Abstract

Fiber photometry has become increasingly popular among neuroscientists as a convenient tool for the recording of genetically defined neuronal population in behaving animals. Here, we report the development of the multi-channel fiber photometry system to simultaneously monitor neural activities in several brain areas of an animal or in different animals. In this system, a galvano-mirror modulates and cyclically couples the excitation light to individual multimode optical fiber bundles. A single photodetector collects excited light and the configuration of fiber bundle assembly and the scanner determines the total channel number. We demonstrated that the system exhibited negligible crosstalk between channels and optical signals could be sampled simultaneously with a sample rate of at least 100 Hz for each channel, which is sufficient for recording calcium signals. Using this system, we successfully recorded GCaMP6 fluorescent signals from the bilateral barrel cortices of a head-restrained mouse in a dual-channel mode, and the orbitofrontal cortices of multiple freely moving mice in a triple-channel mode. The multi-channel fiber photometry system would be a valuable tool for simultaneous recordings of population activities in different brain areas of a given animal and different interacting individuals.

© 2015 Optical Society of America

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References

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2015 (6)

F. Fuhrmann, D. Justus, L. Sosulina, H. Kaneko, T. Beutel, D. Friedrichs, S. Schoch, M. K. Schwarz, M. Fuhrmann, and S. Remy, “Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit,” Neuron 86(5), 1253–1264 (2015).
[Crossref] [PubMed]

Y. Chen, Y. C. Lin, T. W. Kuo, and Z. A. Knight, “Sensory detection of food rapidly modulates arcuate feeding circuits,” Cell 160(5), 829–841 (2015).
[Crossref] [PubMed]

J. N. Betley, S. Xu, Z. F. Cao, R. Gong, C. J. Magnus, Y. Yu, and S. M. Sternson, “Neurons for hunger and thirst transmit a negative-valence teaching signal,” Nature 521(7551), 180–185 (2015).
[Crossref] [PubMed]

C. M. Lewis, C. A. Bosman, and P. Fries, “Recording of brain activity across spatial scales,” Curr. Opin. Neurobiol. 32, 68–77 (2015).
[Crossref] [PubMed]

T. A. Stalnaker, N. K. Cooch, and G. Schoenbaum, “What the orbitofrontal cortex does not do,” Nat. Neurosci. 18(5), 620–627 (2015).
[Crossref] [PubMed]

S. P. Peron, J. Freeman, V. Iyer, C. Guo, and K. Svoboda, “A Cellular Resolution Map of Barrel Cortex Activity during Tactile Behavior,” Neuron 86(3), 783–799 (2015).
[Crossref] [PubMed]

2014 (5)

M. Paukert, A. Agarwal, J. Cha, V. A. Doze, J. U. Kang, and D. E. Bergles, “Norepinephrine controls astroglial responsiveness to local circuit activity,” Neuron 82(6), 1263–1270 (2014).
[Crossref] [PubMed]

H. Adelsberger, A. Zainos, M. Alvarez, R. Romo, and A. Konnerth, “Local domains of motor cortical activity revealed by fiber-optic calcium recordings in behaving nonhuman primates,” Proc. Natl. Acad. Sci. U.S.A. 111(1), 463–468 (2014).
[Crossref] [PubMed]

G. Cui, S. B. Jun, X. Jin, G. Luo, M. D. Pham, D. M. Lovinger, S. S. Vogel, and R. M. Costa, “Deep brain optical measurements of cell type-specific neural activity in behaving mice,” Nat. Protoc. 9(6), 1213–1228 (2014).
[Crossref] [PubMed]

L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157(7), 1535–1551 (2014).
[Crossref] [PubMed]

Z. Liu, J. Zhou, Y. Li, F. Hu, Y. Lu, M. Ma, Q. Feng, J. E. Zhang, D. Wang, J. Zeng, J. Bao, J. Y. Kim, Z. F. Chen, S. El Mestikawy, and M. Luo, “Dorsal raphe neurons signal reward through 5-HT and glutamate,” Neuron 81(6), 1360–1374 (2014).
[Crossref] [PubMed]

2013 (5)

Y. Ziv, L. D. Burns, E. D. Cocker, E. O. Hamel, K. K. Ghosh, L. J. Kitch, A. El Gamal, and M. J. Schnitzer, “Long-term dynamics of CA1 hippocampal place codes,” Nat. Neurosci. 16(3), 264–266 (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]

G. Cui, S. B. Jun, X. Jin, M. D. Pham, S. S. Vogel, D. M. Lovinger, and R. M. Costa, “Concurrent activation of striatal direct and indirect pathways during action initiation,” Nature 494(7436), 238–242 (2013).
[Crossref] [PubMed]

A. Stroh, H. Adelsberger, A. Groh, C. Rühlmann, S. Fischer, A. Schierloh, K. Deisseroth, and A. Konnerth, “Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo,” Neuron 77(6), 1136–1150 (2013).
[Crossref] [PubMed]

D. Feldmeyer, M. Brecht, F. Helmchen, C. C. Petersen, J. F. Poulet, J. F. Staiger, H. J. Luhmann, and C. Schwarz, “Barrel cortex function,” Prog. Neurobiol. 103, 3–27 (2013).
[Crossref] [PubMed]

2012 (2)

C. Grienberger, H. Adelsberger, A. Stroh, R. I. Milos, O. Garaschuk, A. Schierloh, I. Nelken, and A. Konnerth, “Sound-evoked network calcium transients in mouse auditory cortex in vivo,” J. Physiol. 590(4), 899–918 (2012).
[Crossref] [PubMed]

J. Y. Cohen, S. Haesler, L. Vong, B. B. Lowell, and N. Uchida, “Neuron-type-specific signals for reward and punishment in the ventral tegmental area,” Nature 482(7383), 85–88 (2012).
[Crossref] [PubMed]

