Chinese Journal of Lasers, Volume. 51, Issue 1, 0107001(2024)

Implantable Fluorescence Endoscopic Microscopy and Its Application in In Vivo Brain Imaging (Invited)

Fangrui Lin, Chenshuang Zhang, Xiaoqian Lian, and Junle Qu*
Author Affiliations
  • Key Laboratory of Optoelectronic Devices and Systems of the Ministry of Education/Guangdong Province, College of Physics and Optoelectronic Engineering, Shenzhen University, Shenzhen 518060, Guangdong , China
  • show less
    References(111)

    [2] Poo M M, Du J L, Ip N Y et al. China brain project: basic neuroscience, brain diseases, and brain-inspired computing[J]. Neuron, 92, 591-596(2016).

    [3] Inoue M. Genetically encoded calcium indicators to probe complex brain circuit dynamics in vivo[J]. Neuroscience Research, 169, 2-8(2021).

    [4] Iadecola C. The neurovascular unit coming of age: a journey through neurovascular coupling in health and disease[J]. Neuron, 96, 17-42(2017).

    [5] Sweeney M D, Sagare A P, Zlokovic B V. Blood-brain barrier breakdown in Alzheimer disease and other neurodegenerative disorders[J]. Nature Reviews Neurology, 14, 133-150(2018).

    [6] Petrovskaya A, Tverskoi A, Medvedeva A et al. Is blood-brain barrier a probable mediator of non-invasive brain stimulation effects on Alzheimer’s disease?[J]. Communications Biology, 6, 416(2023).

    [7] Dumoulin S O, Fracasso A, van der Zwaag W et al. Ultra-high field MRI: advancing systems neuroscience towards mesoscopic human brain function[J]. NeuroImage, 168, 345-357(2018).

    [8] Miyaoka R S, Lehnert A L. Small animal PET: a review of what we have done and where we are going[J]. Physics in Medicine and Biology, 65, 24TR04(2020).

    [9] Keklikoglou K, Arvanitidis C, Chatzigeorgiou G et al. Micro-CT for biological and biomedical studies: a comparison of imaging techniques[J]. Journal of Imaging, 7, 172(2021).

    [10] Helmchen F, Denk W. Deep tissue two-photon microscopy[J]. Nature Methods, 2, 932-940(2005).

    [11] Hong G S, Diao S, Chang J L et al. Through-skull fluorescence imaging of the brain in a new near-infrared window[J]. Nature Photonics, 8, 723-730(2014).

    [12] Liu H J, Deng X Q, Tong S et al. In vivo deep-brain structural and hemodynamic multiphoton microscopy enabled by quantum dots[J]. Nano Letters, 19, 5260-5265(2019).

    [13] Golovynskyi S, Golovynska I, Stepanova L I et al. Optical windows for head tissues in near-infrared and short-wave infrared regions: approaching transcranial light applications[J]. Journal of Biophotonics, 11, e201800141(2018).

    [14] Xia F, Gevers M, Fognini A et al. Short-wave infrared confocal fluorescence imaging of deep mouse brain with a superconducting nanowire single-photon detector[J]. ACS Photonics, 8, 2800-2810(2021).

    [15] Miller D R, Jarrett J W, Hassan A M et al. Deep tissue imaging with multiphoton fluorescence microscopy[J]. Current Opinion in Biomedical Engineering, 4, 32-39(2017).

    [16] Wang Z C, Zhang W, Guo F et al. Cross-scale optical endoscopic imaging technology[J]. Chinese Optics, 15, 1287-1301(2022).

    [17] Jung J C, Mehta A D, Aksay E et al. In vivo mammalian brain imaging using one-and two-photon fluorescence microendoscopy[J]. Journal of Neurophysiology, 92, 3121-3133(2004).

    [18] Huland D M, Brown C M, Howard S S et al. In vivo imaging of unstained tissues using long gradient index lens multiphoton endoscopic systems[J]. Biomedical Optics Express, 3, 1077-1085(2012).

