Abstract

We introduce a more flexible optogenetics-based mapping system attached on a stereo microscope, which offers automatic light stimulation to individual regions of interest in the cortex that expresses light-activated channelrhodopsin-2 in vivo. Combining simultaneous recording of electromyography from specific forelimb muscles, we demonstrate that this system offers much better efficiency and precision in mapping distinct domains for controlling limb muscles in the mouse motor cortex. Furthermore, the compact and modular design of the system also yields a simple and flexible implementation to different commercial stereo microscopes, and thus could be widely used among laboratories.

© 2016 Optical Society of America

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  1. I. V. Pronichev and D. N. Lenkov, “Functional mapping of the motor cortex of the white mouse by a microstimulation method,” Neurosci. Behav. Physiol. 28(1), 80–85 (1998).
    [Crossref] [PubMed]
  2. J. P. Donoghue and J. N. Sanes, “Peripheral nerve injury in developing rats reorganizes representation pattern in motor cortex,” Proc. Natl. Acad. Sci. U.S.A. 84(4), 1123–1126 (1987).
    [Crossref] [PubMed]
  3. K. Molina-Luna, M. M. Buitrago, B. Hertler, M. Schubring, F. Haiss, W. Nisch, J. B. Schulz, and A. R. Luft, “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” J. Neurosci. Methods 161(1), 118–125 (2007).
    [Crossref] [PubMed]
  4. M. Hallett, “Transcranial magnetic stimulation and the human brain,” Nature 406(6792), 147–150 (2000).
    [Crossref] [PubMed]
  5. D. Schubert, R. Kötter, and J. F. Staiger, “Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits,” Brain Struct. Funct. 212(2), 107–119 (2007).
    [Crossref] [PubMed]
  6. M. E. Carter and L. de Lecea, “Optogenetic investigation of neural circuits in vivo,” Trends Mol. Med. 17(4), 197–206 (2011).
    [Crossref] [PubMed]
  7. M. Häusser and S. L. Smith, “Neuroscience: controlling neural circuits with light,” Nature 446(7136), 617–619 (2007).
    [Crossref] [PubMed]
  8. F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
    [Crossref] [PubMed]
  9. O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
    [Crossref] [PubMed]
  10. B. R. Arenkiel, J. Peca, I. G. Davison, C. Feliciano, K. Deisseroth, G. J. Augustine, M. D. Ehlers, and G. Feng, “In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2,” Neuron 54(2), 205–218 (2007).
    [Crossref] [PubMed]
  11. H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
    [Crossref] [PubMed]
  12. Y. Yao, X. Li, B. Zhang, C. Yin, Y. Liu, W. Chen, S. Zeng, and J. Du, “Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection,” Neuron 89(3), 598–612 (2016).
    [Crossref] [PubMed]
  13. K. Wang, J. Gong, Q. Wang, H. Li, Q. Cheng, Y. Liu, S. Zeng, and Z. Wang, “Parallel pathways convey olfactory information with opposite polarities in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 111(8), 3164–3169 (2014).
    [Crossref] [PubMed]
  14. O. G. Ayling, T. C. Harrison, J. D. Boyd, A. Goroshkov, and T. H. Murphy, “Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice,” Nat. Methods 6(3), 219–224 (2009).
    [Crossref] [PubMed]
  15. T. C. Harrison, O. G. Ayling, and T. H. Murphy, “Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography,” Neuron 74(2), 397–409 (2012).
    [Crossref] [PubMed]
  16. D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo large-scale cortical mapping using channelrhodopsin-2 stimulation in transgenic mice reveals asymmetric and reciprocal relationships between cortical areas,” Front. Neural Circuits 6(11), 11 (2012).
    [PubMed]
  17. G. Silasi, J. D. Boyd, J. Ledue, and T. H. Murphy, “Improved methods for chronic light-based motor mapping in mice: automated movement tracking with accelerometers, and chronic EEG recording in a bilateral thin-skull preparation,” Front. Neural Circuits 7, 123 (2013).
    [Crossref] [PubMed]
  18. R. Hira, F. Ohkubo, Y. R. Tanaka, Y. Masamizu, G. J. Augustine, H. Kasai, and M. Matsuzaki, “In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas,” Front. Neural Circuits 7, 55 (2013).
    [Crossref] [PubMed]
  19. R. Hira, N. Honkura, J. Noguchi, Y. Maruyama, G. J. Augustine, H. Kasai, and M. Matsuzaki, “Transcranial optogenetic stimulation for functional mapping of the motor cortex,” J. Neurosci. Methods 179(2), 258–263 (2009).
    [Crossref] [PubMed]
  20. J. P. Rickgauer and D. W. Tank, “Two-photon excitation of channelrhodopsin-2 at saturation,” Proc. Natl. Acad. Sci. U.S.A. 106(35), 15025–15030 (2009).
    [Crossref] [PubMed]
  21. A. M. Leifer, C. Fang-Yen, M. Gershow, M. J. Alkema, and A. D. T. Samuel, “Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans,” Nat. Methods 8(2), 147–152 (2011).
    [Crossref] [PubMed]
  22. E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
    [Crossref] [PubMed]
  23. J. A. Kleim, S. Barbay, and R. J. Nudo, “Functional reorganization of the rat motor cortex following motor skill learning,” J. Neurophysiol. 80(6), 3321–3325 (1998).
    [PubMed]
  24. A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
    [Crossref] [PubMed]
  25. E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
    [Crossref] [PubMed]
  26. X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
    [Crossref] [PubMed]

