A Gestalt in primary visual cortex? [Elektronische Ressource] : applying neurophysiological methods to capture a psychophysical phenomenon / von Anne Schmidt

AGestaltinPrimaryVisualCortex?
Applyingneurophysiologicalmethodstocapturea
psychophysicalphenomenon



Dissertation
zurErlangungdesDoktorgrades
derNaturwissenschaften




vorgelegtbeimFachbereichPsychologieundSportwissenschaften
derJohannWolfgangGoetheUniversität,Frankfurt/Main



von
AnneSchmidt
ausBernburg




Frankfurt/Main2009
D30

















vomFachbereichPsychologiederJohannWolfgangGoetheUniversitätFrank
furt/MainalsDissertationangenommen.












Dekan:
Prof.Dr.HelfriedMoosbrugger


Gutachter:
Prof.Dr.HelfriedMoosbrugger,J.1W.GoetheUniversitätFrankfurt/Main
Prof.Dr.DieterHeyer,Martin1LutherUniversitätHalle/Saale


DatumderDisputation:
To
RuxandraSireteanu
(1945–2008)






Acknowledgments

Firstofall,IwanttothankmysupervisorattheMax PlanckInstituteforBrainRe1
search, Kerstin E. Schmidt. I am very grateful for the opportunity she gave me to
workinherresearchgroup,herpatienceteachingmeabo utneuroscience,andthe
various chances I got to participate at conferences and cou rse programs. I would
alsoliketothankmyclosecolleaguesandofficematesThom asWunderleandDavid
Eriksson for their enduring support through my data analysis, helping me to over1
comemynon1existentprogrammingskillsandansweringallmyquestionsevenifI
askedthesameoneforthefifthtime.Thankyoualsoto AnaLuizaTurchettiMaia.
Hervisitingyearinourresearchgroupwasoneofmyb estandIwillalwayscherish
herbeautifulfriendship.IwouldliketothankSergi oNeuenschwanderfortechnical
supportinthelab.Thankyoutoallmycolleaguesint hedepartmentofNeurophysi1
ologyattheMaxPlanckInstituteforBrainResearchaswe lltothestaffmembersin
theadministration,ITdepartment,mechanicalworkshop,andanimalhouse.
IthankmyuniversityadvisorsHelfriedMoosbruggerand DieterHeyerfortheir
guidancethroughtheprocessofwritingmythesisinthe departmentofpsychology
andprovidingmewiththeessentialconfidencetogetitdone.
MygratitudegoestomydearfriendswhomImetinFr ankfurtduringthelast
three years who gave me the strength to keep going: Sa rah Weigelt, Christine
Grützner,JuttaMayer,SandraAnti–oursoulsushiletmekeepmymindandsmile;
ValérieWespatat,EllenStädtler,ThomasOrban,Ines Streu–soccer,sauna,andice
creamarethebeststressreleasers;andallthosethatli stenedpatientlyandgaveme
goodadvice:MariaOlkkonen,OvidiuJurjut,BrussLima,U lrikeRadden,PetraJan1
son, Mirko Schmidt, Friederike Wiedemann, Ursula Werder, Birke Stubbendieck,
Hermann Josef Abs, Lauri Stemmler, my friends from Ful bright Alumni, and many
more.
AllmyloveandgratefulnesstomyparentsJörgandElke Schmidtandtomy
brotherKonradSchmidtwhogivemerootswhenIneedtostayonthegroundand
offermewingstoflythroughmylife.


