Invariant visual object recognition and shape processing in rats

ContentslistsavailableatScienceDirect

Behavioural

Brain

Research

j o ur na l h o me p a g e :w w w . e l s e v i e r . c o m / l o c a t e / b b r

Review

Invariant

visual

object

recognition

and

shape

processing

in

rats

Davide

Zoccolan

VisualNeuroscienceLab,InternationalSchoolforAdvancedStudies(SISSA),34136Trieste,Italy

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•Ratsarecapableofinvariantvisualobjectrecognition.

•Ratsspontaneouslyperceivedifferentviewsofavisualobjectassimilartoeachother,thatisasinstancesofthesameobject. •Ratsarecapableofamultifeatural,shape-basedvisualprocessingstrategy.

•Ratscanlearncomplex,configuralvisualdiscriminations.

•Ratsspontaneouslyprocesscompositevisualpatternsaccordingtoperceptualgroupingcues.

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Received21June2014 Receivedinrevisedform 19December2014 Accepted25December2014 Availableonline2January2015 Keywords: Invariantrecognition Rat Rodent Shapeprocessing Patternvision

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Invariantvisualobjectrecognitionistheabilitytorecognizevisualobjectsdespitethevastlydifferent imagesthateachobjectcanprojectontotheretinaduringnaturalvision,dependingonitspositionand sizewithinthevisualfield,itsorientationrelativetotheviewer,etc.Achievinginvariantrecognition representssuchaformidablecomputationalchallengethatisoftenassumedtobeauniquehallmarkof primatevision.Historically,thishaslimitedtheinvasiveinvestigationofitsneuronalunderpinningsto monkeystudies,inspiteofthenarrowrangeofexperimentalapproachesthattheseanimalmodelsallow. Meanwhile,rodentshavebeenlargelyneglectedasmodelsofobjectvision,becauseofthewidespread beliefthattheyareincapableofadvancedvisualprocessing.However,thepowerfularrayof experimen-taltoolsthathavebeendevelopedtodissectneuronalcircuitsinrodentshasmadethesespeciesvery attractivetovisionscientiststoo,promotinganewtideofstudiesthathavestartedtosystematically explorevisualfunctionsinratsandmice.Rats,inparticular,havebeenthesubjectsofseveralbehavioral studies,aimedatassessinghowadvancedobjectrecognitionandshapeprocessingisinthisspecies. Here,Ireviewtheserecentinvestigations,aswellasearlierstudiesofratpatternvision,toprovidean historicaloverviewandacriticalsummaryofthestatusoftheknowledgeaboutratobjectvision.The pictureemergingfromthissurveyisveryencouragingwithregardtothepossibilityofusingratsas complementarymodelstomonkeysinthestudyofhigher-levelvision.

©2015TheAuthor.PublishedbyElsevierB.V.ThisisanopenaccessarticleundertheCCBYlicense (http://creativecommons.org/licenses/by/4.0/).

Contents

1. Introduction... 11

2. Visualornotvisual?... 11

2.1. Therediscoveryofrodentvision ... 12

3. Earlyinvestigationsofratpatternvision ... 12

3.1. Earliestevidenceofinvariantrecognitionandadvancedshapeprocessinginrats... 12

3.2. Gestaltvisualperceptioninrats... 13

3.3. Strengthsandlimitationsofearlyworksonratvisualperception ... 14

∗ Correspondenceto:InternationalSchoolforAdvancedStudies(SISSA),ViaBonomea,265,34136Trieste(TS),Italy.Tel.:+390403787701;fax:+390403787702. E-mailaddress:zoccolan@sissa.it

