Optical neural interfaces

Annual Review of Biomedical Engineering

Volumn 16, Issue , 2014, Pages 103-129

  Warden, Melissa R ^a,b   Cardin, Jessica A ^d   Deisseroth, Karl ^b,c  

^a Department of Obstetrics Gynecology   (United States)

^b Stanford University   (United States)

^c STANFORD UNIVERSITY   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

channelrhodopsin; GCaMP; halorhodopsin; imaging; neurophysiology; optogenetics

Indexed keywords

IMAGING TECHNIQUES; NEURONS; NEUROPHYSIOLOGY;

CHANNELRHODOPSIN; GCAMP; HALORHODOPSIN; NEURAL ACTIVITY; NEURAL INTERFACES; OPTICAL ACTUATORS; OPTOGENETICS; SPECIFIC COMPONENT;

BRAIN;

HALORHODOPSIN; RHODOPSIN; SILICON;

CELL ACTIVITY; ELECTRODE; IMAGING; MULTIPHOTON MICROSCOPY; NERVE CELL; NEUROPHYSIOLOGY; OPTIC NERVE; OPTOGENETICS; REVIEW; ANIMAL; BIOMEDICAL ENGINEERING; BRAIN; CHEMISTRY; ELECTROPHYSIOLOGY; HUMAN; LIGHT; METABOLISM; MOTONEURON; MOUSE; NEUROSCIENCE; OPTICS; PHOTON; PHYSIOLOGY; PROCEDURES; RAT;

ANIMALS; BIOMEDICAL ENGINEERING; BRAIN; ELECTRODES; ELECTROPHYSIOLOGY; HUMANS; LIGHT; MICE; MOTOR NEURONS; NEURONS; NEUROSCIENCES; OPTICS AND PHOTONICS; OPTOGENETICS; PHOTONS; RATS; SILICON;

EID: 84904360700     PISSN: 15239829     EISSN: 15454274     Source Type: Book Series    
DOI: 10.1146/annurev-bioeng-071813-104733     Document Type: Review

References (156)

