Two-photon imaging and analysis of neural network dynamics

Reports on Progress in Physics

Volumn 74, Issue 8, 2011, Pages

  Lütcke, Henry ^a   Helmchen, Fritjof ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79961085495     PISSN: 00344885     EISSN: None     Source Type: Journal    
DOI: 10.1088/0034-4885/74/8/086602     Document Type: Review

References (153)

1. Adesnik H and Scanziani M 2010 Lateral competition for cortical space by layer-specific horizontal circuits Nature 464 1155-60
2. Akemann W, Mutoh H, Perron A, Rossier J and Knopfel T 2010 Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins Nature Methods 7 643-9
3. Andermann M L, Kerlin A M and Reid R C 2010 Chronic cellular imaging of mouse visual cortex during operant behavior and passive viewing Front. Cell Neurosci. 4 3
4. Arieli A, Sterkin A, Grinvald A and Aertsen A 1996 Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses Science 273 1868-71 (Pubitemid 26322498)
5. Ascoli G A et al 2008 Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex Nature Rev. Neurosci. 9 557-68 (Pubitemid 351873463)
6. Ataka K and Pieribone V A 2002 A genetically targetable fluorescent probe of channel gating with rapid kinetics Biophys. J. 82 509-16 (Pubitemid 34289823)
7. Baker B J et al 2008 Genetically encoded fluorescent sensors of membrane potential Brain Cell Biol. 36 53-67
8. Bandyopadhyay S, Shamma S A and Kanold P O 2010 Dichotomy of functional organization in the mouse auditory cortex Nature Neurosci. 13 361-8
9. Bock D D, Lee W C, Kerlin A M, Andermann M L, Hood G, Wetzel A W, Yurgenson S, Soucy E R, Kim H S and Reid R C 2011 Network anatomy and in vivo physiology of visual cortical neurons Nature 471 177-82
10. Botcherby E J, Juskaitis R, Booth M J and Wilson T 2007 Aberration-free optical refocusing in high numerical aperture microscopy Opt. Lett. 32 2007-9 (Pubitemid 351389956)
11. Briggman K L and Denk W 2006 Towards neural circuit reconstruction with volume electron microscopy techniques Curr. Opin. Neurobiol. 16 562-70 (Pubitemid 44466398)
12. Briggman K L, Helmstaedter M and Denk W 2011 Wiring specificity in the direction-selectivity circuit of the retina Nature 471 183-8
13. Buzsaki G 2004 Large-scale recording of neuronal ensembles Nature Neurosci. 7 446-51 (Pubitemid 38544574)
14. Carriles R, Schafer D N, Sheetz K E, Field J J, Cisek R, Barzda V, Sylvester A W and Squier J A 2009 Invited review article: imaging techniques for harmonic and multiphoton absorption fluorescence microscopy Rev. Sci. Instrum. 80 081101
15. Cheng A, Goncalves J T, Golshani P, Arisaka K and Portera-Cailliau C 2011 Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing Nature Methods 8 139-42
16. Chorev E, Epsztein J, Houweling A R, Lee A K and Brecht M 2009 Electrophysiological recordings from behaving animals - going beyond spikes Curr. Opin. Neurobiol. 19 513-9
17. Constantinidis C and Goldman-Rakic P S 2002 Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex J. Neurophysiol. 88 3487-97 (Pubitemid 35448724)
18. Deisseroth K 2011 Optogenetics Nature Methods 8 26-9
19. Denk W and Svoboda K 1997 Photon upmanship: why multiphoton imaging is more than a gimmick Neuron 18 351-7 (Pubitemid 27138784)
20. Denk W and Horstmann H 2004 Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure PLoS Biol. 2 e329
21. Denk W, Strickler J H and Webb W W 1990 Two-photon laser scanning fluorescence microscopy Science 248 73-6