http://dx.doi.org/10.1016/j.bbr.2014.12.053

3.3.1. Limitationsofspatialtwo-alternativeforced-choicetasks... 14

3.3.2. Limitationsinthetestofgeneralization... 15

4. Patternvisionandvisualshapeprocessinginrats... 15

4.1. Insearchofthecriticalstimulusdimensionsunderlyingratpatternvision... 15

4.2. Evidenceofshape-basedvisualobjectrecognitioninrats... 16

4.3. Spatialintegrationofvisualinformationinrats... 17

4.3.1. Configuralvisualdiscriminationinrats... 18

4.3.2. Perceptualgroupinginrats... 18

4.4. Areratstrulycapableofadvancedshapeprocessing?... 19

5. Invariantvisualobjectrecognitionandadvancedshapeprocessinginrats... 20

5.1. Ratsarecapableoftransformation-tolerant(invariant)visualobjectrecognition... 21

5.1.1. Visualprimingasawaytoassesstransformation-tolerantperceptionofvisualobjectsinrats... 23

5.2. Visualprocessingstrategiesunderlyingratobjectvision... 23

5.2.1. Aflexible,mid-levelstrategyunderliesratdiscriminationofsimplegeometricalshapes... 24

5.2.2. Ashape-based,multifeaturalprocessingstrategyunderliesratinvariantvisualobjectrecognition ... 26

5.2.3. Reconcilingfindingsaboutthecomplexityofvisualobjectprocessinginrats... 26

5.3. Ratprocessingofcollinearvisualfeatures ... 28

6. Conclusionsandperspectives... 28

Acknowledgments ... 29

References... 29

1. Introduction

Thegreatestchallengethatanyvisionsystem(whether biolog-icalorartificial)hastofaceistheextractionofthebehaviorally relevantcontentofvisualscenesfromthelargelyvariableimages collected, as an input, by the retina [1–3]. Within thedomain of object recognition, this challenge manifests as the need of recognizingpreviouslyseenobjects,despitethefactthatanynew encounterwiththeseobjectswilloftenresultinradicallydifferent retinalinputimages.Theprocessofrecognizingobjectsinspiteof thissubstantialvariationintheirappearanceiscommonlyknown asinvariantrecognitionor,moreprecisely,transformation-tolerant recognition[3–6].Quiteobviously,theproblemofunderstanding howthebrainachievesinvariantrecognitionistightlylinkedtothe problemofunderstandinghowthebrainprocessesandrepresents theshapeofvisualobjects.Althoughshapeisnotawell-defined concept, intuitively, shape features are those properties of the visualobjectsthatmorereliablyallowdistinguishingeachobject fromanyotheronein theretinalinputimages. Assuch,global visualattributes that are not very diagnosticof object identity (becausetheyarelikelysharedbymanydifferentobjects),such asoverallbrightness,contrast,size,area,etc.,arecommonly con-sideredaslower-levelvisualproperties,ratherthanshapefeatures (andaprocessingstrategyrelyingonsuchfeaturesiscommonly consideredasalower-levelstrategy).Ontheotherhand,specific arrangementsof localstraight and curved boundaries, oriented edges and corners [7–10], as well as oriented and unoriented localcontrastpatterns[11–13]andimagefragments[14,15](i.e., attributesthatmoreuniquelydefinevisualobjects)aretypically viewedasproper,higher-level shape features (anda processing strategy relying onsuchfeatures is commonlyconsidered as a higher-levelstrategy).Bearinginmindthatarigorous(or agreed-upon)definitionofshapefeaturecomplexitydoesnotactuallyexist (e.g.,see[16] for adiscussion), onecould tentativelydefinean advancedvisualprocessingsystemasfollowing–asystem capa-bleofextractingfromtheretinalinputthosehigher-order(shape) features that are diagnostic of object identity acrossthe many (unpredictable)imagetransformationseachobjectundergoes dur-ingnaturalvision.Throughoutthearticle,termssuchaslower-level properties,higher-levelfeaturesandadvancedprocessingstrategywill beusedaccordingtothedefinitionsprovidedabove.

Thesedefinitionsmakeveryexplicitthechallengeatthecore ofobjectvision–therequirementofmaintainingahighdegreeof specificityforthefeaturesdefiningtheidentityofvisualobjects, while,at thesametime,disregarding thehugevariation inthe