2011 (3)

P. Anikeeva, A. S. Andalman, I. Witten, M. Warden, I. Goshen, L. Grosenick, L. A. Gunaydin, L. M. Frank, and K. Deisseroth, “Optetrode: a multichannel readout for optogenetic control in freely moving mice,” Nat. Neurosci. 15(1), 163–170 (2011).
[Crossref] [PubMed]

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. E. Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8(10), 871–878 (2011).
[Crossref] [PubMed]

S. E. Morrison, A. Saez, B. Lau, and C. D. Salzman, “Different time courses for learning-related changes in amygdala and orbitofrontal cortex,” Neuron 71(6), 1127–1140 (2011).
[Crossref] [PubMed]

2010 (3)

C. Zhan and M. Luo, “Diverse patterns of odor representation by neurons in the anterior piriform cortex of awake mice,” J. Neurosci. 30(49), 16662–16672 (2010).
[Crossref] [PubMed]

T. Komiyama, T. R. Sato, D. H. O’Connor, Y. X. Zhang, D. Huber, B. M. Hooks, M. Gabitto, and K. Svoboda, “Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice,” Nature 464(7292), 1182–1186 (2010).
[Crossref] [PubMed]

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

2007 (1)

M. Brecht, “Barrel cortex and whisker-mediated behaviors,” Curr. Opin. Neurobiol. 17(4), 408–416 (2007).
[Crossref] [PubMed]

2005 (2)

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

H. Adelsberger, O. Garaschuk, and A. Konnerth, “Cortical calcium waves in resting newborn mice,” Nat. Neurosci. 8(8), 988–990 (2005).
[Crossref] [PubMed]

2003 (2)

C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
[Crossref] [PubMed]

M. A. Nicolelis, D. Dimitrov, J. M. Carmena, R. Crist, G. Lehew, J. D. Kralik, and S. P. Wise, “Chronic, multisite, multielectrode recordings in macaque monkeys,” Proc. Natl. Acad. Sci. USA 100(19), 11041–11046 (2003).
[Crossref] [PubMed]

2001 (1)

J. O’Doherty, M. L. Kringelbach, E. T. Rolls, J. Hornak, and C. Andrews, “Abstract reward and punishment representations in the human orbitofrontal cortex,” Nat. Neurosci. 4(1), 95–102 (2001).
[Crossref] [PubMed]

2000 (2)

A. Bechara, H. Damasio, and A. R. Damasio, “Emotion, decision making and the orbitofrontal cortex,” Cereb. Cortex 10(3), 295–307 (2000).
[Crossref] [PubMed]

E. T. Rolls, “The orbitofrontal cortex and reward,” Cereb. Cortex 10(3), 284–294 (2000).
[Crossref] [PubMed]

1997 (1)

P. R. Roelfsema, A. K. Engel, P. König, and W. Singer, “Visuomotor integration is associated with zero time-lag synchronization among cortical areas,” Nature 385(6612), 157–161 (1997).
[Crossref] [PubMed]

Adelsberger, H.

H. Adelsberger, A. Zainos, M. Alvarez, R. Romo, and A. Konnerth, “Local domains of motor cortical activity revealed by fiber-optic calcium recordings in behaving nonhuman primates,” Proc. Natl. Acad. Sci. U.S.A. 111(1), 463–468 (2014).
[Crossref] [PubMed]

A. Stroh, H. Adelsberger, A. Groh, C. Rühlmann, S. Fischer, A. Schierloh, K. Deisseroth, and A. Konnerth, “Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo,” Neuron 77(6), 1136–1150 (2013).
[Crossref] [PubMed]

C. Grienberger, H. Adelsberger, A. Stroh, R. I. Milos, O. Garaschuk, A. Schierloh, I. Nelken, and A. Konnerth, “Sound-evoked network calcium transients in mouse auditory cortex in vivo,” J. Physiol. 590(4), 899–918 (2012).
[Crossref] [PubMed]

H. Adelsberger, O. Garaschuk, and A. Konnerth, “Cortical calcium waves in resting newborn mice,” Nat. Neurosci. 8(8), 988–990 (2005).
[Crossref] [PubMed]

Adhikari, A.

L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157(7), 1535–1551 (2014).
[Crossref] [PubMed]

Agarwal, A.

M. Paukert, A. Agarwal, J. Cha, V. A. Doze, J. U. Kang, and D. E. Bergles, “Norepinephrine controls astroglial responsiveness to local circuit activity,” Neuron 82(6), 1263–1270 (2014).
[Crossref] [PubMed]

Airan, R. D.

L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157(7), 1535–1551 (2014).
[Crossref] [PubMed]

Alvarez, M.

H. Adelsberger, A. Zainos, M. Alvarez, R. Romo, and A. Konnerth, “Local domains of motor cortical activity revealed by fiber-optic calcium recordings in behaving nonhuman primates,” Proc. Natl. Acad. Sci. U.S.A. 111(1), 463–468 (2014).
[Crossref] [PubMed]

Andalman, A. S.

P. Anikeeva, A. S. Andalman, I. Witten, M. Warden, I. Goshen, L. Grosenick, L. A. Gunaydin, L. M. Frank, and K. Deisseroth, “Optetrode: a multichannel readout for optogenetic control in freely moving mice,” Nat. Neurosci. 15(1), 163–170 (2011).
[Crossref] [PubMed]

Andrews, C.

J. O’Doherty, M. L. Kringelbach, E. T. Rolls, J. Hornak, and C. Andrews, “Abstract reward and punishment representations in the human orbitofrontal cortex,” Nat. Neurosci. 4(1), 95–102 (2001).
[Crossref] [PubMed]

Anikeeva, P.