2016 (1)

Y. Yao, X. Li, B. Zhang, C. Yin, Y. Liu, W. Chen, S. Zeng, and J. Du, “Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection,” Neuron 89(3), 598–612 (2016).
[Crossref] [PubMed]

2014 (1)

K. Wang, J. Gong, Q. Wang, H. Li, Q. Cheng, Y. Liu, S. Zeng, and Z. Wang, “Parallel pathways convey olfactory information with opposite polarities in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 111(8), 3164–3169 (2014).
[Crossref] [PubMed]

2013 (2)

G. Silasi, J. D. Boyd, J. Ledue, and T. H. Murphy, “Improved methods for chronic light-based motor mapping in mice: automated movement tracking with accelerometers, and chronic EEG recording in a bilateral thin-skull preparation,” Front. Neural Circuits 7, 123 (2013).
[Crossref] [PubMed]

R. Hira, F. Ohkubo, Y. R. Tanaka, Y. Masamizu, G. J. Augustine, H. Kasai, and M. Matsuzaki, “In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas,” Front. Neural Circuits 7, 55 (2013).
[Crossref] [PubMed]

2012 (2)

T. C. Harrison, O. G. Ayling, and T. H. Murphy, “Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography,” Neuron 74(2), 397–409 (2012).
[Crossref] [PubMed]

D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo large-scale cortical mapping using channelrhodopsin-2 stimulation in transgenic mice reveals asymmetric and reciprocal relationships between cortical areas,” Front. Neural Circuits 6(11), 11 (2012).
[PubMed]

2011 (3)

M. E. Carter and L. de Lecea, “Optogenetic investigation of neural circuits in vivo,” Trends Mol. Med. 17(4), 197–206 (2011).
[Crossref] [PubMed]

O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
[Crossref] [PubMed]

A. M. Leifer, C. Fang-Yen, M. Gershow, M. J. Alkema, and A. D. T. Samuel, “Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans,” Nat. Methods 8(2), 147–152 (2011).
[Crossref] [PubMed]

2010 (1)

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

2009 (3)

O. G. Ayling, T. C. Harrison, J. D. Boyd, A. Goroshkov, and T. H. Murphy, “Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice,” Nat. Methods 6(3), 219–224 (2009).
[Crossref] [PubMed]

R. Hira, N. Honkura, J. Noguchi, Y. Maruyama, G. J. Augustine, H. Kasai, and M. Matsuzaki, “Transcranial optogenetic stimulation for functional mapping of the motor cortex,” J. Neurosci. Methods 179(2), 258–263 (2009).
[Crossref] [PubMed]

J. P. Rickgauer and D. W. Tank, “Two-photon excitation of channelrhodopsin-2 at saturation,” Proc. Natl. Acad. Sci. U.S.A. 106(35), 15025–15030 (2009).
[Crossref] [PubMed]

2007 (7)

B. R. Arenkiel, J. Peca, I. G. Davison, C. Feliciano, K. Deisseroth, G. J. Augustine, M. D. Ehlers, and G. Feng, “In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2,” Neuron 54(2), 205–218 (2007).
[Crossref] [PubMed]

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
[Crossref] [PubMed]

M. Häusser and S. L. Smith, “Neuroscience: controlling neural circuits with light,” Nature 446(7136), 617–619 (2007).
[Crossref] [PubMed]

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

K. Molina-Luna, M. M. Buitrago, B. Hertler, M. Schubring, F. Haiss, W. Nisch, J. B. Schulz, and A. R. Luft, “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” J. Neurosci. Methods 161(1), 118–125 (2007).
[Crossref] [PubMed]

A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
[Crossref] [PubMed]

D. Schubert, R. Kötter, and J. F. Staiger, “Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits,” Brain Struct. Funct. 212(2), 107–119 (2007).
[Crossref] [PubMed]

