Abstract

Functional imaging in behaving animals is essential to understanding brain function. However, artifacts resulting from animal motion, including locomotion, can severely corrupt functional measurements. To dampen tissue motion, we designed a new optical window with minimal optical aberrations. Using the newly developed high-speed continuous volumetric imaging system based on an optical phase-locked ultrasound lens, we quantified motion of the cerebral cortex and hippocampal surface during two-photon functional imaging in behaving mice. We find that the out-of-plane motion is generally greater than the axial dimension of the point-spread-function during mouse locomotion, which indicates that high-speed continuous volumetric imaging is necessary to minimize motion artifacts.

© 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]
  39. M. Guizar-Sicairos, S. T. Thurman, and J. R. Fienup, “Efficient subpixel image registration algorithms,” Opt. Lett. 33(2), 156–158 (2008).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  42. S. Laffray, S. Pagès, H. Dufour, P. De Koninck, Y. De Koninck, and D. Côté, “Adaptive movement compensation for in vivo imaging of fast cellular dynamics within a moving tissue,” PLoS One 6(5), e19928 (2011).
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    [Crossref] [PubMed]

2016 (3)

L. Kong and M. Cui, “In vivo deep tissue imaging via iterative multiphoton adaptive compensation technique,” IEEE J. Sel. Top. Quantum Electron. 22(4), 6803010 (2016).
[Crossref]

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

L. Kong, J. Tang, and M. Cui, “Multicolor multiphoton in vivo imaging flow cytometry,” Opt. Express 24(6), 6126–6135 (2016).
[PubMed]

2015 (4)

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (scape) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref] [PubMed]

L. Kong and M. Cui, “In vivo neuroimaging through the highly scattering tissue via iterative multi-photon adaptive compensation technique,” Opt. Express 23(5), 6145–6150 (2015).
[Crossref] [PubMed]

L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
[Crossref] [PubMed]

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “Sped light sheet microscopy: Fast mapping of biological system structure and function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

2014 (3)

C. Vinegoni, S. Lee, P. F. Feruglio, and R. Weissleder, “Advanced motion compensation methods for intravital optical microscopy,” IEEE J. Sel. Top. Quantum Electron. 20(2), 6800709 (2014).
[Crossref] [PubMed]

M. Duocastella, G. Vicidomini, and A. Diaspro, “Simultaneous multiplane confocal microscopy using acoustic tunable lenses,” Opt. Express 22(16), 19293–19301 (2014).
[Crossref] [PubMed]

F. St-Pierre, J. D. Marshall, Y. Yang, Y. Gong, M. J. Schnitzer, and M. Z. Lin, “High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor,” Nat. Neurosci. 17(6), 884–889 (2014).
[Crossref] [PubMed]

2013 (3)

C. G. Clark, G. J. Marchetti, and C. N. Young, “Be still my beating brain--reduction of brain micromotion during in vivo two-photon imaging,” J. Physiol. 591(10), 2379–2380 (2013).
[Crossref] [PubMed]

J. L. Chen, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
[Crossref] [PubMed]

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

2012 (7)

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

N. L. Xu, M. T. Harnett, S. R. Williams, D. Huber, D. H. O’Connor, K. Svoboda, and J. C. Magee, “Nonlinear dendritic integration of sensory and motor input during an active sensing task,” Nature 492(7428), 247–251 (2012).
[Crossref] [PubMed]

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484(7395), 473–478 (2012).
[Crossref] [PubMed]

C. D. Harvey, P. Coen, and D. W. Tank, “Choice-specific sequences in parietal cortex during a virtual-navigation decision task,” Nature 484(7392), 62–68 (2012).
[Crossref] [PubMed]

T. P. Santisakultarm, N. R. Cornelius, N. Nishimura, A. I. Schafer, R. T. Silver, P. C. Doerschuk, W. L. Olbricht, and C. B. Schaffer, “In vivo two-photon excited fluorescence microscopy reveals cardiac- and respiration-dependent pulsatile blood flow in cortical blood vessels in mice,” Am. J. Physiol. Heart Circ. Physiol. 302(7), H1367–H1377 (2012).
[Crossref] [PubMed]

M. Paukert and D. E. Bergles, “Reduction of motion artifacts during in vivo two-photon imaging of brain through heartbeat triggered scanning,” J. Physiol. 590(13), 2955–2963 (2012).
[Crossref] [PubMed]

2011 (4)