L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157(7), 1535–1551 (2014).
[Crossref] [PubMed]

P. Anikeeva, A. S. Andalman, I. Witten, M. Warden, I. Goshen, L. Grosenick, L. A. Gunaydin, L. M. Frank, and K. Deisseroth, “Optetrode: a multichannel readout for optogenetic control in freely moving mice,” Nat. Neurosci. 15(1), 163–170 (2011).
[Crossref] [PubMed]

Astori, S.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Bao, J.

Z. Liu, J. Zhou, Y. Li, F. Hu, Y. Lu, M. Ma, Q. Feng, J. E. Zhang, D. Wang, J. Zeng, J. Bao, J. Y. Kim, Z. F. Chen, S. El Mestikawy, and M. Luo, “Dorsal raphe neurons signal reward through 5-HT and glutamate,” Neuron 81(6), 1360–1374 (2014).
[Crossref] [PubMed]

Baohan, A.

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[Crossref] [PubMed]

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G. Cui, S. B. Jun, X. Jin, G. Luo, M. D. Pham, D. M. Lovinger, S. S. Vogel, and R. M. Costa, “Deep brain optical measurements of cell type-specific neural activity in behaving mice,” Nat. Protoc. 9(6), 1213–1228 (2014).
[Crossref] [PubMed]

G. Cui, S. B. Jun, X. Jin, M. D. Pham, S. S. Vogel, D. M. Lovinger, and R. M. Costa, “Concurrent activation of striatal direct and indirect pathways during action initiation,” Nature 494(7436), 238–242 (2013).
[Crossref] [PubMed]

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G. Cui, S. B. Jun, X. Jin, G. Luo, M. D. Pham, D. M. Lovinger, S. S. Vogel, and R. M. Costa, “Deep brain optical measurements of cell type-specific neural activity in behaving mice,” Nat. Protoc. 9(6), 1213–1228 (2014).
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F. Fuhrmann, D. Justus, L. Sosulina, H. Kaneko, T. Beutel, D. Friedrichs, S. Schoch, M. K. Schwarz, M. Fuhrmann, and S. Remy, “Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit,” Neuron 86(5), 1253–1264 (2015).
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M. Paukert, A. Agarwal, J. Cha, V. A. Doze, J. U. Kang, and D. E. Bergles, “Norepinephrine controls astroglial responsiveness to local circuit activity,” Neuron 82(6), 1263–1270 (2014).
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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).
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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).
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Z. Liu, J. Zhou, Y. Li, F. Hu, Y. Lu, M. Ma, Q. Feng, J. E. Zhang, D. Wang, J. Zeng, J. Bao, J. Y. Kim, Z. F. Chen, S. El Mestikawy, and M. Luo, “Dorsal raphe neurons signal reward through 5-HT and glutamate,” Neuron 81(6), 1360–1374 (2014).
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Y. Ziv, L. D. Burns, E. D. Cocker, E. O. Hamel, K. K. Ghosh, L. J. Kitch, A. El Gamal, and M. J. Schnitzer, “Long-term dynamics of CA1 hippocampal place codes,” Nat. Neurosci. 16(3), 264–266 (2013).
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P. R. Roelfsema, A. K. Engel, P. König, and W. Singer, “Visuomotor integration is associated with zero time-lag synchronization among cortical areas,” Nature 385(6612), 157–161 (1997).
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H. Adelsberger, A. Zainos, M. Alvarez, R. Romo, and A. Konnerth, “Local domains of motor cortical activity revealed by fiber-optic calcium recordings in behaving nonhuman primates,” Proc. Natl. Acad. Sci. U.S.A. 111(1), 463–468 (2014).
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M. A. Nicolelis, D. Dimitrov, J. M. Carmena, R. Crist, G. Lehew, J. D. Kralik, and S. P. Wise, “Chronic, multisite, multielectrode recordings in macaque monkeys,” Proc. Natl. Acad. Sci. USA 100(19), 11041–11046 (2003).
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J. O’Doherty, M. L. Kringelbach, E. T. Rolls, J. Hornak, and C. Andrews, “Abstract reward and punishment representations in the human orbitofrontal cortex,” Nat. Neurosci. 4(1), 95–102 (2001).
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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
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Y. Chen, Y. C. Lin, T. W. Kuo, and Z. A. Knight, “Sensory detection of food rapidly modulates arcuate feeding circuits,” Cell 160(5), 829–841 (2015).
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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
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S. E. Morrison, A. Saez, B. Lau, and C. D. Salzman, “Different time courses for learning-related changes in amygdala and orbitofrontal cortex,” Neuron 71(6), 1127–1140 (2011).
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Y. Chen, Y. C. Lin, T. W. Kuo, and Z. A. Knight, “Sensory detection of food rapidly modulates arcuate feeding circuits,” Cell 160(5), 829–841 (2015).
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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).
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G. Cui, S. B. Jun, X. Jin, G. Luo, M. D. Pham, D. M. Lovinger, S. S. Vogel, and R. M. Costa, “Deep brain optical measurements of cell type-specific neural activity in behaving mice,” Nat. Protoc. 9(6), 1213–1228 (2014).
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G. Cui, S. B. Jun, X. Jin, M. D. Pham, S. S. Vogel, D. M. Lovinger, and R. M. Costa, “Concurrent activation of striatal direct and indirect pathways during action initiation,” Nature 494(7436), 238–242 (2013).
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D. Feldmeyer, M. Brecht, F. Helmchen, C. C. Petersen, J. F. Poulet, J. F. Staiger, H. J. Luhmann, and C. Schwarz, “Barrel cortex function,” Prog. Neurobiol. 103, 3–27 (2013).
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G. Cui, S. B. Jun, X. Jin, G. Luo, M. D. Pham, D. M. Lovinger, S. S. Vogel, and R. M. Costa, “Deep brain optical measurements of cell type-specific neural activity in behaving mice,” Nat. Protoc. 9(6), 1213–1228 (2014).
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C. Zhan and M. Luo, “Diverse patterns of odor representation by neurons in the anterior piriform cortex of awake mice,” J. Neurosci. 30(49), 16662–16672 (2010).
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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
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Z. Liu, J. Zhou, Y. Li, F. Hu, Y. Lu, M. Ma, Q. Feng, J. E. Zhang, D. Wang, J. Zeng, J. Bao, J. Y. Kim, Z. F. Chen, S. El Mestikawy, and M. Luo, “Dorsal raphe neurons signal reward through 5-HT and glutamate,” Neuron 81(6), 1360–1374 (2014).
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L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157(7), 1535–1551 (2014).
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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
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C. Grienberger, H. Adelsberger, A. Stroh, R. I. Milos, O. Garaschuk, A. Schierloh, I. Nelken, and A. Konnerth, “Sound-evoked network calcium transients in mouse auditory cortex in vivo,” J. Physiol. 590(4), 899–918 (2012).
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L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157(7), 1535–1551 (2014).
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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
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S. E. Morrison, A. Saez, B. Lau, and C. D. Salzman, “Different time courses for learning-related changes in amygdala and orbitofrontal cortex,” Neuron 71(6), 1127–1140 (2011).
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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
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C. Grienberger, H. Adelsberger, A. Stroh, R. I. Milos, O. Garaschuk, A. Schierloh, I. Nelken, and A. Konnerth, “Sound-evoked network calcium transients in mouse auditory cortex in vivo,” J. Physiol. 590(4), 899–918 (2012).
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M. A. Nicolelis, D. Dimitrov, J. M. Carmena, R. Crist, G. Lehew, J. D. Kralik, and S. P. Wise, “Chronic, multisite, multielectrode recordings in macaque monkeys,” Proc. Natl. Acad. Sci. USA 100(19), 11041–11046 (2003).
[Crossref] [PubMed]

