TY - JOUR
T1 - Rational Engineering of XCaMPs, a Multicolor GECI Suite for In Vivo Imaging of Complex Brain Circuit Dynamics
AU - Inoue, Masatoshi
AU - Takeuchi, Atsuya
AU - Manita, Satoshi
AU - Horigane, Shin ichiro
AU - Sakamoto, Masayuki
AU - Kawakami, Ryosuke
AU - Yamaguchi, Kazushi
AU - Otomo, Kouhei
AU - Yokoyama, Hiroyuki
AU - Kim, Ryang
AU - Yokoyama, Tatsushi
AU - Takemoto-Kimura, Sayaka
AU - Abe, Manabu
AU - Okamura, Michiko
AU - Kondo, Yayoi
AU - Quirin, Sean
AU - Ramakrishnan, Charu
AU - Imamura, Takeshi
AU - Sakimura, Kenji
AU - Nemoto, Tomomi
AU - Kano, Masanobu
AU - Fujii, Hajime
AU - Deisseroth, Karl
AU - Kitamura, Kazuo
AU - Bito, Haruhiko
N1 - Funding Information:
This work was supported in part by KAKENHI Grants-in-Aid (Brain Information Dynamics, Resonance Bio, CBSN, and PAAMS from MEXT ; TOKUBETSU SUISHIN, KIBAN, WAKATE, and HOUGA from JSPS ( 15H02358 , 16H06276 , 17H06308 , 17H06312 , and 17K19442 to H.B.; 17H06313 and 17H03543 to K.K.; 15K18372 to M.I.; 16H04670 to S.T.-K.; 17K14930 to R.K.; 17K13270 to H.F.; 17H00597 to M.O.; 18J12617 to T.Y.; 17H05941 and 18K19493 to M.S.; 15H05952 to T.I.; 15H05953 to T.N.; 25000015 to K.M.; 16H04650 and 17K19444 to K.S.; Brain/MINDS (to H.B., K.K., T.N., H.Y., and M.S.), SRPBS (to M.K.), and a “Five-star Alliance” in “NJRC Mater. & Dev.” (to T.N. and H.Y.) from AMED ; and grants from HHMI (to K.D.), the Tokyo Society of Medical Sciences (to M.I. and M.S.), Narishige Neuroscience Research Foundation (to S.M.), Grant for Young Researcher from Yamanashi Prefecture (to S.M.), Takeda Science Foundation (to S.M., M.S., S.T.-K., K.K., and H.B.), the Kanae Foundation (to M.I.), the Uehara Foundation (to M.I., K.K., and H.B.), the Frontier Brain Research Grant from University of Yamanashi (to K.K.), Hitachi Global Foundation (H.B.), and Nakatani Foundation (to H.B.). T.Y. was supported by a WINGS-LST Program and a JSPS predoctoral fellowship.
Publisher Copyright:
© 2019 Elsevier Inc.
Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.
PY - 2019/5/16
Y1 - 2019/5/16
N2 - 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: Quadricolor suite of genetically encoded calcium indicators for multiplex recording in the brain.
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: Quadricolor suite of genetically encoded calcium indicators for multiplex recording in the brain.
KW - PV recording
KW - XCaMP
KW - ckkap sequence
KW - genetically encoded calcium indicators
KW - multiplex imaging
KW - non-invasive hippocampal recording
KW - paired pre- and post-synapse recording
KW - two-photon Ca imaging
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U2 - 10.1016/j.cell.2019.04.007
DO - 10.1016/j.cell.2019.04.007
M3 - Article
C2 - 31080068
AN - SCOPUS:85065519867
VL - 177
SP - 1346-1360.e24
JO - Cell
JF - Cell
SN - 0092-8674
IS - 5
ER -