In vivo fiber photometry of neural activity in response to optogenetically manipulated inputs in freely moving mice

Liang Li; Yajie Tang; Leqiang Sun; Khaista Rahman; Kai Huang; Weize Xu; Jinsong Yu; Jinxia Dai; Gang Cao

doi:10.1142/s1793545817430015

[1] C. K. Kim, S. J. Yang, N. Pichamoorthy, N. P. Young, I. Kauvar, J. H. Jennings, T. N. Lerner, A. Berndt, S. Y. Lee, C. Ramakrishnan, T. J. Davidson, M. Inoue, H. Bito, K. Deisseroth, “Simultaneous fast measurement of circuit dynamics at multiple sites across the mammalian brain,” Nat. Methods 13, 325-328 (2016) doi:10.1038/nmeth.3770.

[2] Q. Guo, J. Zhou, Q. Feng, R. Lin, H. Gong, Q. Luo, S. Zeng, M. Luo, L. Fu, “Multi-channel fiber photometry for population neuronal activity recording,” Biomed. Opt. Express 6, 3919-3931 (2015) doi:10.1364/BOE.6.003919.

[3] J. T. Russell, “Imaging calcium signals in vivo: A powerful tool in physiology and pharmacology,” Br. J. Pharmacol. 163, 1605-1625 (2011) doi:10.1111/j.1476-5381.2010.00988.x.

[4] C. Grienberger, A. Konnerth, “Imaging calcium in neurons,” Neuron 73, 862-885 (2012) doi:10.1016/j.neuron.2012.02.011.

[5] J. M. Gee, M. B. Gibbons, M. Taheri, S. Palumbos, S. C. Morris, R. M. Smeal, K. F. Flynn, M. N. Economo, C. G. Cizek, M. R. Capecchi, P. Tvrdik, K. S. Wilcox, J. A. White, “Imaging activity in astrocytes and neurons with genetically encoded calcium indicators following in utero electroporation,” Front. Mol. Neurosci. 8, 10 (2015) doi:10.3389/fnmol.2015.00010.

[6] J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderon, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, L. L. Looger, “Optimization of a GCaMP calcium indicator for neural activity imaging,” J. Neurosci. 32, 13819-13840 (2012) doi:10.1523/JNEUROSCI.2601-12.2012.

[7] Y. Zhao, S. Araki, J. Wu, T. Teramoto, Y. F. Chang, M. Nakano, A. S. Abdelfattah, M. Fujiwara, T. Ishihara, T. Nagai and R. E. Campbell, “An expanded palette of genetically encoded Ca(2)( ++ ) indicators,” Science 333, 1888-1891 (2011) doi:10.1126/science.1208592.

[8] M. I. Kotlikoff, “Genetically encoded Ca2 ++ indicators: Using genetics and molecular design to understand complex physiology,” J. Physiol. 578, 55-67 (2007) doi:10.1113/jphysiol.2006.120212.

[9] E. D. Papadakis, S. A. Nicklin, A. H. Baker, S. J. White, “Promoters and control elements: Designing expression cassettes for gene therapy,” Curr. Gene. Ther. 4, 89-113 (2004).

[10] A. Cetin, S. Komai, M. Eliava, P. H. Seeburg, P. Osten, “Stereotaxic gene delivery in the rodent brain,” Nat. Protoc. 1, 3166-3173 (2006) doi:10.1038/nprot.2006.450.

[11] B. Mathon, M. Nassar, J. Simonnet, C. Le Duigou, S. Clemenceau, R. Miles, D. Fricker, “Increasing the effectiveness of intracerebral injections in adult and neonatal mice: A neurosurgical point of view,” Neurosci. Bull. 31, 685-696 (2015) doi:10.1007/s12264-015-1558-0.

[12] 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, D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499, 295-300 (2013) doi:10.1038/nature12354.

[13] K. S. Girven, D. R. Sparta, “Probing deep brain circuitry: New advances in in vivo calcium measurement strategies,” ACS Chem. Neurosci. (2016) doi:10.1021/acschemneuro.6b00307.

[14] 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, K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157, 1535-1551 (2014) doi:10.1016/j.cell.2014.05.017.

[15] T. Shimano, B. Fyk-Kolodziej, N. Mirza, M. Asako, K. Tomoda, S. Bledsoe, Z. H. Pan, S. Molitor, A. G. Holt, “Assessment of the AAV-mediated expression of channelrhodopsin-2 and halorhodopsin in brainstem neurons mediating auditory signaling,” Brain. Res. 1511, 138-152 (2013) doi:10.1016/j.brainres.2012.10.030.

