{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,20]],"date-time":"2026-04-20T19:00:30Z","timestamp":1776711630219,"version":"3.51.2"},"reference-count":40,"publisher":"Public Library of Science (PLoS)","issue":"9","license":[{"start":{"date-parts":[[2022,9,28]],"date-time":"2022-09-28T00:00:00Z","timestamp":1664323200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["DP2-NS116768"],"award-info":[{"award-number":["DP2-NS116768"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["1845137"],"award-info":[{"award-number":["1845137"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000893","name":"Simons Foundation","doi-asserted-by":"publisher","award":["543003"],"award-info":[{"award-number":["543003"]}],"id":[{"id":"10.13039\/100000893","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000893","name":"Simons Foundation","doi-asserted-by":"publisher","award":["543003"],"award-info":[{"award-number":["543003"]}],"id":[{"id":"10.13039\/100000893","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Imaging neural activity in a behaving animal presents unique challenges in part because motion from an animal\u2019s movement creates artifacts in fluorescence intensity time-series that are difficult to distinguish from neural signals of interest. One approach to mitigating these artifacts is to image two channels simultaneously: one that captures an activity-dependent fluorophore, such as GCaMP, and another that captures an activity-independent fluorophore such as RFP. Because the activity-independent channel contains the same motion artifacts as the activity-dependent channel, but no neural signals, the two together can be used to identify and remove the artifacts. However, existing approaches for this correction, such as taking the ratio of the two channels, do not account for channel-independent noise in the measured fluorescence. Here, we present Two-channel Motion Artifact Correction (TMAC), a method which seeks to remove artifacts by specifying a generative model of the two channel fluorescence that incorporates motion artifact, neural activity, and noise. We use Bayesian inference to infer latent neural activity under this model, thus reducing the motion artifact present in the measured fluorescence traces. We further present a novel method for evaluating ground-truth performance of motion correction algorithms by comparing the decodability of behavior from two types of neural recordings; a recording that had both an activity-dependent fluorophore and an activity-independent fluorophore (GCaMP and RFP) and a recording where both fluorophores were activity-independent (GFP and RFP). A successful motion correction method should decode behavior from the first type of recording, but not the second. We use this metric to systematically compare five models for removing motion artifacts from fluorescent time traces. We decode locomotion from a GCaMP expressing animal 20x more accurately on average than from control when using TMAC inferred activity and outperforms all other methods of motion correction tested, the best of which were ~8x more accurate than control.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010421","type":"journal-article","created":{"date-parts":[[2022,9,28]],"date-time":"2022-09-28T18:34:39Z","timestamp":1664390079000},"page":"e1010421","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":22,"title":["Correcting motion induced fluorescence artifacts in two-channel neural imaging"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9458-0629","authenticated-orcid":true,"given":"Matthew S.","family":"Creamer","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8792-4625","authenticated-orcid":true,"given":"Kevin S.","family":"Chen","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5362-5093","authenticated-orcid":true,"given":"Andrew M.","family":"Leifer","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3638-8831","authenticated-orcid":true,"given":"Jonathan W.","family":"Pillow","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2022,9,28]]},"reference":[{"key":"pcbi.1010421.ref001","doi-asserted-by":"crossref","first-page":"862","DOI":"10.1016\/j.neuron.2012.02.011","article-title":"Imaging Calcium in Neurons","volume":"73","author":"C Grienberger","year":"2012","journal-title":"Neuron"},{"key":"pcbi.1010421.ref002","first-page":"11","article-title":"Large-scale neural recordings call for new insights to link brain and behavior","volume":"25","author":"AE Urai","year":"2022","journal-title":"Nature Neuroscience 2022 25:1"},{"key":"pcbi.1010421.ref003","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1016\/j.neuron.2009.08.009","article-title":"Automated Analysis of Cellular Signals from Large-Scale Calcium Imaging Data","volume":"63","author":"EA Mukamel","year":"2009","journal-title":"Neuron"},{"key":"pcbi.1010421.ref004","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":"EA Pnevmatikakis","year":"2016","journal-title":"Neuron"},{"key":"pcbi.1010421.ref005","first-page":"14","article-title":"Demixing Calcium Imaging Data in C. elegans via Deformable Non-negative Matrix Factorization","volume":"12265","author":"A