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Concepts of All-Optical Physiology

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Part of the Neuromethods book series (NM, volume 133)

Abstract

All-optical physiology represents a methodological approach using light for both readout from and manipulation of individual neurons. This approach paves the way for a true, causal analysis of neuronal activity with single-cell and single action potential resolution and is therefore highly desirable for the investigation of neural networks. The following chapter addresses the general concepts of all-optical interrogations by shedding light on all critical steps needed for these experiments: Calcium-sensitive probes for readout, next-generation two-photon-excitable optogenetic actuators for manipulation and advanced optics for efficient stimulation of and real-time readout from individual neurons. The chapter also provides a step-by-step protocol on an all-optical strategy using an optical parametric oscillator (OPO) for photostimulation of opsin-expressing cells alongside simultaneous two-photon calcium imaging.

Key words

All-optical Two-photon optogenetics Optical parametric oscillator Synthetic and genetically encoded calcium indicators Optogenetic stimulation paradigms 

References

  1. 1.
    Stroh A, Diester I (2012) Optogenetics: a new method for the causal analysis of neuronal networks in vivo. e-Neuroforum 3(4):81–88. doi: 10.1007/s13295-012-0035-8 Google Scholar
  2. 2.
    Emiliani V, Cohen AE, Deisseroth K, Hausser M (2015) All-optical interrogation of neural circuits. J Neurosci 35(41):13917–13926. doi: 10.1523/JNEUROSCI.2916-15.2015 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Akerboom J, Chen TW, Wardill TJ, Tian L, Marvin JS, Mutlu S, Calderon NC, Esposti F, Borghuis BG, Sun XR, Gordus A, Orger MB, Portugues R, Engert F, Macklin JJ, Filosa A, Aggarwal A, Kerr RA, Takagi R, Kracun S, Shigetomi E, Khakh BS, Baier H, Lagnado L, Wang SS, Bargmann CI, Kimmel BE, Jayaraman V, Svoboda K, Kim DS, Schreiter ER, Looger LL (2012) Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 32(40):13819–13840. doi: 10.1523/JNEUROSCI.2601-12.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Prakash R, Yizhar O, Grewe B, Ramakrishnan C, Wang N, Goshen I, Packer AM, Peterka DS, Yuste R, Schnitzer MJ, Deisseroth K (2012) Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation. Nat Methods 9(12):1171–1179. doi: 10.1038/nmeth.2215 CrossRefPubMedGoogle Scholar
  5. 5.
    Rickgauer JP, Deisseroth K, Tank DW (2014) Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields. Nat Neurosci 17(12):1816–1824. doi: 10.1038/nn.3866 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Packer AM, Russell LE, Dalgleish HW, Hausser M (2015) Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo. Nat Methods 12(2):140–146. doi: 10.1038/nmeth.3217 CrossRefPubMedGoogle Scholar
  7. 7.
    Tsien RY (1981) A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290(5806):527–528CrossRefPubMedGoogle Scholar
  8. 8.
    Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248(4951):73–76CrossRefPubMedGoogle Scholar
  9. 9.
    Yuste R, Denk W (1995) Dendritic spines as basic functional units of neuronal integration. Nature 375(6533):682–684. doi: 10.1038/375682a0 CrossRefPubMedGoogle Scholar
  10. 10.
    Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci U S A 100(12):7319–7324. doi: 10.1073/pnas.1232232100 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8(9):1263–1268CrossRefPubMedGoogle Scholar
  12. 12.
    Adelsberger H, Grienberger C, Stroh A, Konnerth A (2014) In vivo calcium recordings and channelrhodopsin-2 activation through an optical fiber. Cold Spring Harb Protoc 2014(10). doi: 10.1101/pdb.prot084145. pdb prot084145
  13. 13.
    Zhang YP, Oertner TG (2007) Optical induction of synaptic plasticity using a light-sensitive channel. Nat Methods 4(2):139–141. doi: 10.1038/nmeth988 CrossRefPubMedGoogle Scholar
  14. 14.
