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Spatial and temporal aspects of neuronal calcium and sodium signals measured with low-affinity fluorescent indicators

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Abstract

Low-affinity fluorescent indicators for Ca2+ or Na+ allow measuring the dynamics of intracellular concentration of these ions with little perturbation from physiological conditions because they are weak buffers. When using synthetic indicators, which are small molecules with fast kinetics, it is also possible to extract spatial and temporal information on the sources of ion transients, their localization, and their disposition. This review examines these important aspects from the biophysical point of view, and how they have been recently exploited in neurophysiological studies. We first analyze the environment where Ca2+ and Na+ indicators are inserted, highlighting the interpretation of the two different signals. Then, we address the information that can be obtained by analyzing the rising phase and the falling phase of the Ca2+ and Na+ transients evoked by different stimuli, focusing on the kinetics of ionic currents and on the spatial interpretation of these measurements, especially on events in axons and dendritic spines. Finally, we suggest how Ca2+ or Na+ imaging using low-affinity synthetic fluorescent indicators can be exploited in future fundamental or applied research.

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References

  1. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, Meyer M (1997) Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci USA 94:1488–1493. https://doi.org/10.1073/pnas.94.4.1488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Ait Ouares K, Canepari M (2020) The origin of physiological local mGluR1 supralinear Ca2+ Signals in cerebellar Purkinje neurons. J Neurosci 40:1795–1809. https://doi.org/10.1523/JNEUROSCI.2406-19.2020

    Article  PubMed  PubMed Central  Google Scholar 

  3. Ait Ouares K, Filipis L, Tzilivaki A, Poirazi P, Canepari M (2019) Two distinct sets of Ca2+ and K+ channels are activated at different membrane potentials by the climbing fiber synaptic potential in Purkinje neuron dendrites. J Neurosci 39:1969–1981. https://doi.org/10.1523/JNEUROSCI.2155-18.2018

    Article  PubMed  PubMed Central  Google Scholar 

  4. Ait Ouares K, Jaafari N, Canepari M (2016) A generalised method to estimate the kinetics of fast Ca2+ currents from Ca2+ imaging experiments. J Neurosci Methods 268:66–77. https://doi.org/10.1016/j.jneumeth.2016.05.005

    Article  PubMed  CAS  Google Scholar 

  5. Ali F, Kwan AC (2020) Interpreting in vivo calcium signals from neuronal cell bodies, axons, and dendrites: a review. Neurophotonics 7:011402. https://doi.org/10.1117/1.NPh.7.1.011402

    Article  PubMed  CAS  Google Scholar 

  6. Anselmi F, Ventalon C, Bègue A, Ogden D, Emiliani V (2011) Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning. Proc Natl Acad Sci USA 108:19504–19509. https://doi.org/10.1073/pnas.1109111108

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Augustine GJ (1994) Combining patch-clamp and optical methods in brain slices. J Neurosci Methods 54:63–169. https://doi.org/10.1016/0165-0270(94)90190-2

    Article  Google Scholar 

  8. Baranauskas G, David Y, Fleidervish IA (2013) Spatial mismatch between the Na+ flux and spike initiation in axon initial segment. Proc Natl Acad Sci USA 110:4051–4056. https://doi.org/10.1073/pnas.1215125110

    Article  PubMed  PubMed Central  Google Scholar 

  9. Bardo S, Cavazzini MG (2006 Feb) Emptage N (2006) The role of the endoplasmic reticulum Ca2+ store in the plasticity of central neurons. Trends Pharmacol Sci. 27(2):78–84. https://doi.org/10.1016/j.tips.2005.12.008

    Article  PubMed  CAS  Google Scholar 

  10. Bloodgood BL, Giessel AJ, Sabatini BL (2009) Biphasic synaptic Ca influx arising from compartmentalized electrical signals in dendritic spines. PLoS Biol 7:e1000190. https://doi.org/10.1371/journal.pbio.1000190