1. Penfield W, Perot P. 1963. The brain's record of auditory and visual experience: a final summary and discussion. Brain 86(4):595-696
2. Salzman CD, Britten KH, Newsome WT. 1990. Cortical microstimulation influences perceptual judgements of motion direction. Nature 346(6280):174-77
3. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, et al. 2005. Deep brain stimulation for treatment-resistant depression. Neuron 45(5):651-60
4. Fenno L, Yizhar O, Deisseroth K. 2011. The development and application of optogenetics. Annu. Rev. Neurosci. 34:389-412
5. Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K. 2011. Optogenetics in neural systems. Neuron 71(1):9-34
6. Knöpfel T. 2012. Genetically encoded optical indicators for the analysis of neuronal circuits. Nat. Rev. Neurosci. 13(10):687-700
7. Looger LL, Griesbeck O. 2012. Genetically encoded neural activity indicators. Curr. Opin. Neurobiol. 22(1):18-23
8. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8(9):1263-68
9. Zhang F, Wang L-P, Brauner M, Liewald JF, Kay K, et al. 2007. Multimodal fast optical interrogation of neural circuitry. Nature 446(7136):633-39
10. Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM, et al. 2002. Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296(5577):2395-98
11. Han X, Boyden ES. 2007. Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PLoS ONE 2(3):e299
12. Zhang F, Prigge M, Beyrière F, Tsunoda SP, Mattis J, et al. 2008. Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri. Nat. Neurosci. 11(6):631-33
13. Berndt A, Yizhar O, Gunaydin L, Hegemann P, Deisseroth K. 2009. Bi-stable neural state switches. Nat. Neurosci. 12(2):229-34
14. Gradinaru V, Zhang F, Ramakrishnan C, Mattis J, Prakash R, et al. 2010. Molecular and cellular principles for diversifying and extending optogenetics. Cell 141:1-12
15. Chow BY, Han X, Dobry AS, Qian X, Chuong AS, et al. 2010. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463(7277):98-102
16. Lin JY, Lin MZ, Steinbach P, Tsien RY. 2009. Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 96(5):1803-14
17. Wang H, Sugiyama Y, Hikima T, Sugano E, Tomita H, et al. 2009. Molecular determinants differentiating photocurrent properties of two channelrhodopsins from Chlamydomonas. J. Biol. Chem. 284(9):5685-96
18. Gunaydin L, Yizhar O, Berndt A, Sohal VS, Deisseroth K, Hegemann P. 2010. Ultrafast optogenetic control. Nat. Neurosci. 13(3):387-92
19. Berndt A, Schoenenberger P, Mattis J, Tye KM, Deisseroth K, et al. 2011. High-efficiency channel-rhodopsins for fast neuronal stimulation at low light levels. Proc. Natl. Acad. Sci. USA 108(18):7595-600
20. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, et al. 2011. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477(7363):171-78
21. Mattis J, Tye KM, Ferenczi E, Ramakrishnan C, O'Shea DJ, et al. 2012. Principles for applying opto-genetic tools derived from direct comparative analysis of microbial opsins. Nat. Methods 9(2):159-72
22. Zemelman BV, Lee GA, Ng M, Miesenböck G. 2002. Selective photostimulation of genetically charged neurons. Neuron 33(1):15-22
23. Banghart M, Borges K, Isacoff E, Trauner D, Kramer RH. 2004. Light-activated ion channels for remote control of neuronal firing. Nat. Neurosci. 7(12):1381-86
24. Lima SQ, Miesenböck G. 2005. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121(1):141-52
25. Prigge M, Schneider F, Tsunoda SP, Shilyansky C, Wietek J, et al. 2012. Color-tuned channel-rhodopsins for multiwavelength optogenetics. J. Biol. Chem. 287(38):31804-12
26. Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A. 2005. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15(24):2279-84
27. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. 2007. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450(7168):420-24
28. Aravanis AM, Wang LP, Zhang F, Meltzer LA, Mogri MZ, et al. 2007. An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J. Neural Eng. 4:S143-56