appearanceofsuchdiagnosticfeatures[17].Computationally, bal-ancingthistrade-offbetweenspecificityandinvariancemakesthe developmentofmachinevisionsystemsextraordinarychallenging [4,5,17,18].Ontheotherhand,humansarecapableofdetecting andclassifyingobjectsoutoftensofthousandsofpossibilities[19] withinafractionofasecond[20,21],whichimpliesthattheirvisual systemimplementsanextremelyefficientandreliablemachinery toprocessobjectinformation.Studiesinnonhumanprimateshave revealedthatsuchaprocessingiscarried outalonga hierarchy of visualcorticalareasknownastheventral visualpathway (or stream)[4,6,22–25].Thispathwaystartsinprimaryvisualcortex andculminatesintheanteriorpartoftheinferotemporalcortex, whichconveysthemostexplicitrepresentationsofvisualobjects– thatis,therepresentationsthatallowtheeasiestread-outofobject identity(andgeneralizationtoidentity-preservingimage transfor-mations)usingsimplelineardecoders[16,26–28].Unfortunately, theneuronal mechanismsunderlyingthe formation of increas-inglyexplicitrepresentationsofvisualobjectsalongtheventral streamarestillpoorlyunderstood.Thisislikelyaconsequenceof theextraordinarycomplexityoftheprimatevisualsystem[29–31] andofthelimitedrangeofexperimentalmanipulationsthat pri-matestudiesallowatthemolecular,synaptic,andcircuitrylevels. Thisdisproportionbetweenthecomplexityoftheneuronal archi-tectureunderinvestigationandthelimitedarrayofexperimental approachesthat areavailabletocarryoutsuchaninvestigation hasrecentlyledseveralvisionscientiststoexplorethepotential of rodentsasmodels ofvisualfunctions.Withregard toobject recognition,whetherrodentscanactuallyserveasusefulmodelsto understanditsneuronalbasiscruciallydependsonhowadvanced theirvisualrecognitionbehavioris.Inthefollowing,Iwillcritically reviewmostoftheliteratureconcernedwithratpatternvision, shapeprocessingandvisualobjectrecognition,arguingthatthere isenough behavioralevidencetosuggestthat thisspecies does embodysomeofthecoremechanismsunderlyinginvariantobject recognition.Assuch,theratand,byhomology,themouse(given thesimilaritybetweenthevisualsystemsofthesespecies[32–35]) mayrepresentapowerfulcomplementarymodeltothenonhuman primateintheinvasiveinvestigationoftheneuronalsubstratesof objectvision.

2. Visualornotvisual?

Rats and mice are the more widespread laboratory animal species,accountingforover 80%ofallresearchanimalsusedin theEuropeanUnion[36].Vision,ontheotherhand,isarguably

oneofthemainresearchtopicsinneuroscience,targetedby disci-plinesasdiverseassystem,cognitive,computational,cellularand developmentalneuroscience [37,38]. Giventhese premises,one couldexpectrodent-basedstudiestobeattheforefrontofvision research,but,historically,thishasnotbeenthecase.Infact,until veryrecently,rodentshavebeenlargelyoverlookedbythevision sciencecommunity,becausetheirbrainshavebeenassumedtolack advancedvisualprocessingmachinery.Suchanassumptionrests ontheobservationthatratsandmicearenocturnal/crepuscular species[36],havemuchlowervisualacuitythanprimates(e.g.,∼1 cycle/deginpigmentedrats[39–46],comparedto30–60cycles/deg inhumanandmacaquefovea[47–53]),andmakeextensiveuseof othersensorymodalities,suchastouch[54–56]andsmell[57–61], whenexploringandinteractingwiththeirenvironment.In addi-tion,neurons inrodent primary visualcortex, while displaying manyofthetuningpropertiesfoundinhighermammalianspecies (e.g.,orientationtuning[62–74]),arenotarrangedintothe func-tionalcorticalmodules,suchastheorientationcolumns[68,73,75], whicharetypicalofnon-humanprimatesandsmallcarnivores. Historically,this hasconfined theresearch onrodent vision to developmentalstudiesofcorticalplasticitymechanisms[76–80] (e.g.,oculardominanceplasticityduringthecriticalperiod)and behavioral/lesionstudiesoflearning,familiarityandmemory(e.g., theanatomical substrates of object recognition memory; for a reviewsee[81–85]).Inotherwords,thevisualabilitiesofratsand micehavebeenthesubjectofinvestigationnotbecauseofan inter-estintorodentvisualprocessingperse,butonlyinsofarasthese speciesprovidedaneasieraccesstotheneuronal/anatomical sub-stratesofplasticityandmemory,ascomparedtomonkeyandcat cortex.