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Bloodgood BL, Sabatini BL (2007) Nonlinear regulation of unitary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines. Neuron 53:249–260. https://doi.org/10.1016/j.neuron.2006.12.017

    Article  PubMed  CAS  Google Scholar 

  12. Canepari M, Mammano F (1999) Imaging neuronal calcium fluorescence at high spatio-temporal resolution. J Neurosci Methods 87:1–11. https://doi.org/10.1016/s0165-0270(98)00127-7

    Article  PubMed  CAS  Google Scholar 

  13. DiGregorio DA, Peskoff A, Vergara JL (1999) Measurement of action potential-induced presynaptic calcium domains at a cultured neuromuscular junction. J Neurosci 19:7846–7859. https://doi.org/10.1523/JNEUROSCI.19-18-07846.1999

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Echevarria-Cooper DM, Hawkins NA, Misra SN, Huffman AM, Thaxton T, Thompson CH, Ben-Shalom R, Nelson AD, Lipkin AM, George AL Jr, Bender KJ, Kearney JA (2022) Cellular and behavioral effects of altered NaV1.2 sodium channel ion permeability in Scn2aK1422E mice. Hum Mol Genet 31:2964–2988. https://doi.org/10.1093/hmg/ddac087

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Faas GC, Schwaller B, Vergara JL, Mody I (2007) Resolving the fast kinetics of cooperative binding: Ca2+ buffering by calretinin. PLoS Biol 5:e311. https://doi.org/10.1371/journal.pbio.0050311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Fierro L, Llano I (1996) High endogenous calcium buffering in Purkinje cells from rat cerebellar slices. J Physiol 496:617–625. https://doi.org/10.1113/jphysiol.1996.sp021713

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Filipis L, Ait Ouares K, Moreau P, Tanese D, Zampini V, Latini A, Bleau C, Bleau C, Graham J, Canepari M (2018) A novel multisite confocal system for rapid Ca2+ imaging from submicron structures in brain slices. J Biophotonics 11(3). https://doi.org/10.1002/jbio.201700197

  18. Filipis L, Blömer LA, Montnach J, De Waard M, Canepari M (2023) Nav1.2 and BK channels interaction shapes the action potential in the axon initial segment. J Physiol 601:1957–1979. https://doi.org/10.1113/JP283801

    Article  PubMed  CAS  Google Scholar 

  19. Filipis L, Canepari M (2021) Optical measurement of physiological sodium currents in the axon initial segment. J Physiol 599:49–66. https://doi.org/10.1113/JP280554

    Article  PubMed  CAS  Google Scholar 

  20. Fleidervish IA, Lasser-Ross N, Gutnick MJ, Ross WN (2010) Na+ imaging reveals little difference in action potential-evoked Na+ influx between axon and soma. Nat Neurosci 13:852–860. https://doi.org/10.1038/nn.2574

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Grienberger C, Konnerth A (2012) Imaging calcium in neurons. Neuron 73:862–885. https://doi.org/10.1016/j.neuron.2012.02.011

    Article  PubMed  CAS  Google Scholar 

  22. Grunditz A, Holbro N, Tian L, Zuo Y, Oertner TG (2008) Spine neck plasticity controls postsynaptic calcium signals through electrical compartmentalization. J Neurosci 28:13457–13466. https://doi.org/10.1523/JNEUROSCI.2702-08.2008

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Guy HR, Conti F (1990) Pursuing the structure and function of voltage-gated channels. Trends Neurosci 13:201–206. https://doi.org/10.1016/0166-2236(90)90160-c

    Article  PubMed  CAS  Google Scholar 

  24. Hanemaaijer NA, Popovic MA, Wilders X, Grasman S, Pavón Arocas O, Kole MH (2020) Ca2+ entry through NaV channels generates submillisecond axonal Ca2+ signaling. Elife 9:e54566. https://doi.org/10.7554/eLife.54566

