{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,29]],"date-time":"2026-01-29T23:14:30Z","timestamp":1769728470660,"version":"3.49.0"},"reference-count":46,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2021,10,1]],"date-time":"2021-10-01T00:00:00Z","timestamp":1633046400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2021,10,1]],"date-time":"2021-10-01T00:00:00Z","timestamp":1633046400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2022,8,27]],"date-time":"2022-08-27T00:00:00Z","timestamp":1661558400000},"content-version":"am","delay-in-days":330,"URL":"http:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"}],"funder":[{"DOI":"10.13039\/501100002241","name":"Japan Science and Technology Agency","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100002241","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Neuroscience Research"],"published-print":{"date-parts":[[2021,10]]},"DOI":"10.1016\/j.neures.2021.02.001","type":"journal-article","created":{"date-parts":[[2021,2,17]],"date-time":"2021-02-17T04:55:33Z","timestamp":1613537733000},"page":"9-18","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":7,"special_numbering":"C","title":["Temporally multiplexed dual-plane imaging of neural activity with four-dimensional precision"],"prefix":"10.1016","volume":"171","author":[{"given":"Masanari","family":"Onda","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ryosuke F.","family":"Takeuchi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Keisuke","family":"Isobe","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0977-1317","authenticated-orcid":false,"given":"Toshiaki","family":"Suzuki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuji","family":"Masaki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nao","family":"Morimoto","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9078-1458","authenticated-orcid":false,"given":"Fumitaka","family":"Osakada","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"78","reference":[{"key":"10.1016\/j.neures.2021.02.001_bib0005","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.neuron.2009.06.014","article-title":"Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors","volume":"63","author":"Alexander","year":"2009","journal-title":"Neuron"},{"key":"10.1016\/j.neures.2021.02.001_bib0010","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1016\/j.neuron.2011.11.013","article-title":"Functional specialization of mouse higher visual cortical areas","volume":"72","author":"Andermann","year":"2011","journal-title":"Neuron"},{"key":"10.1016\/j.neures.2021.02.001_bib0015","doi-asserted-by":"crossref","first-page":"5163","DOI":"10.1073\/pnas.0700293104","article-title":"Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand","volume":"104","author":"Armbruster","year":"2007","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.neures.2021.02.001_bib0020","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/j.neuron.2019.05.014","article-title":"Widespread and highly correlated somato-dendritic activity in cortical layer 5 neurons","volume":"103","author":"Beaulieu-Laroche","year":"2019","journal-title":"Neuron"},{"key":"10.1016\/j.neures.2021.02.001_bib0025","doi-asserted-by":"crossref","first-page":"880","DOI":"10.1016\/j.optcom.2007.10.007","article-title":"An optical technique for remote focusing in microscopy","volume":"281","author":"Botcherby","year":"2008","journal-title":"Opt. Commun."},{"key":"10.1016\/j.neures.2021.02.001_bib0030","doi-asserted-by":"crossref","first-page":"1263","DOI":"10.1038\/nn1525","article-title":"Millisecond-timescale, genetically targeted optical control of neural activity","volume":"8","author":"Boyden","year":"2005","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.neures.2021.02.001_bib0035","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1163\/156856897X00357","article-title":"The psychophysics toolbox","volume":"10","author":"Brainard","year":"1997","journal-title":"Spat. Vis."},{"key":"10.1016\/j.neures.2021.02.001_bib0040","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1038\/nature12354","article-title":"Ultrasensitive fluorescent proteins for imaging neuronal activity","volume":"499","author":"Chen","year":"2013","journal-title":"Nature"},{"key":"10.1016\/j.neures.2021.02.001_bib0045","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1038\/nmeth.1552","article-title":"Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing","volume":"8","author":"Cheng","year":"2011","journal-title":"Nat. Methods"},{"key":"10.1016\/j.neures.2021.02.001_bib0050","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1038\/nn.2842","article-title":"Measuring and interpreting neuronal correlations","volume":"14","author":"Cohen","year":"2011","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.neures.2021.02.001_bib0055","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1038\/76656","article-title":"Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons","volume":"3","author":"Dantzker","year":"2000","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.neures.2021.02.001_bib0060","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1038\/nmeth989","article-title":"Imaging cellular network dynamics in three dimensions using fast 3D laser scanning","volume":"4","author":"G\u00f6bel","year":"2007","journal-title":"Nat. Methods"},{"key":"10.1016\/j.neures.2021.02.001_bib0065","first-page":"880","article-title":"Arbitrary-scan imaging for two-photon microscopy","volume":"2","author":"Grewe","year":"2011","journal-title":"Biomed. Opt. Express"},{"key":"10.1016\/j.neures.2021.02.001_bib0070","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1364\/OL.33.000156","article-title":"Efficient subpixel image registration algorithms","volume":"33","author":"Guizar-Sicairos","year":"2008","journal-title":"Opt. Lett."