29. Gradinaru V, Thompson KR, Zhang F, Mogri M, Kay K, et al. 2007. Targeting and readout strategies for fast optical neural control in vitro and in vivo. J. Neurosci. 27(52):14231-38
30. Zhang F, Gradinaru V, Adamantidis AR, Durand R, Airan RD, et al. 2010. Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat. Protoc. 5(3):439-56
31. Sparta DR, Stamatakis AM, Phillips JL, Hovelsø N, Van Zessen R, Stuber GD. 2012. Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nat. Protoc. 7(1):12-23
32. Witten IB, Lin S-C, Brodsky M, Prakash R, Diester I, et al. 2010. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330(6011):1677-81
33. Tye KM, Prakash R, Kim S-Y, Fenno LE, Grosenick L, et al. 2011. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471(7338):358-62
34. Goshen I, Brodsky M, Prakash R, Wallace J, Gradinaru V, et al. 2011. Dynamics of retrieval strategies for remote memories. Cell 147(3):678-89
35. Warden MR, Selimbeyoglu A, Mirzabekov JJ, Lo M, Thompson KR, et al. 2012. A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge. Nature 492(7429):428-32
36. Tye KM, Mirzabekov JJ, Warden MR, Ferenczi EA, Tsai H-C, et al. 2013. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493(7433):537-41
37. Kim S-Y, Adhikari A, Lee SY, Marshel JH, Kim CK, et al. 2013. Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 496(7444):219-23
38. Wentz CT, Bernstein JG, Monahan P, Guerra A, Rodriguez A, Boyden ES. 2011. A wirelessly powered and controlled device for optical neural control of freely-behaving animals. J. Neural Eng. 8(4):046021
39. Clements I, Gnade A, Rush A, Patten C, Twomey M, Kravitz A. 2013. Miniaturized LED sources for in vivo optogenetic experimentation. Proc. SPIE 8586:85860
40. Huber D, Petreanu L, Ghitani N, Ranade S, Hromádka T, et al. 2008. Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451(7174):61-64
41. Bernstein JG, Han X, Henninger M, Ko EY, Qian X, et al. 2008. Prosthetic systems for therapeutic optical activation and silencing of genetically-targeted neurons. Proc. Soc. Photo-Opt. Instrum. Eng. 6854:68540H
42. Iwai Y, Honda S, Ozeki H, Hashimoto M, Hirase H. 2011. A simple head-mountable LED device for chronic stimulation of optogenetic molecules in freely moving mice. Neurosci. Res. 70(1):124-27
43. Bernstein JG, Boyden ES. 2011. Optogenetic tools for analyzing the neural circuits of behavior. Trends Cogn. Sci. 15(12):592-600
44. Zorzos AN, Boyden ES, Fonstad CG. 2010. Multiwaveguide implantable probe for light delivery to sets of distributed brain targets. Opt. Lett. 35(24):4133-35
45. Zorzos AN, Scholvin J, Boyden ES, Fonstad CG. 2012. Three-dimensional multiwaveguide probe array for light delivery to distributed brain circuits. Opt. Lett. 37(23):4841-43
46. Im M, Cho I, Wu F, Wise KD, Yoon E. 2011. Neural probes integrated with optical mixer/splitter waveguides and multiple stimulation sites. Proc. Int. Conf. Micro Electro Mech. Syst. (MEMS), 24th, Cancun, Mex., Jan. 23-27, pp. 1051-54. New York: IEEE
47. Abaya TVF, Blair S, Tathireddy P, Rieth L, Solzbacher F. 2012. A 3D glass optrode array for optical neural stimulation. Biomed. Opt. Express 3(12):3087-104
48. Abaya TVF, Diwekar M, Blair S, Tathireddy P, Rieth L, et al. 2012. Characterization of a 3D optrode array for infrared neural stimulation. Biomed. Opt. Express 3(9):2200-19
49. Kim T-I, McCall JG, Jung YH, Huang X, Siuda ER, et al. 2013. Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science 340(6129):211-16
50. Ungless MA, Grace AA. 2012. Are you or aren't you? Challenges associated with physiologically identifying dopamine neurons. Trends Neurosci. 35(7):422-30
51. Grace AA, Bunney BS. 1980. Nigral dopamine neurons: intracellular recording and identification with L-dopa injection and histofluorescence. Science 210(4470):654-56
