Focus-tunable microscope for imaging small neuronal processes in freely moving animals

Arutyun Bagramyan; Loïc Tabourin; Ali Rastqar; Narges Karimi; Frédéric Bretzner; Tigran Galstian

doi:10.1364/PRJ.418154

[1] D. Miyamoto, M. Murayama. The fiber-optic imaging and manipulation of neural activity during animal behavior. Neurosci. Res., 103, 1-9(2016).

[2] D. Aharoni, T. M. Hoogland. Circuit investigations with open-source miniaturized microscopes: past, present and future. Front. Cell. Neurosci., 13, 141(2019).

[3] W. Yang, R. Yuste. In vivo imaging of neural activity. Nat. Methods, 14, 349-359(2017).

[4] F.-J. Kao, W. Zong, L. Chen, G. Keiser, A. Gogoi. Advanced miniature microscopy for brain imaging. Advanced Optical Methods for Brain Imaging, 167-187(2019).

[5] J. Oh, C. Lee, B.-K. Kaang. Imaging and analysis of genetically encoded calcium indicators linking neural circuits and behaviors. Korean J. Phys. Pharmacol., 23, 237-249(2019).

[6] I. Mollinedo-Gajate, C. Song, T. Knöpfel. Genetically encoded fluorescent calcium and voltage indicators. Handb. Exp. Pharmacol., 260, 209-229(2019).

[7] E. Greotti, D. De Stefani. Biosensors for detection of calcium. Methods Cell Biol., 155, 337-368(2020).

[8] J. Voigts, M. T. Harnett. An animal-actuated rotational head-fixation system for 2-photon imaging during 2-d navigation(2018).

[9] W. Mittmann, D. J. Wallace, U. Czubayko, J. T. Herb, A. T. Schaefer, L. L. Looger, W. Denk, J. N. D. Kerr. Two-photon calcium imaging of evoked activity from L5 somatosensory neurons in vivo. Nat. Neurosci., 14, 1089-1093(2011).

[10] R. Li, M. Wang, J. Yao, S. Liang, X. Liao, M. Yang, J. Zhang, J. Yan, H. Jia, X. Chen, X. Li. Two-photon functional imaging of the auditory cortex in behaving mice: from neural networks to single spines. Front. Neural Circuits, 12, 33(2018).

[11] P. Ravassard, A. Kees, B. Willers, D. Ho, D. A. Aharoni, J. Cushman, Z. M. Aghajan, M. R. Mehta. Multisensory control of hippocampal spatiotemporal selectivity. Science, 340, 1342-1346(2013).

[12] Z. M. Aghajan, L. Acharya, J. J. Moore, J. D. Cushman, C. Vuong, M. R. Mehta. Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality. Nat. Neurosci., 18, 121-128(2015).

[13] K. Thurley, A. Ayaz. Virtual reality systems for rodents. Curr. Zool., 63, 109-119(2017).

[14] R. van den Brand, J. Heutschi, Q. Barraud, J. DiGiovanna, K. Bartholdi, M. Huerlimann, L. Friedli, I. Vollenweider, E. M. Moraud, S. Duis, N. Dominici, S. Micera, P. Musienko, G. Courtine. Restoring voluntary control of locomotion after paralyzing spinal cord injury. Science, 336, 1182-1185(2012).

[15] U. Sławińska, H. Majczyński, Y. Dai, L. M. Jordan. The upright posture improves plantar stepping and alters responses to serotonergic drugs in spinal rats. J. Physiol., 590, 1721-1736(2012).

[16] B. N. Ozbay, G. L. Futia, M. Ma, V. M. Bright, J. T. Gopinath, E. G. Hughes, D. Restrepo, E. A. Gibson. Three dimensional two-photon brain imaging in freely moving mice using a miniature fiber coupled microscope with active axial-scanning. Sci. Rep., 8, 8108(2018).

[17] F. Helmchen, W. Denk, J. N. D. Kerr. Miniaturization of two-photon microscopy for imaging in freely moving animals. Cold Spring Harb. Protoc., 2013, 904-913(2013).

[18] D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, C. Xu. Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue. Proc. Natl. Acad. Sci. USA, 108, 17598-17603(2011).

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

[20] Y. Zhang, M. L. Akins, K. Murari, J. Xi, M.-J. Li, K. Luby-Phelps, M. Mahendroo, X. Li. A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy. Proc. Natl. Acad. Sci. USA, 109, 12878-12883(2012).

[21] W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. J. Barretto, J. C. Jung, H. Ra, O. Solgaard, M. J. Schnitzer. In vivo brain imaging using a portable 2.9 g two-photon microscope based on a microelectromechanical system scanning mirror. Opt. Lett., 34, 2309-2311(2009).

[22] W. Zong, R. Wu, M. Li, Y. Hu, Y. Li, J. Li, H. Rong, H. Wu, Y. Xu, Y. Lu, H. Jia, M. Fan, Z. Zhou, Y. Zhang, A. Wang, L. Chen, H. Cheng. Fast high-resolution miniature two-photon microscopy for brain imaging in freely behaving mice. Nat. Methods, 14, 713-719(2017).

[23] B. N. Ozbay, J. T. Losacco, R. Cormack, R. Weir, V. M. Bright, J. T. Gopinath, D. Restrepo, E. A. Gibson. Miniaturized fiber-coupled confocal fluorescence microscope with an electrowetting variable focus lens using no moving parts. Opt. Lett., 40, 2553-2556(2015).