22. Denk W, Piston D W and Webb W W 2005 Multi-photon molecular excitation in laser-scanning microscopy Handbook of Biological Confocal Microscopy 2nd edn ed J B Pawley (New York: Plenum)
23. Diaspro A (ed) 2002 Confocal and two-photon microscopy: foundations, applications, and advances (New York: Wiley-Liss)
24. Dimitrov D, He Y, Mutoh H, Baker B J, Cohen L, Akemann W and Knopfel T 2007 Engineering and characterization of an enhanced fluorescent protein voltage sensor PLoS ONE 2 e440
25. Dombeck D A, Graziano M S and Tank D W 2009 Functional clustering of neurons in motor cortex determined by cellular resolution imaging in awake behaving mice J. Neurosci. 29 13751-60
26. Dombeck D A, Khabbaz A N, Collman F, Adelman T L and Tank D W 2007 Imaging large-scale neural activity with cellular resolution in awake, mobile mice Neuron 56 43-57 (Pubitemid 47484173)
27. Dombeck D A, Harvey C D, Tian L, Looger L L and Tank D W 2010 Functional imaging of hippocampal place cells at cellular resolution during virtual navigation Nature Neurosci. 13 1433-40
28. Donnert G, Eggeling C and Hell S W 2007 Major signal increase in fluorescence microscopy through dark-state relaxation Nature Methods 4 81-6 (Pubitemid 46029480)
29. Douglas R J and Martin K A 2009 Inhibition in cortical circuits Curr. Biol. 19 R398-R402
30. Dreosti E, Odermatt B, Dorostkar M M and Lagnado L 2009 A genetically encoded reporter of synaptic activity in vivo Nature Methods 6 883-9
31. Duemani Reddy G, Kelleher K, Fink R and Saggau P 2008 Three-dimensional random access multiphoton microscopy for functional imaging of neuronal activity Nature Neurosci. 11 713-20 (Pubitemid 351748113)
32. Durst M E, Zhu G and Xu C 2006 Simultaneous spatial and temporal focusing for axial scanning Opt. Express 14 12243-54 (Pubitemid 44907566)
33. Ecker A S, Berens P, Keliris G A, Bethge M, Logothetis N K and Tolias A S 2010 Decorrelated neuronal firing in cortical microcircuits Science 327 584-7
34. Feil R, Brocard J, Mascrez B, LeMeur M, Metzger D and Chambon P 1996 Ligand-activated site-specific recombination in mice Proc. Natl Acad. Sci. USA 93 10887-90 (Pubitemid 26333086)
35. Ferezou I, Haiss F, Gentet L J, Aronoff R, Weber B and Petersen C C 2007 Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice Neuron 56 907-23 (Pubitemid 350181347)
36. Gandhi S P, Yanagawa Y and Stryker M P 2008 Delayed plasticity of inhibitory neurons in developing visual cortex Proc. Natl Acad. Sci. USA 105 16797-802
37. Garaschuk O, Milos R I, Grienberger C, Marandi N, Adelsberger H and Konnerth A 2006 Optical monitoring of brain function in vivo: from neurons to networks Pflugers Arch. 453 385-96 (Pubitemid 44764239)
38. Göbel W and Helmchen F 2007a In vivo calcium imaging of neural network function Physiology 22 358-65
39. Göbel W and Helmchen F 2007b New angles on neuronal dendrites in vivo J. Neurophysiol. 98 3770-9
40. Göbel W, Kampa B M and Helmchen F 2007 Imaging cellular network dynamics in three dimensions using fast 3D laser scanning Nature Methods 4 73-9 (Pubitemid 46029479)
41. Gong S, Doughty M, Harbaugh C R, Cummins A, Hatten M E, Heintz N and Gerfen C R 2007 Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs J. Neurosci. 27 9817-23 (Pubitemid 47403991)
42. Göppert-Mayer M 1931 ber Elementarakte mit zwei Quantensprüngen Ann. Phys., Lpz. 9 273
43. Greenberg D S and Kerr J N 2009 Automated correction of fast motion artifacts for two-photon imaging of awake animals J. Neurosci. Methods 176 1-15