2005 (2)

E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
[Crossref] [PubMed]

X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
[Crossref] [PubMed]

2000 (1)

M. Hallett, “Transcranial magnetic stimulation and the human brain,” Nature 406(6792), 147–150 (2000).
[Crossref] [PubMed]

1998 (2)

I. V. Pronichev and D. N. Lenkov, “Functional mapping of the motor cortex of the white mouse by a microstimulation method,” Neurosci. Behav. Physiol. 28(1), 80–85 (1998).
[Crossref] [PubMed]

J. A. Kleim, S. Barbay, and R. J. Nudo, “Functional reorganization of the rat motor cortex following motor skill learning,” J. Neurophysiol. 80(6), 3321–3325 (1998).
[PubMed]

1987 (1)

J. P. Donoghue and J. N. Sanes, “Peripheral nerve injury in developing rats reorganizes representation pattern in motor cortex,” Proc. Natl. Acad. Sci. U.S.A. 84(4), 1123–1126 (1987).
[Crossref] [PubMed]

Adamantidis, A.

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

Alkema, M. J.

A. M. Leifer, C. Fang-Yen, M. Gershow, M. J. Alkema, and A. D. T. Samuel, “Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans,” Nat. Methods 8(2), 147–152 (2011).
[Crossref] [PubMed]

Anselmi, F.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Aravanis, A. M.

A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
[Crossref] [PubMed]

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

Arenkiel, B. R.

B. R. Arenkiel, J. Peca, I. G. Davison, C. Feliciano, K. Deisseroth, G. J. Augustine, M. D. Ehlers, and G. Feng, “In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2,” Neuron 54(2), 205–218 (2007).
[Crossref] [PubMed]

Augustine, G. J.

R. Hira, F. Ohkubo, Y. R. Tanaka, Y. Masamizu, G. J. Augustine, H. Kasai, and M. Matsuzaki, “In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas,” Front. Neural Circuits 7, 55 (2013).
[Crossref] [PubMed]

R. Hira, N. Honkura, J. Noguchi, Y. Maruyama, G. J. Augustine, H. Kasai, and M. Matsuzaki, “Transcranial optogenetic stimulation for functional mapping of the motor cortex,” J. Neurosci. Methods 179(2), 258–263 (2009).
[Crossref] [PubMed]

B. R. Arenkiel, J. Peca, I. G. Davison, C. Feliciano, K. Deisseroth, G. J. Augustine, M. D. Ehlers, and G. Feng, “In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2,” Neuron 54(2), 205–218 (2007).
[Crossref] [PubMed]

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
[Crossref] [PubMed]

Ayling, O. G.

T. C. Harrison, O. G. Ayling, and T. H. Murphy, “Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography,” Neuron 74(2), 397–409 (2012).
[Crossref] [PubMed]

O. G. Ayling, T. C. Harrison, J. D. Boyd, A. Goroshkov, and T. H. Murphy, “Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice,” Nat. Methods 6(3), 219–224 (2009).
[Crossref] [PubMed]

Bamberg, E.

E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
[Crossref] [PubMed]

Barbay, S.

J. A. Kleim, S. Barbay, and R. J. Nudo, “Functional reorganization of the rat motor cortex following motor skill learning,” J. Neurophysiol. 80(6), 3321–3325 (1998).
[PubMed]

Bègue, A.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Boyd, J.

D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo large-scale cortical mapping using channelrhodopsin-2 stimulation in transgenic mice reveals asymmetric and reciprocal relationships between cortical areas,” Front. Neural Circuits 6(11), 11 (2012).
[PubMed]

Boyd, J. D.

G. Silasi, J. D. Boyd, J. Ledue, and T. H. Murphy, “Improved methods for chronic light-based motor mapping in mice: automated movement tracking with accelerometers, and chronic EEG recording in a bilateral thin-skull preparation,” Front. Neural Circuits 7, 123 (2013).
[Crossref] [PubMed]

O. G. Ayling, T. C. Harrison, J. D. Boyd, A. Goroshkov, and T. H. Murphy, “Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice,” Nat. Methods 6(3), 219–224 (2009).
[Crossref] [PubMed]

Boyden, E.

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
[Crossref] [PubMed]

Boyden, E. S.

E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
[Crossref] [PubMed]

Buitrago, M. M.

K. Molina-Luna, M. M. Buitrago, B. Hertler, M. Schubring, F. Haiss, W. Nisch, J. B. Schulz, and A. R. Luft, “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” J. Neurosci. Methods 161(1), 118–125 (2007).
[Crossref] [PubMed]

Carter, M. E.

