Cellular level brain imaging in behaving mammals: An engineering approach

Neuron

Volumn 86, Issue 1, 2015, Pages 140-159

  Hamel, Elizabeth J O ^a   Grewe, Benjamin F ^a   Parker, Jones G ^a,b   Schnitzer, Mark J ^a  

^a STANFORD UNIVERSITY   (United States)

^b PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN; GREEN FLUORESCENT PROTEIN;

ACTION POTENTIAL; ANIMAL BEHAVIOR; BODY MOVEMENT; BRAIN FUNCTION; CONNECTOME; DENDRITE; DENDRITIC SPINE; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER; FUNCTIONAL NEUROIMAGING; GENETIC ANALYSIS; HUMAN; IN VIVO STUDY; INTERNEURON; MOUSE; NERVE FIBER; NONHUMAN; OPTICAL INSTRUMENTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; REVIEW; ANIMAL; BRAIN; CYTOLOGY; MAMMAL; NERVE CELL; NEUROIMAGING; OPTOGENETICS; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; HUMANS; MAMMALS; NEUROIMAGING; NEURONS; OPTOGENETICS;

EID: 84930335595     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.03.055     Document Type: Review

References (180)

1. Ahrens M.B., Orger M.B., Robson D.N., Li J.M., Keller P.J. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 2013, 10:413-420.
2. Akemann W., Mutoh H., Perron A., Rossier J., Knöpfel T. Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat. Methods 2010, 7:643-649.
3. Akemann W., Mutoh H., Perron A., Park Y.K., Iwamoto Y., Knöpfel T. Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein. J.Neurophysiol. 2012, 108:2323-2337.
4. Akerboom J., Carreras Calderón N., Tian L., Wabnig S., Prigge M., Tolö J., Gordus A., Orger M.B., Severi K.E., Macklin J.J., et al. Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front. Mol. Neurosci. 2013, 6:2.
5. Alivisatos A.P., Andrews A.M., Boyden E.S., Chun M., Church G.M., Deisseroth K., Donoghue J.P., Fraser S.E., Lippincott-Schwartz J., Looger L.L., et al. Nanotools for neuroscience and brain activity mapping. ACS Nano 2013, 7:1850-1866.
6. Andermann M.L., Kerlin A.M., Reid R.C. Chronic cellular imaging of mouse visual cortex during operant behavior and passive viewing. Front. Cell. Neurosci. 2010, 4:3.
7. Andermann M.L., Kerlin A.M., Roumis D.K., Glickfeld L.L., Reid R.C. Functional specialization of mouse higher visual cortical areas. Neuron 2011, 72:1025-1039.
8. Andermann M.L., Gilfoy N.B., Goldey G.J., Sachdev R.N., Wölfel M., McCormick D.A., Reid R.C., Levene M.J. Chronic cellular imaging of entire cortical columns in awake mice using microprisms. Neuron 2013, 80:900-913.
9. Anselmi F., Ventalon C., Bègue A., Ogden D., Emiliani V. Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning. Proc. Natl. Acad. Sci. USA 2011, 108:19504-19509.
10. Antić S., Zecević D. Optical signals from neurons with internally applied voltage-sensitive dyes. J.Neurosci. 1995, 15:1392-1405.
11. Aronov D., Tank D.W. Engagement of neural circuits underlying 2D spatial navigation in a rodent virtual reality system. Neuron 2014, 84:442-456.
12. Barretto R.P., Messerschmidt B., Schnitzer M.J. Invivo fluorescence imaging with high-resolution microlenses. Nat. Methods 2009, 6:511-512.
13. Barretto R.P.J., Ko T.H., Jung J.C., Wang T.J., Capps G., Waters A.C., Ziv Y., Attardo A., Recht L., Schnitzer M.J. Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy. Nat. Med. 2011, 17:223-228.
14. Bathellier B., Ushakova L., Rumpel S. Discrete neocortical dynamics predict behavioral categorization of sounds. Neuron 2012, 76:435-449.
15. Batista A.P., Buneo C.A., Snyder L.H., Andersen R.A. Reach plans in eye-centered coordinates. Science 1999, 285:257-260.
16. Bègue A., Papagiakoumou E., Leshem B., Conti R., Enke L., Oron D., Emiliani V. Two-photon excitation in scattering media by spatiotemporally shaped beams and their application in optogenetic stimulation. Biomed. Opt. Express 2013, 4:2869-2879.
17. Bell A.J., Sejnowski T.J. An information-maximization approach to blind separation and blind deconvolution. Neural Comput. 1995, 7:1129-1159.