[24] O. Mano, M. S. Creamer, C. A. Matulis, E. Salazar-Gatzimas, J. Chen, J. A. Zavatone-Veth, D. A. Clark. Using slow frame rate imaging to extract fast receptive fields. Nat. Commun., 10, 4979(2019).

[25] S. A. Lee, K. S. Holly, V. Voziyanov, S. L. Villalba, R. Tong, H. E. Grigsby, E. Glasscock, F. G. Szele, I. Vlachos, T. A. Murray. Gradient index microlens implanted in prefrontal cortex of mouse does not affect behavioral test performance over time. PLoS ONE, 11, e0146533(2016).

[26] W. A. Liberti, L. N. Perkins, D. P. Leman, T. J. Gardner. An open source, wireless capable miniature microscope system. J. Neural Eng., 14, 045001(2017).

[27] K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. E. Gamal, M. J. Schnitzer. Miniaturized integration of a fluorescence microscope. Nat. Methods, 8, 871-878(2011).

[28] D. J. Cai, D. Aharoni, T. Shuman, J. Shobe, J. Biane, W. Song, B. Wei, M. Veshkini, M. La-Vu, J. Lou, S. E. Flores, I. Kim, Y. Sano, M. Zhou, K. Baumgaertel, A. Lavi, M. Kamata, M. Tuszynski, M. Mayford, P. Golshani, A. J. Silva. A shared neural ensemble links distinct contextual memories encoded close in time. Nature, 534, 115-118(2016).

[29] A. Bagramyan. Lightweight 1-photon miniscope for imaging in freely behaving animals at subcellular resolution. IEEE Photon. Technol. Lett., 32, 909-912(2020).

[30] J. I. Arellano, R. Benavides-Piccione, J. DeFelipe, R. Yuste. Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front. Neurosci., 1, 131-143(2007).

[31] W. M. Lee, S. H. Yun. Adaptive aberration correction of GRIN lenses for confocal endomicroscopy. Opt. Lett., 36, 4608-4610(2011).

[32] A. Bagramyan, T. Galstian. Dynamic control of polarization mismatch and coma aberrations in rod-GRIN assemblies. Opt. Express, 27, 14144-14151(2019).

[33] T. V. Galstian. Smart Mini-Cameras(2013).

[34] B. F. Grewe, F. F. Voigt, M. van ’t Hoff, F. Helmchen. Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens. Biomed. Opt. Express, 2, 2035(2011).

[35] P.-G. de Gennes, J. Prost. The Physics of Liquid Crystals(1993).

[36] T. Galstian, K. Asatryan, V. Presniakov, A. Zohrabyan, A. Tork, A. Bagramyan, S. Careau, M. Thiboutot, M. Cotovanu. High optical quality electrically variable liquid crystal lens using an additional floating electrode. Opt. Lett., 41, 3265-3268(2016).

[37] T. Galstian, O. Sova, K. Asatryan, V. Presniakov, A. Zohrabyan, M. Evensen. Optical camera with liquid crystal autofocus lens. Opt. Express, 25, 29945-29964(2017).

[38] A. Bagramyan, T. Galstian, A. Saghatelyan. Motion-free endoscopic system for brain imaging at variable focal depth using liquid crystal lenses. J. Biophoton., 10, 762-774(2017).

[39] L. Li, L. Xiao, J.-H. Wang, Q.-H. Wang. Movable electrowetting optofluidic lens for optical axial scanning in microscopy. Opto-Electron. Adv., 02, 180025(2019).

[40] L. Li, D. Wang, C. Liu, Q.-H. Wang. Zoom microscope objective using electrowetting lenses. Opt. Express, 24, 2931-2940(2016).

[41] G. Barbera, B. Liang, L. Zhang, C. R. Gerfen, E. Culurciello, R. Chen, Y. Li, D.-T. Lin. Spatially compact neural clusters in the dorsal striatum encode locomotion relevant information. Neuron, 92, 202-213(2016).

[42] M. Carlén, R. M. Cassidy, H. Brismar, G. A. Smith, L. W. Enquist, J. Frisén. Functional integration of adult-born neurons. Curr. Biol., 12, 606-608(2002).

[43] D. L. Dickstein, C. M. Weaver, J. I. Luebke, P. R. Hof. Dendritic spine changes associated with normal aging. Neuroscience, 251, 21-32(2013).

[44] Y. Smith, R. M. Villalba, D. V. Raju. Striatal spine plasticity in Parkinson’s disease: pathological or not?. Parkinsonism Relat. Disord., 15, S156-S161(2009).

[45] T. Bittner, M. Fuhrmann, S. Burgold, S. M. Ochs, N. Hoffmann, G. Mitteregger, H. Kretzschmar, F. M. LaFerla, J. Herms. Multiple events lead to dendritic spine loss in triple transgenic Alzheimer’s disease mice. PLoS ONE, 5, e15477(2010).

[46] M. Balbi, M. P. Vanni, G. Silasi, Y. Sekino, L. Bolanos, J. M. LeDue, T. H. Murphy. Targeted ischemic stroke induction and mesoscopic imaging assessment of blood flow and ischemic depolarization in awake mice. Neurophotonics, 4, 035001(2017).