44. Grewe B F and Helmchen F 2009 Optical probing of neuronal ensemble activity Curr. Opin. Neurobiol. 19 520-9
45. Grewe B F, Langer D, Kasper H, Kampa B M and Helmchen F 2010 High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision Nature Methods 7 399-405
46. Grewe B F, Voigt F F, van 't Hoff M and Helmchen F 2011 Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens Biomed. Opt. Express 2 2035-46
47. Grinvald A and Hildesheim R 2004 VSDI: a new era in functional imaging of cortical dynamics Nature Rev. Neurosci. 5 874-85 (Pubitemid 39482156)
48. Gutnisky D A and Dragoi V 2008 Adaptive coding of visual information in neural populations Nature 452 220-4 (Pubitemid 351380238)
49. Hahnloser R H, Kozhevnikov A A and Fee M S 2002 An ultra-sparse code underlies the generation of neural sequences in a songbird Nature 419 65-70 (Pubitemid 34987870)
50. Harris K D, Csicsvari J, Hirase H, Dragoi G and Buzsaki G 2003 Organization of cell assemblies in the hippocampus Nature 424 552-6 (Pubitemid 36975776)
51. 2+ indicator proteins in transgenic mice under TET control PLoS Biol. 2 e163
52. Heim N and Griesbeck O 2004 Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein J. Biol. Chem. 279 14280-6 (Pubitemid 38468968)
53. Heim N, Garaschuk O, Friedrich M W, Mank M, Milos R I, Kovalchuk Y, Konnerth A and Griesbeck O 2007 Improved calcium imaging in transgenic mice expressing a troponin C-based biosensor Nature Methods 4 127-9 (Pubitemid 46454679)
54. Hell S W 2007 Far-field optical nanoscopy Science 316 1153-8 (Pubitemid 46877470)
55. 2+ imaging in the mammalian brain in vivo Eur. J. Pharmacol. 447 119-29 (Pubitemid 34874446)
56. Helmchen F and Denk W 2005 Deep tissue two-photon microscopy Nature Methods 2 932-40 (Pubitemid 43108729)
57. Helmchen F and Tank D W 2011 A single compartment model of calcium dynamics in dendrites and nerve terminals Imaging in Neuroscience: A Laboratory Manual ed F Helmchen and A Konnerth (New York: Cold Spring Harbor Laboratory Press)
58. 2+ signaling in dendrites of pyramidal neurons Biophys. J. 70 1069-81
59. Hires S A, Tian L and Looger L L 2008 Reporting neural activity with genetically encoded calcium indicators Brain Cell Biol. 36 69-86
60. Holekamp T F, Turaga D and Holy T E 2008 Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy Neuron 57 661-72 (Pubitemid 351337670)
61. Hromadka T, Deweese M R and Zador A M 2008 Sparse representation of sounds in the unanesthetized auditory cortex PLoS Biol. 6 e16
62. Hubel D H and Wiesel T N 1959 Receptive fields of single neurones in the cat's striate cortex J. Physiol. 148 574-91
63. Iyer V, Hoogland T M and Saggau P 2006 Fast functional imaging of single neurons using random-access multiphoton (RAMP) microscopy J. Neurophysiol. 95 535-45 (Pubitemid 44698953)
64. Jia H, Rochefort N L, Chen X and Konnerth A 2010 Dendritic organization of sensory input to cortical neurons in vivo Nature 464 1307-12
65. 2+ imaging of dorsal horn neuronal populations in mouse spinal cord J. Physiol. 588 3397-402
66. Junek S, Chen T W, Alevra M and Schild D 2009 Activity correlation imaging: visualizing function and structure of neuronal populations Biophys. J. 96 3801-9
67. Jung R, Creutzfeldt O and Grusser O J 1957 Microphysiology of cortical neurons & their role in sensory and cerebral function Dtsch Med. Wochenschr. 82 1050-9
68. Jurrus E, Hardy M, Tasdizen T, Fletcher P T, Koshevoy P, Chien C B, Denk W and Whitaker R 2009 Axon tracking in serial block-face scanning electron microscopy Med. Image Anal. 13 180-8