S. Laffray, S. Pagès, H. Dufour, P. De Koninck, Y. De Koninck, and D. Côté, “Adaptive movement compensation for in vivo imaging of fast cellular dynamics within a moving tissue,” PLoS One 6(5), e19928 (2011).
[Crossref] [PubMed]

V. Bonin, M. H. Histed, S. Yurgenson, and R. C. Reid, “Local diversity and fine-scale organization of receptive fields in mouse visual cortex,” J. Neurosci. 31(50), 18506–18521 (2011).
[Crossref] [PubMed]

S. Chen, S. Tran, A. Sigler, and T. H. Murphy, “Automated and quantitative image analysis of ischemic dendritic blebbing using in vivo 2-photon microscopy data,” J. Neurosci. Methods 195(2), 222–231 (2011).
[Crossref] [PubMed]

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
[Crossref] [PubMed]

2010 (3)

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

M. L. Andermann, A. M. Kerlin, and R. C. Reid, “Chronic cellular imaging of mouse visual cortex during operant behavior and passive viewing,” Front. Cell. Neurosci. 4, 3 (2010).
[PubMed]

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
[Crossref] [PubMed]

2009 (4)

A. Nimmerjahn, E. A. Mukamel, and M. J. Schnitzer, “Motor behavior activates Bergmann glial networks,” Neuron 62(3), 400–412 (2009).
[Crossref] [PubMed]

D. S. Greenberg and J. N. D. Kerr, “Automated correction of fast motion artifacts for two-photon imaging of awake animals,” J. Neurosci. Methods 176(1), 1–15 (2009).
[Crossref] [PubMed]

D. A. Dombeck, M. S. Graziano, and D. W. Tank, “Functional clustering of neurons in motor cortex determined by cellular resolution imaging in awake behaving mice,” J. Neurosci. 29(44), 13751–13760 (2009).
[Crossref] [PubMed]

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[Crossref] [PubMed]

2008 (2)

M. Guizar-Sicairos, S. T. Thurman, and J. R. Fienup, “Efficient subpixel image registration algorithms,” Opt. Lett. 33(2), 156–158 (2008).
[Crossref] [PubMed]

D. S. Greenberg, A. R. Houweling, and J. N. D. Kerr, “Population imaging of ongoing neuronal activity in the visual cortex of awake rats,” Nat. Neurosci. 11(7), 749–751 (2008).
[Crossref] [PubMed]

2007 (3)

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(1), 43–57 (2007).
[Crossref] [PubMed]

W. Göbel, B. M. Kampa, and F. Helmchen, “Imaging cellular network dynamics in three dimensions using fast 3D laser scanning,” Nat. Methods 4(1), 73–79 (2007).
[Crossref] [PubMed]

A. W. Roe, “Long-term optical imaging of intrinsic signals in anesthetized and awake monkeys,” Appl. Opt. 46(10), 1872–1880 (2007).
[Crossref] [PubMed]

2006 (1)

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
[Crossref] [PubMed]

2005 (1)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref] [PubMed]

2004 (1)

R. Yasuda, E. A. Nimchinsky, V. Scheuss, T. A. Pologruto, T. G. Oertner, B. L. Sabatini, and K. Svoboda, “Imaging calcium concentration dynamics in small neuronal compartments,” Sci. STKE 2004(219), pl5 (2004).
[PubMed]

2003 (1)

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: Multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

2002 (2)

V. Garcés-Chávez, D. McGloin, H. Melville, W. Sibbett, and K. Dholakia, “Simultaneous micromanipulation in multiple planes using a self-reconstructing light beam,” Nature 419(6903), 145–147 (2002).
[Crossref] [PubMed]

B. Wattellier, C. Sauteret, J. C. Chanteloup, and A. Migus, “Beam-focus shaping by use of programmable phase-only filters: Application to an ultralong focal line,” Opt. Lett. 27(4), 213–215 (2002).
[Crossref] [PubMed]

2000 (1)

D. S. Wan, M. Rajadhyaksha, and R. H. Webb, “Analysis of spherical aberration of a water immersion objective: Application to specimens with refractive indices 1.33-1.40,” J. Microsc. 197(3), 274–284 (2000).
[Crossref] [PubMed]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “2-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

1989 (1)

T. Hellmuch, P. Seidel, and A. Siegel, “Spherical aberration in confocal microscopy,” Proc. SPIE 1028, 28–32 (1989).
[Crossref]

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(1), 43–57 (2007).
[Crossref] [PubMed]

Akerboom, J.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[Crossref] [PubMed]

Andalman, A.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “Sped light sheet microscopy: Fast mapping of biological system structure and function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Andermann, M. L.