Atthesametime,someofthemostcompelling,although indi-rect,evidenceabouttheabilityofrodentstoextractbehaviorally relevantinformation from thevisualenvironment and perform non-trivialcomputationsonthevisualinput,canbefoundin non-visionstudies.Infact,rodentshavebeenextensivelystudiedfor theirimpressive spatial navigationabilities, typically displayed whenforagingoverlargerangesaroundtheirnests[86],alsoat dusk,whenvisualcuesare availableandcanplaya keyrole in theirorientingbehavior.Laboratoryrats,inparticular,havebeen found to make not only excellent use of visual cues [87–90], buttopreferentiallyrelyonsuchcues(overolfactoryand audi-torycuesand pathintegration[91–93]), when testedin spatial navigation tasks. At the neuronal level, the most remarkable signature of such a strong dependence of rat spatial behavior onvision is the locking of hippocampal place fields to spatial visualcues, and theirremapping when suchcues are changed [94–99].Aspointedoutinarecentreview[1],althoughthevisual processing implied in navigation cannot simply be equated to theone underlyingobject recognition,still itmustengage sim-ilarlyadvancedmechanisms interms of extractionof ascene’s content (e.g., visual landmarks and their relative spatial loca-tion)from a largely viewpoint- and lighting-dependent retinal input.

2.1. Therediscoveryofrodentvision

Thenotionthatrodentscanactuallyserveasusefulmodelsto studyvision hasonly recentlytaken holdin thevision science community,witha newtide of studiesthat, over thepast few years,havestartedtosystematicallyexplorevisualfunctionsinrats andmice.Theturningpointintheappreciationofrodent mod-elsbyvisionscientistscanbeascribedtotwomainfactors.The firstistheevergrowingarrayofpowerfulexperimentaltools(e.g., optogenetics[100–102]andinvivotwo-photonimaging[75,103]) thathavebeendevelopedtodissectneuronalcircuitsinrodents [104]and,whilepossibletoapplyinotherspecies,arecurrently

far less advanced in (e.g.) non-human primates. The second is the increasingappreciation for rodent cognitiveabilities [105], whichismakingthemattractivemodelstostudycognitive func-tionsascomplex asperceptual decision-making [106,107],rule learning[108]and workingmemory[109].While theaccessto geneticmanipulationhasinspiredaconsiderablenumberof neu-roanatomy[32,33], imaging [73,110,111] and electrophysiology [72,112–115]studiesofmousevisualcortex(culminatingwiththe endowment, bythe AllenInstitutefor Brain Science,of a $300 million budget toa 10-year projectto study themouse visual system[116,117]), thepossibility of testing highly manageable animalmodelsincomplexvisualtasks,suchasshapeprocessing andinvariantobjectrecognition,hasfosteredthebehavioral inves-tigation of rat visual abilities [118–128]. Several reviews have summarized themost recentadvances in theunderstandingof themouse visualsystem [129–131].In this report,I willfocus insteadonthemountingbehavioralevidenceaboutratcapability foradvancedprocessingofvisualshape/objectinformation (Sec-tion5).Thisdiscussionwillbeintroducedbyanhistoricaloverview ofearlyinvestigationsofratvision(Section3),uptomorerecent studiesofshapeprocessingandobjectrecognitioninthisspecies (Section4).

3. Earlyinvestigationsofratpatternvision

Thefirstbehavioralstudiesonratvisiondatebacktoone cen-turyago.Someoftheseearlyinvestigatorsfoundeitherveryscarce [132]orno[133,134]evidenceforpatternvision inalbinorats, whilesomeothersfoundthatwhiteratswerecapableofform dis-crimination(e.g.,discriminationofupwardvs.invertedtriangles [135,136]).Readingthisearlydebateaboutratvisualcapabilities isveryinstructive,becausemanyoftheissuestheseearlyauthors discussedarethesamelaterstudiesalsofacedwhentestingrat visualbehavior:(1) thechoiceof theratstrain (albino vs. pig-mented);(2)thedesign ofthetestingapparatus(e.g.,imposing, ornot,afixedviewingdistance);(3)thepossiblecontributionof othermodalities(e.g.,tactileandolfactory)inexperimentswhere ratsareallowedtoapproachphysicalshapes/objects;and(4)the confoundsduetolow-levelvisualproperties,suchasbrightness and sizeofthe stimuli.Thisdebatewaseventually settledin a seriesofseminalstudiespublishedbyKarlLashley[137,138]and otherauthors[139–145]inthe30s.Lashley,inparticular,using aningeniousjumpingstandapparatus,notonlyobtainedthefirst behavioralmeasureofvisualacuityinpigmentedandalbinorats [43] (laterconfirmedby many studies[39–42,44–46]), butalso providedthemostcompellingevidenceofhistimeaboutthe abil-ityof pigmentedratstosuccessfully discriminatevisualshapes [137,138].