},{"key":"10.1016\/j.neures.2021.02.001_bib0075","doi-asserted-by":"crossref","first-page":"2229","DOI":"10.1016\/j.celrep.2019.04.075","article-title":"Two-color volumetric imaging of neuronal activity of cortical columns","volume":"27","author":"Han","year":"2019","journal-title":"Cell Rep."},{"key":"10.1016\/j.neures.2021.02.001_bib0080","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1038\/nature12654","article-title":"Cortical connectivity and sensory coding","volume":"503","author":"Harris","year":"2013","journal-title":"Nature"},{"key":"10.1016\/j.neures.2021.02.001_bib0085","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1038\/nature23019","article-title":"Synaptic organization of visual space in primary visual cortex","volume":"547","author":"Iacaruso","year":"2017","journal-title":"Nature"},{"key":"10.1016\/j.neures.2021.02.001_bib0090","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1038\/nbt.4184","article-title":"A genetically encoded fluorescent acetylcholine indicator for in vitro and in vivo studies","volume":"36","author":"Jing","year":"2018","journal-title":"Nat. Biotechnol."},{"key":"10.1016\/j.neures.2021.02.001_bib0095","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1038\/nprot.2016.158","article-title":"Automated identification of mouse visual areas with intrinsic signal imaging","volume":"12","author":"Juavinett","year":"2017","journal-title":"Nat. Protoc."},{"key":"10.1016\/j.neures.2021.02.001_bib0100","doi-asserted-by":"crossref","first-page":"1472","DOI":"10.1038\/nn1798","article-title":"Cortical feed-forward networks for binding different streams of sensory information","volume":"9","author":"Kampa","year":"2006","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.neures.2021.02.001_bib0105","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.1016\/j.neuron.2018.10.023","article-title":"Segregated subnetworks of intracortical projection neurons in primary visual cortex","volume":"100","author":"Kim","year":"2018","journal-title":"Neuron"},{"key":"10.1016\/j.neures.2021.02.001_bib0110","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.26839","article-title":"Two-photon calcium imaging of medial prefrontal cortex and hippocampus without cortical invasion","volume":"6","author":"Kondo","year":"2017","journal-title":"Elife"},{"key":"10.1016\/j.neures.2021.02.001_bib0115","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1038\/nn.4516","article-title":"Video-rate volumetric functional imaging of the brain at synaptic resolution","volume":"20","author":"Lu","year":"2017","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.neures.2021.02.001_bib0120","doi-asserted-by":"crossref","first-page":"1040","DOI":"10.1016\/j.neuron.2011.12.004","article-title":"Functional specialization of seven mouse visual cortical areas","volume":"4","author":"Marshel","year":"2011","journal-title":"Neuron"},{"key":"10.1016\/j.neures.2021.02.001_bib0125","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fncir.2014.00092","article-title":"Robust quantification of orientation selectivity and direction selectivity","volume":"8","author":"Mazurek","year":"2014","journal-title":"Front. Neural Circuits"},{"key":"10.1016\/j.neures.2021.02.001_bib0130","doi-asserted-by":"crossref","first-page":"5","DOI":"10.3389\/neuro.04.005.2008","article-title":"SLM microscopy: scanless two-photon imaging and photostimulation using spatial light modulators","volume":"2","author":"Nikolenko","year":"2008","journal-title":"Front. Neural Circuits"},{"key":"10.1016\/j.neures.2021.02.001_bib0135","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1038\/nature03274","article-title":"Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex","volume":"433","author":"Ohki","year":"2005","journal-title":"Nature"},{"key":"10.1016\/j.neures.2021.02.001_bib0140","doi-asserted-by":"crossref","first-page":"1583","DOI":"10.1038\/nprot.2013.094","article-title":"Design and generation of recombinant rabies virus vectors","volume":"8","author":"Osakada","year":"2013","journal-title":"Nat. Protoc."},{"key":"10.1016\/j.neures.2021.02.001_bib0145","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1016\/j.neuron.2011.07.005","article-title":"New rabies virus variants for monitoring and manipulating activity and gene expression in defined neural circuits","volume":"71","author":"Osakada","year":"2011","journal-title":"Neuron"},{"key":"10.1016\/j.neures.2021.02.001_bib0150","doi-asserted-by":"crossref","first-page":"1202","DOI":"10.1038\/nmeth.2249","article-title":"Two-photon optogenetics of dendritic spines and neural circuits","volume":"9","author":"Packer","year":"2012","journal-title":"Nat. Methods"},{"key":"10.1016\/j.neures.2021.02.001_bib0155","doi-asserted-by":"crossref","first-page":"1420","DOI":"10.1126\/science.aat4422","article-title":"Ultrafast neuronal imaging of dopamine dynamics with designed genetically encoded sensors","volume":"360","author":"Patriarchi","year":"2018","journal-title":"Science"},{"key":"10.1016\/j.neures.2021.02.001_bib0160","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1038\/nature13235","article-title":"Emergence