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K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. E. Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8(10), 871–878 (2011).
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T. Komiyama, T. R. Sato, D. H. O’Connor, Y. X. Zhang, D. Huber, B. M. Hooks, M. Gabitto, and K. Svoboda, “Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice,” Nature 464(7292), 1182–1186 (2010).
[Crossref] [PubMed]

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J. O’Doherty, M. L. Kringelbach, E. T. Rolls, J. Hornak, and C. Andrews, “Abstract reward and punishment representations in the human orbitofrontal cortex,” Nat. Neurosci. 4(1), 95–102 (2001).
[Crossref] [PubMed]

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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]

Paukert, M.

M. Paukert, A. Agarwal, J. Cha, V. A. Doze, J. U. Kang, and D. E. Bergles, “Norepinephrine controls astroglial responsiveness to local circuit activity,” Neuron 82(6), 1263–1270 (2014).
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S. P. Peron, J. Freeman, V. Iyer, C. Guo, and K. Svoboda, “A Cellular Resolution Map of Barrel Cortex Activity during Tactile Behavior,” Neuron 86(3), 783–799 (2015).
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D. Feldmeyer, M. Brecht, F. Helmchen, C. C. Petersen, J. F. Poulet, J. F. Staiger, H. J. Luhmann, and C. Schwarz, “Barrel cortex function,” Prog. Neurobiol. 103, 3–27 (2013).
[Crossref] [PubMed]

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G. Cui, S. B. Jun, X. Jin, G. Luo, M. D. Pham, D. M. Lovinger, S. S. Vogel, and R. M. Costa, “Deep brain optical measurements of cell type-specific neural activity in behaving mice,” Nat. Protoc. 9(6), 1213–1228 (2014).
[Crossref] [PubMed]

G. Cui, S. B. Jun, X. Jin, M. D. Pham, S. S. Vogel, D. M. Lovinger, and R. M. Costa, “Concurrent activation of striatal direct and indirect pathways during action initiation,” Nature 494(7436), 238–242 (2013).
[Crossref] [PubMed]

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D. Feldmeyer, M. Brecht, F. Helmchen, C. C. Petersen, J. F. Poulet, J. F. Staiger, H. J. Luhmann, and C. Schwarz, “Barrel cortex function,” Prog. Neurobiol. 103, 3–27 (2013).
[Crossref] [PubMed]

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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]

Remy, S.

F. Fuhrmann, D. Justus, L. Sosulina, H. Kaneko, T. Beutel, D. Friedrichs, S. Schoch, M. K. Schwarz, M. Fuhrmann, and S. Remy, “Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit,” Neuron 86(5), 1253–1264 (2015).
[Crossref] [PubMed]

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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]

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P. R. Roelfsema, A. K. Engel, P. König, and W. Singer, “Visuomotor integration is associated with zero time-lag synchronization among cortical areas,” Nature 385(6612), 157–161 (1997).
[Crossref] [PubMed]

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J. O’Doherty, M. L. Kringelbach, E. T. Rolls, J. Hornak, and C. Andrews, “Abstract reward and punishment representations in the human orbitofrontal cortex,” Nat. Neurosci. 4(1), 95–102 (2001).
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H. Adelsberger, A. Zainos, M. Alvarez, R. Romo, and A. Konnerth, “Local domains of motor cortical activity revealed by fiber-optic calcium recordings in behaving nonhuman primates,” Proc. Natl. Acad. Sci. U.S.A. 111(1), 463–468 (2014).
[Crossref] [PubMed]

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A. Stroh, H. Adelsberger, A. Groh, C. Rühlmann, S. Fischer, A. Schierloh, K. Deisseroth, and A. Konnerth, “Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo,” Neuron 77(6), 1136–1150 (2013).
[Crossref] [PubMed]

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S. E. Morrison, A. Saez, B. Lau, and C. D. Salzman, “Different time courses for learning-related changes in amygdala and orbitofrontal cortex,” Neuron 71(6), 1127–1140 (2011).
[Crossref] [PubMed]