[16] M. J. Krashes, S. Koda, C. Ye, S. C. Rogan, A. C. Adams, D. S. Cusher, E. Maratos-Flier, B. L. Roth, B. B. Lowell, “Rapid, reversible activation of AgRP neurons drives feeding behavior in mice,” J. Clin. Invest. 121, 1424-1428 (2011) doi:10.1172/JCI46229.

[17] N. Zhao, S. Chen, Y. Hong and B. Z. Tang, “A red emitting mitochondria-targeted AIE probe as an indicator for membrane potential and mouse sperm activity,” Chem. Commun. (Camb.) 51, 13599-13602 (2015) doi:10.1039/c5cc04731e.

[18] Z. Han, L. Jin, F. Chen, J. J. Loturco, L. B. Cohen, A. Bondar, J. Lazar and V. A. Pieribone, “Mechanistic studies of the genetically encoded fluorescent protein voltage probe ArcLight,” PLoS One 9, e113873 (2014) doi:10.1371/journal.pone.0113873.

[19] J. S. Marvin, B. G. Borghuis, L. Tian, J. Cichon, M. T. Harnett, J. Akerboom, A. Gordus, S. L. Renninger, T. W. Chen, C. I. Bargmann, M. B. Orger, E. R. Schreiter, J. B. Demb, W. B. Gan, S. A. Hires, L. L. Looger, “An optimized fluorescent probe for visualizing glutamate neurotransmission,” Nat. Methods. 10, 162-170 (2013) doi:10.1038/nmeth.2333.

[20] R. S. Gibson, “A historical review of progress in the assessment of dietary zinc intake as an indicator of population zinc status,” Adv. Nutr. 3, 772-782 (2012) doi:10.3945/an.112.002287.

[21] L. Barnett, J. Platisa, M. Popovic, V. A. Pieribone, T. Hughes, “A fluorescent, genetically-encoded voltage probe capable of resolving action potentials,” PLoS One 7, e43454 (2012) doi:10.1371/journal.pone.0043454.

[22] K. Sreenath, J. R. Allen, M. W. Davidson, L. A. Zhu, “FRET-based indicator for imaging mitochondrial zinc ions,” Chem. Commun. (Camb.) 47, 11730-11732 (2011) doi:10.1039/c1cc14580k.

[23] D. Li, S. Chen, E. A. Bellomo, A. I. Tarasov, C. Kaut, G. A. Rutter, W. H. Li, “Imaging dynamic insulin release using a fluorescent zinc indicator for monitoring induced exocytotic release (ZIMIR),” Proc. Natl. Acad. Sci. USA 108, 21063-21068 (2011) doi:10.1073/pnas.1109773109.

[24] W. Wang, H. Fang, L. Groom, A. Cheng, W. Zhang, J. Liu, X. Wang, K. Li, P. Han, M. Zheng, J. Yin, W. Wang, M. P. Mattson, J. P. Kao, E. G. Lakatta, S. S. Sheu, K. Ouyang, J. Chen, R. T. Dirksen, H. Cheng, “Superoxide flashes in single mitochondria,” Cell 134, 279-290 (2008) doi:10.1016/j.cell.2008.06.017.

[25] H. Kojima, K. Sakurai, K. Kikuchi, S. Kawahara, Y. Kirino, H. Nagoshi, Y. Hirata, T. Akaike, H. Maeda, T. Nagano, “Development of a fluorescent indicator for the bioimaging of nitric oxide,” Biol. Pharm. Bull. 20, 1229-1232 (1997).

[26] R. J. McKenzie, G. F. Azzone and T. E. Conover, “Bulk phase proton fluxes during the generation of membrane potential in rat liver mitochondria,” J. Biol. Chem. 266, 803-809 (1991).

[27] R. L. McKenzie, K. P. Gross, “Two-photon excitation of nitric oxide fluorescence as a temperature indicator in unsteady gasdynamic processes,” Appl. Opt. 20, 2153-2165 (1981) doi:10.1364/AO.20.002153.

[28] T. Tomov, “Pyronin-a fluorescent indicator of membrane potential of the mitochondria. Mechanism of action,” Acta. Physiol. Pharmacol. Bulg. 4, 62-68 (1978).