3.1. Earliestevidenceofinvariantrecognitionandadvanced shapeprocessinginrats

Thejumpingstandapparatus(showninFig.1A)implemented a spatial two-alternative forced-choice procedure, with a rat requiredtojumpagainstatarget(positive)stimuluscardfroma distanceof20cm,whileignoringaflankingnegativestimuluscard. Thecardbearingthenegativestimuluswasfixedrigidly,causing therat tofallinto anet foran incorrectjumptoward it (pun-ishment),whilethecardbearingthepositivestimuluswasheld byalightspring,sothatwhena ratjumpedagainstit,thecard fellbackandallowedtheanimaltoreachalandingplatformwith food(reward).Usingthisapproach,Lashleyfoundthatpigmented ratswere able to discriminatedifferent pairs of 2-dimensional geometricalshapes,suchasanupwardvs. aninvertedtriangle, atrianglevs.a circle,a trianglevs.across,etc.[137,138].More

Fig.1.ExtractsfromLashley’sseminalstudyofratpatternvision.(A)AsketchofthejumpingstandapparatusintroducedbyLashleytotestratsinvisualdiscrimination tasks(seeSection3.1foradescription).(B)Anexampleofvisualpatterndiscrimination,inwhichratsweretrainedinoneofLashley’sexperiments.(C)Alterationsofthe trainedvisualpatterns(showninB)toprobegeneralizationofratrecognitionintransfertrials.(Forinterpretationofthereferencestocolorinthisfigurelegend,thereader isreferredtothewebversionofthisarticle.)

ModifiedfromLashley[138].

importantly,hediscoveredthatonceananimalhadlearnedto dis-criminatetwoshapes,hewasabletogeneralizethisdiscrimination “inspiteofalterationinsize,continuityofsurface,orofoutline[of theshapesandwas]abletodiscoverthefigureinvarious combina-tionswithirrelevantlines”[138](seeFig.1BandC).Inaddition,he alsofoundthat“markedchangesintheluminousintensityofeither figureorground[did]notdisturbreactionsolongasthebrightness relationsoffigureandground[were]notreversed”[138](e.g.,see Fig.1C,toprow).ThesefindingsledLashleytoconcludethatin rats“theremustbesomeprimitivegeneralizationofformwhich goesbeyondtherecognitionofidenticalelements”[138],which iswhat moderninvestigatorswouldrefer toas transformation-invariantor,moreproperly,transformation-tolerantvisualobject recognition(namely,size-tolerant,clutter-tolerantand luminance-tolerantrecognition).Ontheotherhand,Lashleyfoundonlylimited tolerancetoin-planerotation(e.g.,seeFig.1C, centralpanelin thebottomrow)and,byobscuringpartsofthevisualtargets,he found“thatthemajorityofanimals[did]notreacttotheentire figurepresentedinthestimuluspattern.Thelowerorinner mar-ginofthefiguresmostfrequentlydetermine[d]thereaction.[...] Animalsreact[ed]tosuchvarious characters asthe distanceof onefigurefromtheframe,therelative surfaceareasof the fig-ures,a conspicuousprojectingpoint,andthelike”[138].Atthe sametime,Lashleyfoundthatratscouldlearntodiscriminate dis-continuousorientedpatternsmadeofdistinctelements(e.g.,two circlesdefiningeitheradiagonalorahorizontal“line”)andthat, moreimportantly,thisdiscriminationgeneralizedtocontinuous orientedlineswiththesameorientationofthepreviouslylearned discontinuouspatterns. The reversewas alsotrue: rats trained todiscriminatebetweenaverticalandahorizontalgrating(i.e., patternsmadeofmultiple,alternatingblackandwhitestripes, ori-entedeitherverticallyorhorizontally)generalizedwellnotonlyto singlecontinuouslineswiththesameorientation,butalsoto pat-ternsmadeofsingleormultiplediscontinuouslineswiththesame orientation(i.e.,patternsmadeofeitherverticallyorhorizontally alignedarraysofsmallsquares/rectangles).Thesefindingsinduced Lashleytoconcludethat“theconstantstowhich[arat]reactsin otherwisevariablesituationarepropertieswhichcanbederived onlyfromatotalfigure,hencethathisreactionisdependentupon somesortofunificationoftheelementswithinapartofthefield” [138].

