Two-way communication with neural networks in vivo using focused light

Nature Protocols

Volumn 8, Issue 6, 2013, Pages 1184-1203

  Wilson, Nathan R ^a   Schummers, James ^b   Runyan, Caroline A ^a,c   Yan, Sherry X ^a   Chen, Robert E ^a   Deng, Yuting ^a   Sur, Mriganka ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MAX PLANCK FLORIDA INSTITUTE FOR NEUROSCIENCE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; COMPUTER PROGRAM; COMPUTER SYSTEM; CONTROLLED STUDY; DYNAMICS; ELECTRODE; IN VIVO STUDY; INTRACELLULAR RECORDING; LIGHT; LIGHT INTENSITY; MICROSCOPE; MOUSE; NERVE CELL NETWORK; NONHUMAN; OPTICS; PRIORITY JOURNAL; TWO PHOTON MICROSCOPE;

ANIMALS; LIGHT; MICE; MICROSCOPY; NERVE NET; NEURONS; PHOTIC STIMULATION; RHODOPSIN; VISUAL CORTEX;

EID: 84879343441     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2013.063     Document Type: Article

References (52)

1. Schwann, T. & Schleyden, M. Microscopical Researches into the Accordance in the Structure and Growth of Animals and Plants. (Sydenham Society, London, 1847).
2. O'Connor, D.H., Huber, D. & Svoboda, K. Reverse-engineering the mouse brain. Nature 461, 923-929 (2009).
3. Regehr, W.G., Connor, J.A. & Tank, D.W. Optical imaging of calcium accumulation in hippocampal pyramidal cells during synaptic activation. Nature 341, 533-536 (1989).
4. Svoboda, K., Denk, W., Kleinfeld, D. & Tank, D.W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385, 161-165 (1997).
5. Smetters, D., Majewska, A. & Yuste, R. Detecting action potentials in neuronal populations with calcium imaging. Methods 18, 215-221 (1999).
6. Stosiek, C., Garaschuk, O., Holthoff, K. & Konnerth, A. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. USA 100, 7319-7324 (2003).
7. Shoham, S., O'Connor, D.H., Sarkisov, D.V. & Wang, S.S. Rapid neurotransmitter uncaging in spatially defned patterns. Nat. Methods 2, 837-843 (2005).
8. Pettit, D.L., Wang, S.S., Gee, K.R. & Augustine, G.J. Chemical two-photon uncaging: a novel approach to mapping glutamate receptors. Neuron 19, 465-471 (1997).
9. Arenkiel, B.R. et al. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54, 205-218 (2007).
10. Cardin, J.A. et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663-667 (2009).
11. Peron, S. & Svoboda, K. From cudgel to scalpel: toward precise neural control with optogenetics. Nat. Methods 8, 30-34 (2011).
12. Schummers, J., Yu, H. & Sur, M. Tuned responses of astrocytes and their infuence on hemodynamic signals in the visual cortex. Science 320, 1638-1643 (2008).
13. Anastassiou, C.A., Perin, R., Markram, H. & Koch, C. Ephaptic coupling of cortical neurons. Nat. Neurosci. 14, 217-223 (2011).
14. Vervaeke, K., Lorincz, A., Nusser, Z. & Silver, R.A. Gap junctions compensate for sublinear dendritic integration in an inhibitory network. Science 335, 1624-1628 (2012).
15. Zhang, F. et al. Multimodal fast optical interrogation of neural circuitry. Nature 446, 633-639 (2007).
16. Nikolenko, V., Poskanzer, K.E. & Yuste, R. Two-photon photostimulation and imaging of neural circuits. Nat. Methods 4, 943-950 (2007).
17. Guo, Z.V., Hart, A.C. & Ramanathan, S. Optical interrogation of neural circuits in Caenorhabditis elegans. Nat. Methods 6, 891-896 (2009).
18. Nagel, G. et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100, 13940-13945 (2003).
19. Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268 (2005).
20. Valmianski, I. et al. Automatic identifcation of fuorescently labeled brain cells for rapid functional imaging. J. Neurophysiol. 104, 1803-1811 (2010).
21. Lillis, K.P., Eng, A., White, J.A. & Mertz, J. Two-photon imaging of spatially extended neuronal network dynamics with high temporal resolution. J. Neurosci. Methods 172, 178-184 (2008).
22. Grewe, B.F., Langer, D., Kasper, H., Kampa, B.M. & Helmchen, F. High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision. Nat. Methods 7, 399-405 (2010).