52. Swadlow HA. 1998. Neocortical efferent neurons with very slowly conducting axons: strategies for reliable antidromic identification. J. Neurosci. Methods 79(2):131-41
53. Diester I, Nieder A. 2008. Complementary contributions of prefrontal neuron classes in abstract numerical categorization. J. Neurosci. 28(31):7737-47
54. Constantinidis C, Goldman-Rakic PS. 2002. Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. J. Neurophysiol. 88(6):3487-97
55. Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N. 2012. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482(7383):85-88
56. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. 2009. Optical deconstruction of parkinsonian neural circuitry. Science 324(5925):354-59
57. Tsai H-C, Zhang F, Adamantidis A, Stuber GD, Bonci A, et al. 2009. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324(5930):1080-84
58. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, et al. 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459(7247):663-67
59. Royer S, Zemelman BV, Barbic M, Losonczy A, Buzsáki G, Magee JC. 2010. Multi-array silicon probes with integrated optical fibers: light-assisted perturbation and recording of local neural circuits in the behaving animal. Eur. J. Neurosci. 31(12):2279-91
60. Halassa MM, Siegle JH, Ritt JT, Ting JT, Feng G, Moore CI. 2011. Selective optical drive of thalamic reticular nucleus generates thalamic bursts and cortical spindles. Nat. Neurosci. 14(9):1118-20
61. Siegle JH, Carlen M, Meletis K, Tsai L-H, Moore CI, Ritt J. 2011. Chronically implanted hyperdrive for cortical recording and optogenetic control in behaving mice. Proc. Annu. Int. Conf. Eng. Med. Biol. Soc. (EMBS), 33rd, Boston, Aug. 30-Sep. 3, pp. 7529-32. New York: IEEE
62. Anikeeva P, Andalman AS, Witten I, Warden M, Goshen I, et al. 2012. Optetrode: a multichannel readout for optogenetic control in freely moving mice. Nat. Neurosci. 15(1):163-70
63. Stark E, Koos T, Buzsáki G. 2012. Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals. J. Neurophysiol. 108(1):349-63
64. Voigts J, Siegle JH, Pritchett DL, Moore CI. 2013. The flexDrive: an ultra-light implant for optical control and highly parallel chronic recording of neuronal ensembles in freely moving mice. Front. Syst. Neurosci. 7:8
65. Wang J, Borton DA, Zhang J, Burwell RD, Nurmikko AV. 2010. A neurophotonic device for stimulation and recording of neural microcircuits. Proc. Annu. Int. Conf. Eng. Med. Biol. Soc. (EMBS), 32nd, Buenos Aires, Aug. 31-Sep. 4, pp. 2935-38. New York: IEEE
66. Wang J, Wagner F, Borton D, Zhang J, Ozden I, et al. 2012. Integrated device for combined optical neuromodulation and electrical recording for chronic in vivo applications. J. Neural Eng. 9(1):016001
67. Csicsvari J, Henze DA, Jamieson B, Harris KD, Sirota A, et al. 2003. Massively parallel recording of unit and local field potentials with silicon-based electrodes. J. Neurophysiol. 90(2):1314-23
68. Barthó P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsáki G. 2004. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J. Neu-rophysiol. 92(1):600-8
69. McNaughton BL, O'Keefe J, Barnes C. 1983. The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J. Neurosci. Methods 8(4):391-97
70. Wilson M, McNaughton BL. 1993. Dynamics of the hippocampal ensemble code for space. Science 261(5124):1055-58
71. Kloosterman F, Davidson TJ, Gomperts SN, Layton SP, Hale G, et al. 2009. Micro-drive array for chronic in vivo recording: drive fabrication. J. Vis. Exp. (26):e1094
72. Nguyen DP, Layton SP, Hale G, Gomperts SN, Davidson TJ, et al. 2009. Micro-drive array for chronic in vivo recording: tetrode assembly. J. Vis. Exp. (26):e1098
73. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, et al. 2010. Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of channelrhodopsin-2. Nat. Protoc. 5(2):247-54
74. Han X, Qian X, Bernstein JG, Zhou H-H, Franzesi GT, et al. 2009. Millisecond-timescale optical control of neural dynamics in the nonhuman primate brain. Neuron 62(2):191-98