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Helmchen F, Imoto K, Sakmann B (1996) Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. Biophys J 70:1069–1081. https://doi.org/10.1016/S0006-3495(96)79653-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Higley MJ, Sabatini BL (2008) Calcium signaling in dendrites and spines: practical and functional considerations. Neuron 59:902–913. https://doi.org/10.1016/j.neuron.2008.08.020

    Article  PubMed  CAS  Google Scholar 

  27. Hildebrand ME, Isope P, Miyazaki T, Nakaya T, Garcia E, Feltz A, Schneider T, Hescheler J, Kano M, Sakimura K, Watanabe M, Dieudonné S, Snutch TP (2009) Functional coupling between mGluR1 and Cav3.1 T-type calcium channels contributes to parallel fiber-induced fast calcium signaling within Purkinje cell dendritic spines. J Neurosci 29:9668–9682. https://doi.org/10.1523/JNEUROSCI.0362-09.2009

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179–1209. https://doi.org/10.1162/neco.1997.9.6.1179

    Article  PubMed  CAS  Google Scholar 

  29. Holbro N, Grunditz A, Wiegert JS, Oertner TG (2010) AMPA receptors gate spine Ca(2+) transients and spike-timing-dependent potentiation. Proc Natl Acad Sci USA 107:15975–15980. https://doi.org/10.1073/pnas.1004562107

    Article  PubMed  PubMed Central  Google Scholar 

  30. Hsieh LS, Levine ES (2013) Cannabinoid modulation of backpropagating action potential-induced calcium transients in layer 2/3 pyramidal neurons. Cereb Cortex 23:1731–1741. https://doi.org/10.1093/cercor/bhs168

    Article  PubMed  Google Scholar 

  31. Jaafari N, Canepari M (2016) Functional coupling of diverse voltage-gated Ca(2+) channels underlies high fidelity of fast dendritic Ca(2+) signals during burst firing. J Physiol 594:967–983. https://doi.org/10.1113/JP271830

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Jaafari N, De Waard M, Canepari M (2014) Imaging fast calcium currents beyond the limitations of electrode techniques. Biophys J 107:1280–1288. https://doi.org/10.1016/j.bpj.2014.07.059

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Jaafari N, Marret E, Canepari M (2015) Using simultaneous voltage and calcium imaging to study fast Ca2+ channels. Neurophotonics 2:021010. https://doi.org/10.1117/1.NPh.2.2.021010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Kao JP, Tsien RY (1988) Ca2+ binding kinetics of fura-2 and azo-1 from temperature-jump relaxation measurements. Biophys J 53:635–639. https://doi.org/10.1016/S0006-3495(88)83142-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Kaplan JH (2002) Biochemistry of Na,K-ATPase. Annu Rev Biochem 71:511–535. https://doi.org/10.1146/annurev.biochem.71.102201.141218

    Article  PubMed  CAS  Google Scholar 

  36. Katz E, Stoler O, Scheller A, Khrapunsky Y, Goebbels S, Kirchhoff F, Gutnick MJ, Wolf F, Fleidervish IA (2018) Role of sodium channel subtype in action potential generation by neocortical pyramidal neurons. Proc Natl Acad Sci USA 115:E7184–E7192. https://doi.org/10.1073/pnas.1720493115

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Kovalchuk Y, Eilers J, Lisman J, Konnerth A (2000) NMDA receptor-mediated subthreshold Ca(2+) signals in spines of hippocampal neurons. J Neurosci 20:1791–1799. https://doi.org/10.1523/JNEUROSCI.20-05-01791.2000

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Kushmerick MJ, Podolsky RJ (1969) Ionic mobility in muscle cells. Science 166:1297–1298. https://doi.org/10.1126/science.166.3910.1297

    Article  PubMed  CAS  Google Scholar 

  39. Lee SH, Schwaller B, Neher E (2000) Kinetics of Ca2+ binding to parvalbumin in bovine chromaffin cells: implications for [Ca2+] transients of neuronal dendrites. J Physiol 525:419–432. https://doi.org/10.1111/j.1469-7793.2000.t01-2-00419.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Lipkin AM, Cunniff MM, Spratt PWE, Lemke SM, Bender KJ (2021) Functional microstructure of CaV-mediated calcium signaling in the axon initial segment. J Neurosci 41:3764–3776. https://doi.org/10.1523/JNEUROSCI.2843-20.2021

