Photon shot noise limits on optical detection of neuronal spikes and estimation of spike timing

Biophysical Journal
Brian A WiltMark J Schnitzer

Abstract

Optical approaches for tracking neural dynamics are of widespread interest, but a theoretical framework quantifying the physical limits of these techniques has been lacking. We formulate such a framework by using signal detection and estimation theory to obtain physical bounds on the detection of neural spikes and the estimation of their occurrence times as set by photon counting statistics (shot noise). These bounds are succinctly expressed via a discriminability index that depends on the kinetics of the optical indicator and the relative fluxes of signal and background photons. This approach facilitates quantitative evaluations of different indicators, detector technologies, and data analyses. Our treatment also provides optimal filtering techniques for optical detection of spikes. We compare various types of Ca(2+) indicators and show that background photons are a chief impediment to voltage sensing. Thus, voltage indicators that change color in response to membrane depolarization may offer a key advantage over those that change intensity. We also examine fluorescence resonance energy transfer indicators and identify the regimes in which the widely used ratiometric analysis of signals is substantially suboptimal. Overall, by...Continue Reading

References

Jan 1, 1974·The Journal of Membrane Biology·L B CohenC H Wang
Mar 1, 1997·Biophysical Journal·Fritjof HelmchenB Sakmann
Apr 1, 1999·Annual Review of Physiology·W M Usrey, R C Reid
Apr 1, 1999·Annual Review of Physiology·E Covey, J H Casseday
Apr 1, 1999·Annual Review of Physiology·L O Trussell
Apr 1, 1999·Annual Review of Physiology·D Oertel
Feb 8, 2002·Neuron·György Buzsáki
Feb 12, 2004·Science's STKE : Signal Transduction Knowledge Environment·Ryohei YasudaKarel Svoboda
Sep 15, 2005·Proceedings of the National Academy of Sciences of the United States of America·Jason N D KerrFritjof Helmchen
Jan 18, 2006·Journal of Biomedical Optics·Gaddum Duemani Reddy, Peter Saggau
Feb 21, 2006·Proceedings of the National Academy of Sciences of the United States of America·L SacconiW W Webb
Apr 25, 2008·Nature Neuroscience·Gaddum Duemani ReddyPeter Saggau
Jun 17, 2008·Nature Neuroscience·David S GreenbergJason N D Kerr
Jul 4, 2008·Journal of Neurophysiology·Takuya SasakiYuji Ikegaya
Jul 18, 2008·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Thomas HendelDierk F Reiff
Oct 7, 2008·Nature Methods·Benjamin A FlusbergMark J Schnitzer
Oct 23, 2008·Brain Cell Biology·S Andrew HiresLoren L Looger
Jan 23, 2009·Nature Methods·Damian J WallaceMazahir T Hasan
Jan 23, 2009·Nature Methods·Marco MankOliver Griesbeck
Apr 15, 2009·Optics Express·Christoph J EngelbrechtFritjof Helmchen
Jun 27, 2009·Annual Review of Neuroscience·Brian A WiltMark J Schnitzer
Jul 22, 2009·Biophysical Journal·Joshua T VogelsteinLiam Paninski
Sep 26, 2009·Neuron·Eran A MukamelMark J Schnitzer
Dec 4, 2009·Journal of Neurophysiology·Sébastien JouclaChristophe Pouzat
Feb 17, 2010·The Journal of Physiology·Knut HolthoffArthur Konnerth
Jun 18, 2010·Journal of Neurophysiology·Joshua T VogelsteinLiam Paninski
Jan 12, 2011·Neuron·Darcy S PeterkaRafael Yuste
Jul 20, 2011·Biophysical Journal·Corey D AckerLeslie M Loew
Sep 13, 2011·Nature Methods·Kunal K GhoshMark J Schnitzer

Citations

Mar 22, 2013·ACS Nano·A Paul AlivisatosXiaowei Zhuang
Jul 11, 2013·PloS One·Yiyang GongMark J Schnitzer
Apr 24, 2014·Nature Communications·Yiyang GongMark J Schnitzer
Jul 10, 2013·The Journal of Physiology·Hidekazu TsutsuiYasushi Okamura
Jul 6, 2015·Current Opinion in Chemical Biology·Yiyang Gong
Apr 17, 2015·Current Opinion in Neurobiology·Simon PeronKarel Svoboda
Nov 5, 2013·Neuron·Karl Deisseroth, Mark J Schnitzer
Apr 10, 2015·Neuron·Elizabeth J O HamelMark J Schnitzer
Apr 10, 2015·Neuron·Logan GrosenickKarl Deisseroth
Dec 6, 2014·Frontiers in Molecular Neuroscience·Tobias RoseOliver Griesbeck
May 7, 2016·Neuron·Lucas TheisMatthias Bethge
Aug 23, 2016·Frontiers in Synaptic Neuroscience·Ryuichi NakajimaBradley J Baker
Dec 24, 2016·Cell Reports·Tony Hyun KimMark J Schnitzer
Feb 20, 2016·PLoS Computational Biology·Vahid RahmatiStefan J Kiebel
May 1, 2016·Trends in Neurosciences·Douglas StoraceBradley J Baker
Nov 14, 2017·Journal of Neural Engineering·Renaud SchuckSimon R Schultz
May 22, 2018·PLoS Computational Biology·Philipp BerensMatthias Bethge
Nov 14, 2018·Nature Methods·Madhuvanthi KannanVincent A Pieribone
Mar 2, 2018·Nature Communications·Cheng HuangMark J Schnitzer
Apr 13, 2019·Proceedings of the National Academy of Sciences of the United States of America·Somayyeh Soltanian-ZadehSina Farsiu
Sep 11, 2012·Nature Methods·Amy J LamMichael Z Lin
Aug 30, 2016·Nature Neuroscience·Michael Z Lin, Mark J Schnitzer
Aug 30, 2016·Nature Neuroscience·Na JiSpencer L Smith
Aug 30, 2016·Nature Neuroscience·Kenneth D HarrisSpencer L Smith
Aug 3, 2019·PLoS Computational Biology·Luke E RogersonPhilipp Berens
Jul 4, 2018·Scientific Reports·Travis MonkJörg Lücke
Nov 7, 2019·Scientific Reports·Connor Beck, Yiyang Gong
Oct 30, 2019·Nature Methods·Tong ZhangMark J Schnitzer
Aug 3, 2019·Science·Ahmed S AbdelfattahEric R Schreiter
Mar 18, 2015·Biomedical Optics Express·Xiuli LiuShaoqun Zeng
Dec 20, 2018·Light, Science & Applications·Tong LingDaniel Palanker
Mar 14, 2019·Frontiers in Cellular Neuroscience·Madhuvanthi KannanVincent A Pieribone
Nov 2, 2019·Nature Communications·Omer ManoDamon A Clark
Sep 16, 2020·Optics Letters·He ZhangYu-Ping Huang
Oct 22, 2020·Scientific Reports·Huu HoangKeisuke Toyama
Jan 28, 2021·Journal of the American Chemical Society·Monica A GonzalezEvan W Miller
Mar 2, 2021·PLoS Computational Biology·Jilt SebastianMathew Magimai-Doss
Feb 28, 2020·Current Opinion in Biomedical Engineering·Mitchell Clough, Jerry L Chen

Related Concepts

Nerve Impulses
In Silico
Neurons
Signal Processing, Digital
Photons
Fluorescence Resonance Energy Transfer
Optical Imaging
Microscopy
Neuroma
Image Analysis

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