PMID- 31080068 OWN - NLM STAT- MEDLINE DCOM- 20200211 LR - 20200211 IS - 1097-4172 (Electronic) IS - 0092-8674 (Linking) VI - 177 IP - 5 DP - 2019 May 16 TI - Rational Engineering of XCaMPs, a Multicolor GECI Suite for In Vivo Imaging of Complex Brain Circuit Dynamics. PG - 1346-1360.e24 LID - S0092-8674(19)30393-9 [pii] LID - 10.1016/j.cell.2019.04.007 [doi] AB - To decipher dynamic brain information processing, current genetically encoded calcium indicators (GECIs) are limited in single action potential (AP) detection speed, combinatorial spectral compatibility, and two-photon imaging depth. To address this, here, we rationally engineered a next-generation quadricolor GECI suite, XCaMPs. Single AP detection was achieved within 3-10 ms of spike onset, enabling measurements of fast-spike trains in parvalbumin (PV)-positive interneurons in the barrel cortex in vivo and recording three distinct (two inhibitory and one excitatory) ensembles during pre-motion activity in freely moving mice. In vivo paired recording of pre- and postsynaptic firing revealed spatiotemporal constraints of dendritic inhibition in layer 1 in vivo, between axons of somatostatin (SST)-positive interneurons and apical tufts dendrites of excitatory pyramidal neurons. Finally, non-invasive, subcortical imaging using red XCaMP-R uncovered somatosensation-evoked persistent activity in hippocampal CA1 neurons. Thus, the XCaMPs offer a critical enhancement of solution space in studies of complex neuronal circuit dynamics. VIDEO ABSTRACT. CI - Copyright (c) 2019 Elsevier Inc. All rights reserved. FAU - Inoue, Masatoshi AU - Inoue M AD - Department of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; Department of Bioengineering, Stanford University School of Medicine, Stanford, CA 94305, USA. FAU - Takeuchi, Atsuya AU - Takeuchi A AD - Department of Neurophysiology, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan. FAU - Manita, Satoshi AU - Manita S AD - Department of Neurophysiology, Faculty of Medicine, University of Yamanashi, Chuo, Yamanashi 409-3898, Japan. FAU - Horigane, Shin-Ichiro AU - Horigane SI AD - Department of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; Department of Neuroscience I, Research Institute of Environmental Medicine, Nagoya University, Nagoya, Aichi 464-8601, Japan; Department of Molecular/Cellular Neuroscience, Nagoya University Graduate School of Medicine, Nagoya, Aichi 466-8550, Japan. FAU - Sakamoto, Masayuki AU - Sakamoto M AD - Department of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan. FAU - Kawakami, Ryosuke AU - Kawakami R AD - Laboratory of Molecular and Cellular Biophysics, Research Institute for Electronic Science, Hokkaido University, Sapporo, Hokkaido 001-0020, Japan; Department of Molecular Medicine for Pathogenesis, Ehime University Graduate School of Medicine, Toon, Ehime 791-0295, Japan. FAU - Yamaguchi, Kazushi AU - Yamaguchi K AD - Laboratory of Molecular and Cellular Biophysics, Research Institute for Electronic Science, Hokkaido University, Sapporo, Hokkaido 001-0020, Japan. FAU - Otomo, Kouhei AU - Otomo K AD - Laboratory of Molecular and Cellular Biophysics, Research Institute for Electronic Science, Hokkaido University, Sapporo, Hokkaido 001-0020, Japan. FAU - Yokoyama, Hiroyuki AU - Yokoyama H AD - New Industry Creation Hatchery Center (NICHe), Tohoku University, Sendai, Miyagi 980-8579, Japan. FAU - Kim, Ryang AU - Kim R AD - Department of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan. FAU - Yokoyama, Tatsushi AU - Yokoyama T AD - Department of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan. FAU - Takemoto-Kimura, Sayaka AU - Takemoto-Kimura S AD - Department of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; Department of Neuroscience