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Looger LL, Griesbeck O (2012) Genetically encoded neural activity indicators. Curr Opin Neurobiol 22:18–23. https://doi.org/10.1016/j.conb.2011.10.024

    Article  PubMed  CAS  Google Scholar 

  42. Lorincz A, Nusser Z (2010) Molecular identity of dendritic voltage-gated sodium channels. Science 328:906–909. https://doi.org/10.1126/science.1187958

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Majewska A, Brown E, Ross J, Yuste R (2000) Mechanisms of calcium decay kinetics in hippocampal spines: role of spine calcium pumps and calcium diffusion through the spine neck in biochemical compartmentalization. J Neurosci 20:1722–1734. https://doi.org/10.1523/JNEUROSCI.20-05-01722.2000

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Mata AM, Sepúlveda MR (2005) Calcium pumps in the central nervous system. Brain Res Brain Res Rev 49:398–405. https://doi.org/10.1016/j.brainresrev.2004.11.004

    Article  PubMed  CAS  Google Scholar 

  45. Matthews EA, Dietrich D (2015) Buffer mobility and the regulation of neuronal calcium domains. Front Cell Neurosci 9:48. https://doi.org/10.3389/fncel.2015.00048

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Minta A, Tsien RY (1989) Fluorescent indicators for cytosolic sodium. J Biol Chem 264:19449–19457

    Article  PubMed  CAS  Google Scholar 

  47. Miyakawa H, Lev-Ram V, Lasser-Ross N, Ross WN (1992) Calcium transients evoked by climbing fiber and parallel fiber synaptic inputs in guinea pig cerebellar Purkinje neurons. J Neurophysiol 68:1178–11789. https://doi.org/10.1152/jn.1992.68.4.1178

    Article  PubMed  CAS  Google Scholar 

  48. Miyazaki K, Lisman JE, Ross W (2019) Improvements in simultaneous sodium and calcium imaging. Front Cell Neurosci 12:514. https://doi.org/10.3389/fncel.2018.00514

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Miyazaki K, Ross WN (2015) Simultaneous sodium and calcium imaging from dendrites and axons. eNeuro 2:ENEURO.0092-15.2015. https://doi.org/10.1523/ENEURO.0092-15.2015

    Article  PubMed  PubMed Central  Google Scholar 

  50. Miyazaki K, Ross WN (2017) Sodium dynamics in pyramidal neuron dendritic spines: synaptically evoked entry predominantly through AMPA receptors and removal by diffusion. J Neurosci 37:9964–9976. https://doi.org/10.1523/JNEUROSCI.1758-17.2017

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Miyazaki K, Ross WN (2022) Fast synaptically activated calcium and sodium kinetics in hippocampal pyramidal neuron dendritic spines. eNeuro 9:ENEURO.0396-22.2022. https://doi.org/10.1523/ENEURO.0396-22.2022

    Article  PubMed  PubMed Central  Google Scholar 

  52. Mondragão MA, Schmidt H, Kleinhans C, Langer J, Kafitz KW, Rose CR (2016) Extrusion versus diffusion: mechanisms for recovery from sodium loads in mouse CA1 pyramidal neurons. J Physiol 594:5507–5527. https://doi.org/10.1113/JP272431

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Murphy JG, Gutzmann JJ, Lin L, Hu J, Petralia RS, Wang YX, Hoffman DA (2022) R-type voltage-gated Ca2+ channels mediate A-type K+ current regulation of synaptic input in hippocampal dendrites. Cell Rep 38:110264. https://doi.org/10.1016/j.celrep.2021.110264

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Nägerl UV, Novo D, Mody I, Vergara JL (2000) Binding kinetics of calbindin-D(28k) determined by flash photolysis of caged Ca(2+). Biophys J 79:3009–3018. https://doi.org/10.1016/S0006-3495(00)76537-4