1Abstract
‘Thewholeismorethanthesumofitsparts.’Thiside ahasbeenbroughtforwardby
psychologists such as Max Wertheimer who formulated Gestal t laws that describe
ourperception.Onelawisthatofcollinearity:elemen tsthatcorrespondintheirlocal
orientationtotheirglobalaxisofalignmentforma collinearline,comparedtoanon1
collinear line where local and global orientations are orthogonal. Psychophysical
studies revealed a perceptual advantage for collinear o ver non1collinear stimulus
context.Itwassuggestedthatthisbehavioralfindingco uldberelatedtounderlying
neuronalmechanismsalreadyintheprimaryvisualcorte x(V1).
Studies have shown that neurons in V1 are linked accordin g to a common
fate: cells responding to collinearly aligned contours a re predominantly intercon1
nectedbyanisotropiclong1rangelateralconnections.Inthecat,thesameholdstrue
forvisualinterhemisphericconnections.Inthepresentst udywe aimedtotesthow
theperceptualadvantageofacollinearlineisrefle ctedintheanatomicalproperties
withinorbetweenthetwoprimaryvisualcortices.Weappliedtwoneurophysiological
methods,electrodeandopticalrecording,andreversiblydeactivatedthetopographi1
callycorrespondingcontralateralregionbycoolingineightanesthetizedcats.
Inelectrophysiologyexperimentsourresultsrevealedth atinfluencesbystimu1
luscontextsignificantlydependonaunit’sorientation preference.Verticalpreferring
units had on average a higher spike rate for collinear over non1collinear context.
Horizontalpreferringunitsshowedtheoppositeresult. Opticalimagingexperiments
confirmedthesefindingsforcorticalareasassignedtove rticalorientationpreference.
Further,whendeactivatingthecontralateralregionthespikerateforhorizontalpre1
ferringunitsintheintacthemispheresignificantlyde creasedinresponsetoacollin1
earstimuluscontext.Mostoftheopticalimagingexperimentsrevealedadecreasein
corticalactivityinresponsetoeitherstimuluscontextcrossingtheverticalmidline.
Inconclusion,ourresultssupportthenotionthatmodul atinginfluencesfrom
stimuluscontextcanbequitevariable.Wesuggestthat thekindofinfluencemayde1
pendonacell’sorientationpreference.Theperceptua ladvantageofacollinearline
asoneoftheGestaltlawsproposesisnotuniformlyre presentedintheactivityofin1
dividualcellsinV1.However,itislikelythatthecom binedactivityofmanyV1neu1
rons serves to activate neurons further up the processing st ream which eventually
leadstotheperceptualphenomenon.
2Tableofcontents

Acknowledgements.…..…………………………………………………………………………….………..1
Abstract…………………………………………………………………..................................................…..2
TableofContents………………………………………………………………………………………….….3

1 INTRODUCTION........................................................................................... 5
1.1 GestaltPsychology....................................................................................... 7
1.2 PsychophysicalStudiesonCollinearity.................. .................................... 10
1.3 TheVisualSystem–anOverview.............................................................. 15
1.4 TheCatPrimaryVisualCortex(V1) ........................................................... 19
1.4.1 TopographicRepresentationoftheVisualField........ .......................... 19
1.4.2 OrientationSelectivityofNeuronsinV1............. ................................. 22
1.4.3 LateralInteractionsBetweenV1Neurons........................................... 24
1.4.4 VisualCallosalConnections................................................................ 32
1.5 SummaryofResearchHypotheses............................................................ 37
2 MATERIALSANDMETHODS..................................................................... 38
2.1 Animals&Surgery................................... ................................................... 38
2.2 IndependentVariables ............................................................................... 42
2.2.1 VisualStimulusConditions.................................................................. 43
2.2.2 ThermalDeactivation .......................................................................... 49
2.3 ExperimentsUsingOpticalImagingofIntrinsicSignals .. ........................... 51
2.3.1 OpticalImagingSetup......................................................................... 51
2.3.2 PrincipleoftheIntrinsicOpticalSignal.............. .................................. 53
2.3.3 OpticalRecordingPreparations .......................................................... 56
2.3.4 OpticalImagingDataAcquisition ........................................................ 61
2.3.5 OpticalImagingDataProcessing........................................................ 65
2.3.6 DependentVariablederivedfromOpticalRecording .......................... 69
2.4 ExperimentsusingElectrophysiologyRecording ........... ............................ 70
2.4.1 ElectrophysiologySetup...................................................................... 70
2.4.2 PrincipleofElectrophysiologicalRecording ........................................ 77
2.4.3 RecordingPreparationsforElectrophysiologyExperiments ............... 79
2.4.4 ElectrophysiologyDataAcquisition ..................................................... 83
2.4.5 ElectrophysiologyDataProcessing..................................................... 85
32.4.6 HistologicalPost1Processing.............................................................. 87
2.4.7 DependentVariableDerivedfromElectrophysiologyRecording......... 90
2.5 ExperimentalDesign .................................................................................. 92
3 RESULTS.................................................................................................... 95
3.1 ResultsfromElectrophysiologyExperiments ............ ................................. 95
3.1.1 ContextEffectonRecordedSpikingActivity ....................................... 96
3.1.2 CoolingEffectonRecordedSpikingActivity ....................................... 99
3.2 ResultsfromOpticalImagingExperiments .............. ................................ 103
3.2.1 ContextualEffectonImagedCorticalSignal..................................... 105
3.2.2 CoolingEffectonImagedCorticalSignal.......................................... 107
4 DISCUSSION............................................................................................ 111
4.1 Surround