M. L. Andermann, A. M. Kerlin, and R. C. Reid, “Chronic cellular imaging of mouse visual cortex during operant behavior and passive viewing,” Front. Cell. Neurosci. 4, 3 (2010).
[PubMed]

Arisaka, K.

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[Crossref] [PubMed]

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T. P. Santisakultarm, N. R. Cornelius, N. Nishimura, A. I. Schafer, R. T. Silver, P. C. Doerschuk, W. L. Olbricht, and C. B. Schaffer, “In vivo two-photon excited fluorescence microscopy reveals cardiac- and respiration-dependent pulsatile blood flow in cortical blood vessels in mice,” Am. J. Physiol. Heart Circ. Physiol. 302(7), H1367–H1377 (2012).
[Crossref] [PubMed]

Smith, C. W.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

St-Pierre, F.

F. St-Pierre, J. D. Marshall, Y. Yang, Y. Gong, M. J. Schnitzer, and M. Z. Lin, “High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor,” Nat. Neurosci. 17(6), 884–889 (2014).
[Crossref] [PubMed]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, “2-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Sun, Y.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Svoboda, K.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

N. L. Xu, M. T. Harnett, S. R. Williams, D. Huber, D. H. O’Connor, K. Svoboda, and J. C. Magee, “Nonlinear dendritic integration of sensory and motor input during an active sensing task,” Nature 492(7428), 247–251 (2012).
[Crossref] [PubMed]

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484(7395), 473–478 (2012).
[Crossref] [PubMed]

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[Crossref] [PubMed]

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
[Crossref] [PubMed]

R. Yasuda, E. A. Nimchinsky, V. Scheuss, T. A. Pologruto, T. G. Oertner, B. L. Sabatini, and K. Svoboda, “Imaging calcium concentration dynamics in small neuronal compartments,” Sci. STKE 2004(219), pl5 (2004).
[PubMed]

Szalay, G.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Tang, J.

L. Kong, J. Tang, and M. Cui, “Multicolor multiphoton in vivo imaging flow cytometry,” Opt. Express 24(6), 6126–6135 (2016).
[PubMed]

L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
[Crossref] [PubMed]

Tank, D. W.

C. D. Harvey, P. Coen, and D. W. Tank, “Choice-specific sequences in parietal cortex during a virtual-navigation decision task,” Nature 484(7392), 62–68 (2012).
[Crossref] [PubMed]

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
[Crossref] [PubMed]

D. A. Dombeck, M. S. Graziano, and D. W. Tank, “Functional clustering of neurons in motor cortex determined by cellular resolution imaging in awake behaving mice,” J. Neurosci. 29(44), 13751–13760 (2009).
[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(1), 43–57 (2007).
[Crossref] [PubMed]

Thurman, S. T.

M. Guizar-Sicairos, S. T. Thurman, and J. R. Fienup, “Efficient subpixel image registration algorithms,” Opt. Lett. 33(2), 156–158 (2008).
[Crossref] [PubMed]

Tian, L.

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484(7395), 473–478 (2012).
[Crossref] [PubMed]

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
[Crossref] [PubMed]

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[Crossref] [PubMed]

Tomer, R.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “Sped light sheet microscopy: Fast mapping of biological system structure and function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Tran, S.

S. Chen, S. Tran, A. Sigler, and T. H. Murphy, “Automated and quantitative image analysis of ischemic dendritic blebbing using in vivo 2-photon microscopy data,” J. Neurosci. Methods 195(2), 222–231 (2011).
[Crossref] [PubMed]

Veress, M.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Vicidomini, G.

M. Duocastella, G. Vicidomini, and A. Diaspro, “Simultaneous multiplane confocal microscopy using acoustic tunable lenses,” Opt. Express 22(16), 19293–19301 (2014).
[Crossref] [PubMed]

Vinegoni, C.

C. Vinegoni, S. Lee, P. F. Feruglio, and R. Weissleder, “Advanced motion compensation methods for intravital optical microscopy,” IEEE J. Sel. Top. Quantum Electron. 20(2), 6800709 (2014).
[Crossref] [PubMed]

Vizi, E. S.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Voigt, F. F.

J. L. Chen, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
[Crossref] [PubMed]

Voleti, V.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (scape) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref] [PubMed]

Wan, D. S.

D. S. Wan, M. Rajadhyaksha, and R. H. Webb, “Analysis of spherical aberration of a water immersion objective: Application to specimens with refractive indices 1.33-1.40,” J. Microsc. 197(3), 274–284 (2000).
[Crossref] [PubMed]

Wardill, T. J.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Wattellier, B.