    [19] Kim J K, Choi J W, Yun S H A. 350-μm side-view optical probe for imaging the murine brain in vivo from the cortex to the hypothalamus[J]. Journal of Biomedical Optics, 18, 050502(2013).

    [20] Bocarsly M E, Jiang W C, Wang C et al. Minimally invasive microendoscopy system for in vivo functional imaging of deep nuclei in the mouse brain[J]. Biomedical Optics Express, 6, 4546-4556(2015).

    [21] Jennings J H, Kim C K, Marshel J H et al. Interacting neural ensembles in orbitofrontal cortex for social and feeding behaviour[J]. Nature, 565, 645-649(2019).

    [22] Li Y, Mathis A, Grewe B F et al. Neuronal representation of social information in the medial amygdala of awake behaving mice[J]. Cell, 171, 1176-1190(2017).

    [23] Butiaeva L I, Kokoeva M V. High-resolution intravital imaging of the murine hypothalamus using GRIN lenses and confocal microscopy[J]. STAR Protocols, 3, 101193(2022).

    [24] Lee S A, Holly K S, Voziyanov V et al. Gradient index microlens implanted in prefrontal cortex of mouse does not affect behavioral test performance over time[J]. PLoS One, 11, e0146533(2016).

    [25] Pernici C D, Kemp B S, Murray T A. Time course images of cellular injury and recovery in murine brain with high-resolution GRIN lens system[J]. Scientific Reports, 9, 7946(2019).

    [26] Hsiao Y T, Wang A Y C, Lee T Y et al. Using baseplating and a miniscope preanchored with an objective lens for calcium transient research in mice[J]. Journal of Visualized Experiments: JoVE, e62611(2021).

    [27] Carrier-Ruiz A, Sugaya Y, Kumar D et al. Calcium imaging of adult-born neurons in freely moving mice[J]. STAR Protocols, 2, 100238(2021).

    [28] Zhang L F, Liang B, Barbera G et al. Miniscope GRIN lens system for calcium imaging of neuronal activity from deep brain structures in behaving animals[J]. Current Protocols in Neuroscience, 86, e56(2019).

    [29] Li J S, Zhu L W, Ye T et al. Relationship of neurovascular units and neurodegenerative diseases(review)[J]. Chinese Journal of Rehabilitation Theory and Practice, 24, 287-289(2018).

    [30] Chen Z H, Hambardzumyan D. Immune microenvironment in glioblastoma subtypes[J]. Frontiers in Immunology, 9, 1004(2018).

    [31] Larjavaara S, Mäntylä R, Salminen T et al. Incidence of gliomas by anatomic location[J]. Neuro-Oncology, 9, 319-325(2007).

    [32] Venkataramani V, Yang Y, Schubert M C et al. Glioblastoma hijacks neuronal mechanisms for brain invasion[J]. Cell, 185, 2899-2917(2022).

    [33] Elisaveta S, Jorg D, Cole Andrew J. The complexities underlying epilepsy in people with glioblastoma[J]. The Lancet Neurology, 22, 505-516(2023).

    [34] Barretto R P J, Ko T H, Jung J C et al. Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy[J]. Nature Medicine, 17, 223-228(2011).

    [35] Toader A C, Regalado J M, Li Y R et al. Anteromedial thalamus gates the selection and stabilization of long-term memories[J]. Cell, 186, 1369-1381(2023).

    [36] Barretto R P J, Messerschmidt B, Schnitzer M J. In vivo fluorescence imaging with high-resolution microlenses[J]. Nature Methods, 6, 511-512(2009).

    [37] Teresa A M, Michael J L. Singlet gradient index lens for deep in vivo multiphoton microscopy[J]. Journal of Biomedical Optics, 17, 021106(2012).

    [38] Antonini A, Sattin A, Moroni M et al. Extended field-of-view ultrathin microendoscopes for high-resolution two-photon imaging with minimal invasiveness[J]. eLife, 9, e58882(2020).