    Wilson NR, Runyan CA, Wang FL, Sur M (2012) Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488(7411):343–348. doi: 10.1038/nature11347 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Stroh A, Adelsberger H, Groh A, Ruhlmann C, Fischer S, Schierloh A, Deisseroth K, Konnerth A (2013) Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo. Neuron 77(6):1136–1150. doi: 10.1016/j.neuron.2013.01.031 CrossRefPubMedGoogle Scholar
  16. 16.
    Schmid F, Wachsmuth L, Schwalm M, Prouvot PH, Jubal ER, Fois C, Pramanik G, Zimmer C, Faber C, Stroh A (2016) Assessing sensory versus optogenetic network activation by combining (o)fMRI with optical Ca2+ recordings. J Cereb Blood Flow Metab 36(11):1885–1900. doi: 10.1177/0271678X15619428 CrossRefPubMedGoogle Scholar
  17. 17.
    Akerboom J, Carreras Calderon N, Tian L, Wabnig S, Prigge M, Tolo J, Gordus A, Orger MB, Severi KE, Macklin JJ, Patel R, Pulver SR, Wardill TJ, Fischer E, Schuler C, Chen TW, Sarkisyan KS, Marvin JS, Bargmann CI, Kim DS, Kugler S, Lagnado L, Hegemann P, Gottschalk A, Schreiter ER, Looger LL (2013) Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci 6:2. doi: 10.3389/fnmol.2013.00002 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Rickgauer JP, Tank DW (2009) Two-photon excitation of channelrhodopsin-2 at saturation. Proc Natl Acad Sci U S A 106(35):15025–15030. doi: 10.1073/pnas.0907084106 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Inoue M, Takeuchi A, Horigane S, Ohkura M, Gengyo-Ando K, Fujii H, Kamijo S, Takemoto-Kimura S, Kano M, Nakai J, Kitamura K, Bito H (2015) Rational design of a high-affinity, fast, red calcium indicator R-CaMP2. Nat Methods 12(1):64–70. doi: 10.1038/nmeth.3185 CrossRefPubMedGoogle Scholar
  20. 20.
    Tischbirek C, Birkner A, Jia H, Sakmann B, Konnerth A (2015) Deep two-photon brain imaging with a red-shifted fluorometric Ca2+ indicator. Proc Natl Acad Sci U S A 112(36):11377–11382. doi: 10.1073/pnas.1514209112 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Klapoetke NC, Murata Y, Kim SS, Pulver SR, Birdsey-Benson A, Cho YK, Morimoto TK, Chuong AS, Carpenter EJ, Tian Z, Wang J, Xie Y, Yan Z, Zhang Y, Chow BY, Surek B, Melkonian M, Jayaraman V, Constantine-Paton M, Wong GK, Boyden ES (2014) Independent optical excitation of distinct neural populations. Nat Methods 11(3):338–346. doi: 10.1038/nmeth.2836 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Kleinlogel S, Feldbauer K, Dempski RE, Fotis H, Wood PG, Bamann C, Bamberg E (2011) Ultra light-sensitive and fast neuronal activation with the Ca(2)+−permeable channelrhodopsin CatCh. Nat Neurosci 14(4):513–518. doi: 10.1038/nn.2776 CrossRefPubMedGoogle Scholar
  23. 23.
    Chaigneau E, Ronzitti E, Gajowa MA, Soler-Llavina GJ, Tanese D, Brureau AY, Papagiakoumou E, Zeng H, Emiliani V (2016) Two-photon holographic stimulation of ReaChR. Front Cell Neurosci 10:234. doi: 10.3389/fncel.2016.00234 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Ronzitti E, Conti R, Papagiakoumou E, Tanese D, Zampini V, Chaigneau E, Foust AJ, Klapoetke N, Boyden ES, Emiliani V (2016) Sub-millisecond optogenetic control of neuronal firing with two-photon holographic photoactivation of Chronos. bioRxiv. doi: 10.1101/062182
  25. 25.
    Oron D, Tal E, Silberberg Y (2005) Scanningless depth-resolved microscopy. Opt Express 13(5):1468–1476CrossRefPubMedGoogle Scholar
  26. 26.
    Gradinaru V, Zhang F, Ramakrishnan C, Mattis J, Prakash R, Diester I, Goshen I, Thompson KR, Deisseroth K (2010) Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141(1):154–165. doi: 10.1016/j.cell.2010.02.037. [doi].S0092-8674(10)00190-X [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Chuong AS, Miri ML, Busskamp V, Matthews GA, Acker LC, Sorensen AT, Young A, Klapoetke NC, Henninger MA, Kodandaramaiah SB, Ogawa M, Ramanlal SB, Bandler RC, Allen BD, Forest CR, Chow BY, Han X, Lin Y, Tye KM, Roska B, Cardin JA, Boyden ES (2014) Noninvasive optical inhibition with a red-shifted microbial rhodopsin. Nat Neurosci 17(8):1123–1129. doi: 10.1038/nn.3752 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Wietek J, Wiegert JS, Adeishvili N, Schneider F, Watanabe H, Tsunoda SP, Vogt A, Elstner M, Oertner TG, Hegemann P (2014) Conversion of channelrhodopsin into a light-gated chloride channel. Science 344(6182):409–412. doi: 10.1126/science.1249375 CrossRefPubMedGoogle Scholar