    Article  PubMed  PubMed Central  Google Scholar 

  55. Nevian T, Sakmann B (2006) Spine Ca2+ signaling in spike-timing-dependent plasticity. J Neurosci 26:11001–11013. https://doi.org/10.1523/JNEUROSCI.1749-06.2006

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Noguchi J, Matsuzaki M, Ellis-Davies GC, Kasai H (2005) Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 46:609–622. https://doi.org/10.1016/j.neuron.2005.03.015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Ogden D, Khodakhah K, Carter T, Thomas M, Capiod T (1995) Analogue computation of transient changes of intracellular free Ca2+ concentration with the low affinity Ca2+ indicator furaptra during whole-cell patch-clamp recording. Pflugers Arch 429:587–591. https://doi.org/10.1007/BF00704165

    Article  PubMed  CAS  Google Scholar 

  58. Pankratov Y, Lalo U (2014) Calcium permeability of ligand-gated Ca2+ channels. Eur J Pharmacol 739:60–73. https://doi.org/10.1016/j.ejphar.2013.11.017

    Article  PubMed  CAS  Google Scholar 

  59. Paredes RM, Etzler JC, Watts LT, Zheng W, Lechleiter JD (2008) Chemical calcium indicators. Methods 46:143–151. https://doi.org/10.1016/j.ymeth.2008.09.025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Ramirez JE, Stell BM (2016) Calcium imaging reveals coordinated simple spike pauses in populations of cerebellar Purkinje cells. Cell Rep 17:3125–3132. https://doi.org/10.1016/j.celrep.2016.11.075

    Article  PubMed  CAS  Google Scholar 

  61. Roder P, Hille C (2014) ANG-2 for quantitative Na+ determination in living cells by time-resolved fluorescence microscopy. Photochem Photobiol Sci 13:1699–1710. https://doi.org/10.1039/c4pp00061g

    Article  PubMed  CAS  Google Scholar 

  62. Rose CR, Konnerth A (2001) NMDA receptor-mediated Na+ signals in spines and dendrites. J Neurosci 21:4207–4214. https://doi.org/10.1523/JNEUROSCI.21-12-04207.2001

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Rose CR, Kovalchuk Y, Eilers J, Konnerth A (1999) Two-photon Na+ imaging in spines and fine dendrites of central neurons. Pflugers Arch 439:201–207. https://doi.org/10.1007/s004249900123

    Article  PubMed  CAS  Google Scholar 

  64. Ross WN, Miyazaki K, Popovic MA, Zecevic D (2015) Imaging with organic indicators and high-speed charge-coupled device cameras in neurons: some applications where these classic techniques have advantages. Neurophotonics 2:021005. https://doi.org/10.1117/1.NPh.2.2.021005

    Article  PubMed  Google Scholar 

  65. Rossi B, Ogden D, Llano I, Tan YP, Marty A, Collin T (2012) Current and calcium responses to local activation of axonal NMDA receptors in developing cerebellar molecular layer interneurons. PLoS One 7:e39983. https://doi.org/10.1371/journal.pone.0039983

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Sabatini BL, Maravall M, Svoboda K (2001) Ca(2+) signaling in dendritic spines. Curr Opin Neurobiol 11:349–356. https://doi.org/10.1016/s0959-4388(00)00218-x

    Article  PubMed  CAS  Google Scholar 

  67. Sabatini BL, Oertner TG, Svoboda K (2002) The life cycle of Ca2+ ions in dendritic spines. Neuron 33:439–452. https://doi.org/10.1016/s0896-6273(02)00573-1

    Article  PubMed  CAS  Google Scholar 

  68. Sabatini BL, Regehr WG (1998) Optical measurement of presynaptic calcium currents. Biophys J 74:1549–1563. https://doi.org/10.1016/S0006-3495(98)77867-1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Sabatini BL, Svoboda K (2000) Analysis of calcium channels in single spines using optical fluctuation analysis. Nature 408:589–593. https://doi.org/10.1038/35046076