18. Berdyyeva T., Otte S., Aluisio L., Ziv Y., Burns L.D., Dugovic C., Yun S., Ghosh K.K., Schnitzer M.J., Lovenberg T., Bonaventure P. Zolpidem reduces hippocampal neuronal activity in freely behaving mice: a large scale calcium imaging study with miniaturized fluorescence microscope. PLoS ONE 2014, 9:e112068.
19. Blauvelt D.G., Sato T.F., Wienisch M., Knöpfel T., Murthy V.N. Distinct spatiotemporal activity in principal neurons of the mouse olfactory bulb in anesthetized and awake states. Front. Neural Circuits 2013, 7:46.
20. Bouchard M.B., Voleti V., Mendes C.S., Lacefield C., Grueber W.B., Mann R.S., Bruno R.M., Hillman E.M. Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms. Nat. Photonics 2015, 9:113-119.
21. Boyd A.M., Kato H.K., Komiyama T., Isaacson J.S. Broadcasting of cortical activity to the olfactory bulb. Cell Rep. 2015, 10:1032-1039.
22. BRAIN 2025: A Scientific Vision 2014, BRAIN Initiative, U.S. Department ofHealth & Human Services (HHS). http://www.braininitiative.nih.gov/2025/index.htm.
23. Brown G.D., Yamada S., Sejnowski T.J. Independent component analysis at the neural cocktail party. Trends Neurosci. 2001, 24:54-63.
24. Broxton M., Grosenick L., Yang S., Cohen N., Andalman A., Deisseroth K., Levoy M. Wave optics theory and 3-D deconvolution for the lightfield microscope. Opt. Express 2013, 21:25418-25439.
25. Cao G., Platisa J., Pieribone V.A., Raccuglia D., Kunst M., Nitabach M.N. Genetically targeted optical electrophysiology in intact neural circuits. Cell 2013, 154:904-913.
26. Carandini M., Shimaoka D., Rossi L.F., Sato T.K., Benucci A., Knöpfel T. Imaging the awake visual cortex with a genetically encoded voltage indicator. J.Neurosci. 2015, 35:53-63.
27. Carey R.M., Verhagen J.V., Wesson D.W., Pírez N., Wachowiak M. Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J.Neurophysiol. 2009, 101:1073-1088.
28. Chen J.L., Andermann M.L., Keck T., Xu N.L., Ziv Y. Imaging neuronal populations in behaving rodents: paradigms for studying neural circuits underlying behavior in the mammalian cortex. J.Neurosci. 2013, 33:17631-17640.
29. Chen J.L., Carta S., Soldado-Magraner J., Schneider B.L., Helmchen F. Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex. Nature 2013, 499:336-340.
30. Chen T.-W., Wardill T.J., Sun Y., Pulver S.R., Renninger S.L., Baohan A., Schreiter E.R., Kerr R.A., Orger M.B., Jayaraman V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
31. Chia T.H., Levene M.J. Microprisms for invivo multilayer cortical imaging. J.Neurophysiol. 2009, 102:1310-1314.
32. Chow B.Y., Han X., Dobry A.S., Qian X., Chuong A.S., Li M., Henninger M.A., Belfort G.M., Lin Y., Monahan P.E., Boyden E.S. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 2010, 463:98-102.
33. Chung K., Wallace J., Kim S.Y., Kalyanasundaram S., Andalman A.S., Davidson T.J., Mirzabekov J.J., Zalocusky K.A., Mattis J., Denisin A.K., et al. Structural and molecular interrogation of intact biological systems. Nature 2013, 497:332-337.
34. Clancy K.B., Koralek A.C., Costa R.M., Feldman D.E., Carmena J.M. Volitional modulation of optically recorded calcium signals during neuroprosthetic learning. Nat. Neurosci. 2014, 17:807-809.
35. Cyranoski D. Marmosets are stars of Japan's ambitious brain project. Nature 2014, 514:151-152.
36. Dimitrov D., He Y., Mutoh H., Baker B.J., Cohen L., Akemann W., Knöpfel T. Engineering and characterization of an enhanced fluorescent protein voltage sensor. PLoS ONE 2007, 2:e440.
37. Dombeck D.A., Khabbaz A.N., Collman F., Adelman T.L., Tank D.W. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 2007, 56:43-57.
38. Dombeck D.A., Graziano M.S., Tank D.W. Functional clustering of neurons in motor cortex determined by cellular resolution imaging in awake behaving mice. J.Neurosci. 2009, 29:13751-13760.
39. Dombeck D.A., Harvey C.D., Tian L., Looger L.L., Tank D.W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat. Neurosci. 2010, 13:1433-1440.
