Kilohertz two-photon fluorescence microscopy imaging of neural
activity  in vivo

Wu, Jianglai; Liang, Yajie; Chen, Shuo; Hsu, Ching-Lung; Chavarha, Mariya; Evans, Stephen W; Shi, Dongqing; Lin, Michael Z.; Tsia, Kevin K.; Ji, Na

doi:10.1038/s41592-020-0762-7

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Kilohertz two-photon fluorescence microscopy imaging of neural activity in vivo

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Author(s): Jianglai Wu ¹ ^, ² ^, ³ , Yajie Liang ³ , Shuo Chen ¹ , Ching-Lung Hsu ³ , Mariya Chavarha ⁴ , Stephen W Evans ⁴ , Dongqing Shi ⁴ , Michael Z Lin ⁴ , Kevin K Tsia ² ^, ^* , Na Ji ¹ ^, ³ ^, ⁵ ^, ⁶ ^, ⁷ ^, ^*

Publication date (Electronic): 02 March 2020

Journal: Nature methods

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Abstract

Understanding information processing in the brain requires us to monitor neural activity at high spatiotemporal resolution. Using an ultrafast two-photon fluorescence microscope (2PFM) empowered by all-optical laser scanning, we imaged neural activity in vivo at up to 3,000 frames per second and submicron spatial resolution. This ultrafast imaging method enabled monitoring of both supra- and sub-threshold electrical activity down to 345 μm below the brain surface in head-fixed awake mice.

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Most cited references 21

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Theta oscillations in the hippocampus.

György Buzsáki (2002)

Theta oscillations represent the "on-line" state of the hippocampus. The extracellular currents underlying theta waves are generated mainly by the entorhinal input, CA3 (Schaffer) collaterals, and voltage-dependent Ca(2+) currents in pyramidal cell dendrites. The rhythm is believed to be critical for temporal coding/decoding of active neuronal ensembles and the modification of synaptic weights. Nevertheless, numerous critical issues regarding both the generation of theta oscillations and their functional significance remain challenges for future research.

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Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance.

Linda Madisen, Aleena Garner, Daisuke Shimaoka … (2015)

An increasingly powerful approach for studying brain circuits relies on targeting genetically encoded sensors and effectors to specific cell types. However, current approaches for this are still limited in functionality and specificity. Here we utilize several intersectional strategies to generate multiple transgenic mouse lines expressing high levels of novel genetic tools with high specificity. We developed driver and double reporter mouse lines and viral vectors using the Cre/Flp and Cre/Dre double recombinase systems and established a new, retargetable genomic locus, TIGRE, which allowed the generation of a large set of Cre/tTA-dependent reporter lines expressing fluorescent proteins, genetically encoded calcium, voltage, or glutamate indicators, and optogenetic effectors, all at substantially higher levels than before. High functionality was shown in example mouse lines for GCaMP6, YCX2.60, VSFP Butterfly 1.2, and Jaws. These novel transgenic lines greatly expand the ability to monitor and manipulate neuronal activities with increased specificity.

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An optimized fluorescent probe for visualizing glutamate neurotransmission

Jonathan S. Marvin, Bart G. Borghuis, Lin Tian … (2013)

We describe an intensity-based glutamate-sensing fluorescent reporter (“iGluSnFR”) with signal-to-noise ratio and kinetics appropriate for in vivo imaging. We engineered iGluSnFR in vitro to maximize its fluorescence change, and validated its utility for visualizing glutamate release by neurons and astrocytes in increasingly intact neurological systems. In hippocampal culture, iGluSnFR detected single field stimulus-evoked glutamate release events. In pyramidal neurons in acute brain slices, glutamate uncaging at single spines showed that iGluSnFR responds robustly and specifically to glutamate in situ, and responses correlate with voltage changes. In mouse retina, iGluSnFR-expressing neurons showed intact light-evoked excitatory currents, and the sensor revealed tonic glutamate signaling in response to light stimuli. In worms, glutamate signals preceded and predicted post-synaptic calcium transients. In zebrafish, iGluSnFR revealed spatial organization of direction-selective synaptic activity in the optic tectum. Finally, in mouse forelimb motor cortex, iGluSnFR expression in layer V pyramidal neurons revealed task-dependent single-spine activity during running.

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Author and article information

Journal

Journal ID (nlm-journal-id): 101215604

Journal ID (pubmed-jr-id): 32338

Journal ID (nlm-ta): Nat Methods

Journal ID (iso-abbrev): Nat. Methods

Title: Nature methods

ISSN (Print): 1548-7091

ISSN (Electronic): 1548-7105

Publication date Nihms-submitted: 14 March 2020

Publication date (Electronic): 02 March 2020

Publication date (Print): March 2020

Publication date PMC-release: 02 September 2020

Volume: 17

Issue: 3

Pages: 287-290

Affiliations

[1 ]Department of Physics, University of California, Berkeley, California, USA

[2 ]Department of Electrical and Electronic Engineering, The University of Hong Kong, Pokfulam Road, Hong Kong, China

[3 ]Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, USA

[4 ]Department of Bioengineering, Stanford University, Stanford, California, USA

[5 ]Department of Molecular and Cell Biology, University of California, Berkeley, California, USA

[6 ]Helen Wills Neuroscience Institute, University of California, Berkeley, California, USA

[7 ]Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

Author notes

AUTHOR CONTRIBUTIONS

N.J. conceived of the project; M.L., K.K.T., and N.J. supervised research; J.W., K.K.T., and N.J. designed FACED module; Y.L., S.C., C.L.H. prepared samples; M.C. created ASAP3; M.C., S.E., and D.S. characterized ASAP3 and ASAP3-expressing viruses; J.W. collected and analyzed the data; J.W. and N.J. wrote the manuscript with inputs from all authors.

[* ]To whom correspondence should be addressed: tsia@ 123456hku.hk , jina@ 123456berkeley.edu

Article

Manuscript ID: NIHMS1551714

DOI: 10.1038/s41592-020-0762-7

PMC ID: 7199528

PubMed ID: 32123392

SO-VID: 704a07b3-1f08-4328-9b38-2bcbd1d909f0

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Kilohertz two-photon fluorescence microscopy imaging of neural activity in vivo

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Neuronal Signaling

Most cited references 21

Theta oscillations in the hippocampus.

Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance.

An optimized fluorescent probe for visualizing glutamate neurotransmission

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