3.2. Gestaltvisualperceptioninrats

Thesecontrastingobservations(i.e.,thelackof“react[ion]to theentire[stimulus]figure”insometestsandtheprocessingof “properties...derived...fromatotalfigure”insomeothertests [138])anticipatedcontemporaryattemptsatdeterminingthe crit-icalvisualfeaturesunderlyingratdiscriminationofvisualpatterns, andtheensuingdebateaboutwhetherratsareactuallycapableof processingshapeinformationacrossalargespanofanobject’s sur-faceor,instead,simplyrelyonlocal,lower-levelimageproperties [120,121,146,147](seeSections4.2,4.4and5.2).Inthelanguage ofLashley’stime,thesefindingscouldbeinterpretedasevidence against or in favor of rat ability to process the total organiza-tionof visualpatterns,by relyingonthespontaneousgrouping ofsensoryelementsintowholeformpercepts,aspostulatedby Gestaltpsychology.Thistopicwasthesubjectofaseriesof stud-ies by two of Lashley’s contemporaries:Paul Fieldand Isadore Krechevsky,concerned,respectively,withtheroleofconcept for-mation [140,141,145]and perceptual grouping[143,144] in rat visualperception.

Inparticular,Krechevsky[143,144]carriedoutaseriesof exper-imentsinwhich,usingLashley’sjumpingstand,ratsweretrained todiscriminatebetweentwoarraysmadeofthesamenumberof identicalconstituentelements(smallsquares),whoseproximity waslargeralongtheverticaldimensioninonearray(thus form-ingapatternofcolumns)andalongthehorizontaldimensionin theotherarray(thusformingapatternofrows).Notonlydidrats learntoperformthisdiscriminationveryeffectively(thusshowing acapabilitytoprocessthespatialdistributionoftheconstituent elementsof thetrained patterns), but,when tested in general-ization trials, theyshowed a preference for a grating made of continuouslineswiththesameorientationoftheoriginallylearned training-positivearrayoverthepositivearrayitself.Forinstance, ratstrainedtorespondto(i.e.,jump toward)apattern ofrows (the positivestimulus; seeFig.2A,right)and avoid amatching patternofcolumns(thenegativestimulus;seeFig.2A,left),when presentedwiththesamepatternofrowsandanever-seen-before horizontalgrating(seeFig.2B),spontaneouslychosethesecond overthefirstinthelargemajorityofthetransfer/generalization trials.Interestingly,suchapreferenceforthecontinuousgratings wasnotobservedincasesinwhichratshadbeenoriginallytrained

Fig.2.ThevisualpatternsusedbyKrechevskyinhisseminalstudyofperceptual groupinginrats.(A)Ratswereinitiallytrainedtodiscriminateanegative(−) col-umnpatternfromapositive(+)rowpattern.(B)Whenrequiredtochoosebetween thetraining-positiverowpatternandacontinuoushorizontalgrating,mostrats consistentlychosethelatter.

ModifiedfromKrechevsky[143,144].

todiscriminateapositivecolumn(orrow)patternfroma nega-tivepatternmadeofasmallernumberofelements,arrangedso astoformanX[143].Basedonthesefindings,Krechevsky con-cludedthatrat“perceptualprocess[...]involvestheoperationof ‘forcesofattraction’betweenthemembersofavisualgroupofsuch anatureastomaketherattopreferthecontinuousgestaltover thatofthediscontinuousgropingeventhoughtheoriginal train-ing[was]onthediscontinuousstimulus-complex”[143].However, theemergenceofsuchapreferenceforthecontinuousgestaltwas notfullyspontaneous,i.e.,purelyrootedintothe“autochthonous forcesoforganization”[143]ofthestimuluspatterns,butdepended ontheneed oftheanimal to extractsucha gestalt to success-fullyaccomplish the task. Hence, thefailure of the continuous gestalttoemergewhenthecolumn/rowpatternshadtobe dis-criminatedfromtheXpatterns,wherealower-levelrecognition strategy(e.g.,onebasedoncomparingtheoverallbrightnessofthe patterns)wouldsufficetosucceedinthetask.Translatedinto con-temporaryterms,Krechevsky’sfindings(laterconfirmedbyseveral studies[148–153];seeSection4.3.2)canbeconsideredasthefirst solidevidenceofratabilitytointegratetheconstituentfeatures ofvisualpatternsintoconfiguralrepresentations,uptothepoint ofextractingfromthetrainingpatternsabstractshapedimensions, suchasverticalnessandhorizontalness.Perhapsmoreimportantly, Krechevsky’sinterpretationoftheimpactoftaskcomplexityonthe emergenceofgestaltperceptsanticipatedtheconclusionsreached bythemostrecentstudiesofratobjectrecognitionaboutthecrucial roleoftaskdemands/constraintsindeterminingthecomplexityof ratrecognitionstrategy[118,120].Ontheotherhand,Krechevsky’s conclusionsareobviouslylimitedbyhislackofknowledgeabout theexistenceoforientation-selectivefiltersinratprimaryvisual cortex(V1)[62–66,74].InSection4.3.2,Iwilldiscusstowhatextent