    Article  PubMed  CAS  Google Scholar 

  70. Sakmann B, Neher E (1984) Patch clamp techniques for studying ionic channels in excitable membranes. Annu Rev Physiol 46:455–472. https://doi.org/10.1146/annurev.ph.46.030184.002323

    Article  PubMed  CAS  Google Scholar 

  71. Scheuss V, Yasuda R, Sobczyk A, Svoboda K (2006) Nonlinear [Ca2+] signaling in dendrites and spines caused by activity-dependent depression of Ca2+ extrusion. J Neurosci 26:8183–8194. https://doi.org/10.1523/JNEUROSCI.1962-06.2006

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Schmidt H, Stiefel KM, Racay P, Schwaller B, Eilers J (2003) Mutational analysis of dendritic Ca2+ kinetics in rodent Purkinje cells: role of parvalbumin and calbindin D28k. J Physiol 551:13–32. https://doi.org/10.1113/jphysiol.2002.035824

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Shvartsman A, Kotler O, Stoler O, Khrapunsky Y, Melamed I, Fleidervish IA (2021) Subcellular distribution of persistent sodium conductance in cortical pyramidal neurons. J Neurosci 41:6190–6201. https://doi.org/10.1523/JNEUROSCI.2989-20.2021

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Sobczyk A, Scheuss V, Svoboda K (2005) NMDA receptor subunit-dependent [Ca2+] signaling in individual hippocampal dendritic spines. J Neurosci 25:6037–6046. https://doi.org/10.1523/JNEUROSCI.1221-05.2005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Strobel C, Sullivan RKP, Stratton P, Sah P (2017) Calcium signalling in medial intercalated cell dendrites and spines. J Physiol 595:5653–5669. https://doi.org/10.1113/JP274261

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Stuart GJ, Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69–72. https://doi.org/10.1038/367069a0

    Article  PubMed  CAS  Google Scholar 

  77. Vennekens R, Menigoz A, Nilius B (2012) TRPs in the brain. Rev Physiol Biochem Pharmacol 163:27–64. https://doi.org/10.1007/112_2012_8

    Article  PubMed  Google Scholar 

  78. Yu FH, Catterall WA (2004) The VGL-chanome: a protein superfamily specialized for electrical signaling and ionic homeostasis. Sci STKE 2004(253):re15. https://doi.org/10.1126/stke.2532004re15

    Article  PubMed  Google Scholar 

  79. Yuste R, Majewska A, Cash SS, Denk W (1999) Mechanisms of calcium influx into hippocampal spines: heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J Neurosci 19:1976–1987. https://doi.org/10.1523/JNEUROSCI.19-06-01976.1999

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Zhang Y, Looger LL (2023) Fast and sensitive GCaMP calcium indicators for neuronal imaging. J Physiol. https://doi.org/10.1113/JP283832

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Funding

This work was supported for MC by the Agence Nationale de la Recherche through the Labex Ion Channels Science and Therapeutics (program number ANR-11-LABX-0015) and for WNR by the National Institute of Health (grant R01NS099122) and by the US-Israel Binational Science Foundation (Grant No.: 2017163).

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  1. LIPhy, CNRS, Univ. Grenoble Alpes, F-38000, Grenoble, France

    Marco Canepari

  2. Laboratories of Excellence, Ion Channel Science and Therapeutics, Valbonne, France

    Marco Canepari

  3. Institut National de la Santé et Recherche Médicale, Paris, France

    Marco Canepari

  4. Department of Physiology, New York Medical College, Valhalla, NY, 10595, USA

    William N. Ross

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Canepari, M., Ross, W.N. Spatial and temporal aspects of neuronal calcium and sodium signals measured with low-affinity fluorescent indicators. Pflugers Arch - Eur J Physiol 476, 39–48 (2024). https://doi.org/10.1007/s00424-023-02865-1

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