75. 2+ based on green fluorescent proteins and calmodulin. Nature 388(6645):882-87
76. 2+. Cell Calcium 22(3):209-16
77. 2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence: a new class of fluorescent indicators. J. Biol. Chem. 272(20):13270-74
78. 2+ probe composed of a single green fluorescent protein. Nat. Biotechnol. 19(2):137-41
79. 2+ imaging of dendritic spines. Anal. Chem. 77(18):5861-69
80. 2+ indicator GCaMP2. Proc. Natl. Acad. Sci. USA 103(12):4753-58
81. 2+ indicators. Science 333(6051):1888-91
82. Akerboom J, Chen T-W, Wardill TJ, Tian L, Marvin JS, et al. 2012. Optimization of a GCaMP calcium indicator for neural activity imaging. J. Neurosci. 32(40):13819-40
83. Akerboom J, Carreras Calderón N, Tian L, Wabnig S, Prigge M, et al. 2013. Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front. Mol. Neurosci. 6:2
84. Hires SA, Tian L, Looger LL. 2008. Reporting neural activity with genetically encoded calcium indicators. Brain Cell Biol. 36(1-4):69-86
85. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, et al. 2009. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6(12):875-81
86. Tian L, Akerboom J, Schreiter ER, Looger LL. 2012. Neural activity imaging with genetically encoded calcium indicators. Prog. Brain Res. 196:79-94
87. Tian L, Hires SA, Looger LL. 2012. Imaging neuronal activity with genetically encoded calcium indicators. Cold Spring Harb. Protoc. 2012(6):647-56
88. Dugué GP, Akemann W, Knöpfel T. 2012. A comprehensive concept of optogenetics. Prog. Brain Res. 196:1-28
89. Alford SC, Wu J, Zhao Y, Campbell RE, Knöpfel T. 2013. Optogenetic reporters. Biol. Cell 105(1):14-29
90. Chen T-W, Wardill TJ, Sun Y, Pulver SR, Renninger SL, et al. 2013. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499(7458):295-300
91. Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT, et al. 2013. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat. Methods 10(2):162-70
92. Adelsberger H, Garaschuk O, Konnerth A. 2005. Cortical calcium waves in resting newborn mice. Nat. Neurosci. 8(8):988-90
93. Ferezou I, Bolea S, Petersen CCH. 2006. Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50(4):617-29
94. Murayama M, Pérez-Garci E, Lüscher H-R, Larkum ME. 2007. Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats. J. Neurophysiol. 98(3):1791-805
95. Murayama M, Pérez-Garci E, Nevian T, Bock T, Senn W, Larkum ME. 2009. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457:1137-41
96. Gunaydin LA, Grosenick L, Finkelstein JC, Kauvar IV, Fenno LE, et al. 2014. Natural neural projection dynamics underlying social behavior. Cell. In press
97. Lütcke H, Murayama M, Hahn T, Margolis DJ, Astori S, 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
98. Cui G, Jun SB, Jin X, Pham MD, Vogel SS, et al. 2013. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494(7436):238-42
99. Helmchen F, Fee MS, Tank DW, Denk W. 2001. A miniature head-mounted two-photon microscope: high-resolution brain imaging in freely moving animals. Neuron 31(6):903-12
100. Flusberg BA, Jung JC, Cocker ED, Anderson EP, Schnitzer MJ. 2005. In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope. Opt. Lett. 30(17):2272-74
101. Flusberg BA, Nimmerjahn A, Cocker ED, Mukamel EA, Barretto RPJ, et al. 2008. High-speed, miniaturized fluorescence microscopy in freely moving mice. Nat. Methods 5(11):935-38
102. Sawinski J, Wallace DJ, Greenberg DS, Grossmann S, Denk W, Kerr JND. 2009. Visually evoked activity in cortical cells imaged in freely moving animals. Proc. Natl. Acad. Sci. USA 106(46):19557-62
103. Ghosh KK, Burns LD, Cocker ED, Nimmerjahn A, Ziv Y, et al. 2011. Miniaturized integration of a fluorescence microscope. Nat. Methods 8(10):871-78
104. Jung JC, Mehta AD, Aksay E, Stepnoski R, Schnitzer MJ. 2004. In vivo mammalian brain imaging using one-and two-photon fluorescence microendoscopy. J. Neurophysiol. 92(5):3121-33
