Skip to main content
SpringerLink
Log in

Holographic Functional Calcium Imaging of Neuronal Circuit Activity

  • Chapter
  • First Online:
Advanced Optical Methods for Brain Imaging

Part of the book series: Progress in Optical Science and Photonics ((POSP,volume 5))

Abstract

Functional imaging provides efficient optical recording of Ca2+ activity from single neurons as well as networks of neurons forming a circuit. Sufficient spatial resolution needs to be achieved in order to resolve cell bodies as well as fine neuronal structures such as dendrites and spines. On the other hand, the temporal resolution should be sufficient to capture Ca2+ events from multiple sites across the sample. Here, we briefly describe various imaging modalities and focus on two-photon holographic multi-foci excitation to perform multi-site Ca2+ imaging. Holographically projected multi-foci can be used to excite two-photon fluorescence from multiple sites along the dendritic tree of a single neuron or multiple cell bodies in a neuronal network. By simultaneously projecting multiple foci onto the sample, the fluorescence emanating from the different foci can be collected simultaneously using a camera, thereby setting the temporal resolution to the frame-rate of the camera. We describe the generation of appropriate holograms as well as discuss the limitations of the approach. We also discuss a solution to improve the signal-to-noise ratio via the application of temporal gating. The multi-foci holographic technique is a promising approach to perform high-speed optical recording of neuronal activity.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. D.E. Clapham, Calcium signaling. Cell 131, 1047–1058 (2007)

    Article  Google Scholar 

  2. C. Grienberger, A. Konnerth, Imaging calcium in neurons. Neuron 73, 862–885 (2012)

    Article  Google Scholar 

  3. M.J. Higley, B.L. Sabatini, Calcium signaling in dendrites and spines: practical and functional considerations. Neuron 59, 902–913 (2008)

    Article  Google Scholar 

  4. W.A. Catterall, Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Dev. Biol. 16, 521–555 (2000)

    Article  Google Scholar 

  5. B. Hille, Ion Channels of Excitable Membranes, 3rd edn. (Sunderland, MA, Sinauer Associates, 2001)

    Google Scholar 

  6. H. Miyakawa, W.N. Ross, D. Jaffe, J.C. Callaway, N. Lasser-Ross, J.E. Lisman, D. Johnston, Synaptically activated increases in Ca2+ concentration in hippocampal CA1 pyramidal cells are primarily due to voltage gated Ca2+ channels. Neuron 9, 1163–1173 (1992)

    Article  Google Scholar 

  7. H. Markram, B. Sakmann, Calcium transients in dendrites of neocortical neurons evoked by single sub-threshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. Proc. Natl. Acad. Sci. U.S.A. 91, 5207–5211 (1994)

    Article  Google Scholar 

  8. B.R. Christie, L.S. Eliot, K. Ito, H. Miyakawa, D. Johnston, Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx. J. Neurophysiol. 73, 2553–2557 (1995)

    Article  Google Scholar 

  9. E. Carafoli, Calcium pump of the plasma membrane. Physiol. Rev. 71, 129–153 (1991)

    Article  Google Scholar 

  10. M.J. Berridge, P. Lipp, M.D. Bootman, The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11–21 (2000)

    Article  Google Scholar 

  11. A.J. Verkhratsky, O.H. Petersen, Neuronal calcium stores. Cell Calcium 24, 333–343 (1998)

    Article  Google Scholar 

  12. S. Smith, G. Augustine, Calcium ions, active zones and synaptic transmitter release. Trends Neurosci. 11, 458–464 (1988)

    Article  Google Scholar 

  13. D.W. Tank, M. Sugimori, J.A. Connor, R.R. Llinas, Spatially resolved calcium dynamics of mammalian Purkinje cells in cerebellar slice. Science 242, 773–778 (1988)

    Article  Google Scholar 

  14. R. Yuste, L.C. Katz, Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6, 333–344 (1991)

    Article  Google Scholar 

  15. R. Yuste, M.J. Gutnick, D. Saar, K.R. Delaney, D.W. Tank, Ca2+ accumulations in dendrites of neocortical pyramidal neurons: an apical band. Neuron 13, 23–43 (1994)

    Article  Google Scholar 

  16. M.E. Larkum, K.M.M. Kaiser, B. Sakmann, Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of backpropagating action potentials. Proc. Natl. Acad. Sci. U.S.A. 96, 14600–14604 (1999)

    Article  Google Scholar 

  17. M. Cameron, O. Kékesi, J.W. Morley, J. Tapson, P.P. Breen, A. van Schaik, Y. Buskila, Calcium imaging of AM dyes following prolonged incubation in acute neuronal tissue. PLOS One 11, 0155468 (2016)