thetuningpropertiesofV1neuronscanaccountforKrechevsky’s findings,aswellasformorerecentstudiesofperceptualgrouping inrats.

3.3. Strengthsandlimitationsofearlyworksonratvisual perception

Overall,theearlystudiesbyLashleyand hiscontemporaries indicateacapabilityofratstousetheirvisiontodiscriminatevisual patternsandgeneralizetovariationsofpreviouslylearned discrim-inations(e.g.,duetosizechangesofthetargetstimulioraddition ofbackgroundclutter).Thesefindingssuggestthatratsareable to,atleasttosomedegree,abstracttheirrecognitionfromthe spe-cificretinalinputpatternsproducedbytheirencounterswithvisual objects.Assuch,Lashley’sandrelatedworkcanbeconsideredasthe firstdemonstrationthatratsarecapableofanon-trivialprocessing strategyofvisualpatterns,i.e.,astrategythatisnotsimplybased onmatchingidentical(ornearlyidentical) retinalinputs across consecutiveencounters.However,oneshouldbecarefulto inter-pretthesefindingsasconclusiveevidenceforratinvariantobject recognition.

Infact,Lashley’sstudieswereaffectedbyalackofsystematicity –althoughalargenumberofexperimentswereperformed,with manydifferentvisualstimuliandmanipulations,onlyafewratsper conditionweretestedandasmallnumberoftrialswascollectedper animal.Inaddition,onlyasmallnumberoftransformationsofthe trainedvisualpatternswastested,andacrossalimitedvariation range.Krechevsky’sexperimentsweremorefocused,more thor-oughintermsofthenumberoftestedratsandcollectedtrialsper animal,and,assuch,statisticallymorerigorous.Still,Krechevsky’s conclusionswerealsolimitedbythelittlevariationofthepatterns testedinhisexperiments(e.g.,thespatialfrequencyandphaseof thegratingswerenotvaried).Morecritically,alltheseearlystudies basedonLashley’sjumpingstandwereaffectedbytwo method-ologicalissuesthatlimitedthescopeoftheirconclusions,asfar asinvariantrecognitionisconcerned.Itisworthdiscussingthese methodologicallimitations,sincetheycanbefoundinmanystudies ofratvision,includingsomeveryrecentones[121,146].

3.3.1. Limitationsofspatialtwo-alternativeforced-choicetasks ThemajorissueinLashley’sandrelatedworkistheuseofa spatialtwo-alternativeforced-choiceprocedure.Byconstruction, thiskindoftaskrequiresasubjecttodiscriminatebetweentwo simultaneouslypresentedvisualpatterns.Asaconsequence, dis-criminationcanbebasedonthedirectcomparisonoflower-level visual attributes (e.g., local luminance or contrast), whose rel-ativemagnitudeis, generally,preservedacrosstransformations, especiallywhenbothpatternsareequallytransformed,asinthe caseofLashley’sstudy.Asanexample,ratdiscriminationofa tri-angle froma square could bebased oncomparingthe relative luminanceofthebottomhalvesofthesepatterns,without nec-essarilyprocessinganyactualshapeattribute(e.g.,orientationof edges,presenceandsharpnessofcorners,etc.).Ifthesepatternsare equallyscaledortranslated,ortheiroverallluminosityisequally reduced/increased,theratwillstillcorrectlydiscriminatethem, sincetherelative brightnessoftheirbottomhalveswillremain unchanged(thesquare’sbottomhalfwillalwaysbebrighterthan thetriangle’sbottomhalf), defactoacting asa transformation-invariant,low-level,diagnosticimagefeature.Sucharecognition strategy,whiledefinitelymoresophisticatedthanasimple match-ing of retinalinputs to fixedtemplates, shouldanywaynot be consideredasanadvancedprocessingstrategy,becauseitwould notengagehigher-order,transformation-tolerantrepresentations ofshapefeatures.Lashley’swork,aswellasotherratvision stud-iesbasedontwo-alternativeforced-choicetaskswithidentically transformedstimuli[121,146],cannotdifferentiatebetweensuch