M. E. Carter and L. de Lecea, “Optogenetic investigation of neural circuits in vivo,” Trends Mol. Med. 17(4), 197–206 (2011).
[Crossref] [PubMed]

Chen, S.

D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo large-scale cortical mapping using channelrhodopsin-2 stimulation in transgenic mice reveals asymmetric and reciprocal relationships between cortical areas,” Front. Neural Circuits 6(11), 11 (2012).
[PubMed]

Chen, W.

Y. Yao, X. Li, B. Zhang, C. Yin, Y. Liu, W. Chen, S. Zeng, and J. Du, “Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection,” Neuron 89(3), 598–612 (2016).
[Crossref] [PubMed]

Cheng, Q.

K. Wang, J. Gong, Q. Wang, H. Li, Q. Cheng, Y. Liu, S. Zeng, and Z. Wang, “Parallel pathways convey olfactory information with opposite polarities in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 111(8), 3164–3169 (2014).
[Crossref] [PubMed]

Chiel, H.

X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
[Crossref] [PubMed]

Davidson, T. J.

O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
[Crossref] [PubMed]

Davison, I. G.

B. R. Arenkiel, J. Peca, I. G. Davison, C. Feliciano, K. Deisseroth, G. J. Augustine, M. D. Ehlers, and G. Feng, “In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2,” Neuron 54(2), 205–218 (2007).
[Crossref] [PubMed]

de Lecea, L.

M. E. Carter and L. de Lecea, “Optogenetic investigation of neural circuits in vivo,” Trends Mol. Med. 17(4), 197–206 (2011).
[Crossref] [PubMed]

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

de Sars, V.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Deisseroth, K.

O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
[Crossref] [PubMed]

B. R. Arenkiel, J. Peca, I. G. Davison, C. Feliciano, K. Deisseroth, G. J. Augustine, M. D. Ehlers, and G. Feng, “In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2,” Neuron 54(2), 205–218 (2007).
[Crossref] [PubMed]

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
[Crossref] [PubMed]

A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
[Crossref] [PubMed]

E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
[Crossref] [PubMed]

Donoghue, J. P.

J. P. Donoghue and J. N. Sanes, “Peripheral nerve injury in developing rats reorganizes representation pattern in motor cortex,” Proc. Natl. Acad. Sci. U.S.A. 84(4), 1123–1126 (1987).
[Crossref] [PubMed]

Du, J.

Y. Yao, X. Li, B. Zhang, C. Yin, Y. Liu, W. Chen, S. Zeng, and J. Du, “Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection,” Neuron 89(3), 598–612 (2016).
[Crossref] [PubMed]

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B. R. Arenkiel, J. Peca, I. G. Davison, C. Feliciano, K. Deisseroth, G. J. Augustine, M. D. Ehlers, and G. Feng, “In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2,” Neuron 54(2), 205–218 (2007).
[Crossref] [PubMed]

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E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
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A. M. Leifer, C. Fang-Yen, M. Gershow, M. J. Alkema, and A. D. T. Samuel, “Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans,” Nat. Methods 8(2), 147–152 (2011).
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B. R. Arenkiel, J. Peca, I. G. Davison, C. Feliciano, K. Deisseroth, G. J. Augustine, M. D. Ehlers, and G. Feng, “In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2,” Neuron 54(2), 205–218 (2007).
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B. R. Arenkiel, J. Peca, I. G. Davison, C. Feliciano, K. Deisseroth, G. J. Augustine, M. D. Ehlers, and G. Feng, “In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2,” Neuron 54(2), 205–218 (2007).
[Crossref] [PubMed]

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
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O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
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A. M. Leifer, C. Fang-Yen, M. Gershow, M. J. Alkema, and A. D. T. Samuel, “Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans,” Nat. Methods 8(2), 147–152 (2011).
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E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
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K. Wang, J. Gong, Q. Wang, H. Li, Q. Cheng, Y. Liu, S. Zeng, and Z. Wang, “Parallel pathways convey olfactory information with opposite polarities in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 111(8), 3164–3169 (2014).
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O. G. Ayling, T. C. Harrison, J. D. Boyd, A. Goroshkov, and T. H. Murphy, “Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice,” Nat. Methods 6(3), 219–224 (2009).
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X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
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K. Molina-Luna, M. M. Buitrago, B. Hertler, M. Schubring, F. Haiss, W. Nisch, J. B. Schulz, and A. R. Luft, “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” J. Neurosci. Methods 161(1), 118–125 (2007).
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H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
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X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
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X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
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T. C. Harrison, O. G. Ayling, and T. H. Murphy, “Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography,” Neuron 74(2), 397–409 (2012).
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O. G. Ayling, T. C. Harrison, J. D. Boyd, A. Goroshkov, and T. H. Murphy, “Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice,” Nat. Methods 6(3), 219–224 (2009).
[Crossref] [PubMed]