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S. E. Morrison, A. Saez, B. Lau, and C. D. Salzman, “Different time courses for learning-related changes in amygdala and orbitofrontal cortex,” Neuron 71(6), 1127–1140 (2011).
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T. Komiyama, T. R. Sato, D. H. O’Connor, Y. X. Zhang, D. Huber, B. M. Hooks, M. Gabitto, and K. Svoboda, “Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice,” Nature 464(7292), 1182–1186 (2010).
[Crossref] [PubMed]

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A. Stroh, H. Adelsberger, A. Groh, C. Rühlmann, S. Fischer, A. Schierloh, K. Deisseroth, and A. Konnerth, “Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo,” Neuron 77(6), 1136–1150 (2013).
[Crossref] [PubMed]

C. Grienberger, H. Adelsberger, A. Stroh, R. I. Milos, O. Garaschuk, A. Schierloh, I. Nelken, and A. Konnerth, “Sound-evoked network calcium transients in mouse auditory cortex in vivo,” J. Physiol. 590(4), 899–918 (2012).
[Crossref] [PubMed]

Schnitzer, M. J.

Y. Ziv, L. D. Burns, E. D. Cocker, E. O. Hamel, K. K. Ghosh, L. J. Kitch, A. El Gamal, and M. J. Schnitzer, “Long-term dynamics of CA1 hippocampal place codes,” Nat. Neurosci. 16(3), 264–266 (2013).
[Crossref] [PubMed]

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. E. Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8(10), 871–878 (2011).
[Crossref] [PubMed]

Schoch, S.

F. Fuhrmann, D. Justus, L. Sosulina, H. Kaneko, T. Beutel, D. Friedrichs, S. Schoch, M. K. Schwarz, M. Fuhrmann, and S. Remy, “Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit,” Neuron 86(5), 1253–1264 (2015).
[Crossref] [PubMed]

Schoenbaum, G.

T. A. Stalnaker, N. K. Cooch, and G. Schoenbaum, “What the orbitofrontal cortex does not do,” Nat. Neurosci. 18(5), 620–627 (2015).
[Crossref] [PubMed]

Schreiter, E. R.

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]

Schwarz, C.

D. Feldmeyer, M. Brecht, F. Helmchen, C. C. Petersen, J. F. Poulet, J. F. Staiger, H. J. Luhmann, and C. Schwarz, “Barrel cortex function,” Prog. Neurobiol. 103, 3–27 (2013).
[Crossref] [PubMed]

Schwarz, M. K.

F. Fuhrmann, D. Justus, L. Sosulina, H. Kaneko, T. Beutel, D. Friedrichs, S. Schoch, M. K. Schwarz, M. Fuhrmann, and S. Remy, “Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit,” Neuron 86(5), 1253–1264 (2015).
[Crossref] [PubMed]

Singer, W.

P. R. Roelfsema, A. K. Engel, P. König, and W. Singer, “Visuomotor integration is associated with zero time-lag synchronization among cortical areas,” Nature 385(6612), 157–161 (1997).
[Crossref] [PubMed]

Sosulina, L.

F. Fuhrmann, D. Justus, L. Sosulina, H. Kaneko, T. Beutel, D. Friedrichs, S. Schoch, M. K. Schwarz, M. Fuhrmann, and S. Remy, “Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit,” Neuron 86(5), 1253–1264 (2015).
[Crossref] [PubMed]

Sprengel, R.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Staiger, J. F.

D. Feldmeyer, M. Brecht, F. Helmchen, C. C. Petersen, J. F. Poulet, J. F. Staiger, H. J. Luhmann, and C. Schwarz, “Barrel cortex function,” Prog. Neurobiol. 103, 3–27 (2013).
[Crossref] [PubMed]

Stalnaker, T. A.

T. A. Stalnaker, N. K. Cooch, and G. Schoenbaum, “What the orbitofrontal cortex does not do,” Nat. Neurosci. 18(5), 620–627 (2015).
[Crossref] [PubMed]

Sternson, S. M.

J. N. Betley, S. Xu, Z. F. Cao, R. Gong, C. J. Magnus, Y. Yu, and S. M. Sternson, “Neurons for hunger and thirst transmit a negative-valence teaching signal,” Nature 521(7551), 180–185 (2015).
[Crossref] [PubMed]

Stosiek, C.

C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
[Crossref] [PubMed]

Stroh, A.

A. Stroh, H. Adelsberger, A. Groh, C. Rühlmann, S. Fischer, A. Schierloh, K. Deisseroth, and A. Konnerth, “Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo,” Neuron 77(6), 1136–1150 (2013).
[Crossref] [PubMed]

C. Grienberger, H. Adelsberger, A. Stroh, R. I. Milos, O. Garaschuk, A. Schierloh, I. Nelken, and A. Konnerth, “Sound-evoked network calcium transients in mouse auditory cortex in vivo,” J. Physiol. 590(4), 899–918 (2012).
[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.

S. P. Peron, J. Freeman, V. Iyer, C. Guo, and K. Svoboda, “A Cellular Resolution Map of Barrel Cortex Activity during Tactile Behavior,” Neuron 86(3), 783–799 (2015).
[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]

T. Komiyama, T. R. Sato, D. H. O’Connor, Y. X. Zhang, D. Huber, B. M. Hooks, M. Gabitto, and K. Svoboda, “Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice,” Nature 464(7292), 1182–1186 (2010).
[Crossref] [PubMed]

Tang, W.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

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L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157(7), 1535–1551 (2014).
[Crossref] [PubMed]

Uchida, N.

J. Y. Cohen, S. Haesler, L. Vong, B. B. Lowell, and N. Uchida, “Neuron-type-specific signals for reward and punishment in the ventral tegmental area,” Nature 482(7383), 85–88 (2012).
[Crossref] [PubMed]

Vogel, S. S.

