A visualization pipeline for <i>in vivo</i> two-photon volumetric astrocytic calcium imaging

Qian Sun; Yusi Hu; Saiyue Deng; Yanyu Xiong; Zhili Huang

doi:10.7555/JBR.36.20220099

Volume 36 Issue 5

Sep. 2022

Turn off MathJax

Article Contents

Article Navigation > The Journal of Biomedical Research > 2022 > 36(5): 358-367

Qian Sun, Yusi Hu, Saiyue Deng, Yanyu Xiong, Zhili Huang. A visualization pipeline for in vivo two-photon volumetric astrocytic calcium imaging[J]. The Journal of Biomedical Research, 2022, 36(5): 358-367. doi: 10.7555/JBR.36.20220099

Citation:

Qian Sun, Yusi Hu, Saiyue Deng, Yanyu Xiong, Zhili Huang. A visualization pipeline for in vivo two-photon volumetric astrocytic calcium imaging[J]. The Journal of Biomedical Research, 2022, 36(5): 358-367. doi: 10.7555/JBR.36.20220099

Citation:

PDF( 15708 KB)

A visualization pipeline for in vivo two-photon volumetric astrocytic calcium imaging

doi: 10.7555/JBR.36.20220099

Qian Sun^{1, △},
Yusi Hu^{1, 2, △},
Saiyue Deng³,
Yanyu Xiong^{1, 2},
Zhili Huang^{1, 2
,
,}

1.
Department of Pharmacology, School of Basic Medical Science, Fudan University, Shanghai 200032, China
2.
State Key Laboratory of Medical Neurobiology, Institutes of Brain Science and Collaborative Innovation Center for Brain Science, Fudan University, Shanghai 200032, China
3.
Department of Neurology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430030, China

Funds: This study was supported in part by Shanghai Committee of Science and Technology (Grant No. 20ZR1403500) and the Shanghai Medical Research Council. The cartoon image was obtained from Scidraw.io.

More Information

Corresponding author: Zhili Huang, Department of Pharmacology, School of Basic Medical Science, Fudan University, 130 Dong'an Road, Shanghai 200032, China. Tel/Fax: +86-21-54237043/+86-21-54237103, E-mail: huangzl@fudan.edu.cn
Received: 2022-05-01
Revised: 2022-06-19
Accepted: 2022-07-11

Published: 2022-08-10

Issue Date: 2022-09-28

Abstract

Abstract

Astrocytes, the multi-functional glial cells with the most abundant population in the brain, integrate information across their territories to regulate neuronal synaptic and cerebrovascular activities. Astrocytic calcium (Ca²⁺) signaling is the major readout of cellular functional state of astrocytes. The conventional two-photon in vivo imaging usually focuses on a single horizontal focal plane to capture the astrocytic Ca²⁺ signals, which leaves >80% spatial information undetected. To fully probe the Ca²⁺ activity across the whole astrocytic territory, we developed a pipeline for imaging and visualizing volumetric astrocytic Ca²⁺ time-lapse images. With the pipeline, we discovered a new signal distribution pattern from three-dimensional (3D) astrocytic Ca²⁺ imaging data of mice under isoflurane anesthetic states. The tools developed in this study enable a better understanding of the spatiotemporal patterns of astrocytic activity in 3D space.
- astrocyte,
- calcium imaging,
- three-dimensional visualization

CLC number: R338.2, Document code: A
The authors reported no conflict of interests.
^△These authors contributed equally to this work.

FullText(HTML)

References(40)