69. Kara P and Boyd J D 2009 A micro-architecture for binocular disparity and ocular dominance in visual cortex Nature 458 627-31
70. Kerlin A M, Andermann M L, Berezovskii V K and Reid R C 2010 Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex Neuron 67 858-71
71. Kerr J N and Denk W 2008 Imaging in vivo: watching the brain in action Nature Rev. Neurosci. 9 195-205 (Pubitemid 351278394)
72. Kerr J N, Greenberg D and Helmchen F 2005 Imaging input and output of neocortical networks in vivo Proc. Natl Acad. Sci. USA 102 14063-8 (Pubitemid 41377703)
73. Kerr J N, de Kock C P, Greenberg D S, Bruno R M, Sakmann B and Helmchen F 2007 Spatial organization of neuronal population responses in layer 2/3 of rat barrel cortex J. Neurosci. 27 13316-28 (Pubitemid 350220486)
74. Kirkby P A, Srinivas Nadella K M and Silver R A 2010 A compact acousto-optic lens for 2D and 3D femtosecond based 2-photon microscopy Opt. Express 18 13721-45
75. Kitamura K, Judkewitz B, Kano M, Denk W and Hausser M 2008 Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo Nature Methods 5 61-7
76. Komiyama T, Sato T R, O'Connor D H, Zhang Y X, Huber D, Hooks B M, Gabitto M and Svoboda K 2010 Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice Nature 464 1182-6
77. Kremer Y, Leger J F, Lapole R, Honnorat N, Candela Y, Dieudonne S and Bourdieu L 2008 A spatio-temporally compensated acousto-optic scanner for two-photon microscopy providing large field of view Opt. Express 16 10066-76
78. Kuhn B, Denk W and Bruno R M 2008 In vivo two-photon voltage-sensitive dye imaging reveals top-down control of cortical layers 1 and 2 during wakefulness Proc. Natl Acad. Sci. USA 105 7588-93 (Pubitemid 351830062)
79. Kurtz R, Fricke M, Kalb J, Tinnefeld P and Sauer M 2006 Application of multiline two-photon microscopy to functional in vivo imaging J. Neurosci. Methods 151 276-86 (Pubitemid 43294450)
80. Kwan A C, Dietz S B, Webb W W and Harris-Warrick R M 2009 Activity of Hb9 interneurons during fictive locomotion in mouse spinal cord J. Neurosci. 29 11601-13
81. Lee D, Port N L, Kruse W and Georgopoulos A P 1998 Variability and correlated noise in the discharge of neurons in motor and parietal areas of the primate cortex J. Neurosci. 18 1161-70 (Pubitemid 28112937)
82. Leybaert L, de Meyer A, Mabilde C and Sanderson M J 2005 A simple and practical method to acquire geometrically correct images with resonant scanning-based line scanning in a custom-built video-rate laser scanning microscope J. Microsc. 219 133-40 (Pubitemid 41413518)
83. Li B and Acton S T 2007 Active contour external force using vector field convolution for image segmentation IEEE Trans. Image Process. 16 2096-106 (Pubitemid 47225461)
84. Li Y, Van Hooser S D, Mazurek M, White L E and Fitzpatrick D 2008 Experience with moving visual stimuli drives the early development of cortical direction selectivity Nature 456 952-6
85. Lillis K P, Eng A, White J A and Mertz J 2008 Two-photon imaging of spatially extended neuronal network dynamics with high temporal resolution J. Neurosci. Methods 172 178-84
86. Luo L, Callaway E M and Svoboda K 2008 Genetic dissection of neural circuits Neuron 57 634-60 (Pubitemid 351335341)
87. Lütcke H et al 2010 Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice Front. Neural Circuits 4 9
88. Mank M and Griesbeck O 2008 Genetically encoded calcium indicators Chem. Rev. 108 1550-64 (Pubitemid 351796397)