G. Cui, S. B. Jun, X. Jin, G. Luo, M. D. Pham, D. M. Lovinger, S. S. Vogel, and R. M. Costa, “Deep brain optical measurements of cell type-specific neural activity in behaving mice,” Nat. Protoc. 9(6), 1213–1228 (2014).
[Crossref] [PubMed]

G. Cui, S. B. Jun, X. Jin, M. D. Pham, S. S. Vogel, D. M. Lovinger, and R. M. Costa, “Concurrent activation of striatal direct and indirect pathways during action initiation,” Nature 494(7436), 238–242 (2013).
[Crossref] [PubMed]

Vong, L.

J. Y. Cohen, S. Haesler, L. Vong, B. B. Lowell, and N. Uchida, “Neuron-type-specific signals for reward and punishment in the ventral tegmental area,” Nature 482(7383), 85–88 (2012).
[Crossref] [PubMed]

Wang, D.

Z. Liu, J. Zhou, Y. Li, F. Hu, Y. Lu, M. Ma, Q. Feng, J. E. Zhang, D. Wang, J. Zeng, J. Bao, J. Y. Kim, Z. F. Chen, S. El Mestikawy, and M. Luo, “Dorsal raphe neurons signal reward through 5-HT and glutamate,” Neuron 81(6), 1360–1374 (2014).
[Crossref] [PubMed]

Warden, M.

P. Anikeeva, A. S. Andalman, I. Witten, M. Warden, I. Goshen, L. Grosenick, L. A. Gunaydin, L. M. Frank, and K. Deisseroth, “Optetrode: a multichannel readout for optogenetic control in freely moving mice,” Nat. Neurosci. 15(1), 163–170 (2011).
[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]

Wise, S. P.

M. A. Nicolelis, D. Dimitrov, J. M. Carmena, R. Crist, G. Lehew, J. D. Kralik, and S. P. Wise, “Chronic, multisite, multielectrode recordings in macaque monkeys,” Proc. Natl. Acad. Sci. USA 100(19), 11041–11046 (2003).
[Crossref] [PubMed]

Witten, I.

P. Anikeeva, A. S. Andalman, I. Witten, M. Warden, I. Goshen, L. Grosenick, L. A. Gunaydin, L. M. Frank, and K. Deisseroth, “Optetrode: a multichannel readout for optogenetic control in freely moving mice,” Nat. Neurosci. 15(1), 163–170 (2011).
[Crossref] [PubMed]

Xu, S.

J. N. Betley, S. Xu, Z. F. Cao, R. Gong, C. J. Magnus, Y. Yu, and S. M. Sternson, “Neurons for hunger and thirst transmit a negative-valence teaching signal,” Nature 521(7551), 180–185 (2015).
[Crossref] [PubMed]

Yang, Y.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Yu, Y.

J. N. Betley, S. Xu, Z. F. Cao, R. Gong, C. J. Magnus, Y. Yu, and S. M. Sternson, “Neurons for hunger and thirst transmit a negative-valence teaching signal,” Nature 521(7551), 180–185 (2015).
[Crossref] [PubMed]

Zainos, A.

H. Adelsberger, A. Zainos, M. Alvarez, R. Romo, and A. Konnerth, “Local domains of motor cortical activity revealed by fiber-optic calcium recordings in behaving nonhuman primates,” Proc. Natl. Acad. Sci. U.S.A. 111(1), 463–468 (2014).
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Zalocusky, K. A.

L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157(7), 1535–1551 (2014).
[Crossref] [PubMed]

Zeng, J.

Z. Liu, J. Zhou, Y. Li, F. Hu, Y. Lu, M. Ma, Q. Feng, J. E. Zhang, D. Wang, J. Zeng, J. Bao, J. Y. Kim, Z. F. Chen, S. El Mestikawy, and M. Luo, “Dorsal raphe neurons signal reward through 5-HT and glutamate,” Neuron 81(6), 1360–1374 (2014).
[Crossref] [PubMed]

Zhan, C.

C. Zhan and M. Luo, “Diverse patterns of odor representation by neurons in the anterior piriform cortex of awake mice,” J. Neurosci. 30(49), 16662–16672 (2010).
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Zhang, J. E.

Z. Liu, J. Zhou, Y. Li, F. Hu, Y. Lu, M. Ma, Q. Feng, J. E. Zhang, D. Wang, J. Zeng, J. Bao, J. Y. Kim, Z. F. Chen, S. El Mestikawy, and M. Luo, “Dorsal raphe neurons signal reward through 5-HT and glutamate,” Neuron 81(6), 1360–1374 (2014).
[Crossref] [PubMed]

Zhang, Y. X.

T. Komiyama, T. R. Sato, D. H. O’Connor, Y. X. Zhang, D. Huber, B. M. Hooks, M. Gabitto, and K. Svoboda, “Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice,” Nature 464(7292), 1182–1186 (2010).
[Crossref] [PubMed]

Zhou, J.

Z. Liu, J. Zhou, Y. Li, F. Hu, Y. Lu, M. Ma, Q. Feng, J. E. Zhang, D. Wang, J. Zeng, J. Bao, J. Y. Kim, Z. F. Chen, S. El Mestikawy, and M. Luo, “Dorsal raphe neurons signal reward through 5-HT and glutamate,” Neuron 81(6), 1360–1374 (2014).
[Crossref] [PubMed]

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Y. Ziv, L. D. Burns, E. D. Cocker, E. O. Hamel, K. K. Ghosh, L. J. Kitch, A. El Gamal, and M. J. Schnitzer, “Long-term dynamics of CA1 hippocampal place codes,” Nat. Neurosci. 16(3), 264–266 (2013).
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K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. E. Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8(10), 871–878 (2011).
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Zum Alten Borgloh, S. M.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Cell (2)