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M. Häusser and S. L. Smith, “Neuroscience: controlling neural circuits with light,” Nature 446(7136), 617–619 (2007).
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X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
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X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
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K. Molina-Luna, M. M. Buitrago, B. Hertler, M. Schubring, F. Haiss, W. Nisch, J. B. Schulz, and A. R. Luft, “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” J. Neurosci. Methods 161(1), 118–125 (2007).
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R. Hira, F. Ohkubo, Y. R. Tanaka, Y. Masamizu, G. J. Augustine, H. Kasai, and M. Matsuzaki, “In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas,” Front. Neural Circuits 7, 55 (2013).
[Crossref] [PubMed]

R. Hira, N. Honkura, J. Noguchi, Y. Maruyama, G. J. Augustine, H. Kasai, and M. Matsuzaki, “Transcranial optogenetic stimulation for functional mapping of the motor cortex,” J. Neurosci. Methods 179(2), 258–263 (2009).
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R. Hira, N. Honkura, J. Noguchi, Y. Maruyama, G. J. Augustine, H. Kasai, and M. Matsuzaki, “Transcranial optogenetic stimulation for functional mapping of the motor cortex,” J. Neurosci. Methods 179(2), 258–263 (2009).
[Crossref] [PubMed]

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E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Kasai, H.

R. Hira, F. Ohkubo, Y. R. Tanaka, Y. Masamizu, G. J. Augustine, H. Kasai, and M. Matsuzaki, “In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas,” Front. Neural Circuits 7, 55 (2013).
[Crossref] [PubMed]

R. Hira, N. Honkura, J. Noguchi, Y. Maruyama, G. J. Augustine, H. Kasai, and M. Matsuzaki, “Transcranial optogenetic stimulation for functional mapping of the motor cortex,” J. Neurosci. Methods 179(2), 258–263 (2009).
[Crossref] [PubMed]

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
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J. A. Kleim, S. Barbay, and R. J. Nudo, “Functional reorganization of the rat motor cortex following motor skill learning,” J. Neurophysiol. 80(6), 3321–3325 (1998).
[PubMed]

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D. Schubert, R. Kötter, and J. F. Staiger, “Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits,” Brain Struct. Funct. 212(2), 107–119 (2007).
[Crossref] [PubMed]

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X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
[Crossref] [PubMed]

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G. Silasi, J. D. Boyd, J. Ledue, and T. H. Murphy, “Improved methods for chronic light-based motor mapping in mice: automated movement tracking with accelerometers, and chronic EEG recording in a bilateral thin-skull preparation,” Front. Neural Circuits 7, 123 (2013).
[Crossref] [PubMed]

D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo large-scale cortical mapping using channelrhodopsin-2 stimulation in transgenic mice reveals asymmetric and reciprocal relationships between cortical areas,” Front. Neural Circuits 6(11), 11 (2012).
[PubMed]

Leifer, A. M.

A. M. Leifer, C. Fang-Yen, M. Gershow, M. J. Alkema, and A. D. T. Samuel, “Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans,” Nat. Methods 8(2), 147–152 (2011).
[Crossref] [PubMed]

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I. V. Pronichev and D. N. Lenkov, “Functional mapping of the motor cortex of the white mouse by a microstimulation method,” Neurosci. Behav. Physiol. 28(1), 80–85 (1998).
[Crossref] [PubMed]

Li, H.

K. Wang, J. Gong, Q. Wang, H. Li, Q. Cheng, Y. Liu, S. Zeng, and Z. Wang, “Parallel pathways convey olfactory information with opposite polarities in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 111(8), 3164–3169 (2014).
[Crossref] [PubMed]

Li, X.

Y. Yao, X. Li, B. Zhang, C. Yin, Y. Liu, W. Chen, S. Zeng, and J. Du, “Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection,” Neuron 89(3), 598–612 (2016).
[Crossref] [PubMed]

X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
[Crossref] [PubMed]

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D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo large-scale cortical mapping using channelrhodopsin-2 stimulation in transgenic mice reveals asymmetric and reciprocal relationships between cortical areas,” Front. Neural Circuits 6(11), 11 (2012).
[PubMed]

