All-Optical Methods to Study Neuronal Function

424 Pages·2023·19.652 MB·English

by  Eirini Papagiakoumou

Neuromethods 191
Eirini Papagiakoumou Editor
All-Optical
Methods to
Study Neuronal
Function
N
EUROMETHODS
SeriesEditor
Wolfgang Walz
University ofSaskatchewan
Saskatoon, SK,Canada
Forfurther volumes:
http://www.springer.com/series/7657
Neuromethodspublishescutting-edgemethodsandprotocolsinallareasofneuroscienceas
wellastranslationalneurologicalandmentalresearch.Eachvolumeintheseriesofferstested
laboratoryprotocols,step-by-stepmethodsforreproduciblelabexperimentsandaddresses
methodologicalcontroversiesandpitfallsinordertoaidneuroscientistsinexperimentation.
Neuromethodsfocusesontraditionalandemergingtopicswithwide-rangingimplicationsto
brain function, such as electrophysiology, neuroimaging, behavioral analysis, genomics,
neurodegeneration,translationalresearchandclinicaltrials.Neuromethodsprovidesinvesti-
gators and trainees with highly useful compendiums of key strategies and approaches for
successful research in animal and human brain function including translational “bench to
bedside”approachestomentalandneurologicaldiseases.
All-Optical Methods to Study
Neuronal Function
Edited by
Eirini Papagiakoumou
Institut de la Vision, Sorbonne Université, INSERM, CNRS, Paris, France
Editor
EiriniPapagiakoumou
InstitutdelaVision
SorbonneUniversite´,INSERM,CNRS
Paris,France
ISSN0893-2336 ISSN1940-6045 (electronic)
Neuromethods
ISBN978-1-0716-2763-1 ISBN978-1-0716-2764-8 (eBook)
https://doi.org/10.1007/978-1-0716-2764-8
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Preface to the Series
Experimental life sciences have two basic foundations: concepts and tools. The Neuro-
methods series focuses on the tools and techniques unique to the investigation of the
nervous system and excitable cells. It will not, however, shortchange the concept side of
thingsascarehasbeentakentointegratethesetoolswithinthecontextoftheconceptsand
questions under investigation. In this way, the series is unique in that it not only collects
protocols but also includes theoretical background information and critiques which led to
themethodsandtheirdevelopment.Thus,itgivesthereaderabetterunderstandingofthe
origin of the techniques and their potential future development. The Neuromethods
publishing program strikes a balance between recent and exciting developments like those
concerningnewanimalmodelsofdisease,imaging,invivomethods,andmore established
techniques, including, for example, immunocytochemistry and electrophysiological tech-
nologies.Newtraineesinneurosciencesstillneedasoundfootingintheseoldermethodsin
order toapplyacriticalapproachtotheir results.
Under theguidanceofitsfounders,AlanBoultonandGlenBaker,theNeuromethods
serieshasbeenasuccesssinceitsfirstvolumepublishedthroughHumanaPressin1985.The
seriescontinuestoflourishthroughmanychangesovertheyears.Itisnowpublishedunder
theumbrellaofSpringerProtocols.Whilemethodsinvolvingbrainresearchhavechangeda
lot since theseriesstarted, thepublishingenvironmentand technologyhavechanged even
more radically. Neuromethods has the distinct layout and style of the Springer Protocols
program,designedspecificallyfor readabilityandeaseofreferenceinalaboratorysetting.
Thecarefulapplicationofmethodsispotentiallythemostimportantstepintheprocess
of scientific inquiry. In the past, new methodologies led the way in developing new dis-
ciplines in the biological and medical sciences. For example, physiology emerged out of
anatomyinthenineteenthcenturybyharnessingnewmethodsbasedonthenewlydiscov-
eredphenomenonofelectricity.Nowadays,therelationshipsbetweendisciplinesandmeth-
ods are more complex. Methods are now widely shared between disciplines and research
areas. New developments in electronic publishing make it possible for scientists that
encounter new methods to quickly find sources of information electronically. The design
of individual volumes and chapters in this series takes this new access technology into
account. Springer Protocols makes it possible to download single protocols separately. In
addition, Springer makes its print-on-demand technology available globally. A print copy
canthereforebeacquiredquicklyandforacompetitivepriceanywhereintheworld.
Saskatoon,SK,Canada WolfgangWalz
v
Preface
Control and monitoring of neuronal activity with light, what is often called all-optical
manipulationofneurons,isadmittedlythemostadequatemethodforaddressingquestions
regarding communication of neurons in a neural circuit or between different circuits. The
bigandcontinuouslyexpandingtoolboxofmolecularphotosensitiveprobes thatactivate/
inhibit or image (through membrane voltage or calcium changes) neuronal activity, in
combination with the development of original light-microscopy methods for stimulating
these probes, has tremendously contributed to this direction and led to innovative experi-
mental concepts, where neurons can be manipulated either as entities or as ensembles.