40. Duemani Reddy G., Kelleher K., Fink R., Saggau P. Three-dimensional random access multiphoton microscopy for functional imaging of neuronal activity. Nat. Neurosci. 2008, 11:713-720.
41. Engelbrecht C.J., Johnston R.S., Seibel E.J., Helmchen F. Ultra-compact fiber-optic two-photon microscope for functional fluorescence imaging invivo. Opt. Express 2008, 16:5556-5564.
42. Ferezou I., Bolea S., Petersen C.C. Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 2006, 50:617-629.
43. Ferezou I., Haiss F., Gentet L.J., Aronoff R., Weber B., Petersen C.C.H. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 2007, 56:907-923.
44. Flusberg B.A., Jung J.C., Cocker E.D., Anderson E.P., Schnitzer M.J. Invivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope. Opt. Lett. 2005, 30:2272-2274.
45. Flusberg B.A., Nimmerjahn A., Cocker E.D., Mukamel E.A., Barretto R.P.J., Ko T.H., Burns L.D., Jung J.C., Schnitzer M.J. High-speed, miniaturized fluorescence microscopy in freely moving mice. Nat. Methods 2008, 5:935-938.
46. Flytzanis N.C., Bedbrook C.N., Chiu H., Engqvist M.K., Xiao C., Chan K.Y., Sternberg P.W., Arnold F.H., Gradinaru V. Archaerhodopsin variants with enhanced voltage-sensitive fluorescence in mammalian and Caenorhabditis elegans neurons. Nat. Commun. 2014, 5:4894.
47. Freeman J., Vladimirov N., Kawashima T., Mu Y., Sofroniew N.J., Bennett D.V., Rosen J., Yang C.T., Looger L.L., Ahrens M.B. Mapping brain activity at scale with cluster computing. Nat. Methods 2014, 11:941-950.
48. Funahashi S., Bruce C.J., Goldman-Rakic P.S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J.Neurophysiol. 1989, 61:331-349.
49. Fuster J.M., Alexander G.E. Neuron activity related to short-term memory. Science 1971, 173:652-654.
50. Ghosh K.K., Burns L.D., Cocker E.D., Nimmerjahn A., Ziv Y., Gamal A.E., Schnitzer M.J. Miniaturized integration of a fluorescence microscope. Nat. Methods 2011, 8:871-878.
51. Glickfeld L.L., Andermann M.L., Bonin V., Reid R.C. Cortico-cortical projections in mouse visual cortex are functionally target specific. Nat. Neurosci. 2013, 16:219-226.
52. Göbel W., Kerr J.N.D., Nimmerjahn A., Helmchen F. Miniaturized two-photon microscope based on a flexible coherent fiber bundle and a gradient-index lens objective. Opt. Lett. 2004, 29:2521-2523.
53. Göbel W., Kampa B.M., Helmchen F. Imaging cellular network dynamics in three dimensions using fast 3D laser scanning. Nat. Methods 2007, 4:73-79.
54. Gong Y., Li J.Z., Schnitzer M.J. Enhanced Archaerhodopsin Fluorescent Protein Voltage Indicators. PLoS ONE 2013, 8:e66959.
55. Gong Y., Wagner M.J., Zhong Li J., Schnitzer M.J. Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors. Nat. Commun. 2014, 5:3674.
56. Greenberg D.S., Kerr J.N. Automated correction of fast motion artifacts for two-photon imaging of awake animals. J.Neurosci. Methods 2009, 176:1-15.
57. Greenberg D.S., Houweling A.R., Kerr J.N.D. Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat. Neurosci. 2008, 11:749-751.
58. Grewe B.F., Langer D., Kasper H., Kampa B.M., Helmchen F. High-speed invivo calcium imaging reveals neuronal network activity with near-millisecond precision. Nat. Methods 2010, 7:399-405.
59. Grinvald A., Frostig R.D., Siegel R.M., Bartfeld E. High-resolution optical imaging of functional brain architecture in the awake monkey. Proc. Natl. Acad. Sci. USA 1991, 88:11559-11563.
60. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
61. Hama H., Kurokawa H., Kawano H., Ando R., Shimogori T., Noda H., Fukami K., Sakaue-Sawano A., Miyawaki A. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat. Neurosci. 2011, 14:1481-1488.
62. Harvey C.D., Collman F., Dombeck D.A., Tank D.W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 2009, 461:941-946.
63. Harvey C.D., Coen P., Tank D.W. Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 2012, 484:62-68.
64. Helmchen F., Imoto K., Sakmann B. Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. Biophys. J. 1996, 70:1069-1081.
65. Helmchen F., Svoboda K., Denk W., Tank D.W. Invivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat. Neurosci. 1999, 2:989-996.