    Article  Google Scholar 

  18. O.L. Barreto-Chang, R.E. Dolmetsch, Calcium imaging of cortical neurons using Fura-2 AM. J. Vis. Exp. 23, 3–5 (2009)

    Google Scholar 

  19. J. Nakai, M. Ohkura, K. Imoto, A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nat. Biotech. 19, 137–141 (2001)

    Article  Google Scholar 

  20. T. Nagai, A. Sawano, E.S. Park, A. Miyawaki, Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proc. Natl. Acad. Sci. U.S.A. 98, 3197–3202 (2001)

    Article  Google Scholar 

  21. M.T. Hasan, R.W. Friedrich, T. Euler, M.E. Larkum, G. Giese, M. Both, J. Duebel, J. Waters, H. Bujard, O. Griesback, R.Y. Tsien, T. Nagai, A. Miyawaki, W. Denk, Functional fluorescent Ca2+ indicator proteins in transgenic mice under TET control. PLoS Biol. 2, 763–775 (2004)

    Article  Google Scholar 

  22. N. Heim, O. Garaschuk, M.W. Friedrich, M. Mank, R.I. Milos, Y. Kovalchuk, A. Konnerth, O. Griesbeck, Improved calcium imaging in transgenic mice expressing a troponin C-based biosensor. Nat. Methods 4, 127–129 (2007)

    Article  Google Scholar 

  23. L. Tian, S.A. Hires, T. Mao, D. Huber, S.H. Chiappe, S.H. Chalasani, L. Petreanu, J. Akerboom, S.A. McKinney, E.R. Schreiter, C.I. Bargmann, V. Jayaraman, K. Svoboda, L.L. Looger, Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6, 875–881 (2009)

    Article  Google Scholar 

  24. J. Ackerboom et al., Optimization of a GCaMP Calcium indicator for neural activity imaging. J. Neurosci. 32, 13819–13840 (2012)

    Article  Google Scholar 

  25. L.M. Palmer, A.S. Shai, J.E. Reeve, H.L. Anderson, O. Paulsen, M.E. Larkum, NMDA spikes enhance action potential generation during sensory input. Nat. Neurosci. 17(3), 383–390 (2014)

    Article  Google Scholar 

  26. N. Xu, M.T. Harnett, S.R. Williams, D. Huber, D.H. O’Connor, K. Svoboda, J.C. Magee, Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 492(7428), 247–251 (2012)

    Article  Google Scholar 

  27. J.G. Borst, F. Helmchen, B. Sakmann, Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J. Physiol. 489(3), 825–840 (1995)

    Article  Google Scholar 

  28. F. Helmchen, K. Imoto, B. Sakmann, Ca2 + buffering and action potential-evoked Ca2 + signaling in dendrites of pyramidal neurons. Biophys. J. 70(2), 1069–1081 (1996)

    Article  Google Scholar 

  29. F. Helmchen, J.G. Borst, B. Sakmann, Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys. J. 72(3), 1458–1471 (1997)

    Article  Google Scholar 

  30. J.A. Connor, Digital imaging of free calcium changes and of spatial gradients in growing processes in single, mammalian central nervous system cells. Proc. Natl. Acad. Sci. U.S.A. 83, 6179–6183 (1986)

    Article  Google Scholar 

  31. N. Lasser-Ross, H. Miyakawa, V. Lev-Ram, S.R. Young, W.N. Ross, High time resolution fluorescence imaging with a CCD camera. J. Neurosci. Methods 36, 253–261 (1991)

    Article  Google Scholar 

  32. D.A. Williams, F.S. Fay, Intracellular calibration of the fluorescent calcium indicator Fura-2. Cell Calcium 11, 75–83 (1990)

    Article  Google Scholar 

  33. J. Eilers, G. Callewaert, C. Armstrong, A. Konnerth, Calcium signaling in a narrow somatic submembrane shell during synaptic activity in cerebellar Purkinje neurons. Proc. Natl. Acad. Sci. U S A 92, 10272–10276 (1995)

    Article  Google Scholar 

  34. A.H. Voie, D.H. Burns, F.A. Spelman, Orthogonal-plane fluorescence optical sectioning: three-dimensional imaging of macroscopic biological speciments. J. Microsc. 170, 229–336 (1993)

    Article  Google Scholar 

  35. J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, E.H. Stelzer, Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305, 1007–1009 (2004)

    Article  Google Scholar 

  36. J. Huisken, D.Y.R. Stainier, Selective plane illumination microscopy techniques in developmental biology. Development 136, 1963–1975 (2009)

    Article  Google Scholar 

  37. M. Ahrens, M. Orger, D.N. Robson, J.M. Li, P.J. Keller, Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 10, 413–420 (2013)