B. Wattellier, C. Sauteret, J. C. Chanteloup, and A. Migus, “Beam-focus shaping by use of programmable phase-only filters: Application to an ultralong focal line,” Opt. Lett. 27(4), 213–215 (2002).
[Crossref] [PubMed]

Webb, R. H.

D. S. Wan, M. Rajadhyaksha, and R. H. Webb, “Analysis of spherical aberration of a water immersion objective: Application to specimens with refractive indices 1.33-1.40,” J. Microsc. 197(3), 274–284 (2000).
[Crossref] [PubMed]

Webb, W. W.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: Multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “2-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Weissleder, R.

C. Vinegoni, S. Lee, P. F. Feruglio, and R. Weissleder, “Advanced motion compensation methods for intravital optical microscopy,” IEEE J. Sel. Top. Quantum Electron. 20(2), 6800709 (2014).
[Crossref] [PubMed]

Wiegert, J. S.

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484(7395), 473–478 (2012).
[Crossref] [PubMed]

Williams, R. M.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: Multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Williams, S. R.

N. L. Xu, M. T. Harnett, S. R. Williams, D. Huber, D. H. O’Connor, K. Svoboda, and J. C. Magee, “Nonlinear dendritic integration of sensory and motor input during an active sensing task,” Nature 492(7428), 247–251 (2012).
[Crossref] [PubMed]

Wilson, T.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Xu, N. L.

N. L. Xu, M. T. Harnett, S. R. Williams, D. Huber, D. H. O’Connor, K. Svoboda, and J. C. Magee, “Nonlinear dendritic integration of sensory and motor input during an active sensing task,” Nature 492(7428), 247–251 (2012).
[Crossref] [PubMed]

Yang, S.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “Sped light sheet microscopy: Fast mapping of biological system structure and function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Yang, W.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Yang, Y.

F. St-Pierre, J. D. Marshall, Y. Yang, Y. Gong, M. J. Schnitzer, and M. Z. Lin, “High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor,” Nat. Neurosci. 17(6), 884–889 (2014).
[Crossref] [PubMed]

Yasuda, R.

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
[Crossref] [PubMed]

R. Yasuda, E. A. Nimchinsky, V. Scheuss, T. A. Pologruto, T. G. Oertner, B. L. Sabatini, and K. Svoboda, “Imaging calcium concentration dynamics in small neuronal compartments,” Sci. STKE 2004(219), pl5 (2004).
[PubMed]

Young, C. N.

C. G. Clark, G. J. Marchetti, and C. N. Young, “Be still my beating brain--reduction of brain micromotion during in vivo two-photon imaging,” J. Physiol. 591(10), 2379–2380 (2013).
[Crossref] [PubMed]

Yu, Y.

L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
[Crossref] [PubMed]

Yurgenson, S.

V. Bonin, M. H. Histed, S. Yurgenson, and R. C. Reid, “Local diversity and fine-scale organization of receptive fields in mouse visual cortex,” J. Neurosci. 31(50), 18506–18521 (2011).
[Crossref] [PubMed]

Yuste, R.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Zipfel, W. R.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: Multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Am. J. Physiol. Heart Circ. Physiol. (1)

T. P. Santisakultarm, N. R. Cornelius, N. Nishimura, A. I. Schafer, R. T. Silver, P. C. Doerschuk, W. L. Olbricht, and C. B. Schaffer, “In vivo two-photon excited fluorescence microscopy reveals cardiac- and respiration-dependent pulsatile blood flow in cortical blood vessels in mice,” Am. J. Physiol. Heart Circ. Physiol. 302(7), H1367–H1377 (2012).
[Crossref] [PubMed]

Appl. Opt. (1)

A. W. Roe, “Long-term optical imaging of intrinsic signals in anesthetized and awake monkeys,” Appl. Opt. 46(10), 1872–1880 (2007).
[Crossref] [PubMed]

Cell (1)

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “Sped light sheet microscopy: Fast mapping of biological system structure and function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Front. Cell. Neurosci. (1)

M. L. Andermann, A. M. Kerlin, and R. C. Reid, “Chronic cellular imaging of mouse visual cortex during operant behavior and passive viewing,” Front. Cell. Neurosci. 4, 3 (2010).
[PubMed]

IEEE J. Sel. Top. Quantum Electron. (2)