66. Helmchen F., Fee M.S., Tank D.W., Denk W. A miniature head-mounted two-photon microscope. high-resolution brain imaging in freely moving animals. Neuron 2001, 31:903-912.
67. Helmchen F., Denk W., Kerr J.N. Miniaturization of two-photon microscopy for imaging in freely moving animals. Cold Spring Harb. Protoc. 2013, 2013:904-913.
68. Hendel T., Mank M., Schnell B., Griesbeck O., Borst A., Reiff D.F. Fluorescence changes of genetic calcium indicators and OGB-1 correlated with neural activity and calcium invivo and invitro. J.Neurosci. 2008, 28:7399-7411.
69. Heys J.G., Rangarajan K.V., Dombeck D.A. The functional micro-organization of grid cells revealed by cellular-resolution imaging. Neuron 2014, 84:1079-1090.
70. Hires S.A., Tian L., Looger L.L. Reporting neural activity with genetically encoded calcium indicators. Brain Cell Biol. 2008, 36:69-86.
71. Hochbaum D.R., Zhao Y., Farhi S.L., Klapoetke N., Werley C.A., Kapoor V., Zou P., Kralj J.M., Maclaurin D., Smedemark-Margulies N., et al. All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat. Methods 2014, 11:825-833.
72. Holekamp T.F., Turaga D., Holy T.E. Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy. Neuron 2008, 57:661-672.
73. Hölscher C., Schnee A., Dahmen H., Setia L., Mallot H.A. Rats are able to navigate in virtual environments. J.Exp. Biol. 2005, 208:561-569.
74. Horton N.G., Wang K., Kobat D., Clark C.G., Wise F.W., Schaffer C.B., Xu C. Invivo three-photon microscopy of subcortical structures within an intact mouse brain. Nat. Photonics 2013, 7. 10.1038/nphoton.2012.336.
75. Huber D., Gutnisky D.A., Peron S., O'Connor D.H., Wiegert J.S., Tian L., Oertner T.G., Looger L.L., Svoboda K. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 2012, 484:473-478.
76. Hyvärinen A., Oja E. Independent component analysis: algorithms and applications. Neural Netw. 2000, 13:411-430.
77. Inoue M., Takeuchi A., Horigane S., Ohkura M., Gengyo-Ando K., Fujii H., Kamijo S., Takemoto-Kimura S., Kano M., Nakai J., et al. Rational design of a high-affinity, fast, red calcium indicator R-CaMP2. Nat. Methods 2015, 12:64-70.
78. Jennings J.H., Ung R.L., Resendez S.L., Stamatakis A.M., Taylor J.G., Huang J., Veleta K., Kantak P.A., Aita M., Shilling-Scrivo K., et al. Visualizing hypothalamic network dynamics for appetitive and consummatory behaviors. Cell 2015, 160:516-527.
79. Ji N., Milkie D.E., Betzig E. Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues. Nat. Methods 2010, 7:141-147.
80. Jin L., Han Z., Platisa J., Wooltorton J.R., Cohen L.B., Pieribone V.A. Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe. Neuron 2012, 75:779-785.
81. Jung J.C., Schnitzer M.J. Multiphoton endoscopy. Opt. Lett. 2003, 28:902-904.
82. Jung J.C., Mehta A.D., Aksay E., Stepnoski R., Schnitzer M.J. Invivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy. J.Neurophysiol. 2004, 92:3121-3133.
83. Kaifosh P., Lovett-Barron M., Turi G.F., Reardon T.R., Losonczy A. Septo-hippocampal GABAergic signaling across multiple modalities in awake mice. Nat. Neurosci. 2013, 16:1182-1184.
84. Kato H.K., Chu M.W., Isaacson J.S., Komiyama T. Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 2012, 76:962-975.
85. Katona G., Szalay G., Maák P., Kaszás A., Veress M., Hillier D., Chiovini B., Vizi E.S., Roska B., Rózsa B. Fast two-photon invivo imaging with three-dimensional random-access scanning in large tissue volumes. Nat. Methods 2012, 9:201-208.
86. Keck T., Keller G.B., Jacobsen R.I., Eysel U.T., Bonhoeffer T., Hübener M. Synaptic scaling and homeostatic plasticity in the mouse visual cortex invivo. Neuron 2013, 80:327-334.
87. Keller G.B., Bonhoeffer T., Hübener M. Sensorimotor mismatch signals in primary visual cortex of the behaving mouse. Neuron 2012, 74:809-815.
88. Kerlin A.M., Andermann M.L., Berezovskii V.K., Reid R.C. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 2010, 67:858-871.