References

[1]	Zhou B, Zuo Y, Jiang R. Astrocyte morphology: diversity, plasticity, and role in neurological diseases[J]. CNS Neurosci Ther, 2019, 25(6): 665–673. doi: 10.1111/cns.13123
[2]	Araque A, Carmignoto G, Haydon PG, et al. Gliotransmitters travel in time and space[J]. Neuron, 2014, 81(4): 728–739. doi: 10.1016/j.neuron.2014.02.007
[3]	Chung WS, Allen NJ, Eroglu C. Astrocytes control synapse formation, function, and elimination[J]. Cold Spring Harb Perspect Biol, 2015, 7(9): a020370. doi: 10.1101/cshperspect.a020370
[4]	Perea G, Navarrete M, Araque A. Tripartite synapses: astrocytes process and control synaptic information[J]. Trends Neurosci, 2009, 32(8): 421–431. doi: 10.1016/j.tins.2009.05.001
[5]	Tran CHT, Peringod G, Gordon GR. Astrocytes integrate behavioral state and vascular signals during functional hyperemia[J]. Neuron, 2018, 100(5): 1133–1148.e3. doi: 10.1016/j.neuron.2018.09.045
[6]	Otsu Y, Couchman K, Lyons DG, et al. Calcium dynamics in astrocyte processes during neurovascular coupling[J]. Nat Neurosci, 2015, 18(2): 210–218. doi: 10.1038/nn.3906
[7]	Institoris Á, Rosenegger DG, Gordon GR. Arteriole dilation to synaptic activation that is sub-threshold to astrocyte endfoot Ca²⁺ transients[J]. J Cereb Blood Flow Metab, 2015, 35(9): 1411–1415. doi: 10.1038/jcbfm.2015.141
[8]	Di Castro MA, Chuquet J, Liaudet N, et al. Local Ca²⁺ detection and modulation of synaptic release by astrocytes[J]. Nat Neurosci, 2011, 14(10): 1276–1284. doi: 10.1038/nn.2929
[9]	Perea G, Araque A. Astrocytes potentiate transmitter release at single hippocampal synapses[J]. Science, 2007, 317(5841): 1083–1086. doi: 10.1126/science.1144640
[10]	Bazargani N, Attwell D. Astrocyte calcium signaling: the third wave[J]. Nat Neurosci, 2016, 19(2): 182–189. doi: 10.1038/nn.4201
[11]	Buskila Y, Bellot-Saez A, Morley JW. Generating brain waves, the power of astrocytes[J]. Front Neurosci, 2019, 13: 1125. doi: 10.3389/fnins.2019.01125
[12]	Ding F, O'Donnell J, Thrane AS, et al. α₁-Adrenergic receptors mediate coordinated Ca²⁺ signaling of cortical astrocytes in awake, behaving mice[J]. Cell Calcium, 2013, 54(6): 387–394. doi: 10.1016/j.ceca.2013.09.001
[13]	Poskanzer KE, Yuste R. Astrocytic regulation of cortical UP states[J]. Proc Natl Acad Sci U S A, 2011, 108(45): 18453–18458. doi: 10.1073/pnas.1112378108
[14]	Volterra A, Liaudet N, Savtchouk I. Astrocyte Ca²⁺ signalling: an unexpected complexity[J]. Nat Rev Neurosci, 2014, 15(5): 327–335. doi: 10.1038/nrn3725
[15]	Shigetomi E, Bushong EA, Haustein MD, et al. Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses[J]. J Gen Physiol, 2013, 141(5): 633–647. doi: 10.1085/jgp.201210949
[16]	Ujita S, Sasaki T, Asada A, et al. cAMP-dependent calcium oscillations of astrocytes: an implication for pathology[J]. Cereb Cortex, 2017, 27(2): 1602–1614. doi: 10.1093/cercor/bhv310
[17]	Nimmerjahn A, Bergles DE. Large-scale recording of astrocyte activity[J]. Curr Opin Neurobiol, 2015, 32: 95–106. doi: 10.1016/j.conb.2015.01.015
[18]	Pacholko AG, Wotton CA, Bekar LK. Astrocytes-the ultimate effectors of long-range neuromodulatory networks?[J]. Front Cell Neurosci, 2020, 14: 581075. doi: 10.3389/fncel.2020.581075
[19]	Kiyoshi CM, Du Y, Zhong S, et al. Syncytial isopotentiality: a system-wide electrical feature of astrocytic networks in the brain[J]. GLIA, 2018, 66(12): 2756–2769. doi: 10.1002/glia.23525
[20]	Rusakov DA. Disentangling calcium-driven astrocyte physiology[J]. Nat Rev Neurosci, 2015, 16(4): 226–233. doi: 10.1038/nrn3878
[21]	Ingiosi AM, Hayworth CR, Harvey DO, et al. A role for astroglial calcium in mammalian sleep and sleep regulation[J]. Curr Biol, 2020, 30(22): 4373–4383.e7. doi: 10.1016/j.cub.2020.08.052