of reproducible spatiotemporal activity during motor learning","volume":"510","author":"Peters","year":"2014","journal-title":"Nature"},{"key":"10.1016\/j.neures.2021.02.001_bib0165","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.neuron.2015.11.037","article-title":"Simultaneous denoising, deconvolution, and demixing of calcium imaging data","volume":"89","author":"Pnevmatikakis","year":"2016","journal-title":"Neuron"},{"key":"10.1016\/j.neures.2021.02.001_bib0170","doi-asserted-by":"crossref","first-page":"29","DOI":"10.3389\/fncir.2014.00029","article-title":"Simultaneous imaging of neural activity in three dimensions","volume":"8","author":"Quirin","year":"2014","journal-title":"Front. Neural Circuits"},{"key":"10.1016\/j.neures.2021.02.001_bib0175","doi-asserted-by":"crossref","first-page":"5639","DOI":"10.1523\/JNEUROSCI.22-13-05639.2002","article-title":"Orientation selectivity in macaque V1: diversity and laminar dependence","volume":"22","author":"Ringach","year":"2002","journal-title":"J. Neurosci."},{"key":"10.1016\/j.neures.2021.02.001_bib0180","doi-asserted-by":"crossref","first-page":"1127","DOI":"10.1016\/j.neuron.2017.10.017","article-title":"Local order within global disorder: synaptic architecture of visual space","volume":"96","author":"Scholl","year":"2017","journal-title":"Neuron"},{"key":"10.1016\/j.neures.2021.02.001_bib0185","doi-asserted-by":"crossref","first-page":"1","DOI":"10.7554\/eLife.14472","article-title":"A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging","volume":"5","author":"Sofroniew","year":"2016","journal-title":"Elife"},{"key":"10.1016\/j.neures.2021.02.001_bib0190","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1038\/nbt.3594","article-title":"Wide field-of-view, multi-region, two-photon imaging of neuronal activity in the mammalian brain","volume":"34","author":"Stirman","year":"2016","journal-title":"Nat. Biotechnol."},{"key":"10.1016\/j.neures.2021.02.001_bib0195","doi-asserted-by":"crossref","first-page":"7319","DOI":"10.1073\/pnas.1232232100","article-title":"In vivo two-photon calcium imaging of neuronal networks","volume":"100","author":"Stosiek","year":"2003","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.neures.2021.02.001_bib0200","doi-asserted-by":"crossref","first-page":"77","DOI":"10.3389\/fncir.2019.00077","article-title":"Multiplex neural circuit tracing with G-Deleted rabies viral vectors","volume":"13","author":"Suzuki","year":"2020","journal-title":"Front. Neural Circuits"},{"key":"10.1016\/j.neures.2021.02.001_bib0205","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1038\/s41586-018-0654-5","article-title":"Shared and distinct transcriptomic cell types across neocortical areas","volume":"563","author":"Tasic","year":"2018","journal-title":"Nature"},{"key":"10.1016\/j.neures.2021.02.001_bib0210","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-018-06058-8","article-title":"Super-wide-field two-photon imaging with a micro-optical device moving in post-objective space","volume":"9","author":"Terada","year":"2018","journal-title":"Nat. Commun."},{"key":"10.1016\/j.neures.2021.02.001_bib0215","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.neuron.2019.10.016","article-title":"Somatic and dendritic encoding of spatial variables in retrosplenial cortex differs during 2D navigation","volume":"105","author":"Voigts","year":"2020","journal-title":"Neuron"},{"key":"10.1016\/j.neures.2021.02.001_bib0220","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/j.neuron.2015.12.012","article-title":"Simultaneous multi-plane imaging of neural circuits","volume":"89","author":"Yang","year":"2016","journal-title":"Neuron"},{"key":"10.1016\/j.neures.2021.02.001_bib0225","doi-asserted-by":"crossref","first-page":"868","DOI":"10.1038\/nature03252","article-title":"Excitatory cortical neurons from fine-scale functional networks","volume":"5","author":"Yoshimura","year":"2005","journal-title":"Nature"},{"key":"10.1016\/j.neures.2021.02.001_bib0230","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/0896-6273(91)90243-S","article-title":"Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters","volume":"6","author":"Yuste","year":"1991","journal-title":"Neuron"}],"container-title":["Neuroscience Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0168010221000407?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0168010221000407?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,29]],"date-time":"2025-09-29T10:30:36Z","timestamp":1759141836000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0168010221000407"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10]]},"references-count":46,"alternative-id":["S0168010221000407"],"URL":"https:\/\/doi.org\/10.1016\/j.neures.2021.02.001","relation":{},"ISSN":["0168-0102"],"issn-type":[{"value":"0168-0102","type":"print"}],"subject":[],"published":{"date-parts":[[2021,10]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Temporally multiplexed dual-plane imaging of neural activity with four-dimensional precision","name":"articletitle","label":"Article Title"},{"value":"Neuroscience Research","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.neures.2021.02.001","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2021 Elsevier B.V. and Japan Neuroscience Society. All rights reserved.","name":"copyright","label":"Copyright"}]}}