89. Kerr J.N.D., Greenberg D., Helmchen F. Imaging input and output of neocortical networks invivo. Proc. Natl. Acad. Sci. USA 2005, 102:14063-14068.
90. Kitamura K., Judkewitz B., Kano M., Denk W., Häusser M. Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons invivo. Nat. Methods 2008, 5:61-67.
91. Kobat D., Horton N.G., Xu C. Invivo two-photon microscopy to 1.6-mm depth in mouse cortex. J.Biomed. Opt. 2011, 16:106014.
92. Komiyama T., Sato T.R., O'Connor D.H., Zhang Y.-X., Huber D., Hooks B.M., Gabitto M., Svoboda K. Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 2010, 464:1182-1186.
93. Kralj J.M., Hochbaum D.R., Douglass A.D., Cohen A.E. Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 2011, 333:345-348.
94. Kralj J.M., Douglass A.D., Hochbaum D.R., Maclaurin D., Cohen A.E. Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat. Methods 2012, 9:90-95.
95. Kuchibhotla K.V., Wegmann S., Kopeikina K.J., Hawkes J., Rudinskiy N., Andermann M.L., Spires-Jones T.L., Bacskai B.J., Hyman B.T. Neurofibrillary tangle-bearing neurons are functionally integrated in cortical circuits invivo. Proc. Natl. Acad. Sci. USA 2014, 111:510-514.
96. Kuhn B., Denk W., Bruno R.M. Invivo two-photon voltage-sensitive dye imaging reveals top-down control of cortical layers 1 and 2 during wakefulness. Proc. Natl. Acad. Sci. USA 2008, 105:7588-7593.
97. Lanyi J.K. Bacteriorhodopsin. Annu. Rev. Physiol. 2004, 66:665-688.
98. Lecoq J., Schnitzer M.J. An infrared fluorescent protein for deeper imaging. Nat. Biotechnol. 2011, 29:715-716.
99. Lecoq J., Savall J., Vučinić D., Grewe B.F., Kim H., Li J.Z., Kitch L.J., Schnitzer M.J. Visualizing mammalian brain area interactions by dual-axis two-photon calcium imaging. Nat. Neurosci. 2014, 17:1825-1829.
100. Levene M.J., Dombeck D.A., Kasischke K.A., Molloy R.P., Webb W.W. Invivo multiphoton microscopy of deep brain tissue. J.Neurophysiol. 2004, 91:1908-1912.
101. Levoy M., Zhang Z., McDowall I. Recording and controlling the 4D light field in a microscope using microlens arrays. J.Microsc. 2009, 235:144-162.
102. Lovett-Barron M., Kaifosh P., Kheirbek M.A., Danielson N., Zaremba J.D., Reardon T.R., Turi G.F., Hen R., Zemelman B.V., Losonczy A. Dendritic inhibition in the hippocampus supports fear learning. Science 2014, 343:857-863.
103. Low R.J., Gu Y., Tank D.W. Cellular resolution optical access to brain regions in fissures: imaging medial prefrontal cortex and grid cells in entorhinal cortex. Proc. Natl. Acad. Sci. USA 2014, 111:18739-18744.
104. Marshall J.D., Schnitzer M.J. Optical strategies for sensing neuronal voltage using quantum dots and other semiconductor nanocrystals. ACS Nano 2013, 7:4601-4609.
105. Maruyama R., Maeda K., Moroda H., Kato I., Inoue M., Miyakawa H., Aonishi T. Detecting cells using non-negative matrix factorization on calcium imaging data. Neural Netw. 2014, 55:11-19.
106. Marvin J.S., Borghuis B.G., Tian L., Cichon J., Harnett M.T., Akerboom J., Gordus A., Renninger S.L., Chen T.W., Bargmann C.I., et al. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat. Methods 2013, 10:162-170.
107. Masamizu Y., Tanaka Y.R., Tanaka Y.H., Hira R., Ohkubo F., Kitamura K., Isomura Y., Okada T., Matsuzaki M. Two distinct layer-specific dynamics of cortical ensembles during learning of a motor task. Nat. Neurosci. 2014, 17:987-994.
108. McIsaac R.S., Engqvist M.K., Wannier T., Rosenthal A.Z., Herwig L., Flytzanis N.C., Imasheva E.S., Lanyi J.K., Balashov S.P., Gradinaru V., Arnold F.H. Directed evolution of a far-red fluorescent rhodopsin. Proc. Natl. Acad. Sci. USA 2014, 111:13034-13039.
109. McKeown M.J., Makeig S., Brown G.G., Jung T.P., Kindermann S.S., Bell A.J., Sejnowski T.J. Analysis of fMRI data by blind separation into independent spatial components. Hum. Brain Mapp. 1998, 6:160-188.