L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157(7), 1535–1551 (2014).
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Y. Chen, Y. C. Lin, T. W. Kuo, and Z. A. Knight, “Sensory detection of food rapidly modulates arcuate feeding circuits,” Cell 160(5), 829–841 (2015).
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Cereb. Cortex (2)

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M. Brecht, “Barrel cortex and whisker-mediated behaviors,” Curr. Opin. Neurobiol. 17(4), 408–416 (2007).
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C. M. Lewis, C. A. Bosman, and P. Fries, “Recording of brain activity across spatial scales,” Curr. Opin. Neurobiol. 32, 68–77 (2015).
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Front. Neural Circuits (1)

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

J. Neurosci. (1)

C. Zhan and M. Luo, “Diverse patterns of odor representation by neurons in the anterior piriform cortex of awake mice,” J. Neurosci. 30(49), 16662–16672 (2010).
[Crossref] [PubMed]

J. Physiol. (1)

C. Grienberger, H. Adelsberger, A. Stroh, R. I. Milos, O. Garaschuk, A. Schierloh, I. Nelken, and A. Konnerth, “Sound-evoked network calcium transients in mouse auditory cortex in vivo,” J. Physiol. 590(4), 899–918 (2012).
[Crossref] [PubMed]

Nat. Methods (2)

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. E. Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8(10), 871–878 (2011).
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F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
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Nat. Neurosci. (5)

Y. Ziv, L. D. Burns, E. D. Cocker, E. O. Hamel, K. K. Ghosh, L. J. Kitch, A. El Gamal, and M. J. Schnitzer, “Long-term dynamics of CA1 hippocampal place codes,” Nat. Neurosci. 16(3), 264–266 (2013).
[Crossref] [PubMed]

H. Adelsberger, O. Garaschuk, and A. Konnerth, “Cortical calcium waves in resting newborn mice,” Nat. Neurosci. 8(8), 988–990 (2005).
[Crossref] [PubMed]

P. Anikeeva, A. S. Andalman, I. Witten, M. Warden, I. Goshen, L. Grosenick, L. A. Gunaydin, L. M. Frank, and K. Deisseroth, “Optetrode: a multichannel readout for optogenetic control in freely moving mice,” Nat. Neurosci. 15(1), 163–170 (2011).
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J. O’Doherty, M. L. Kringelbach, E. T. Rolls, J. Hornak, and C. Andrews, “Abstract reward and punishment representations in the human orbitofrontal cortex,” Nat. Neurosci. 4(1), 95–102 (2001).
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T. A. Stalnaker, N. K. Cooch, and G. Schoenbaum, “What the orbitofrontal cortex does not do,” Nat. Neurosci. 18(5), 620–627 (2015).
[Crossref] [PubMed]

Nat. Protoc. (1)

G. Cui, S. B. Jun, X. Jin, G. Luo, M. D. Pham, D. M. Lovinger, S. S. Vogel, and R. M. Costa, “Deep brain optical measurements of cell type-specific neural activity in behaving mice,” Nat. Protoc. 9(6), 1213–1228 (2014).
[Crossref] [PubMed]

Nature (6)

P. R. Roelfsema, A. K. Engel, P. König, and W. Singer, “Visuomotor integration is associated with zero time-lag synchronization among cortical areas,” Nature 385(6612), 157–161 (1997).
[Crossref] [PubMed]

J. N. Betley, S. Xu, Z. F. Cao, R. Gong, C. J. Magnus, Y. Yu, and S. M. Sternson, “Neurons for hunger and thirst transmit a negative-valence teaching signal,” Nature 521(7551), 180–185 (2015).
[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]

J. Y. Cohen, S. Haesler, L. Vong, B. B. Lowell, and N. Uchida, “Neuron-type-specific signals for reward and punishment in the ventral tegmental area,” Nature 482(7383), 85–88 (2012).
[Crossref] [PubMed]

G. Cui, S. B. Jun, X. Jin, M. D. Pham, S. S. Vogel, D. M. Lovinger, and R. M. Costa, “Concurrent activation of striatal direct and indirect pathways during action initiation,” Nature 494(7436), 238–242 (2013).
[Crossref] [PubMed]

T. Komiyama, T. R. Sato, D. H. O’Connor, Y. X. Zhang, D. Huber, B. M. Hooks, M. Gabitto, and K. Svoboda, “Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice,” Nature 464(7292), 1182–1186 (2010).
[Crossref] [PubMed]

Neuron (6)

F. Fuhrmann, D. Justus, L. Sosulina, H. Kaneko, T. Beutel, D. Friedrichs, S. Schoch, M. K. Schwarz, M. Fuhrmann, and S. Remy, “Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit,” Neuron 86(5), 1253–1264 (2015).
[Crossref] [PubMed]

A. Stroh, H. Adelsberger, A. Groh, C. Rühlmann, S. Fischer, A. Schierloh, K. Deisseroth, and A. Konnerth, “Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo,” Neuron 77(6), 1136–1150 (2013).
[Crossref] [PubMed]

Z. Liu, J. Zhou, Y. Li, F. Hu, Y. Lu, M. Ma, Q. Feng, J. E. Zhang, D. Wang, J. Zeng, J. Bao, J. Y. Kim, Z. F. Chen, S. El Mestikawy, and M. Luo, “Dorsal raphe neurons signal reward through 5-HT and glutamate,” Neuron 81(6), 1360–1374 (2014).
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M. Paukert, A. Agarwal, J. Cha, V. A. Doze, J. U. Kang, and D. E. Bergles, “Norepinephrine controls astroglial responsiveness to local circuit activity,” Neuron 82(6), 1263–1270 (2014).
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S. P. Peron, J. Freeman, V. Iyer, C. Guo, and K. Svoboda, “A Cellular Resolution Map of Barrel Cortex Activity during Tactile Behavior,” Neuron 86(3), 783–799 (2015).
[Crossref] [PubMed]