    Article  Google Scholar 

  38. S. Wolf, W. Supatto, G. Debregeas, P. Mahou, S.G. Kruglik, J. Sintes, E. Beaurepaire, R. Candelier, Whole-brain functional imaging with two-photon light-sheet microscopy. Nat. Methods 12, 379–380 (2015)

    Article  Google Scholar 

  39. W. Denk, D.W. Piston, W. Web, Two-photon laser scanning fluorescence microscopy. Science 248, 73 (1990)

    Article  Google Scholar 

  40. N.G. Horton, K. Wang, D. Kobat, C.G. Clark, F.W. Wise, C.B. Schaffer, C. Xu, In vivo three-photon microscopy of subcortical structures within an intact mouse brain. Nat. Photonics 7, 205–209 (2013)

    Article  Google Scholar 

  41. K. Svoboda, W. Denk, D. Kleinfeld, D. Tank, In-vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385, 161 (1997)

    Article  Google Scholar 

  42. F. Helmchen, K. Svoboda, W. Denk, D.W. Tank, In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat. Neurosci. 2, 989–996 (1999)

    Article  Google Scholar 

  43. F. Helmchen, W. Denk, Deep tissue two-photon microscopy. Nat. Methods 2, 932–940 (2005)

    Article  Google Scholar 

  44. P. Saggau, A. Bullen, S.S. Patel, Acousto-optic random-access laser scanning microscopy: fundamentals and applications to optical recording of neuronal activity. Cell. Mol. Biol. 44, 827–846 (1998)

    Google Scholar 

  45. G.D. Reddy, K. Kelleher, R. Fink, P. Saggau, Three-dimensional random access multi-photon microscopy for functional imaging of neuronal activity. Nat. Neurosci. 11, p713 (2008)

    Article  Google Scholar 

  46. G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E.S. Vizi, B. Roska, B. Rózsa, Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes. Nat. Methods 9, 201–208 (2012)

    Article  Google Scholar 

  47. P. Dufour, M. Piché, Y. De Koninck, N. McCarthy, Two-photon excitation fluorescence microscopy with a high depth of field using an axicon. Appl. Opt. 45, 9246–9252 (2006)

    Article  Google Scholar 

  48. G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, Y. De Koninck, Extended two-photon microscopy in live samples with Bessel beams: steadier focus, faster volume scans, and simpler stereoscopic imaging. Front. Cell Neurosci. 8, 139 (2014)

    Google Scholar 

  49. A. Song, A. Charles, S.A. Koay, J.L. Gauthier, S.Y. Thiberge, J.W. Pillow, D.W. Tank, Volumetric two-photon imaging of neurons using stereoscopy (vTwINS). Nat. Methods 14, 420–426 (2017)

    Article  Google Scholar 

  50. V. Nikolenko, B. Watson, R. Araya, A. Woodruff, D. Peterka, R. Yuste, SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators. Front Neural Circuits 2, 5 (2008)

    Article  Google Scholar 

  51. V.R. Daria, C. Stricker, R. Bowman, S. Redman, H.A. Bachor, Arbitrary multisite two-photon excitation in four dimensions. Appl. Phys. Lett. 95 (2009)

    Article  Google Scholar 

  52. M. Dal Maschio, F. Difato, R. Beltramo, A. Blau, F. Benfenati, T. Fellin, Simultaneous two-photon imaging and photo-stimulation with structured light illumination. Opt. Express 18, 18720–18731 (2010)

    Article  Google Scholar 

  53. S. Bovetti, C. Moretti, S. Zucca, M. Dal Maschio, P. Bonifazi, T. Fellin, Simultaneous high-speed imaging and optogenetic inhibition in the intact mouse brain. Sci. Rep. 7 (2017)

    Article  Google Scholar 

  54. M. Ducros, Y.G. Houssen, J. Bradley, V. de Sars, S. Charpak, Encoded multisite two-photon microscopy. Proc. Natl. Acad. Sci. U.S.A. 110, 13138–13143 (2013)

    Article  Google Scholar 

  55. J. Liesener, M. Reicherter, T. Haist, H.J. Tiziani, Multi-functional optical tweezers using computer-generated holograms. Opt. Commun. 185, 77–82 (2000)

    Article  Google Scholar 

  56. D. Palima, V.R. Daria, Effect of spurious diffraction orders in arbitrary multi-foci patterns produced via phase-only holograms. Appl. Opt. 45, 6689–6693 (2006)

    Article  Google Scholar 

  57. J. Goodman, Introduction to Fourier Optics, 3rd edn. (Roberts & Company, US, 2005)

    Google Scholar 

  58. J. Curtis, C. Schmitz, J. Spatz, Symmetry dependence of holograms for optical trapping. Opt. Lett. 30, 2086–2088 (2005)