Indeed, the use of light offers suitable spatiotemporal resolution to manipulate neurons at
single-cellspecificity.Atthesametime,itgivesaccesstoalargepopulationofcellssimulta-
neouslyviascanless,parallelilluminationmethods.
Neural circuit studies are more conclusive for addressing biological questions when
performedinvivo. Inthissense,they necessitatethree-dimensional(3D)accessibility both
for activation and imaging, at physiological time scales (few-ms scale activation and imag-
ing). 3D imaging approaches enable today using complementary strategies to access
volumes extending up to hundreds of micrometers in the axial direction. On the contrary,
the development of 3D photoactivation methods is more recent. These systems use
computer-generated holography (CGH), a technique based on phase modulation of the
excitation beam’s wavefront, to create multiple excitation regions of interest. Thanks to
3D-CGH, used eithersolely (parallel methods) or in its diffraction-limit version in combi-
nationwithscanningoftheholographicbeamlets,itisnowadayspossibletosimultaneously
activate multiple neurons providing both the adequate temporal resolution, as well as the
spatialresolutionfornearsingle-cellprecision.Highspatialresolutionandselectivityisoften
assuredbyimplementingthosemethodswithtwo-photonexcitation.
Although the first experiments of all-optical manipulation of neuronal activity per-
formed activation of neurons via uncaging of caged glutamate, the term all-optical today
ismostlyrelatedtothecombinationoffunctionalimagingandoptogeneticactivation.There
is a growing number of studies using optogenetics and calcium imaging to explore several
hypothesesincellularandsystemsneuroscience,neverthelessafullopticalneuronalcontrol
remains a challenge in terms of achieving reliable delivery and expression of sensors and
actuators in the same neurons, eliminating the crosstalk between imaging and activation,
andrecordingandstimulatingwithsingle-neuronandsingle-action-potentialprecision.
Inthisvolume,weopttogiveanoverviewofthemethodsthathavebeenusedsofarin
all-opticalexperiments,butalsotopresentotherpromisingapproachespotentiallyusefulin
this domain. The book is addressed to people experienced in different disciplines, such as
physicists, engineers, and neuroscientists; therefore, it starts by providing some basic but
fundamentalbackgroundinformationintermsofbothphysiologyandopticsinthecontext
of all-optical two-photon neurophysiology experiments (Chap. 1), followed by some
prompts for the selection of appropriate actuators and sensors, and functional imaging
methodologies that drive the choice of both, together with the suitable laser sources for
two-photonexcitation(Chaps.1and2).
vii
viii Preface
Wethenpresent,indetail,opticalmethodsthathavebeenusedforphotoactivationand
imaging.Thereadercanfindthedesignprinciplesand,insomecases,hardwareimplemen-
tationformethodslikegeneralizedphasecontrast(Chap.1),computer-generatedhologra-
phyandscanningapproaches(Chaps.3and4),temporalfocusing(Chaps.1and4),aswell
as guidance to the entire workflow for an all-optical experiment in circuit neuroscience
(Chap. 5). In Chap. 6, possibilities and limitations of optogenetic actuators are discussed
within the context of an all-optical single-beam experiment by giving insights into the
photophysical properties of actuators. Detailed methods are provided in Chap. 7 on a
miniatureheadmountedtwo-photonfiber-coupledmicroscopeforimagingneuronalactiv-
ity in vivo in freely moving animals, while Chap. 8 discusses how 3D holographic optoge-
neticscanbeaddedtoahome-builtlightsheetmicroscope.
This book also attributes a part on innovative imaging techniques that could be
implemented in the framework of an all-optical electrophysiology experiment. Chapter 9
pronouncesthetheoriesoftemporalfocusingincombinationwithsingle-pixeldetectionfor
imaging of fast collective biological processes at depth, over a widefield and at high
spatiotemporal resolution. Chapter 10 presents alternative imaging methods at synaptic
resolution, such as two-photon fluorescence microscopy equipped with Bessel focus scan-
ningtechnologyandwidefieldfluorescencemicroscopywithopticalsectioningability.
The implementation of simultaneous two-photon imaging and holographic optoge-
neticsinconjunctionwithpopulationanalyticaltoolsor withpsychophysicalmeasurements
ofevokedsyntheticperceptstoconfirmapreciserelationshipbetweenopticalmanipulations
andbehaviorispresentedinChaps.11and12.