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

C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
[Crossref] [PubMed]

H. Adelsberger, A. Zainos, M. Alvarez, R. Romo, and A. Konnerth, “Local domains of motor cortical activity revealed by fiber-optic calcium recordings in behaving nonhuman primates,” Proc. Natl. Acad. Sci. U.S.A. 111(1), 463–468 (2014).
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Proc. Natl. Acad. Sci. USA (1)

M. A. Nicolelis, D. Dimitrov, J. M. Carmena, R. Crist, G. Lehew, J. D. Kralik, and S. P. Wise, “Chronic, multisite, multielectrode recordings in macaque monkeys,” Proc. Natl. Acad. Sci. USA 100(19), 11041–11046 (2003).
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D. Feldmeyer, M. Brecht, F. Helmchen, C. C. Petersen, J. F. Poulet, J. F. Staiger, H. J. Luhmann, and C. Schwarz, “Barrel cortex function,” Prog. Neurobiol. 103, 3–27 (2013).
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J. Cha, D. Kim, G. W. Cheon, and J. U. Kang, “Spatially Multiplexed Fiber-optic SLM Microscopy for Applications of Optogenetics,” in Imaging Systems and Applications, (Optical Society of America, 2015), IM4A. 2.

H. Adelsberger, C. Grienberger, A. Stroh, and A. Konnerth, “In vivo calcium recordings and channelrhodopsin-2 activation through an optical fiber,” Cold Spring Harb Protoc 2014, pdb prot084145 (2014).

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Figures (6)

Fig. 1
Fig. 1 Multi-channel fiber photometry system. (A) Schematic diagram of the extensible multi-channel fiber photometry system. A 488 nm laser is successively coupled to each multimode optical fiber by using the galvano mirror. The excited fluorescent light is then collected by the same optical fiber and detected by the PMT. (B) Schematic diagram of the custom designed multimode fiber bundles for the dual-channel mode (upper) and the triple-channel mode (lower). Both types of fiber bundles are custom designed. Each comprises of the corresponding number of multimode optical fibers aligned in the form of a single line and fixed into the ceramic ferrules.
Fig. 2
Fig. 2 Schematic representation of data acquisition and channel separation for the 2-channel system. The coupling blocks are used to represent the time when the laser is coupled to one of the fibers. Red color is for channel 1 while blue is for channel 2. During recording, the sample clock rate of the DAQ card is several times larger than the sample frequency (f = 100 Hz). The sampled data was grouped according to the coupling block and then averaged to an actual sample value for each channel.
Fig. 3
Fig. 3 The scanner control method and system performance evaluation in the dual-channel mode. (A) Scanner control waveform for dual-channel mode. Red and blue colors are used to represent channel 1 and channel 2, respectively. The scanner input voltage was set to U for channel 1 detection and –U for channel 2 detection. It was set to 0 for scanner protection. The time of one cycle equals the multiplicative inverse of the sampling frequency. (B) The output intensity at the distal end of two individual optical fibers when the scanner input voltage was set to U, 0, and –U. (C) The extinction ratio of each channel. (D) The coupling efficiency of each channel with varying sampling rates. (E) Autofluorescence signals acquired in the dual-channel mode with a white paper as sample.
Fig. 4
Fig. 4 Scanner control and system performance of triple-channel mode. (A) Scanner control waveform for the triple-channel mode. Red, green, and blue colors represent channel 1, 2, and 3, respectively. The scanner input voltage was set to U for channel 1 detection, 0 for channel 2, and –U for channel 3. The time of one cycle equals the multiplicative inverse of the sampling frequency. (B) The output intensity at the distal end of each optical fiber in three states of the scanner. (C) The extinction ratio of each channel. (D) Autofluorescence signals acquired in the triple-channel mode with a white paper as sample.
Fig. 5
Fig. 5 Simultaneous recording of calcium signal from the bilateral barrel cortices in a head-restrained behaving mouse. (A) Schematic diagram of the whisker stimulation experiment. Channels 1 and 2 detected the left and right barrel cortex, respectively. We stimulated whiskers using a trigger-controlled air stream. The trigger signal and the calcium signal were synchronously recorded. (B) GCaMP6 expression (green) in the barrel cortex. The coronal slice is 1.4 mm posterior to bregma. Abbreviations: S1BF, primary somatosensory cortex, barrel field. (C) Calcium signals acquired simultaneously in the bilateral barrel cortices during the whisker stimulation experiment. The red and blue vertical bars mark the time given for the right and left whisker stimulation, respectively. (D) Averaged calcium transient in response to the contralateral whisker stimulation. Red and blue indicate signals from channel 1 and 2. Solid lines represent average calcium transients, whereas the shaded areas indicate SEM.
Fig. 6
Fig. 6 Simultaneous recording of calcium signal from the orbitofrontal cortices (OFC) of three freely moving mice. (A) Schematic diagram of the water approach experiment. Each channel was used to record from the OFC of one thirsty mouse. Only one mouse was allowed to approach sucrose solution at any given moment, (B) Fluorescent photomicrograph of a coronal slice showing GCaMP6m expression in the OFC. The coronal slice is 2.45 mm anterior to bregma. The dashed line shows where the fiber has been implanted. Abbreviations: LO, lateral orbital cortex. (C) Calcium signals acquired simultaneously in the three freely moving mice during the water approach experiment. The red, green, and blue vertical bars mark the time at which the corresponding mouse approached the water. (D) Averaged calcium transient from the three individual mice. Red, green, and blue solid lines represent signals from channels 1, 2, and 3, respectively. Signals were aligned by water approach by mouse 1, 2, and 3 for the left, middle, and right panels, respectively.

Equations (2)

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Ext=10 log 10 ( I on / I off ),
Z=(F F 0 )/σF,

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