  29. 29.
    Giordmaine JM, R. (1965) Tunable coherent parametric oscillation in LiNbO3 at optical frequencies. Phys Rev Lett (APS) 14:973CrossRefGoogle Scholar
  30. 30.
    Johnson MJ, Haub JG, Orr BJ (1995) Continuously tunable narrow-band operation of an injection-seeded ring-cavity optical parametric oscillator: spectroscopic applications. Opt Lett 20(11):1277–1279CrossRefPubMedGoogle Scholar
  31. 31.
    Masters BR, So PT, Gratton E (1997) Multiphoton excitation fluorescence microscopy and spectroscopy of in vivo human skin. Biophys J 72(6):2405–2412. doi: 10.1016/S0006-3495(97)78886-6 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Herz J, Siffrin V, Hauser AE, Brandt AU, Leuenberger T, Radbruch H, Zipp F, Niesner RA (2010) Expanding two-photon intravital microscopy to the infrared by means of optical parametric oscillator. Biophys J 98(4):715–723. doi: 10.1016/j.bpj.2009.10.035 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22(12):1567–1572. doi: 10.1038/nbt1037 CrossRefPubMedGoogle Scholar
  34. 34.
    Andresen V, Alexander S, Heupel WM, Hirschberg M, Hoffman RM, Friedl P (2009) Infrared multiphoton microscopy: subcellular-resolved deep tissue imaging. Curr Opin Biotechnol 20(1):54–62. doi: 10.1016/j.copbio.2009.02.008 CrossRefPubMedGoogle Scholar
  35. 35.
    Fois C, Prouvot PH, Stroh A (2014) A roadmap to applying optogenetics in neuroscience. Methods Mol Biol 1148:129–147. doi: 10.1007/978-1-4939-0470-9_9 CrossRefPubMedGoogle Scholar
  36. 36.
    Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O'Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT, Stehfest K, Fudim R, Ramakrishnan C, Huguenard JR, Hegemann P, Deisseroth K (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477(7363):171–178. doi: 10.1038/nature10360 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Tsien RY (1980) New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19(11):2396–2404CrossRefPubMedGoogle Scholar
  38. 38.
    Grienberger C, Konnerth A (2012) Imaging calcium in neurons. Neuron 73(5):862–885. doi: 10.1016/j.neuron.2012.02.011 CrossRefPubMedGoogle Scholar
  39. 39.
    Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15(8):303–308CrossRefPubMedGoogle Scholar
  40. 40.
    Neher E, Augustine GJ (1992) Calcium gradients and buffers in bovine chromaffin cells. J Physiol 450:273–301CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Paredes RM, Etzler JC, Watts LT, Zheng W, Lechleiter JD (2008) Chemical calcium indicators. Methods 46(3):143–151. doi: 10.1016/j.ymeth.2008.09.025 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Rochefort NL, Garaschuk O, Milos RI, Narushima M, Marandi N, Pichler B, Kovalchuk Y, Konnerth A (2009) Sparsification of neuronal activity in the visual cortex at eye-opening. Proc Natl Acad Sci U S A 106(35):15049–15054. doi: 10.1073/pnas.0907660106 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Tian L, Hires SA, Looger LL (2012) Imaging neuronal activity with genetically encoded calcium indicators. Cold Spring Harb Protoc 2012(6):647–656. doi: 10.1101/pdb.top069609 CrossRefPubMedGoogle Scholar
  44. 44.
    Nakai J, Ohkura M, Imoto K (2001) A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19(2):137–141. doi: 10.1038/84397 CrossRefPubMedGoogle Scholar
  45. 45.
    Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6(12):875–881. doi: 10.1038/nmeth.1398 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Zhao Y, Araki S, Wu J, Teramoto T, Chang YF, Nakano M, Abdelfattah AS, Fujiwara M, Ishihara T, Nagai T, Campbell RE (2011) An expanded palette of genetically encoded Ca(2)(+) indicators. Science 333(6051):1888–1891. doi: 10.1126/science.1208592 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Truong K, Sawano A, Mizuno H, Hama H, Tong KI, Mal TK, Miyawaki A, Ikura M (2001) FRET-based in vivo Ca2+ imaging by a new calmodulin-GFP fusion molecule. Nat Struct Biol 8(12):1069–1073. doi: 10.1038/nsb728 CrossRefPubMedGoogle Scholar