C. Vinegoni, S. Lee, P. F. Feruglio, and R. Weissleder, “Advanced motion compensation methods for intravital optical microscopy,” IEEE J. Sel. Top. Quantum Electron. 20(2), 6800709 (2014).
[Crossref] [PubMed]

L. Kong and M. Cui, “In vivo deep tissue imaging via iterative multiphoton adaptive compensation technique,” IEEE J. Sel. Top. Quantum Electron. 22(4), 6803010 (2016).
[Crossref]

J. Microsc. (1)

D. S. Wan, M. Rajadhyaksha, and R. H. Webb, “Analysis of spherical aberration of a water immersion objective: Application to specimens with refractive indices 1.33-1.40,” J. Microsc. 197(3), 274–284 (2000).
[Crossref] [PubMed]

J. Neurosci. (2)

D. A. Dombeck, M. S. Graziano, and D. W. Tank, “Functional clustering of neurons in motor cortex determined by cellular resolution imaging in awake behaving mice,” J. Neurosci. 29(44), 13751–13760 (2009).
[Crossref] [PubMed]

V. Bonin, M. H. Histed, S. Yurgenson, and R. C. Reid, “Local diversity and fine-scale organization of receptive fields in mouse visual cortex,” J. Neurosci. 31(50), 18506–18521 (2011).
[Crossref] [PubMed]

J. Neurosci. Methods (2)

D. S. Greenberg and J. N. D. Kerr, “Automated correction of fast motion artifacts for two-photon imaging of awake animals,” J. Neurosci. Methods 176(1), 1–15 (2009).
[Crossref] [PubMed]

S. Chen, S. Tran, A. Sigler, and T. H. Murphy, “Automated and quantitative image analysis of ischemic dendritic blebbing using in vivo 2-photon microscopy data,” J. Neurosci. Methods 195(2), 222–231 (2011).
[Crossref] [PubMed]

J. Physiol. (3)

J. L. Chen, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
[Crossref] [PubMed]

M. Paukert and D. E. Bergles, “Reduction of motion artifacts during in vivo two-photon imaging of brain through heartbeat triggered scanning,” J. Physiol. 590(13), 2955–2963 (2012).
[Crossref] [PubMed]

C. G. Clark, G. J. Marchetti, and C. N. Young, “Be still my beating brain--reduction of brain micromotion during in vivo two-photon imaging,” J. Physiol. 591(10), 2379–2380 (2013).
[Crossref] [PubMed]

Nat. Biotechnol. (1)

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: Multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Nat. Methods (7)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref] [PubMed]

L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
[Crossref] [PubMed]

W. Göbel, B. M. Kampa, and F. Helmchen, “Imaging cellular network dynamics in three dimensions using fast 3D laser scanning,” Nat. Methods 4(1), 73–79 (2007).
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B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
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L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[Crossref] [PubMed]

Nat. Neurosci. (3)

F. St-Pierre, J. D. Marshall, Y. Yang, Y. Gong, M. J. Schnitzer, and M. Z. Lin, “High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor,” Nat. Neurosci. 17(6), 884–889 (2014).
[Crossref] [PubMed]

D. S. Greenberg, A. R. Houweling, and J. N. D. Kerr, “Population imaging of ongoing neuronal activity in the visual cortex of awake rats,” Nat. Neurosci. 11(7), 749–751 (2008).
[Crossref] [PubMed]

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
[Crossref] [PubMed]

Nat. Photonics (1)

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (scape) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref] [PubMed]

Nature (5)

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484(7395), 473–478 (2012).
[Crossref] [PubMed]

N. L. Xu, M. T. Harnett, S. R. Williams, D. Huber, D. H. O’Connor, K. Svoboda, and J. C. Magee, “Nonlinear dendritic integration of sensory and motor input during an active sensing task,” Nature 492(7428), 247–251 (2012).
[Crossref] [PubMed]

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

C. D. Harvey, P. Coen, and D. W. Tank, “Choice-specific sequences in parietal cortex during a virtual-navigation decision task,” Nature 484(7392), 62–68 (2012).
[Crossref] [PubMed]

V. Garcés-Chávez, D. McGloin, H. Melville, W. Sibbett, and K. Dholakia, “Simultaneous micromanipulation in multiple planes using a self-reconstructing light beam,” Nature 419(6903), 145–147 (2002).
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Neuron (4)

A. Nimmerjahn, E. A. Mukamel, and M. J. Schnitzer, “Motor behavior activates Bergmann glial networks,” Neuron 62(3), 400–412 (2009).
[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(1), 43–57 (2007).
[Crossref] [PubMed]