    [39] Lee W M, Yun S H. Adaptive aberration correction of GRIN lenses for confocal endomicroscopy[J]. Optics Letters, 36, 4608-4610(2011).

    [40] Wang C, Ji N. Pupil-segmentation-based adaptive optical correction of a high-numerical-aperture gradient refractive index lens for two-photon fluorescence endoscopy[J]. Optics Letters, 37, 2001-2003(2012).

    [41] Wang C, Ji N. Characterization and improvement of three-dimensional imaging performance of GRIN-lens-based two-photon fluorescence endomicroscopes with adaptive optics[J]. Optics Express, 21, 27142-27154(2013).

    [42] Zhang Q R, Pan D S, Ji N. High-resolution in vivo optical-sectioning widefield microendoscopy[J]. Optica, 7, 1287-1290(2020).

    [43] Levene M J, Dombeck D A, Kasischke K A et al. In vivo multiphoton microscopy of deep brain tissue[J]. Journal of Neurophysiology, 91, 1908-1912(2004).

    [44] Moretti C, Antonini A, Bovetti S et al. Scanless functional imaging of hippocampal networks using patterned two-photon illumination through GRIN lenses[J]. Biomedical Optics Express, 7, 3958-3967(2016).

    [45] Meng G H, Liang Y J, Sarsfield S et al. High-throughput synapse-resolving two-photon fluorescence microendoscopy for deep-brain volumetric imaging in vivo[J]. eLife, 8, e40805(2019).

    [46] Qin Z Y, Chen C P, He S C et al. Adaptive optics two-photon endomicroscopy enables deep-brain imaging at synaptic resolution over large volumes[J]. Science Advances, 6, eabc6521(2020).

    [47] Chien Y F, Lin J Y, Yeh P T et al. Dual GRIN lens two-photon endoscopy for high-speed volumetric and deep brain imaging[J]. Biomedical Optics Express, 12, 162-172(2020).

    [48] Helmchen F, Fee M S, Tank D W et al. A miniature head-mounted two-photon microscope: high-resolution brain imaging in freely moving animals[J]. Neuron, 31, 903-912(2001).

    [49] Kerr J N, Nimmerjahn A. Functional imaging in freely moving animals[J]. Current Opinion in Neurobiology, 22, 45-53(2012).

    [50] Ghosh K K, Burns L D, Cocker E D et al. Miniaturized integration of a fluorescence microscope[J]. Nature Methods, 8, 871-878(2011).

    [51] Sawinski J, Denk W. Miniature random-access fiber scanner for in vivo multiphoton imaging[J]. Journal of Applied Physics, 102, 034701(2007).

    [52] Zong W J, Wu R L, Li M L et al. Fast high-resolution miniature two-photon microscopy for brain imaging in freely behaving mice[J]. Nature Methods, 14, 713-719(2017).

    [53] Klioutchnikov A, Wallace D J, Sawinski J et al. A three-photon head-mounted microscope for imaging all layers of visual cortex in freely moving mice[J]. Nature Methods, 20, 610-616(2023).

    [54] Zhao C Z, Chen S Y, Zhang L F et al. Miniature three-photon microscopy maximized for scattered fluorescence collection[J]. Nature Methods, 20, 617-622(2023).

    [55] Grewe B F, Gründemann J, Kitch L J et al. Neural ensemble dynamics underlying a long-term associative memory[J]. Nature, 543, 670-675(2017).

    [56] Barbera G, Jun R, Zhang Y et al. A miniature fluorescence microscope for multi-plane imaging[J]. Scientific Reports, 12, 16686(2022).

    [57] Zong W J, Obenhaus H A, Skytøen E R et al. Large-scale two-photon calcium imaging in freely moving mice[J]. Cell, 185, 1240-1256(2022).