Nejatbakhsh","year":"2020","journal-title":"Lecture Notes in Computer Science (including subseries Lecture Notes in Artificial Intelligence and Lecture Notes in Bioinformatics)"},{"key":"pcbi.1010421.ref006","doi-asserted-by":"crossref","first-page":"e1005423","DOI":"10.1371\/journal.pcbi.1005423","article-title":"Fast online deconvolution of calcium imaging data","volume":"13","author":"J Friedrich","year":"2017","journal-title":"PLOS Computational Biology"},{"key":"pcbi.1010421.ref007","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1016\/j.neuron.2016.12.041","article-title":"Neuroscience Needs Behavior: Correcting a Reductionist Bias","volume":"93","author":"JW Krakauer","year":"2017","journal-title":"Neuron"},{"key":"pcbi.1010421.ref008","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.neuron.2019.09.038","article-title":"Computational Neuroethology: A Call to Action","volume":"104","author":"SR Datta","year":"2019","journal-title":"Neuron"},{"key":"pcbi.1010421.ref009","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.neuron.2007.08.003","article-title":"Imaging Large-Scale Neural Activity with Cellular Resolution in Awake","volume":"56","author":"DA Dombeck","year":"2007","journal-title":"Mobile Mice. Neuron"},{"key":"pcbi.1010421.ref010","doi-asserted-by":"crossref","first-page":"6083","DOI":"10.1523\/JNEUROSCI.1032-07.2007","article-title":"Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients","volume":"27","author":"DA Clark","year":"2007","journal-title":"J Neurosci"},{"key":"pcbi.1010421.ref011","article-title":"Decoding locomotion from population neural activity in moving C","volume":"10","author":"KM Hallinen","year":"2021","journal-title":"Elegans. Elife"},{"key":"pcbi.1010421.ref012","article-title":"EMC2: A versatile algorithm for robust tracking of calcium dynamics from individual neurons in behaving animals","author":"T Lagache","year":"2021","journal-title":"bioRxiv"},{"key":"pcbi.1010421.ref013","article-title":"Fast deep neural correspondence for tracking and identifying neurons in C","volume":"10","author":"X Yu","year":"2021","journal-title":"elegans using semi-synthetic training. Elife"},{"key":"pcbi.1010421.ref014","doi-asserted-by":"crossref","first-page":"e1005517","DOI":"10.1371\/journal.pcbi.1005517","article-title":"Automatically tracking neurons in a moving and deforming brain","volume":"13","author":"JP Nguyen","year":"2017","journal-title":"PLOS Computational Biology"},{"key":"pcbi.1010421.ref015","doi-asserted-by":"crossref","first-page":"1372","DOI":"10.1109\/TIP.2005.852787","article-title":"Automatic tracking of individual fluorescence particles: Application to the study of chromosome dynamics","volume":"14","author":"D Sage","year":"2005","journal-title":"IEEE Transactions on Image Processing"},{"key":"pcbi.1010421.ref016","doi-asserted-by":"crossref","first-page":"1384","DOI":"10.1109\/TIP.2005.852794","article-title":"Single quantum dot tracking based on perceptual grouping using minimal paths in a spatiotemporal volume","volume":"14","author":"S Bonneau","year":"2005","journal-title":"IEEE Transactions on Image Processing"},{"key":"pcbi.1010421.ref017","doi-asserted-by":"crossref","first-page":"1","DOI":"10.7554\/eLife.60321","article-title":"Graphical-model framework for automated annotation of cell identities in dense cellular images","volume":"10","author":"S Chaudhary","year":"2021","journal-title":"Elife"},{"key":"pcbi.1010421.ref018","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/j.jsb.2005.06.002","article-title":"Feature point tracking and trajectory analysis for video imaging in cell biology","volume":"151","author":"IF Sbalzarini","year":"2005","journal-title":"Journal of Structural Biology"},{"key":"pcbi.1010421.ref019","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1038\/nmeth.1237","article-title":"Robust single-particle tracking in live-cell time-lapse sequences","volume":"5","author":"K Jaqaman","year":"2008","journal-title":"Nature Methods"},{"key":"pcbi.1010421.ref020","doi-asserted-by":"crossref","first-page":"2736","DOI":"10.1109\/TPAMI.2013.97","article-title":"Multiple hypothesis tracking for cluttered biological image sequences","volume":"35","author":"N Chenouard","year":"2013","journal-title":"IEEE Transactions on Pattern Analysis and Machine Intelligence"},{"key":"pcbi.1010421.ref021","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.jneumeth.2017.07.031","article-title":"NoRMCorre: An online algorithm for piecewise rigid motion correction of calcium imaging data","volume":"291","author":"EA Pnevmatikakis","year":"2017","journal-title":"Journal of Neuroscience Methods"},{"key":"pcbi.1010421.ref022","doi-asserted-by":"crossref","first-page":"E1082","DOI":"10.1073\/pnas.1507109113","article-title":"Pan-neuronal imaging in roaming Caenorhabditis elegans","volume":"113","author":"V Venkatachalam","year":"2016","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1010421.ref023","doi-asserted-by":"crossref","first-page":"E1074","DOI":"10.1073\/pnas.1507110112","article-title":"Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans","volume":"113","author":"JP