I, Research Institute of Environmental Medicine, Nagoya University, Nagoya, Aichi 464-8601, Japan; Department of Molecular/Cellular Neuroscience, Nagoya University Graduate School of Medicine, Nagoya, Aichi 466-8550, Japan; Precursory Research for Embryonic Science and Technology (PRESTO), Japan Science and Technology Agency, Saitama, Japan. FAU - Abe, Manabu AU - Abe M AD - Department of Cellular Neurobiology, Brain Research Institute, Niigata University, Niigata, Niigata 951-8585, Japan. FAU - Okamura, Michiko AU - Okamura M AD - Department of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan. FAU - Kondo, Yayoi AU - Kondo Y AD - Department of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan. FAU - Quirin, Sean AU - Quirin S AD - Department of Bioengineering, Stanford University School of Medicine, Stanford, CA 94305, USA. FAU - Ramakrishnan, Charu AU - Ramakrishnan C AD - Department of Bioengineering, Stanford University School of Medicine, Stanford, CA 94305, USA. FAU - Imamura, Takeshi AU - Imamura T AD - Department of Molecular Medicine for Pathogenesis, Ehime University Graduate School of Medicine, Toon, Ehime 791-0295, Japan. FAU - Sakimura, Kenji AU - Sakimura K AD - Department of Cellular Neurobiology, Brain Research Institute, Niigata University, Niigata, Niigata 951-8585, Japan. FAU - Nemoto, Tomomi AU - Nemoto T AD - Laboratory of Molecular and Cellular Biophysics, Research Institute for Electronic Science, Hokkaido University, Sapporo, Hokkaido 001-0020, Japan; Core Research for Evolutional Science and Technology (CREST), Japan Agency for Medical Research and Development, Tokyo, Japan. FAU - Kano, Masanobu AU - Kano M AD - Department of Neurophysiology, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; International Research Center for Neurointelligence, The University of Tokyo, Tokyo, Japan. FAU - Fujii, Hajime AU - Fujii H AD - Department of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan. FAU - Deisseroth, Karl AU - Deisseroth K AD - Department of Bioengineering, Stanford University School of Medicine, Stanford, CA 94305, USA. FAU - Kitamura, Kazuo AU - Kitamura K AD - Department of Neurophysiology, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; Department of Neurophysiology, Faculty of Medicine, University of Yamanashi, Chuo, Yamanashi 409-3898, Japan. FAU - Bito, Haruhiko AU - Bito H AD - Department of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; International Research Center for Neurointelligence, The University of Tokyo, Tokyo, Japan. Electronic address: hbito@m.u-tokyo.ac.jp. LA - eng GR - HHMI/Howard Hughes Medical Institute/United States PT - Journal Article PT - Research Support, Non-U.S. Gov't DEP - 20190509 PL - United States TA - Cell JT - Cell JID - 0413066 SB - IM MH - Action Potentials/*physiology MH - Animals MH - Axons/*metabolism MH - Cerebral Cortex/cytology/*metabolism MH - Female MH - Hippocampus/cytology/*metabolism MH - Interneurons/cytology/*metabolism MH - Mice MH - Mice, Transgenic MH - Pyramidal Cells/cytology/*metabolism MH - Rats MH - Rats, Sprague-Dawley OTO - NOTNLM OT - PV recording OT - XCaMP OT - ckkap sequence OT - genetically encoded calcium indicators OT - multiplex imaging OT - non-invasive hippocampal recording OT - paired pre- and post-synapse recording OT - two-photon Ca(2+) imaging EDAT- 2019/05/14 06:00 MHDA- 2020/02/12 06:00 CRDT- 2019/05/14 06:00 PHST- 2018/11/19 00:00 [received] PHST- 2019/02/28 00:00 [revised] PHST- 2019/04/02 00:00 [accepted] PHST- 2019/05/14 06:00 [pubmed] PHST- 2020/02/12 06:00 [medline] PHST- 2019/05/14 06:00 [entrez] AID - S0092-8674(19)30393-9 [pii] AID - 10.1016/j.cell.2019.04.007 [doi] PST - ppublish SO - Cell. 2019 May 16;177(5):1346-1360.e24. doi: 10.1016/j.cell.2019.04.007. Epub 2019 May 9.