89. Mank M et al 2008 A genetically encoded calcium indicator for chronic in vivo two-photon imaging Nature Methods 5 805-11
90. Mao T, O'Connor D H, Scheuss V, Nakai J and Svoboda K 2008 Characterization and subcellular targeting of GCaMP-type genetically-encoded calcium indicators PLoS ONE 3 e1796
91. Mennerick S, Chisari M, Shu H J, Taylor A, Vasek M, Eisenman L N and Zorumski C F 2010 Diverse voltage-sensitive dyes modulate GABAA receptor function J. Neurosci. 30 2871-9
92. Miri A, Daie K, Burdine R D, Aksay E and Tank D W 2011 Regression-based identification of behavior-encoding neurons during large-scale optical imaging of neural activity at cellular resolution J. Neurophysiol. 105 964-80
93. Miyawaki A 2003 Fluorescence imaging of physiological activity in complex systems using GFP-based probes Curr. Opin. Neurobiol 13 591-6 (Pubitemid 37431188)
94. 2+ based on green fluorescent proteins and calmodulin Nature 388 882-7 (Pubitemid 27377061)
95. Moreaux L and Laurent G 2008 A simple method to reconstruct firing rates from dendritic calcium signals Front. Neurosci. 2 176-85
96. Mountcastle V B, Davies P W and Berman A L 1957 Response properties of neurons of cat's somatic sensory cortex to peripheral stimuli J. Neurophysiol. 20 374-407
97. Mukamel E A, Nimmerjahn A and Schnitzer M J 2009 Automated analysis of cellular signals from large-scale calcium imaging data Neuron 63 747-60
98. 2+ by circularly permuted yellow fluorescent proteins Proc. Natl Acad. Sci. USA 101 10554-9 (Pubitemid 38955780)
99. 2+ imaging of local neuronal circuits Neuron 53 789-803 (Pubitemid 46367554)
100. Nagy A 2000 Cre recombinase: the universal reagent for genome tailoring Genesis 26 99-109 (Pubitemid 30158089)
101. Nevian T and Helmchen F 2007 Calcium indicator loading of neurons using single-cell electroporation Pflugers Arch. 454 675-88 (Pubitemid 46872899)
102. Niesner R, Andresen V, Neumann J, Spiecker H and Gunzer M 2007 The power of single and multibeam two-photon microscopy for high-resolution and high-speed deep tissue and intravital imaging Biophys. J. 93 2519-29 (Pubitemid 47511151)
103. Niessing J and Friedrich R W 2010 Olfactory pattern classification by discrete neuronal network states Nature 465 47-52
104. Nikolenko V, Watson B O, Araya R, Woodruff A, Peterka D S and Yuste R 2008 SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators Front. Neural Circuits 2 5
105. Nimmerjahn A, Mukamel E A and Schnitzer M J 2009 Motor behavior activates Bergmann glial networks Neuron 62 400-12
106. Nimmerjahn A, Kirchhoff F, Kerr J N and Helmchen F 2004 Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo Nature Methods 1 31-7
107. O'Donovan M J, Ho S, Sholomenko G and Yee W 1993 Real-time imaging of neurons retrogradely and anterogradely labelled with calcium-sensitive dyes J. Neurosci. Methods 46 91-106 (Pubitemid 23061019)
108. Ohiorhenuan I E, Mechler F, Purpura K P, Schmid A M, Hu Q and Victor J D 2010 Sparse coding and high-order correlations in fine-scale cortical networks Nature 466 617-21
109. Ohki K, Chung S, Ch'ng Y H, Kara P and Reid R C 2005 Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex Nature 433 597-603 (Pubitemid 40282986)
110. Ohki K, Chung S, Kara P, Hubener M, Bonhoeffer T and Reid R C 2006 Highly ordered arrangement of single neurons in orientation pinwheels Nature 442 925-8 (Pubitemid 44285948)
