injection. a) Changes in blood flow speeds, normalized to the mean baseline value, between t = 7 − 12 min. b) Changes in HbO. c) Changes in HbR.

Tables (1)

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Table 1 Mean changes in monitored hemodynamic parameters during motor arrest in a single imaging session in a single animal.

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