105. Kerr JND, Nimmerjahn A. 2012. Functional imaging in freely moving animals. Curr. Opin. Neurobiol. 22(1):45-53
106. Lütcke H, Margolis DJ, Helmchen F. 2013. Steady or changing? Long-term monitoring of neuronal population activity. Trends Neurosci. 36(7):375-84
107. Regehr WG, Tank DW. 1991. Selective fura-2 loading of presynaptic terminals and nerve cell processes by local perfusion in mammalian brain slice. J. Neurosci. Methods 37:111-19
108. O'Donovan MJ, Ho S, Sholomenko G, Yee W. 1993. Real-time imaging of neurons retrogradely and anterogradely labelled with calcium-sensitive dyes. J. Neurosci. Methods 46(2):91-106
109. Nimmerjahn A, Kirchhoff F, Kerr JND, Helmchen F. 2004. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods 1(1):31-37
110. 2+ sensor. Nat. Methods 5(9):797-804
111. 2+ indicator proteins in transgenic mice under TET control. PLoS Biol. 2(6):e163
112. Zariwala HA, Borghuis BG, Hoogland TM, Madisen L, Tian L, et al. 2012. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J. Neurosci. 32(9):3131-41
113. 2+ entry into hippocampal neurons.Nature 357(6375):244-46
114. Denk W, Yuste R, Svoboda K, Tank DW. 1996. Imaging calcium dynamics in dendritic spines. Curr. Opin. Neurobiol. 6(3):372-78
115. 2+ indicators and photophysical considerations for optogenetic applications. ACS Chem. Neurosci. 4(6):963-72
116. 2+ indicator for detecting optically evoked action potentials. PLoS ONE 7(7):e39933
117. Li Y, Tsien RW. 2012. pHTomato, a red, genetically encoded indicator that enables multiplex interrogation of synaptic activity. Nat. Neurosci. 15(7):1047-53
118. Hires SA, Zhu Y, Tsien RY. 2008. Optical measurement of synaptic glutamate spillover and reuptake by linker optimized glutamate-sensitive fluorescent reporters. Proc. Natl. Acad. Sci. USA 105(11):4411-16
119. Ungerstedt U. 1984. Measurement of neurotransmitter release by intracranial dialysis. In Measurement of Neurotransmitter Release In Vivo, ed. CA Marsden, pp. 81-107. New York: Wiley
120. Moghaddam B, Bunney BS. 1990. Acute effects of typical and atypical antipsychotic drugs on the release of dopamine from prefrontal cortex, nucleus accumbens, and striatum of the rat: an in vivo microdialysis study. J. Neurochem. 54(5):1755-60
121. Stamford JA, Justice JB. 1996. Probing brain chemistry. Anal. Chem. 68(11):359A-63A
122. Phillips PEM, Stuber GD, Heien MLAV, Wightman RM, Carelli RM. 2003. Subsecond dopamine release promotes cocaine seeking. Nature 422(6932):614-18
123. Siegel MS, Isacoff EY. 1997. A genetically encoded optical probe of membrane voltage. Neuron 19(4):735-41
124. Cacciatore TW, Brodfuehrer PD, Gonzalez JE, Jiang T, Adams SR, et al. 1999. Identification of neural circuits by imaging coherent electrical activity with FRET-based dyes. Neuron 23(3):449-59
125. Sakai R, Repunte-Canonigo V, Raj CD, Knöpfel T. 2001. Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein. Eur. J. Neurosci. 13(12):2314-18
126. Ataka K, Pieribone VA. 2002. A genetically targetable fluorescent probe of channel gating with rapid kinetics. Biophys. J. 82(1):509-16
127. Akemann W, Mutoh H, Perron A, Rossier J, Knöpfel T. 2010. Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat. Methods 7(8):643-49
128. Kralj JM, Hochbaum DR, Douglass AD, Cohen AE. 2011. Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 333(6040):345-48
129. Kralj JM, Douglass AD, Hochbaum DR, Maclaurin D, Cohen AE. 2012. Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat. Methods 9(1):90-95
130. Perron A, Akemann W, Mutoh H, Knöpfel T. 2012. Genetically encoded probes for optical imaging of brain electrical activity. Prog. Brain Res. 196:63-77
131. Gong Y, Li JZ, Schnitzer MJ. 2013. Enhanced archaerhodopsin fluorescent protein voltage indicators. PLoS ONE 8(6):e66959