111. Okun M and Lampl I 2008 Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities Nature Neurosci. 11 535-7 (Pubitemid 351595199)
112. Olivier N, Mermillod-Blondin A, Arnold C B and Beaurepaire E 2009 Two-photon microscopy with simultaneous standard and extended depth of field using a tunable acoustic gradient-index lens Opt. Lett. 34 1684-6
113. Otsu Y, Bormuth V, Wong J, Mathieu B, Dugue G P, Feltz A and Dieudonne S 2008 Optical monitoring of neuronal activity at high frame rate with a digital random-access multiphoton (RAMP) microscope J. Neurosci. Methods 173 259-70
114. Ozden I, Lee H M, Sullivan M R and Wang S S 2008 Identification and clustering of event patterns from in vivo multiphoton optical recordings of neuronal ensembles J. Neurophysiol. 100 495-503
115. Petersen C C, Grinvald A and Sakmann B 2003 Spatiotemporal dynamics of sensory responses in layer 2/3 of rat barrel cortex measured in vivo by voltage-sensitive dye imaging combined with whole-cell voltage recordings and neuron reconstructions J. Neurosci. 23 1298-309 (Pubitemid 36258908)
116. Petreanu L, Huber D, Sobczyk A and Svoboda K 2007 Channelrhodopsin-2- assisted circuit mapping of long-range callosal projections Nature Neurosci. 10 663-8 (Pubitemid 46652447)
117. Poulet J F and Petersen C C 2008 Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice Nature 454 881-5
118. Ranganathan G N and Koester H J 2010 Optical recording of neuronal spiking activity from unbiased populations of neurons with high spike detection efficiency and high temporal precision J. Neurophysiol. 104 1812-24
119. Rochefort N L, Garaschuk O, Milos R I, Narushima M, Marandi N, Pichler B, Kovalchuk Y and Konnerth A 2009 Sparsification of neuronal activity in the visual cortex at eye-opening Proc. Natl Acad. Sci. USA 106 15049-54
120. Rothschild G, Nelken I and Mizrahi A 2010 Functional organization and population dynamics in the mouse primary auditory cortex Nature Neurosci. 13 353-60
121. Saggau P 2006 New methods and uses for fast optical scanning Curr. Opin. Neurobiol. 16 543-50 (Pubitemid 44466400)
122. Saito T and Nakatsuji N 2001 Efficient gene transfer into the embryonic mouse brain using in vivo electroporation Dev. Biol. 240 237-46 (Pubitemid 33141120)
123. Sakai R, Repunte-Canonigo V, Raj C D and Knopfel T 2001 Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein Eur. J. Neurosci. 13 2314-8 (Pubitemid 32664317)
124. Salzberg B M, Grinvald A, Cohen L B, Davila H V and Ross W N 1977 Optical recording of neuronal activity in an invertebrate central nervous system: simultaneous monitoring of several neurons J. Neurophysiol. 40 1281-91 (Pubitemid 8233139)
125. Sasaki T, Takahashi N, Matsuki N and Ikegaya Y 2008 Fast and accurate detection of action potentials from somatic calcium fluctuations J. Neurophysiol. 100 1668-76
126. Sato T R, Gray N W, Mainen Z F and Svoboda K 2007 The functional microarchitecture of the mouse barrel cortex PLoS Biol. 5 e189
127. Sawinski J, Wallace D J, Greenberg D S, Grossmann S, Denk W and Kerr J N 2009 Visually evoked activity in cortical cells imaged in freely moving animals Proc. Natl Acad. Sci. USA 106 19557-62
128. Shigetomi E, Kracun S, Sofroniew M V and Khakh B S 2010 A genetically targeted optical sensor to monitor calcium signals in astrocyte processes Nature Neurosci. 13 759-66
129. Siegel M S and Isacoff E Y 1997 A genetically encoded optical probe of membrane voltage Neuron 19 735-41 (Pubitemid 27471378)