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
[Crossref] [PubMed]

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Opt. Express (3)

L. Kong, J. Tang, and M. Cui, “Multicolor multiphoton in vivo imaging flow cytometry,” Opt. Express 24(6), 6126–6135 (2016).
[PubMed]

M. Duocastella, G. Vicidomini, and A. Diaspro, “Simultaneous multiplane confocal microscopy using acoustic tunable lenses,” Opt. Express 22(16), 19293–19301 (2014).
[Crossref] [PubMed]

L. Kong and M. Cui, “In vivo neuroimaging through the highly scattering tissue via iterative multi-photon adaptive compensation technique,” Opt. Express 23(5), 6145–6150 (2015).
[Crossref] [PubMed]

Opt. Lett. (2)

M. Guizar-Sicairos, S. T. Thurman, and J. R. Fienup, “Efficient subpixel image registration algorithms,” Opt. Lett. 33(2), 156–158 (2008).
[Crossref] [PubMed]

B. Wattellier, C. Sauteret, J. C. Chanteloup, and A. Migus, “Beam-focus shaping by use of programmable phase-only filters: Application to an ultralong focal line,” Opt. Lett. 27(4), 213–215 (2002).
[Crossref] [PubMed]

PLoS One (1)

S. Laffray, S. Pagès, H. Dufour, P. De Koninck, Y. De Koninck, and D. Côté, “Adaptive movement compensation for in vivo imaging of fast cellular dynamics within a moving tissue,” PLoS One 6(5), e19928 (2011).
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Proc. Natl. Acad. Sci. U.S.A. (1)

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Supplementary Material (2)

NameDescription
» Visualization 1: MP4 (180 KB)      Volume view of the dendrites and spines.
» Visualization 2: MP4 (801 KB)      Volumetric imaging of calcium transient in the dendrites and spines. Up panel: MIP along z; down panel: volumetric view.

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Figures (5)

Fig. 1
Fig. 1 Photos of functional imaging in behaving mice and the design of optical windows. (a) Photo of a head-restrained mouse running on a linear treadmill. HP: head-post, Obj: objective lens. (b) Photo of the mouse skull. S1: primary barrel cortex, V1: primary visual cortex, CA1: cornu ammonis, field 1. The CA1 is beneath the cerebral cortex. (c, d) 3D rendering and side view of the optical window design for cerebral cortex imaging. (e, f) 3D rendering and side view of the optical window design for hippocampus imaging. C: cerebral cortex, H: hippocampus.

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Fig. 2
Fig. 2 Functional imaging of dendrite and dendritic spines in S1 cortex for a mouse running on a linear treadmill at liberty. (a) Volume view of the dendrite and dendritic spines (see also Visualization 1). Size: 77 × 15.4 × 40 µm3. (b) Maximum intensity projection of the volume along z axis. (c) Running speed of the mouse and brain motion quantified from the functional imaging in Visualization 2. (d) Quiver plot of brain motion. (e) and (f) Fluorescence dynamics ΔF/F of the dendritic shafts and dendritic spines marked by the yellow arrows and red triangles in (b), respectively. Left: signal after registration; right: signal without registration. The artifacts are highlighted by the black dash boxes.

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Fig. 3
Fig. 3 Motion quantification during functional imaging of S1 cortex for mice running on a linear treadmill with air-puff stimulations applied onto the whiskers. (a-c) Typical motion in S1 cortex. The running speeds are shown in red curves at top rows of each figure, where the gray bars show the time when air-puff stimulation was applied. (b) and (c) are quantified from data of a mouse, but acquired on different days. (d) Summary of motion quantification in 3 mice. Max IPM: maximum in-plane motion; Max OPM: maximum out-of-plane motion.

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Fig. 4
Fig. 4 Motion quantifications during functional imaging of V1 cortex for mice running on a linear treadmill with air-puff stimulations to the whiskers and visual stimulations. (a-c) Typical motion in V1 cortex. The running speeds are shown in red curves at top rows of each figure, where the gray bars show the time when the visual stimulation and air-puff stimulation were on. (b) and (c) are quantified from data of consecutive trials with a mouse. (d) Summary of motion quantifications in 3 mice.

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Fig. 5
Fig. 5 Motion quantifications during functional imaging of hippocampal surface for mice running on a linear treadmill at liberty. (a-b) Typical motion at hippocampal surface of 2 mice. The running speeds are shown in red curves at top rows of each figure. The out-of-plane motion was not apparent in (a), while there was slow axial drift in (b).

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