110. Miller J.E., Ayzenshtat I., Carrillo-Reid L., Yuste R. Visual stimuli recruit intrinsically generated cortical ensembles. Proc. Natl. Acad. Sci. USA 2014, 111:E4053-E4061.
111. Miri A., Daie K., Burdine R.D., Aksay E., Tank D.W. Regression-based identification of behavior-encoding neurons during large-scale optical imaging of neural activity at cellular resolution. J.Neurophysiol. 2011, 105:964-980.
112. Mohajerani M.H., McVea D.A., Fingas M., Murphy T.H. Mirrored bilateral slow-wave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice. J.Neurosci. 2010, 30:3745-3751.
113. Mohajerani M.H., Chan A.W., Mohsenvand M., LeDue J., Liu R., McVea D.A., Boyd J.D., Wang Y.T., Reimers M., Murphy T.H. Spontaneous cortical activity alternates between motifs defined by regional axonal projections. Nat. Neurosci. 2013, 16:1426-1435.
114. Mukamel E.A., Nimmerjahn A., Schnitzer M.J. Automated analysis of cellular signals from large-scale calcium imaging data. Neuron 2009, 63:747-760.
115. Muller A., Joseph V., Slesinger P.A., Kleinfeld D. Cell-based reporters reveal invivo dynamics of dopamine and norepinephrine release in murine cortex. Nat. Methods 2014, 11:1245-1252.
116. Murayama M., Larkum M.E. Enhanced dendritic activity in awake rats. Proc. Natl. Acad. Sci. USA 2009, 106:20482-20486.
117. Murayama M., Pérez-Garci E., Lüscher H.-R., Larkum M.E. Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats. J.Neurophysiol. 2007, 98:1791-1805.
118. Murayama M., Pérez-Garci E., Nevian T., Bock T., Senn W., Larkum M.E. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 2009, 457:1137-1141.
119. Nakai J., Ohkura M., Imoto K. A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat. Biotechnol. 2001, 19:137-141.
120. Newsome W.T., Britten K.H., Movshon J.A. Neuronal correlates of a perceptual decision. Nature 1989, 341:52-54.
121. Nikolenko V., Peterka D.S., Araya R., Woodruff A., Yuste R. Spatial light modulator microscopy. Cold Spring Harb. Protoc. 2013, 2013:1132-1141.
122. Nimmerjahn A., Kirchhoff F., Kerr J.N., Helmchen F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex invivo. Nat. Methods 2004, 1:31-37.
123. Nimmerjahn A., Mukamel E.A., Schnitzer M.J. Motor behavior activates Bergmann glial networks. Neuron 2009, 62:400-412.
124. O'Connor D.H., Peron S.P., Huber D., Svoboda K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 2010, 67:1048-1061.
125. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971, 34:171-175.
126. Ohki K., Chung S., Ch'ng Y.H., Kara P., Reid R.C. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 2005, 433:597-603.
127. Ohkura M., Sasaki T., Sadakari J., Gengyo-Ando K., Kagawa-Nagamura Y., Kobayashi C., Ikegaya Y., Nakai J. Genetically encoded green fluorescent Ca2+ indicators with improved detectability for neuronal Ca2+ signals. PLoS ONE 2012, 7:e51286.
128. Ozden I., Lee H.M., Sullivan M.R., Wang S.S.-H. Identification and clustering of event patterns from invivo multiphoton optical recordings of neuronal ensembles. J.Neurophysiol. 2008, 100:495-503.
129. Packer A.M., Peterka D.S., Hirtz J.J., Prakash R., Deisseroth K., Yuste R. Two-photon optogenetics of dendritic spines and neural circuits. Nat. Methods 2012, 9:1202-1205.
130. Packer A.M., Russell L.E., Dalgleish H.W., Häusser M. Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution invivo. Nat. Methods 2015, 12:140-146.
131. Patterson M.A., Lagier S., Carleton A. Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage. Proc. Natl. Acad. Sci. USA 2013, 110:E3340-E3349.
132. Peterka D.S., Takahashi H., Yuste R. Imaging voltage in neurons. Neuron 2011, 69:9-21.
133. Peters A.J., Chen S.X., Komiyama T. Emergence of reproducible spatiotemporal activity during motor learning. Nature 2014, 510:263-267.
134. Petreanu L., Gutnisky D.A., Huber D., Xu N.L., O'Connor D.H., Tian L., Looger L., Svoboda K. Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 2012, 489:299-303.