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Y. Yao, X. Li, B. Zhang, C. Yin, Y. Liu, W. Chen, S. Zeng, and J. Du, “Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection,” Neuron 89(3), 598–612 (2016).
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K. Wang, J. Gong, Q. Wang, H. Li, Q. Cheng, Y. Liu, S. Zeng, and Z. Wang, “Parallel pathways convey olfactory information with opposite polarities in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 111(8), 3164–3169 (2014).
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K. Molina-Luna, M. M. Buitrago, B. Hertler, M. Schubring, F. Haiss, W. Nisch, J. B. Schulz, and A. R. Luft, “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” J. Neurosci. Methods 161(1), 118–125 (2007).
[Crossref] [PubMed]

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X. Li, D. V. Gutierrez, M. G. Hanson, J. Han, M. D. Mark, H. Chiel, P. Hegemann, L. T. Landmesser, and S. Herlitze, “Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin,” Proc. Natl. Acad. Sci. U.S.A. 102(49), 17816–17821 (2005).
[Crossref] [PubMed]

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R. Hira, N. Honkura, J. Noguchi, Y. Maruyama, G. J. Augustine, H. Kasai, and M. Matsuzaki, “Transcranial optogenetic stimulation for functional mapping of the motor cortex,” J. Neurosci. Methods 179(2), 258–263 (2009).
[Crossref] [PubMed]

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R. Hira, F. Ohkubo, Y. R. Tanaka, Y. Masamizu, G. J. Augustine, H. Kasai, and M. Matsuzaki, “In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas,” Front. Neural Circuits 7, 55 (2013).
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H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
[Crossref] [PubMed]

Matsuzaki, M.

R. Hira, F. Ohkubo, Y. R. Tanaka, Y. Masamizu, G. J. Augustine, H. Kasai, and M. Matsuzaki, “In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas,” Front. Neural Circuits 7, 55 (2013).
[Crossref] [PubMed]

R. Hira, N. Honkura, J. Noguchi, Y. Maruyama, G. J. Augustine, H. Kasai, and M. Matsuzaki, “Transcranial optogenetic stimulation for functional mapping of the motor cortex,” J. Neurosci. Methods 179(2), 258–263 (2009).
[Crossref] [PubMed]

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
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A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
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O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
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A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
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D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo large-scale cortical mapping using channelrhodopsin-2 stimulation in transgenic mice reveals asymmetric and reciprocal relationships between cortical areas,” Front. Neural Circuits 6(11), 11 (2012).
[PubMed]

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K. Molina-Luna, M. M. Buitrago, B. Hertler, M. Schubring, F. Haiss, W. Nisch, J. B. Schulz, and A. R. Luft, “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” J. Neurosci. Methods 161(1), 118–125 (2007).
[Crossref] [PubMed]

Murphy, T. H.

G. Silasi, J. D. Boyd, J. Ledue, and T. H. Murphy, “Improved methods for chronic light-based motor mapping in mice: automated movement tracking with accelerometers, and chronic EEG recording in a bilateral thin-skull preparation,” Front. Neural Circuits 7, 123 (2013).
[Crossref] [PubMed]

D. H. Lim, M. H. Mohajerani, J. Ledue, J. Boyd, S. Chen, and T. H. Murphy, “In vivo large-scale cortical mapping using channelrhodopsin-2 stimulation in transgenic mice reveals asymmetric and reciprocal relationships between cortical areas,” Front. Neural Circuits 6(11), 11 (2012).
[PubMed]

T. C. Harrison, O. G. Ayling, and T. H. Murphy, “Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography,” Neuron 74(2), 397–409 (2012).
[Crossref] [PubMed]

O. G. Ayling, T. C. Harrison, J. D. Boyd, A. Goroshkov, and T. H. Murphy, “Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice,” Nat. Methods 6(3), 219–224 (2009).
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E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
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K. Molina-Luna, M. M. Buitrago, B. Hertler, M. Schubring, F. Haiss, W. Nisch, J. B. Schulz, and A. R. Luft, “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” J. Neurosci. Methods 161(1), 118–125 (2007).
[Crossref] [PubMed]

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R. Hira, N. Honkura, J. Noguchi, Y. Maruyama, G. J. Augustine, H. Kasai, and M. Matsuzaki, “Transcranial optogenetic stimulation for functional mapping of the motor cortex,” J. Neurosci. Methods 179(2), 258–263 (2009).
[Crossref] [PubMed]

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
[Crossref] [PubMed]

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J. A. Kleim, S. Barbay, and R. J. Nudo, “Functional reorganization of the rat motor cortex following motor skill learning,” J. Neurophysiol. 80(6), 3321–3325 (1998).
[PubMed]

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R. Hira, F. Ohkubo, Y. R. Tanaka, Y. Masamizu, G. J. Augustine, H. Kasai, and M. Matsuzaki, “In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas,” Front. Neural Circuits 7, 55 (2013).
[Crossref] [PubMed]

Papagiakoumou, E.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

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H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
[Crossref] [PubMed]

B. R. Arenkiel, J. Peca, I. G. Davison, C. Feliciano, K. Deisseroth, G. J. Augustine, M. D. Ehlers, and G. Feng, “In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2,” Neuron 54(2), 205–218 (2007).
[Crossref] [PubMed]

Pronichev, I. V.