[22]	Bojarskaite L, Bjørnstad DM, Pettersen KH, et al. Astrocytic Ca²⁺ signaling is reduced during sleep and is involved in the regulation of slow wave sleep[J]. Nat Commun, 2020, 11(1): 3240. doi: 10.1038/s41467-020-17062-2
[23]	Thrane AS, Rangroo Thrane V, Zeppenfeld D, et al. General anesthesia selectively disrupts astrocyte calcium signaling in the awake mouse cortex[J]. Proc Natl Acad Sci U S A, 2012, 109(46): 18974–18979. doi: 10.1073/pnas.1209448109
[24]	Bindocci E, Savtchouk I, Liaudet N, et al. Three-dimensional Ca²⁺ imaging advances understanding of astrocyte biology[J]. Science, 2017, 356(6339): eaai8185. doi: 10.1126/science.aai8185
[25]	Hildebrandt IJ, Su H, Weber WA. Anesthesia and other considerations for in vivo imaging of small animals[J]. ILAR J, 2008, 49(1): 17–26. doi: 10.1093/ilar.49.1.17
[26]	Savtchouk I, Carriero G, Volterra A. Studying axon-astrocyte functional interactions by 3D two-photon Ca²⁺ imaging: a practical guide to experiments and "big data" analysis[J]. Front Cell Neurosci, 2018, 12: 98. doi: 10.3389/fncel.2018.00098
[27]	Sitdikova G, Zakharov A, Janackova S, et al. Isoflurane suppresses early cortical activity[J]. Ann Clin Transl Neurol, 2014, 1(1): 15–26. doi: 10.1002/acn3.16
[28]	Sullender CT, Richards LM, He F, et al. Dynamics of isoflurane-induced vasodilation and blood flow of cerebral vasculature revealed by multi-exposure speckle imaging[J]. J Neurosci Methods, 2022, 366: 109434. doi: 10.1016/j.jneumeth.2021.109434
[29]	Hudetz AG. General anesthesia and human brain connectivity[J]. Brain Connect, 2012, 2(6): 291–302. doi: 10.1089/brain.2012.0107
[30]	Akerboom J, Chen TW, Wardill TJ, et al. Optimization of a GCaMP calcium indicator for neural activity imaging[J]. J Neurosci, 2012, 32(40): 13819–13840. doi: 10.1523/JNEUROSCI.2601-12.2012
[31]	Rasmussen R, Nedergaard M, Petersen NC. Sulforhodamine 101, a widely used astrocyte marker, can induce cortical seizure-like activity at concentrations commonly used[J]. Sci Rep, 2016, 6(1): 30433. doi: 10.1038/srep30433
[32]	Matyash V, Kettenmann H. Heterogeneity in astrocyte morphology and physiology[J]. Brain Res Rev, 2010, 63(1–2): 2–10. doi: 10.1016/j.brainresrev.2009.12.001
[33]	Lanjakornsiripan D, Pior BJ, Kawaguchi D, et al. Layer-specific morphological and molecular differences in neocortical astrocytes and their dependence on neuronal layers[J]. Nat Commun, 2018, 9(1): 1623. doi: 10.1038/s41467-018-03940-3
[34]	Pnevmatikakis EA, Soudry D, Gao Y, et al. Simultaneous denoising, deconvolution, and demixing of calcium imaging data[J]. Neuron, 2016, 89(2): 285–299. doi: 10.1016/j.neuron.2015.11.037
[35]	Radstake FDW, Raaijmakers EAL, Luttge R, et al. CALIMA: the semi-automated open-source calcium imaging analyzer[J]. Comput Methods Programs Biomed, 2019, 179: 104991. doi: 10.1016/j.cmpb.2019.104991
[36]	Giovannucci A, Friedrich J, Gunn P, et al. CaImAn an open source tool for scalable calcium imaging data analysis[J]. eLife, 2019, 8: e38173. doi: 10.7554/eLife.38173
[37]	Wang Y, DelRosso NV, Vaidyanathan TV, et al. Accurate quantification of astrocyte and neurotransmitter fluorescence dynamics for single-cell and population-level physiology[J]. Nat Neurosci, 2019, 22(11): 1936–1944. doi: 10.1038/s41593-019-0492-2
[38]	Scharwächter L, Schmitt FJ, Pallast N, et al. Network analysis of neuroimaging in mice[J]. Neuroimage, 2022, 253: 119110. doi: 10.1016/j.neuroimage.2022.119110
[39]	Ding Z, Newton AT, Xu R, et al. Spatio-temporal correlation tensors reveal functional structure in human brain[J]. PLoS One, 2013, 8(12): e82107. doi: 10.1371/journal.pone.0082107
[40]	Hashimoto Y, Ogata Y, Honda M, et al. Deep feature extraction for resting-state functional MRI by self-supervised learning and application to schizophrenia diagnosis[J]. Front Neurosci, 2021, 15: 696853. doi: 10.3389/fnins.2021.696853