    [58] Shekhtmeyster P, Carey E M, Duarte D et al. Multiplex translaminar imaging in the spinal cord of behaving mice[J]. Nature Communications, 14, 1427(2023).

    [59] Flusberg B A, Jung J C, Cocker E D et al. In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope[J]. Optics Letters, 30, 2272-2274(2005).

    [60] Fan J T, Suo J L, Wu J M et al. Video-rate imaging of biological dynamics at centimetre scale and micrometre resolution[J]. Nature Photonics, 13, 809-816(2019).

    [61] Yang M K, Zhou Z Q, Zhang J X et al. MATRIEX imaging: multiarea two-photon real-time in vivo explorer[J]. Light: Science & Applications, 8, 109(2019).

    [62] Pochechuev M S, Solotenkov M A, Fedotov I V et al. Multisite cell-and neural-dynamics-resolving deep brain imaging in freely moving mice with implanted reconnectable fiber bundles[J]. Journal of Biophotonics, 13, e202000081(2020).

    [63] Choi Y, Yoon C, Kim M et al. Scanner-free and wide-field endoscopic imaging by using a single multimode optical fiber[J]. Physical Review Letters, 109, 203901(2012).

    [64] Bianchi S, di Leonardo R. A multi-mode fiber probe for holographic micromanipulation and microscopy[J]. Lab on a Chip, 12, 635-639(2012).

    [65] Vellekoop I M, Mosk A P. Focusing coherent light through opaque strongly scattering media[J]. Optics Letters, 32, 2309-2311(2007).

    [66] Mosk A P, Lagendijk A, Lerosey G et al. Controlling waves in space and time for imaging and focusing in complex media[J]. Nature Photonics, 6, 283-292(2012).

    [67] Horstmeyer R, Ruan H W, Yang C. Guidestar-assisted wavefront-shaping methods for focusing light into biological tissue[J]. Nature Photonics, 9, 563-571(2015).

    [68] Tzang O, Caravaca-Aguirre A M, Wagner K et al. Adaptive wavefront shaping for controlling nonlinear multimode interactions in optical fibres[J]. Nature Photonics, 12, 368-374(2018).

    [69] Amitonova L V, de Boer J F. Endo-microscopy beyond the abbe and Nyquist limits[J]. Light: Science & Applications, 9, 81(2020).

    [70] Caravaca-Aguirre A M, Piestun R. Single multimode fiber endoscope[J]. Optics Express, 25, 1656-1665(2017).

    [71] Fischer B, Sternklar S. Image transmission and interferometry with multimode fibers using self-pumped phase conjugation[J]. Applied Physics Letters, 46, 113-114(1985).

    [72] Popoff S M, Lerosey G, Carminati R et al. Measuring the transmission matrix in optics: an approach to the study and control of light propagation in disordered media[J]. Physical Review Letters, 104, 100601(2010).

    [73] Čižmár T, Dholakia K. Exploiting multimode waveguides for pure fibre-based imaging[J]. Nature Communications, 3, 1027(2012).

    [74] Farahi S, Ziegler D, Papadopoulos I N et al. Dynamic bending compensation while focusing through a multimode fiber[J]. Optics Express, 21, 22504-22514(2013).

    [75] Gu R Y, Mahalati R N, Kahn J M. Design of flexible multi-mode fiber endoscope[J]. Optics Express, 23, 26905-26918(2015).

    [76] Gordon G S D, Gataric M, Ramos A G C P et al. Characterizing optical fiber transmission matrices using metasurface reflector stacks for lensless imaging without distal access[J]. Physical Review X, 9, 041050(2019).

    [77] Li S H, Horsley S A R, Tyc T et al. Memory effect assisted imaging through multimode optical fibres[J]. Nature Communications, 12, 3751(2021).

    [78] Huang B Y, Li J, Yao B W et al. Enhancing image resolution of confocal fluorescence microscopy with deep learning[J]. PhotoniX, 4, 1-22(2023).