130. So P T, Dong C Y, Masters B R and Berland K M 2000 Two-photon excitation fluorescence microscopy Annu. Rev. Biomed. Eng. 2 399-429
131. 2+ imaging in transgenic mice J. Neurosci. 27 2145-9
132. Song S, Sjöström P J, Reigl M, Nelson S and Chklovskii D B 2005 Highly nonrandom features of synaptic connectivity in local cortical circuits PLoS Biol. 3 e68
133. Stettler D D and Axel R 2009 Representations of odor in the piriform cortex Neuron 63 854-64
134. Stosiek C, Garaschuk O, Holthoff K and Konnerth A 2003 In vivo two-photon calcium imaging of neuronal networks Proc. Natl Acad. Sci. USA 100 7319-24 (Pubitemid 36706436)
135. Sullivan M R, Nimmerjahn A, Sarkisov D V, Helmchen F and Wang S S 2005 In vivo calcium imaging of circuit activity in cerebellar cortex J. Neurophysiol. 94 1636-44 (Pubitemid 41061393)
136. Svoboda K and Yasuda R 2006 Principles of two-photon excitation microscopy and its applications to neuroscience Neuron 50 823-39 (Pubitemid 43850693)
137. Svoboda K, Denk W, Kleinfeld D and Tank D W 1997 In vivo dendritic calcium dynamics in neocortical pyramidal neurons Nature 385 161-5 (Pubitemid 27034217)
138. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K and Kaneko T 2003 Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse J. Comp. Neurol. 467 60-79 (Pubitemid 37339758)
139. Tian L et al 2009 Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators Nature Methods 6 875-81
140. Tsien R Y 1989 Fluorescent probes of cell signaling Annu. Rev. Neurosci. 12 227-53
141. Turaga S C, Murray J F, Jain V, Roth F, Helmstaedter M, Briggman K, Denk W and Seung H S 2010 Convolutional networks can learn to generate affinity graphs for image segmentation Neural. Comput. 22 511-38
142. Valmianski I, Shih A Y, Driscoll J D, Matthews D W, Freund Y and Kleinfeld D 2010 Automatic identification of fluorescently labeled brain cells for rapid functional imaging J. Neurophysiol. 104 1803-11
143. Verma I M and Weitzman M D 2005 Gene therapy: twenty-first century medicine Annu. Rev. Biochem. 74 711-38 (Pubitemid 40995522)
144. Vogelstein J T, Packer A M, Machado T A, Sippy T, Babadi B, Yuste R and Paninski L 2010 Fast nonnegative deconvolution for spike train inference from population calcium imaging J. Neurophysiol. 104 3691-704
145. Wachowiak M and Cohen L B 2001 Representation of odorants by receptor neuron input to the mouse olfactory bulb Neuron 32 723-35 (Pubitemid 33145204)
146. 2+ sensor Nature Methods 5 797-804
147. Waters J and Helmchen F 2004 Boosting of action potential backpropagation by neocortical network activity in vivo J. Neurosci. 24 11127-36 (Pubitemid 40012972)
148. 2+ influx into dendritic tufts of layer 2/3 neocortical pyramidal neurons in vitro and in vivo J. Neurosci. 23 8558-67 (Pubitemid 37158755)
149. Wolfe J, Houweling A R and Brecht M 2010 Sparse and powerful cortical spikes Curr. Opin. Neurobiol. 20 306-12
150. 2+ imaging Nature Methods 3 377-83
151. Zeng S, Lv X, Zhan C, Chen W R, Xiong W, Jacques S L and Luo Q 2006 Simultaneous compensation for spatial and temporal dispersion of acousto-optical deflectors for two-dimensional scanning with a single prism Opt. Lett. 31 1091-3 (Pubitemid 43837462)
152. Zipfel W R, Williams R M and Webb W W 2003 Nonlinear magic: multiphoton microscopy in the biosciences Nature Biotechnol. 21 1369-77 (Pubitemid 37356624)
153. Zohary E, Shadlen M N and Newsome W T 1994 Correlated neuronal discharge rate and its implications for psychophysical performance Nature 370 140-3 (Pubitemid 24229125)