23. Rothschild, G., Nelken, I. & Mizrahi, A. Functional organization and population dynamics in the mouse primary auditory cortex. Nat. Neurosci. 13, 353-360 (2010).
24. Wilson, N.R., Runyan, C.A., Wang, F.L. & Sur, M. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488, 343-348 (2012).
25. Gerits, A. et al. Optogenetically induced behavioral and functional network changes in primates. Curr. Biol. 22, 1722-1726 (2012).
26. Adamantidis, A.R. et al. Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J. Neurosci. 31, 10829-10835 (2011).
27. Grinvald, A. & Hildesheim, R. VSDI: a new era in functional imaging of cortical dynamics. Nat. Rev. Neurosci. 5, 874-885 (2004).
28. Tian, L. et al. Imaging neural activity in worms, fies and mice with improved GCaMP calcium indicators. Nat. Methods 6, 875-881 (2009).
29. Chow, B.Y. et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463, 98-102 (2010).
30. Li, Y. & Tsien, R.W. pHTomato, a red, genetically encoded indicator that enables multiplex interrogation of synaptic activity. Nat. Neurosci. 15, 1047-1053 (2012).
31. Zariwala, H.A. et al. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J. Neurosci. 32, 3131-3141 (2012).
32. Madisen, L. et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 15, 793-802 (2012).
33. Sanjana, N.E. et al. A transcription activator-like effector toolbox for genome engineering. Nat. Protoc. 7, 171-192 (2012).
34. Miyamichi, K. et al. Cortical representations of olfactory input by trans-synaptic tracing. Nature 472, 191-196 (2011).
35. Bock, D.D. et al. Network anatomy and in vivo physiology of visual cortical neurons. Nature 471, 177-182 (2011).
36. Alivisatos, A.P. et al. The brain activity map project and the challenge of functional connectomics. Neuron 74, 970-974 (2012).
37. Pologruto, T.A., Sabatini, B.L. & Svoboda, K. ScanImage: fexible software for operating laser scanning microscopes. Biomed. Eng. Online 2, 13 (2003).
38. Wagenaar, D.A. & Potter, S.M. A versatile all-channel stimulator for electrode arrays, with real-time control. J. Neural. Eng. 1, 39-45 (2004).
39. Asaad, W.F. & Eskandar, E.N. A fexible software tool for temporally-precise behavioral control in Matlab. J. Neurosci. Methods 174, 245-258 (2008).
40. Suter, B.A. et al. Ephus: multipurpose data acquisition software for neuroscience experiments. Front. Neural. Circuits 4, 100 (2010).
41. Katona, G. et al. Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes. Nat. Methods 9, 201-208 (2012).
42. Reddy, G.D. & Saggau, P. Fast three-dimensional laser scanning scheme using acousto-optic defectors. J. Biomed. Opt. 10, 064038 (2005).
43. 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 67, 858-871 (2010).
44. Oertner, T.G. The Lego-logic of optogenetics. Nat. Methods 8, 1011-1013 (2011).
45. Knopfel, T. Genetically encoded optical indicators for the analysis of neuronal circuits. Nat. Rev. Neurosci. 13, 687-700 (2012).
46. 2+ imaging. Nat. Methods 3, 377-383 (2006).
47. Vogelstein, J.T. et al. Spike inference from calcium imaging using sequential Monte Carlo methods. Biophys. J. 97, 636-655 (2009).
48. Petreanu, L., Huber, D., Sobczyk, A. & Svoboda, K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10, 663-668 (2007).
49. Rickgauer, J.P. & Tank, D.W. Two-photon excitation of channelrhodopsin-2 at saturation. Proc. Natl. Acad. Sci. USA 106, 15025-15030 (2009).
50. Hirase, H., Nikolenko, V., Goldberg, J.H. & Yuste, R. Multiphoton stimulation of neurons. J. Neurobiol. 51, 237-247 (2002).
51. Hirase, H., Nikolenko, V. & Yuste, R. Multiphoton stimulation of neurons and spines. Cold Spring Harb. Protoc. 2012, 472-475 (2012).
52. Vaziri, A. & Emiliani, V. Reshaping the optical dimension in optogenetics. Curr. Opin. Neurobiol. 22, 128-137 (2012).