Nguyen","year":"2016","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1010421.ref024","first-page":"1","article-title":"Whole-Body Imaging of Neural and Muscle Activity during Behavior in Hydra vulgaris: Effect of Osmolarity on Contraction Bursts","volume":"7","author":"W Yamamoto","year":"2020","journal-title":"eN?euro"},{"key":"pcbi.1010421.ref025","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1016\/j.cub.2019.01.060","article-title":"Characterization of Proprioceptive System Dynamics in Behaving Drosophila Larvae Using High-Speed Volumetric Microscopy","volume":"29","author":"RD Vaadia","year":"2019","journal-title":"Current Biology"},{"key":"pcbi.1010421.ref026","doi-asserted-by":"crossref","first-page":"1371","DOI":"10.1016\/j.celrep.2018.10.013","article-title":"Recording Neural Activity in Unrestrained Animals with Three-Dimensional Tracking Two-Photon Microscopy","volume":"25","author":"D Karagyozov","year":"2018","journal-title":"Cell Reports"},{"key":"pcbi.1010421.ref027","first-page":"1107","article-title":"Pan-neuronal calcium imaging with cellular resolution in freely swimming zebrafish","volume":"14","author":"DH Kim","year":"2017","journal-title":"Nature Methods 2017 14:11"},{"key":"pcbi.1010421.ref028","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.28158","article-title":"Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (Danio rerio)","volume":"6","author":"L Cong","year":"2017","journal-title":"Elife"},{"key":"pcbi.1010421.ref029","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/S0896-6273(00)81196-4","article-title":"Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans","volume":"26","author":"R Kerr","year":"2000","journal-title":"Neuron"},{"key":"pcbi.1010421.ref030","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1038\/nature12354","article-title":"Ultrasensitive fluorescent proteins for imaging neuronal activity","volume":"499","author":"T-W Chen","year":"2013","journal-title":"Nature"},{"key":"pcbi.1010421.ref031","doi-asserted-by":"crossref","DOI":"10.3389\/fncir.2014.00028","article-title":"Simultaneous optogenetic manipulation and calcium imaging in freely moving C. elegans","volume":"8","author":"FB Shipley","year":"2014","journal-title":"Front Neural Circuits"},{"key":"pcbi.1010421.ref032","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1016\/j.cell.2015.09.034","article-title":"Global Brain Dynamics Embed the Motor Command Sequence of Caenorhabditis elegans","volume":"163","author":"S Kato","year":"2015","journal-title":"Cell"},{"key":"pcbi.1010421.ref033","author":"Y Wu","year":"2021","journal-title":"Rapid detection and recognition of whole brain activity in a freely behaving Caenorhabditis elegans"},{"key":"pcbi.1010421.ref034","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1152\/ajpheart.00574.2003","article-title":"Correction of motion artifact in transmembrane voltage-sensitive fluorescent dye emission in hearts","volume":"287","author":"DCS Tai","year":"2004","journal-title":"American Journal of Physiology\u2014Heart and Circulatory Physiology"},{"key":"pcbi.1010421.ref035","article-title":"Scalable Bayesian inference for high-dimensional neural receptive fields","volume":"212217","author":"MC Aoi","year":"2017","journal-title":"bioRxiv"},{"key":"pcbi.1010421.ref036","article-title":"Predicting natural behavior from whole-brain neural dynamics","volume":"445643","author":"M Scholz","year":"2018","journal-title":"bioRxiv"},{"key":"pcbi.1010421.ref037","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1016\/j.celrep.2018.12.088","article-title":"Comparative Evaluation of Genetically Encoded Voltage Indicators","volume":"26","author":"Y Bando","year":"2019","journal-title":"Cell Reports"},{"key":"pcbi.1010421.ref038","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1016\/j.cell.2015.07.014","article-title":"Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits","volume":"162","author":"TN Lerner","year":"2015","journal-title":"Cell"},{"key":"pcbi.1010421.ref039","first-page":"1","article-title":"Delineation of an insula-BNST circuit engaged by struggling behavior that regulates avoidance in mice","volume":"12","author":"JR Luchsinger","year":"2021","journal-title":"Nature Communications 2021 12:1"},{"key":"pcbi.1010421.ref040","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1038\/s41593-019-0502-4","article-title":"Single-trial neural dynamics are dominated by richly varied movements","volume":"22","author":"S Musall","year":"2019","journal-title":"Nature Neuroscience"}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010421","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,28]],"date-time":"2022-09-28T18:35:21Z","timestamp":1664390121000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010421"}},"subtitle":[],"editor":[{"given":"Matthieu","family":"Louis","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2022,9,28]]},"references-count":40,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9,28]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1010421","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,28]]}}}