Finally,inChap.13,anapproachforlabel-freeimagingispresented:stimulatedRaman
scattering(SRS)microscopy,anon-linearimagingmethodfor visualizingamoleculebased
on its chemical properties, and the way to integrate it in a commercial multiphoton
microscope,eventuallyusefulforlabel-freefunctionalimaging.
Theuseofall-opticalmethodsforstudyingtheneuralfunctionisamultiparametricand
arduous project to setup. It entails a multidisciplinary know-how both for developing the
optical system and the adequate biological preparation, and sometimes expensive equip-
ment, especially when multiphoton excitation is considered. We hope that this book can
serveasaguidetofacilitatethefirstrequirement,establishingausefulreferenceforgroups
startingtheiractivityinthisdomain,andgiveinsightsontheopticalsystems,thechoiceof
actuators and sensors, but also stimulate ideas for ground-breaking configurations and
experiments.
InstitutdelaVision EiriniPapagiakoumou
SorbonneUniversite´,INSERM,CNRS,Paris,France
Contents
PrefacetotheSeries ........................................................... v
Preface ..................................................................... vii
Contributors................................................................. xi
1 OpticalManipulationandRecordingofNeuralActivitywith
WavefrontEngineering ..... ........ ....... ....... ........ ....... ........ 1
RuthR.Sims,ImaneBendifallah,KrisBlanchard,DimitriiTanese,
ValentinaEmiliani,andEiriniPapagiakoumou
2 BalancingtheFluorescenceImagingBudgetforAll-Optical
NeurophysiologyExperiments....... ....... ....... ........ ....... ........ 49
PeterQuicke,CarmelL.Howe,andAmandaJ.Foust
3 Light-BasedNeuronalCircuitProbinginLivingBrainsatHigh
Resolution:ConstraintsandLayoutsforIntegratingNeuronalActivity
RecordingandModulationinThreeDimensions .... ........ ....... .. ...... 75
MatteoBruzzone,EnricoChiarello,AndreaMaset,AramMegighian,
ClaudiaLodovichi,andMarcodalMaschio
4 High-SpeedAll-OpticalNeuralInterfaceswith3DTemporally
FocusedHolography....... ........ ....... ....... ........ ....... ........ 101
IanAnt(cid:1)onOldenburg,HayleyAnneBounds,andNicolasC.Pe´gard
5 AnAll-OpticalPhysiologyPipelineTowardHighlySpecificand
Artifact-FreeCircuitMapping....... ....... ....... ........ ....... ........ 137
HendrikBackhaus,NicolasRuffini,AnnaWierczeiko,
andAlbrechtStroh
6 SpatialandTemporalConsiderationsofOptogeneticToolsin
anAll-OpticalSingle-BeamExperiment...... ....... ....... ...... .. ........ 165
DamarisHolderandMatthiasPrigge
7 MiniatureMultiphotonMicroscopesforRecordingNeuralActivity
inFreelyMovingAnimals........... ....... ....... ........ ....... ........ 187
BarisN.Ozbay,GregoryL.Futia,MingMa,ConnorMcCullough,
MichaelD.Young,DiegoRestrepo,andEmilyA.Gibson
8 OptogeneticsandLight-SheetMicroscopy.......... ........ ....... ........ 231
LauraMaddalena,PaoloPozzi,Nicolo` G.Ceffa
BasvanderHoeven,andElizabethC.Carroll
9 WidefieldMultiphotonImagingatDepthwithTemporalFocusing ........... 263
PhilipWijesingheandKishanDholakia
10 High-SpeedNeuralImagingwithSynapticResolution:Bessel
FocusScanningTwo-PhotonMicroscopyandOptical-Sectioning
WidefieldMicroscopy ...... ........ ....... ....... ........ ....... ........ 293
GuanghanMeng,QinrongZhang,andNaJi
11 OpticalandAnalyticalMethodstoVisualizeandManipulate
CorticalEnsemblesandBehavior .... ....... ....... ........ ....... ........ 331
LuisCarrillo-Reid,WeijianYang,andRafaelYuste
ix
x Contents
12 IlluminatingNeuralComputationUsingPrecision
Optogenetics-ControlledSyntheticPerception ...... ........ ....... ........ 363
JonathanV.Gill,GiladM.Lerman,EdmundChong,
DmitryRinberg,andShyShoham
13 SpectrallyFocusedStimulatedRamanScattering(sf-SRS)
MicroscopyforLabel-FreeInvestigationsofMolecularMechanisms
inLivingOrganisms........ ........ ....... ....... ........ ....... ........ 393
Tama´sVa´czi,La´szl(cid:1)o Himics,MatteoBruzzone,Mikl(cid:1)osVeres,
andMarcodalMaschio
Index .......... ........ ....... ........ ....... ....... ........ ....... ........ 417