132. Baker BJ, Kosmidis EK, Vucinic D, Falk CX, Cohen LB, et al. 2005. Imaging brain activity with voltageand calcium-sensitive dyes. Cell. Mol. Neurobiol. 25(2):245-82
133. Froemke RC, Kumar VS, Czkwianianc P, Yuste R. 2002. Analysis of multineuronal activation patterns from calcium-imaging experiments in brain slices. Trends Cardiovasc. Med. 12(6):247-52
134. Stosiek C, Garaschuk O, Holthoff K, Konnerth A. 2003. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. USA 100:7319-24
135. Duff Davis M, Schmidt JJ. 2000. In vivo spectrometric calcium flux recordings of intrinsic caudate-putamen cells and transplanted IMR-32 neuroblastoma cells using miniature fiber optrodes in anesthetized and awake rats and monkeys. J. Neurosci. Methods 99(1-2):9-23
136. 2+ concentration during anoxia: feasibility of a fiber-optic plate microscope system for in vivo experiments. Brain Res. 732(1-2):61-68
137. Denk W, Svoboda K. 1997. Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 18(3):351-57
138. Svoboda K, Yasuda R. 2006. Principles of two-photon excitation microscopy and its applications to neuroscience. Neuron 50(6):823-39
139. Flusberg BA, Cocker ED, Piyawattanametha W, Jung JC, Cheung ELM, Schnitzer MJ. 2005. Fiberoptic fluorescence imaging. Nat. Methods 2(12):941-50
140. Denk W, Strickler JH, Webb WW. 1990. Two-photon laser scanning fluorescence microscopy. Science 248(4951):73-76
141. Svoboda K, Denk W, Kleinfeld D, Tank DW. 1997. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385(6612):161-65
142. Kleinfeld D, Mitra PP, Helmchen F, Denk W. 1998. Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc. Natl. Acad. Sci. USA 95(26):15741-46
143. Dombeck D, Khabbaz AN, Collman F, Adelman TL, Tank DW. 2007. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56(1):43-57
144. Laffray S, Pagès S, Dufour H, De Koninck P, De Koninck Y, Côté D. 2011. Adaptive movement compensation forinvivo imagingoffast cellular dynamics withinamoving tissue.PLoS ONE 6(5):e19928
145. Paukert M, Bergles DE. 2012. Reduction of motion artifacts during in vivo two-photon imaging of brain through heartbeat triggered scanning. J. Physiol. 590:2955-63
146. Chen JL, Pfaffli OA, Voigt FF, Margolis DJ, Helmchen F. 2013. Online correction of licking-induced brain motion during two-photon imaging with a tunable lens. J. Physiol. 591(19):4689-98
147. Levene MJ, Dombeck D, Kasischke KA, Molloy RP, Webb WW. 2004. In vivo multiphoton microscopy of deep brain tissue. J. Neurophysiol. 91(4):1908-12
148. Ziv Y, Burns LD, Cocker ED, Hamel EO, Ghosh KK, et al. 2013. Long-term dynamics of CA1 hippocampal place codes. Nat. Neurosci. 16(3):264-66
149. Towne C, Montgomery KL, Iyer SM, Deisseroth K, Delp SL. 2013. Optogenetic control of targeted peripheral axons in freely moving animals. PLoS ONE 8(8):e72691
150. Liske H, Towne C, Anikeeva P, Zhao S, Feng G, et al. 2013. Optical inhibition of motor nerve and muscle activity in vivo. Muscle Nerve 47(6):916-21
151. Llewellyn ME, Thompson KR, Deisseroth K, Delp SL. 2010. Orderly recruitment of motor units under optical control in vivo. Nat Med. 16(10):1161-65
152. Prakash R, Yizhar O, Grewe B, Ramakrishnan C, Wang N, et al. 2012. Two-photon optogenetic toolbox for fast inhibition, excitation, and bistable modulation. Nat. Methods 9:1171-79
153. Packer AM, Peterka DS, Hirtz JJ, Prakash R, Deisseroth K, Yuste R. 2012. Two-photon optogenetics of dendritic spines and neuronal circuits in 3D. Nat. Methods 9(12):1202-5
154. Deisseroth K, Schnitzer M. 2013. Engineering approachesto illuminating brain structure and dynamics. Neuron 80(3):568-77
155. Airan RD, Thompson KR, Fenno LE, Bernstein H, Deisseroth K. 2009. Temporally precise in vivo control of intracellular signaling. Nature 458:1025-29
156. Zhang F, Aravanis AM, Adamantidis A, de Lecea L, Deisseroth K. 2007. Circuit-breakers: optical technologies for probing neural signals and systems. Nat. Rev. Neurosci. 8(8):577-81