    [79] Shen B L, Liu S W, Li Y P et al. Deep learning autofluorescence-harmonic microscopy[J]. Light, Science & Applications, 11, 76(2022).

    [80] Liao J H, Zhang C S, Xu X C et al. Deep-MSIM: fast image reconstruction with deep learning in multifocal structured illumination microscopy[J]. Advanced Science, 10, e2300947(2023).

    [81] Fan P F, Zhao T R, Su L. Deep learning the high variability and randomness inside multimode fibers[J]. Optics Express, 27, 20241-20258(2019).

    [82] Fan P F, Wang Y F, Ruddlesden M et al. Deep learning enabled scalable calibration of a dynamically deformed multimode fiber[J]. Advanced Photonics Research, 3, 2100304(2022).

    [83] Nicholas B, Tristan K, Lamb Erin S et al. Transfer learning and generalization of a neural-network-based multimode fiber position and imaging sensor under thermal perturbations[J]. Optical Fiber Technology, 70, 102855(2022).

    [84] Plöschner M, Čižmár T. Compact multimode fiber beam-shaping system based on GPU accelerated digital holography[J]. Optics Letters, 40, 197-200(2015).

    [85] Vasquez-Lopez S A, Turcotte R, Koren V et al. Subcellular spatial resolution achieved for deep-brain imaging in vivo using a minimally invasive multimode fiber[J]. Light: Science & Applications, 7, 110(2018).

    [86] Turtaev S, Leite I T, Altwegg-Boussac T et al. High-fidelity multimode fibre-based endoscopy for deep brain in vivo imaging[J]. Light: Science & Applications, 7, 92(2018).

    [87] Shay O, Antonio C A, Rafael P et al. Minimally invasive multimode optical fiber microendoscope for deep brain fluorescence imaging[J]. Biomedical Optics Express, 9, 1492-1509(2018).

    [88] Silveira B M, Pikálek T, Stibůrek M et al. Side-view holographic endomicroscopy via a custom-terminated multimode fibre[J]. Optics Express, 29, 23083-23095(2021).

    [89] Stibůrek M, Ondráčková P, Tučková T et al. 110 μm thin endo-microscope for deep-brain in vivo observations of neuronal connectivity, activity and blood flow dynamics[J]. Nature Communications, 14, 1897(2023).

    [90] Wen Z, Dong Z Y, Deng Q L et al. Single multimode fibre for in vivo light-field-encoded endoscopic imaging[J]. Nature Photonics, 17, 679-687(2023).

    [91] Sato M, Motegi Y, Yagi S et al. Fast varifocal two-photon microendoscope for imaging neuronal activity in the deep brain[J]. Biomedical Optics Express, 8, 4049-4060(2017).

    [92] Sanai N, Eschbacher J, Hattendorf G et al. Intraoperative confocal microscopy for brain tumors: a feasibility analysis in humans[J]. Operative Neurosurgery, 68, 282-290(2011).

    [93] Martirosyan N L, Eschbacher J M, Kalani M Y S et al. Prospective evaluation of the utility of intraoperative confocal laser endomicroscopy in patients with brain neoplasms using fluorescein sodium: experience with 74 cases[J]. Neurosurgical Focus, 40, E11(2016).

    [94] Teng C W, Huang V, Arguelles G R et al. Applications of indocyanine green in brain tumor surgery: review of clinical evidence and emerging technologies[J]. Neurosurgical Focus, 50, E4(2021).

    [95] Ritz R, Feigl G C, Schuhmann M U et al. Use of 5-ALA fluorescence guided endoscopic biopsy of a deep-seated primary malignant brain tumor[J]. Journal of Neurosurgery, 114, 1410-1413(2011).

    [96] Leroy H A, Vermandel M, Lejeune J P et al. Fluorescence guided resection and glioblastoma in 2015: a review[J]. Lasers in Surgery and Medicine, 47, 441-451(2015).