  48. 48.
    Shimomura O, Johnson FH, Saiga Y (1962) Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 59:223–239CrossRefPubMedGoogle Scholar
  49. 49.
    Xu X, Soutto M, Xie Q, Servick S, Subramanian C, von Arnim AG, Johnson CH (2007) Imaging protein interactions with bioluminescence resonance energy transfer (BRET) in plant and mammalian cells and tissues. Proc Natl Acad Sci U S A 104(24):10264–10269. doi: 10.1073/pnas.0701987104 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Takai A, Nakano M, Saito K, Haruno R, Watanabe TM, Ohyanagi T, Jin T, Okada Y, Nagai T (2015) Expanded palette of Nano-lanterns for real-time multicolor luminescence imaging. Proc Natl Acad Sci U S A 112(14):4352–4356. doi: 10.1073/pnas.1418468112 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Garaschuk O, Konnerth A (2010, 2010) In vivo two-photon calcium imaging using multicell bolus loading. Cold Spring Harb Protoc 10. doi: 10.1101/pdb.prot5482. pdb prot5482
  52. 52.
    Shevtsova Z, Malik JM, Michel U, Bahr M, Kugler S (2005) Promoters and serotypes: targeting of adeno-associated virus vectors for gene transfer in the rat central nervous system in vitro and in vivo. Exp Physiol 90(1):53–59. doi: 10.1113/expphysiol.2004.028159 CrossRefPubMedGoogle Scholar
  53. 53.
    Zhang F, Gradinaru V, Adamantidis AR, Durand R, Airan RD, de Lecea L, Deisseroth K (2010) Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat Protoc 5(3):439–456. doi: 10.1038/nprot.2009.226. [doi] nprot.2009.226 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Zhang F, Vierock J, Yizhar O, Fenno LE, Tsunoda S, Kianianmomeni A, Prigge M, Berndt A, Cushman J, Polle J, Magnuson J, Hegemann P, Deisseroth K (2011) The microbial opsin family of optogenetic tools. Cell 147(7):1446–1457. doi: 10.1016/j.cell.2011.12.004 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Venkatachalam V, Cohen AE (2014) Imaging GFP-based reporters in neurons with multiwavelength optogenetic control. Biophys J 107(7):1554–1563. doi: 10.1016/j.bpj.2014.08.020 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Helmchen F, Denk W (2005) Deep tissue two-photon microscopy. Nat Methods 2(12):932–940. doi: 10.1038/nmeth818 CrossRefPubMedGoogle Scholar
  57. 57.
    Rein ML, Deussing JM (2012) The optogenetic (r)evolution. Mol Genet Genomics 287(2):95–109. doi: 10.1007/s00438-011-0663-7 CrossRefPubMedGoogle Scholar
  58. 58.
    Steriade M (2006) Grouping of brain rhythms in corticothalamic systems. Neuroscience 137(4):1087–1106. doi: 10.1016/j.neuroscience.2005.10.029. [doi] S0306-4522(05)01153-X [pii]CrossRefPubMedGoogle Scholar
  59. 59.
    Roome CJ, Kuhn B (2014) Chronic cranial window with access port for repeated cellular manipulations, drug application, and electrophysiology. Front Cell Neurosci 8:379. doi: 10.3389/fncel.2014.00379 PubMedPubMedCentralGoogle Scholar
  60. 60.
    Yousef T, Bonhoeffer T, Kim DS, Eysel UT, Toth E, Kisvarday ZF (1999) Orientation topography of layer 4 lateral networks revealed by optical imaging in cat visual cortex (area 18). Eur J Neurosci 11(12):4291–4308CrossRefPubMedGoogle Scholar
  61. 61.
    Arieli A, Grinvald A, Slovin H (2002) Dural substitute for long-term imaging of cortical activity in behaving monkeys and its clinical implications. J Neurosci Methods 114(2):119–133CrossRefPubMedGoogle Scholar
  62. 62.
    Goldey GJ, Roumis DK, Glickfeld LL, Kerlin AM, Reid RC, Bonin V, Schafer DP, Andermann ML (2014) Removable cranial windows for long-term imaging in awake mice. Nat Protoc 9(11):2515–2538. doi: 10.1038/nprot.2014.165 CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media LLC 2018

Authors and Affiliations

  1. 1.Focus Program Translational Neurosciences and Institute for Microscopic Anatomy and NeurobiologyUniversity Medical Center of the Johannes Gutenberg University MainzMainzGermany

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