135. Pfeiffer B.E., Foster D.J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 2013, 497:74-79.
136. Piyawattanametha W., Cocker E.D., Burns L.D., Barretto R.P., Jung J.C., Ra H., Solgaard O., Schnitzer M.J. Invivo brain imaging using a portable 2.9g two-photon microscope based on a microelectromechanical systems scanning mirror. Opt. Lett. 2009, 34:2309-2311.
137. Prakash R., Yizhar O., Grewe B., Ramakrishnan C., Wang N., Goshen I., Packer A.M., Peterka D.S., Yuste R., Schnitzer M.J., Deisseroth K. Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation. Nat. Methods 2012, 9:1171-1179.
138. Prevedel R., Yoon Y.G., Hoffmann M., Pak N., Wetzstein G., Kato S., Schrödel T., Raskar R., Zimmer M., Boyden E.S., Vaziri A. Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy. Nat. Methods 2014, 11:727-730.
139. Quirin S., Jackson J., Peterka D.S., Yuste R. Simultaneous imaging of neural activity in three dimensions. Front. Neural Circuits 2014, 8:29.
140. Raffi M., Siegel R.M. Functional architecture of spatial attention in the parietal cortex of the behaving monkey. J.Neurosci. 2005, 25:5171-5186.
141. Ravassard P., Kees A., Willers B., Ho D., Aharoni D., Cushman J., Aghajan Z.M., Mehta M.R. Multisensory control of hippocampal spatiotemporal selectivity. Science 2013, 340:1342-1346.
142. Reidl J., Starke J., Omer D.B., Grinvald A., Spors H. Independent component analysis of high-resolution imaging data identifies distinct functional domains. Neuroimage 2007, 34:94-108.
143. Reutsky-Gefen I., Golan L., Farah N., Schejter A., Tsur L., Brosh I., Shoham S. Holographic optogenetic stimulation of patterned neuronal activity for vision restoration. Nat. Commun. 2013, 4:1509.
144. Rickgauer J.P., Deisseroth K., Tank D.W. Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields. Nat. Neurosci. 2014, 17:1816-1824.
145. Rueckel M., Mack-Bucher J.A., Denk W. Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing. Proc. Natl. Acad. Sci. USA 2006, 103:17137-17142.
146. Runyan C.A., Schummers J., Van Wart A., Kuhlman S.J., Wilson N.R., Huang Z.J., Sur M. Response features of parvalbumin-expressing interneurons suggest precise roles for subtypes of inhibition in visual cortex. Neuron 2010, 67:847-857.
147. Sasaki T., Takahashi N., Matsuki N., Ikegaya Y. Fast and accurate detection of action potentials from somatic calcium fluctuations. J.Neurophysiol. 2008, 100:1668-1676.
148. Sawinski J., Wallace D.J., Greenberg D.S., Grossmann S., Denk W., Kerr J.N.D. Visually evoked activity in cortical cells imaged in freely moving animals. Proc. Natl. Acad. Sci. USA 2009, 106:19557-19562.
149. Scott B.B., Brody C.D., Tank D.W. Cellular resolution functional imaging in behaving rats using voluntary head restraint. Neuron 2013, 80:371-384.
150. Seidemann E., Arieli A., Grinvald A., Slovin H. Dynamics of depolarization and hyperpolarization in the frontal cortex and saccade goal. Science 2002, 295:862-865.
151. Sheffield M.E., Dombeck D.A. Calcium transient prevalence across the dendritic arbour predicts place field properties. Nature 2015, 517:200-204.
152. Sjulson L., Miesenböck G. Optical recording of action potentials and other discrete physiological events: a perspective from signal detection theory. Physiology (Bethesda) 2007, 22:47-55.
153. Soden M.E., Jones G.L., Sanford C.A., Chung A.S., Güler A.D., Chavkin C., Luján R., Zweifel L.S. Disruption of dopamine neuron activity pattern regulation through selective expression of a human KCNN3 mutation. Neuron 2013, 80:997-1009.
154. Sofroniew N.J., Cohen J.D., Lee A.K., Svoboda K. Natural whisker-guided behavior by head-fixed mice in tactile virtual reality. J.Neurosci. 2014, 34:9537-9550.
155. St-Pierre F., Marshall J.D., Yang Y., Gong Y., Schnitzer M.J., Lin M.Z. High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat. Neurosci. 2014, 17:884-889.
156. Stirman J.N., Smith I.T., Kudenov M.W., Smith S.L. Wide field-of-view, twin-region two-photon imaging across extended cortical networks. bioRxiv. 2014, 10.1101/011320.
157. Stosiek C., Garaschuk O., Holthoff K., Konnerth A. Invivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. USA 2003, 100:7319-7324.