    [97] Pavlov V, Meyronet D, Meyer-Bisch V et al. Intraoperative probe-based confocal laser endomicroscopy in surgery and stereotactic biopsy of low-grade and high-grade gliomas: a feasibility study in humans[J]. Neurosurgery, 79, 604-612(2016).

    [98] Breuskin D, Szczygielski J, Urbschat S et al. Confocal laser endomicroscopy in neurosurgery: an alternative to instantaneous sections?[J]. World Neurosurgery, 100, 180-185(2017).

    [99] Charalampaki P, Nakamura M, Athanasopoulos D et al. Confocal-assisted multispectral fluorescent microscopy for brain tumor surgery[J]. Frontiers in Oncology, 9, 583(2019).

    [100] Irakliy A, Park M T, Gooldy T C et al. Real-time intraoperative surgical telepathology using confocal laser endomicroscopy[J]. Neurosurgical Focus, 52, E9(2022).

    [101] Levchenko S M, Pliss A, Peng X et al. Fluorescence lifetime imaging for studying DNA compaction and gene activities[J]. Light: Science & Applications, 10, 224(2021).

    [102] Lin F R, Zhang C S, Zhao Y H et al. In vivo two-photon fluorescence lifetime imaging microendoscopy based on fiber-bundle[J]. Optics Letters, 47, 2137-2140(2022).

    [103] Liu Y F, Al-salihi M, Guo Y et al. Halogen-doped phosphorescent carbon dots for grayscale patterning[J]. Light: Science & Applications, 11, 163(2022).

    [104] Chia T H, Williamson A, Spencer D D et al. Multiphoton fluorescence lifetime imaging of intrinsic fluorescence in human and rat brain tissue reveals spatially distinct NADH binding[J]. Optics Express, 16, 4237-4249(2008).

    [105] Berezin M Y, Achilefu S. Fluorescence lifetime measurements and biological imaging[J]. Chemical Reviews, 110, 2641-2684(2010).

    [106] Kantelhardt S R, Kalasauskas D, König K et al. In vivo multiphoton tomography and fluorescence lifetime imaging of human brain tumor tissue[J]. Journal of Neuro-Oncology, 127, 473-482(2016).

    [107] Butte P V, Mamelak A N, Nuno M et al. Fluorescence lifetime spectroscopy for guided therapy of brain tumors[J]. NeuroImage, 54, S125-S135(2011).

    [108] Fang Q Y, Papaioannou T, Jo J A et al. Time-domain laser-induced fluorescence spectroscopy apparatus for clinical diagnostics[J]. Review of Scientific Instruments, 75, 151-162(2004).

    [109] Sun Y H, Hatami N, Yee M et al. Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery[J]. Journal of Biomedical Optics, 15, 056022(2010).

    [110] Marcu L, Hartl B A. Fluorescence lifetime spectroscopy and imaging in neurosurgery[J]. IEEE Journal of Selected Topics in Quantum Electronics, 18, 1465-1477(2012).

    [111] Alfonso-Garcia A, Bec J, Sridharan Weaver S et al. Real-time augmented reality for delineation of surgical margins during neurosurgery using autofluorescence lifetime contrast[J]. Journal of Biophotonics, 13, e201900108(2020).

    Tools

    Get Citation

    Copy Citation Text

    Fangrui Lin, Chenshuang Zhang, Xiaoqian Lian, Junle Qu. Implantable Fluorescence Endoscopic Microscopy and Its Application in In Vivo Brain Imaging (Invited)[J]. Chinese Journal of Lasers, 2024, 51(1): 0107001

    Download Citation

    EndNote(RIS)BibTexPlain Text
    Save article for my favorites
    Paper Information

    Category: biomedical photonics and laser medicine

    Received: Sep. 20, 2023

    Accepted: Oct. 26, 2023

    Published Online: Jan. 22, 2024

    The Author Email: Qu Junle (jlqu@szu.edu.cn)

    DOI:10.3788/CJL231225

    Topics