Evidence map›Paper›PMID 23459413›Full record

ArticleFrontiers in molecular neuroscience2013

Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics.

Jasper Akerboom, Nicole Carreras Calderón, Lin Tian, Sebastian Wabnig, Matthias Prigge, Johan Tolö, Andrew Gordus, Michael B Orger, Kristen E Severi, John J Macklin and 16 more

Abstract read
In one paragraph

Article in Frontiers in molecular neuroscience, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 418 papers.

0numbers the graph read from it
0cells of the map it votes in
418citing papers in PubMed
–field-weighted citation impact
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

418 citing papers in PubMed.

  1. Review
  2. Review
  3. Host-derived stimuli alter intracellular calcium levels inApplied and environmental microbiology · 2026
    Article
  4. Restoration of mitochondrial CaJournal of molecular and cellular cardiology · 2026
    Article
  5. Review
  6. Article
  7. Article
  8. Inorganic phosphate and the rapid mobilization of metabolic energy in neurons.Proceedings of the National Academy of Sciences of the United States of America · 2026
    Article
  9. Subcellular calcium dynamics and organelle perturbations in resistosome-mediated cell death.Proceedings of the National Academy of Sciences of the United States of America · 2026
    Article
  10. Article
  11. Article
  12. Article
  13. Review
  14. Article
  15. A dual-color miniature endoscope for calcium imaging in behaving mice.bioRxiv : the preprint server for biology · 2026
    Article
  16. Article
  17. Astrocyte CBJournal of neuroinflammation · 2026
    Article
  18. Imaging CaMethods in molecular biology (Clifton, N.J.) · 2026
    Article
  19. Review
  20. Article

358 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

26 authors.

Jasper AkerboomJanelia Farm Research Campus, Howard Hughes Medical Institute Ashburn, VA, USA.
Nicole Carreras Calderón
Lin Tian
Sebastian Wabnig
Matthias Prigge
Johan Tolö
Andrew Gordus
Michael B Orger
Kristen E Severi
John J Macklin
Ronak Patel
Stefan R Pulver
Trevor J Wardill
Elisabeth Fischer
Christina Schüler
Tsai-Wen Chen
Karen S Sarkisyan
Jonathan S Marvin
Cornelia I Bargmann
Douglas S Kim
Sebastian Kügler
Leon Lagnado
Peter Hegemann
Alexander Gottschalk
Eric R Schreiter
Loren L Looger

Funding

Medical Research Council MC_U105178794
6 · The paper itself

Abstract

Genetically encoded calcium indicators (GECIs) are powerful tools for systems neuroscience. Here we describe red, single-wavelength GECIs, "RCaMPs," engineered from circular permutation of the thermostable red fluorescent protein mRuby. High-resolution crystal structures of mRuby, the red sensor RCaMP, and the recently published red GECI R-GECO1 give insight into the chromophore environments of the Ca(2+)-bound state of the sensors and the engineered protein domain interfaces of the different indicators. We characterized the biophysical properties and performance of RCaMP sensors in vitro and in vivo in Caenorhabditis elegans, Drosophila larvae, and larval zebrafish. Further, we demonstrate 2-color calcium imaging both within the same cell (registering mitochondrial and somatic [Ca(2+)]) and between two populations of cells: neurons and astrocytes. Finally, we perform integrated optogenetics experiments, wherein neural activation via channelrhodopsin-2 (ChR2) or a red-shifted variant, and activity imaging via RCaMP or GCaMP, are conducted simultaneously, with the ChR2/RCaMP pair providing independently addressable spectral channels. Using this paradigm, we measure calcium responses of naturalistic and ChR2-evoked muscle contractions in vivo in crawling C. elegans. We systematically compare the RCaMP sensors to R-GECO1, in terms of action potential-evoked fluorescence increases in neurons, photobleaching, and photoswitching. R-GECO1 displays higher Ca(2+) affinity and larger dynamic range than RCaMP, but exhibits significant photoactivation with blue and green light, suggesting that integrated channelrhodopsin-based optogenetics using R-GECO1 may be subject to artifact. Finally, we create and test blue, cyan, and yellow variants engineered from GCaMP by rational design. This engineered set of chromatic variants facilitates new experiments in functional imaging and optogenetics.

Indexed as

calcium imaginggenetically encoded calcium indicatormulti-color imagingoptogeneticsprotein engineering

Identifiers

PMID23459413
PMCPMC3586699

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.