158. Sun X.R., Badura A., Pacheco D.A., Lynch L.A., Schneider E.R., Taylor M.P., Hogue I.B., Enquist L.W., Murthy M., Wang S.S. Fast GCaMPs for improved tracking of neuronal activity. Nat. Commun. 2013, 4:2170.
159. Susaki E.A., Tainaka K., Perrin D., Kishino F., Tawara T., Watanabe T.M., Yokoyama C., Onoe H., Eguchi M., Yamaguchi S., et al. Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis. Cell 2014, 157:726-739.
160. Svoboda K., Helmchen F., Denk W., Tank D.W. Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex invivo. Nat. Neurosci. 1999, 2:65-73.
161. Tanigawa H., Lu H.D., Roe A.W. Functional organization for color and orientation in macaque V4. Nat. Neurosci. 2010, 13:1542-1548.
162. Thévenaz P., Ruttimann U.E., Unser M. A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 1998, 7:27-41.
163. Tian L., Hires S.A., Mao T., Huber D., Chiappe M.E., Chalasani S.H., Petreanu L., Akerboom J., McKinney S.A., Schreiter E.R., et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 2009, 6:875-881.
164. Tian L., Yang Y., Wysocki L.M., Arnold A.C., Hu A., Ravichandran B., Sternson S.M., Looger L.L., Lavis L.D. Selective esterase-ester pair for targeting small molecules with cellular specificity. Proc. Natl. Acad. Sci. USA 2012, 109:4756-4761.
165. Tomer R., Ye L., Hsueh B., Deisseroth K. Advanced CLARITY for rapid and high-resolution imaging of intact tissues. Nat. Protoc. 2014, 9:1682-1697.
166. Tsutsui H., Karasawa S., Okamura Y., Miyawaki A. Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat. Methods 2008, 5:683-685.
167. Verhagen J.V., Wesson D.W., Netoff T.I., White J.A., Wachowiak M. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat. Neurosci. 2007, 10:631-639.
168. Vogelstein J.T., Packer A.M., Machado T.A., Sippy T., Babadi B., Yuste R., Paninski L. Fast nonnegative deconvolution for spike train inference from population calcium imaging. J.Neurophysiol. 2010, 104:3691-3704.
169. Wang C., Liu R., Milkie D.E., Sun W., Tan Z., Kerlin A., Chen T.W., Kim D.S., Ji N. Multiplexed aberration measurement for deep tissue imaging invivo. Nat. Methods 2014, 11:1037-1040.
170. Watson B.O., Nikolenko V., Araya R., Peterka D.S., Woodruff A., Yuste R. Two-photon microscopy with diffractive optical elements and spatial light modulators. Front. Neurosci. 2010, 4:29.
171. Wilt B.A., Burns L.D., Wei Ho E.T., Ghosh K.K., Mukamel E.A., Schnitzer M.J. Advances in light microscopy for neuroscience. Annu. Rev. Neurosci. 2009, 32:435-506.
172. Wilt B.A., Fitzgerald J.E., Schnitzer M.J. Photon shot noise limits on optical detection of neuronal spikes and estimation of spike timing. Biophys. J. 2013, 104:51-62.
173. 2± indicators and photophysical considerations for optogenetic applications. ACS Chem. Neurosci. 2013, 4:963-972.
174. Xu N.L., Harnett M.T., Williams S.R., Huber D., O'Connor D.H., Svoboda K., Magee J.C. Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 2012, 492:247-251.
175. Yaksi E., Friedrich R.W. Reconstruction of firing rate changes across neuronal populations by temporally deconvolved Ca2+ imaging. Nat. Methods 2006, 3:377-383.
176. Yang B., Treweek J.B., Kulkarni R.P., Deverman B.E., Chen C.K., Lubeck E., Shah S., Cai L., Gradinaru V. Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 2014, 158:945-958.
177. Zhang Q.F., Wen Y., Zhang D., She L., Wu J.Y., Dan Y., Poo M.M. Priming with real motion biases visual cortical response to bistable apparent motion. Proc. Natl. Acad. Sci. USA 2012, 109:20691-20696.
178. 2+ indicators. Science 2011, 333:1888-1891.
179. Ziv Y., Burns L.D., Cocker E.D., Hamel E.O., Ghosh K.K., Kitch L.J., El Gamal A., Schnitzer M.J. Long-term dynamics of CA1 hippocampal place codes. Nat. Neurosci. 2013, 16:264-266.
180. Zou P., Zhao Y., Douglass A.D., Hochbaum D.R., Brinks D., Werley C.A., Harrison D.J., Campbell R.E., Cohen A.E. Bright and fast multicoloured voltage reporters via electrochromic FRET. Nat. Commun. 2014, 5:4625.