I. V. Pronichev and D. N. Lenkov, “Functional mapping of the motor cortex of the white mouse by a microstimulation method,” Neurosci. Behav. Physiol. 28(1), 80–85 (1998).
[Crossref] [PubMed]

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H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
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J. P. Rickgauer and D. W. Tank, “Two-photon excitation of channelrhodopsin-2 at saturation,” Proc. Natl. Acad. Sci. U.S.A. 106(35), 15025–15030 (2009).
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A. M. Leifer, C. Fang-Yen, M. Gershow, M. J. Alkema, and A. D. T. Samuel, “Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans,” Nat. Methods 8(2), 147–152 (2011).
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A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
[Crossref] [PubMed]

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D. Schubert, R. Kötter, and J. F. Staiger, “Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits,” Brain Struct. Funct. 212(2), 107–119 (2007).
[Crossref] [PubMed]

Schubring, M.

K. Molina-Luna, M. M. Buitrago, B. Hertler, M. Schubring, F. Haiss, W. Nisch, J. B. Schulz, and A. R. Luft, “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” J. Neurosci. Methods 161(1), 118–125 (2007).
[Crossref] [PubMed]

Schulz, J. B.

K. Molina-Luna, M. M. Buitrago, B. Hertler, M. Schubring, F. Haiss, W. Nisch, J. B. Schulz, and A. R. Luft, “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” J. Neurosci. Methods 161(1), 118–125 (2007).
[Crossref] [PubMed]

Silasi, G.

G. Silasi, J. D. Boyd, J. Ledue, and T. H. Murphy, “Improved methods for chronic light-based motor mapping in mice: automated movement tracking with accelerometers, and chronic EEG recording in a bilateral thin-skull preparation,” Front. Neural Circuits 7, 123 (2013).
[Crossref] [PubMed]

Smith, S. L.

M. Häusser and S. L. Smith, “Neuroscience: controlling neural circuits with light,” Nature 446(7136), 617–619 (2007).
[Crossref] [PubMed]

Staiger, J. F.

D. Schubert, R. Kötter, and J. F. Staiger, “Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits,” Brain Struct. Funct. 212(2), 107–119 (2007).
[Crossref] [PubMed]

Tanaka, Y. R.

R. Hira, F. Ohkubo, Y. R. Tanaka, Y. Masamizu, G. J. Augustine, H. Kasai, and M. Matsuzaki, “In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas,” Front. Neural Circuits 7, 55 (2013).
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Tank, D. W.

J. P. Rickgauer and D. W. Tank, “Two-photon excitation of channelrhodopsin-2 at saturation,” Proc. Natl. Acad. Sci. U.S.A. 106(35), 15025–15030 (2009).
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Wang, D.

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
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Wang, H.

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
[Crossref] [PubMed]

Wang, K.

K. Wang, J. Gong, Q. Wang, H. Li, Q. Cheng, Y. Liu, S. Zeng, and Z. Wang, “Parallel pathways convey olfactory information with opposite polarities in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 111(8), 3164–3169 (2014).
[Crossref] [PubMed]

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A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
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K. Wang, J. Gong, Q. Wang, H. Li, Q. Cheng, Y. Liu, S. Zeng, and Z. Wang, “Parallel pathways convey olfactory information with opposite polarities in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 111(8), 3164–3169 (2014).
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Wang, Z.

K. Wang, J. Gong, Q. Wang, H. Li, Q. Cheng, Y. Liu, S. Zeng, and Z. Wang, “Parallel pathways convey olfactory information with opposite polarities in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 111(8), 3164–3169 (2014).
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Yao, Y.

Y. Yao, X. Li, B. Zhang, C. Yin, Y. Liu, W. Chen, S. Zeng, and J. Du, “Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection,” Neuron 89(3), 598–612 (2016).
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Y. Yao, X. Li, B. Zhang, C. Yin, Y. Liu, W. Chen, S. Zeng, and J. Du, “Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection,” Neuron 89(3), 598–612 (2016).
[Crossref] [PubMed]

Yizhar, O.

O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
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Zeng, S.