    Article  Google Scholar 

  59. C. Xu, W.W. Webb, Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm. J. Opt. Soc. Am. B 13, 481–491 (1996)

    Article  Google Scholar 

  60. N. Spruston, Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 9, 206–221 (2008)

    Article  Google Scholar 

  61. G.J. Stuart, N. Spruston, Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J. Neurosci. 18, 3501–3510 (1998)

    Article  Google Scholar 

  62. B.W. Mel, Synaptic integration in an excitable dendritic tree. J. Neurophysiol. 70, 1086–1101 (1993)

    Article  Google Scholar 

  63. M. Larkum, T. Nevian, M. Sandler, A. Polsky, J. Schiller, Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 325, 756–760 (2009)

    Article  Google Scholar 

  64. S.D. Antic, W.L. Zhou, A.R. Moore, S.M. Short, K.D. Ikonomu, The decade of the dendritic NMDA spike. J. Neurosci. Res. 88, 2991–3001 (2010)

    Article  Google Scholar 

  65. G.J. Stuart, N. Spruston, Dendritic integration: 60 years of progress. Nat. Neurosci. 18(12), 1713–1721 (2015)

    Article  Google Scholar 

  66. M.A. Go, C. Stricker, S. Redman, H.A. Bachor, V.R. Daria, Three-dimensional two-photon multi-site photostimulation. J. Biophotonics 5, 745–753 (2012)

    Article  Google Scholar 

  67. M.A. Go, M.S. To, C. Stricker, S. Redman, H.A. Bachor, G.J. Stuart, V.R. Daria, Four-dimensional multi-site photolysis of caged neurotransmitters. Front Cell Neurosci. 7, 231 (2013)

    Article  Google Scholar 

  68. G.J. Stuart, B. Sakmann, Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367, 69–72 (1994)

    Article  Google Scholar 

  69. M.E. Larkum, K.M.M. Kaiser, B. Sakmann, Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. Proc. Natl. Acad. Sci. U.S.A. 96, 14600–14604 (1999)

    Article  Google Scholar 

  70. J. Schiller, Y. Schiller, G. Stuart, B. Sakmann. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. 505, 605–616 (1997)

    Article  Google Scholar 

  71. M.L. Castanares, V. Gautam, J. Drury, H. Bachor, V.R. Daria, Efficient multi-site two-photon functional imaging of neuronal circuits. Biomed. Opt. Express 7, 5325–5334 (2016)

    Article  Google Scholar 

  72. V. Gautam, S. Naureen, N. Shahid, Q. Gao, Y. Wang, D. Nisbet, C. Jagadish, V.R. Daria, Engineering highly interconnected neuronal networks on nanowire scaffolds. Nanoletters 17, 3369–3375 (2017)

    Article  Google Scholar 

  73. L.M. Palmer, A.S. Shai, J.E. Reeve, H.L. Anderson, O. Paulsen, M.E. Larkum, NMDA spikes enhance action potential generation during sensory input. Nat. Neurosci. 17, 383–390 (2014)

    Article  Google Scholar 

  74. S.D. Antic, Action potentials in basal and oblique dendrites of rat neocortical pyramidal neurons. J. Physiol. 550, 35–50 (2003)

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Australian Research Council Discovery Project (DP140101555) and the National Health and Medical Research Council (PG1105944). The authors also like to thank Dr. Vini Gautam for the hippocampal cultures and Prof. Hans-A Bachor for the relevant discussions.

Author information

Authors and Affiliations

  1. John Curtin School of Medical Research, The Australian National University, Canberra, 0200 ACT, Australia

    Michael Castanares, Greg J. Stuart & Vincent Daria

Authors
  1. Michael Castanares
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Greg J. Stuart
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vincent Daria
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vincent Daria .

Editor information

Editors and Affiliations

  1. Institute of Biophotonics, National Yang-Ming University, Taipei, Taiwan

    Fu-Jen Kao

  2. Department of Electrical and Computer Engineering, Boston University, Boston, Massachusetts, USA

    Gerd Keiser

  3. Institute of Biophotonics, National Yang-Ming University, Taipei, Taiwan

    Ankur Gogoi

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Castanares, M., Stuart, G.J., Daria, V. (2019). Holographic Functional Calcium Imaging of Neuronal Circuit Activity. In: Kao, FJ., Keiser, G., Gogoi, A. (eds) Advanced Optical Methods for Brain Imaging. Progress in Optical Science and Photonics, vol 5. Springer, Singapore. https://doi.org/10.1007/978-981-10-9020-2_8

Download citation

  • DOI: https://doi.org/10.1007/978-981-10-9020-2_8

  • Published:

  • Publisher Name: Springer, Singapore

  • Print ISBN: 978-981-10-9019-6

  • Online ISBN: 978-981-10-9020-2

  • eBook Packages: EngineeringEngineering (R0)

Publish with us

Policies and ethics

Search

Navigation