Y. Yao, X. Li, B. Zhang, C. Yin, Y. Liu, W. Chen, S. Zeng, and J. Du, “Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection,” Neuron 89(3), 598–612 (2016).
[Crossref] [PubMed]

K. Wang, J. Gong, Q. Wang, H. Li, Q. Cheng, Y. Liu, S. Zeng, and Z. Wang, “Parallel pathways convey olfactory information with opposite polarities in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 111(8), 3164–3169 (2014).
[Crossref] [PubMed]

Zhang, B.

Y. Yao, X. Li, B. Zhang, C. Yin, Y. Liu, W. Chen, S. Zeng, and J. Du, “Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection,” Neuron 89(3), 598–612 (2016).
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Zhang, F.

H. Wang, J. Peca, M. Matsuzaki, K. Matsuzaki, J. Noguchi, L. Qiu, D. Wang, F. Zhang, E. Boyden, K. Deisseroth, H. Kasai, W. C. Hall, G. Feng, and G. J. Augustine, “High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice,” Proc. Natl. Acad. Sci. U.S.A. 104(19), 8143–8148 (2007).
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F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
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E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
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A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
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Figures (7)

Fig. 1
Fig. 1 Photostimulator-based stage scanning system. (a) Optical schematic diagram. The rectangles with dashed lines indicate the body of the stereo microscope. (b) Photo of the photostimulator constructed on a commercial SZX7 microscope.
Fig. 2
Fig. 2 The optical resolution below the objective. (a) The intensity profile is shown in the X/Y axis at two magnifications (upper, 0.8 × ; lower, 2.8 × ). (b) Relation between optical resolution and stereo microscope magnification.
Fig. 3
Fig. 3 System performance test. (a) Relation between laser power and the magnification of the stereo microscope. (b) Relation between the actual location and the expected location. (c) Repeated positioning accuracy in the X/Y direction (the error bars indicate the accuracy at different distances).
Fig. 4
Fig. 4 Measuring the noise of the EMG signals. (a) Noise signal with periodic electromagnetic interference. (b) Frequency analysis before shielding. (c) Frequency analysis after electrical shielding and grounding. (d) Frequency analysis after shielding.
Fig. 5
Fig. 5 Light-induced EMG. (a) Image of the vasculature in the right hemisphere of the cortex (the yellow triangle marks the bregma). (b) Relation between the EMG amplitude and stimulation time. (c) Relation between the EMG amplitude and laser power. (d) Relation between the EMG amplitude and laser spot magnification.
Fig. 6
Fig. 6 In vivo optogenetic mapping of the primary motor cortex and precise cortical representations of different forelimb muscles. (A): A picture showing the exposed motor cortex from 2.5 mm ahead of the bregma to 1.4 mm behind the bregma and from 0.5 mm to 3.5 mm lateral to the midline. The motor cortex undergoing photostimulation was divided into 14 × 10 arrays of pixels (0.3 mm spacing), covering a total of 13 mm2. The cross indicates each position of laser photostimulation, and the star indicates the bregma. Scale bar: 2 mm. (B): Primary motor cortex map constructed using optogenetic methods, with different colors indicating different parts. (C): Percentage of different types of body movements represented in the primary motor cortex. The caudal forelimb (CF) is shown in blue, the rostral forelimb (RF) is shown in yellow, the jaw (J) is shown in dark blue, the trunk (T) in shown in green, the neck (N) is shown in purple, the vibrissa (V) are shown in red, and the hindlimb (H) is shown in orange. (D): Accumulated areas representing different types of body movements with standard errors. (E): Primary motor cortex map constructed using optogenetic methods, with different colors indicating the different forelimb muscles. (F): Percentage of different types of forelimb movements represented in the primary motor cortex. The triceps muscle (Tr) is shown in purple, the wrist extension muscle (WE) in shown in gray, the biceps muscle (Bi) is shown in dark blue, the forearm flexor muscles (F) are shown in green, and the finger extension muscles (FE) are shown in orange. (G): Accumulated areas representing the different types of forelimb muscles with standard error.
Fig. 7
Fig. 7 Generation of the MEP map and optogenetic-electromyography mapping of the forelimb muscles in representative normal mice. (A): An example MEP trace evoked by the laser. The dotted line indicates the firing of the laser. (B): The MEP traces evoked by the laser were projected at all positions of M1. The recording electrode and the reference electrode Strong muscle activities could be recorded especially in the center of the cortex, with the muscle evoked potential as large as 1 mV, while in some other areas at the corners, no muscle evoked potentials could be recorded. (C): From left to right: Pictures showing the motor cortical representations of the triceps, forearm extensors and biceps on both sides of a normal transgenic mouse. The brightness encodes the MEP signal amplitude. The brighter the color, the larger the MEP amplitude.

Equations (1)

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ω S a m p l e = 50 Z o o m R a t i o O b j M a g ( μ m )

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