alow-levelstrategyandatrulyinvariant,shape-basedprocessingof visualobjects.Thisdoesnotmeanthat,ingeneral,two-alternative forced-choiceprocedurescannotbeusedtostudyshapeprocessing (see,asanexample,Simpson’sandGaffan’swork[147],discussed inSection4.2).Alsoinvariantrecognitioncan,inprinciple,betested usingtheseprocedures,provided thatthestimulishown tothe animals are independently transformed in each trial.However, this isvery impractical,becauseofthecombinatorial explosion thatwouldresultfrombuildingeverypossiblepairoftransformed stimuli(especiallywhenthestimuliaretransformedalongmany differentdimensions–size,position,in-planerotation, etc.).As showninSection5,amorepracticalandeffectivesolutionisto useataskwhereasingle,isolatedstimulusispresentedineach trial[118–120].

3.3.2. Limitationsinthetestofgeneralization

Anotherissue, when probinginvariant object recognitionin animalsubjects,istotest generalizationof recognitiontonovel viewsofpreviouslylearnedobjects,withoutgivinganyfeedback abouttheidentityoftheseviews(bymeansofrewardand/or pun-ishment).Thisisobviously verychallenging,because,ideally, it wouldrequireananimaltoperformlargenumbersofunrewarded trials.Howeverimpractical,failuretowithholdfeedbackimplies aninabilitytotestpuregeneralizationofrecognition,sincethe testedanimalscould,inprinciple, learnand memorizethe cor-rectassociationbetweennewobjectviewsandreward,without necessarilyperceivingsuchnewviewsassimilartotheonesthey originallylearned.Inotherwords,asetofperceptuallyunrelated (fortheanimals)objectviewscouldbearbitrarilyassociated,in memory, tothesamecategory, onlybecauseof thecontinuous trainingreceivedduringthetask. Lashley’sapproach toaddress thisissue,soastotestgeneralizationofpattern discrimination, wasactuallywelldesigned,giventhetechnologicallimitsofhis time.Aftertrainingarattodiscriminateapairofvisualpatterns (usingrewardand punishment asdescribed above), theanimal wastested ina series of“critical”(i.e.,generalization)trials, in whichhewas“allowedafreechoicebetween[transformed ver-sionsofthepatterns],receivingfoodateverytrial,regardlessof thepattern chosen”[138].Usingthesepunishment-freetrialsis obviouslyagoodapproximationtoapuretestofgeneralization, yetis notcompletelyrobust, asacknowledgedbyLashely him-self[138]andKrechevsky[143].Sinceananimalreceivesreward nomatterwhatstimulushechooses,hecould,inprinciple,learn toconsistently respondto(i.e.,jump toward) a noveltest pat-tern,basedonthepositivefeedbackhereceivesonthefirst(or thefirstfew) trials.Thatis,a rat thathappens torespond cor-rectlyon thefirst trial, purely by chance,would be reinforced inhisinitial(random)choicebytherewardhereceives.Onthe otherhand, as reportedby Lashley,an animal responding ran-domly,wheninitiallyconfrontedwithtwonovelpatterns,could learn“thatnochoiceisnecessarywhennewfiguresarepresented andpromptly[adopt]apositionhabit[...]evenwithfigureswhich inearliertestsgave perfecttransfer” [138].Theseshortcomings donotfullyunderminethevalidityofLashley’stransfertests,but couldhave ledto eitheran overestimationor an underestima-tionofthegeneralizationability ofratsthatwere,respectively, eitherinitiallysuccessfulorunsuccessfulwithnewtestpatterns. Moreingeneral,theapproachoftestinggeneralizationby reward-ingwhateverchoiceananimalmakesonnovelstimuli,whilenot perfect,isacceptable,aslongasdatafrommultipleanimalsare pooledtoobtaingroupaverageperformances(inwhichpossible overestimations and underestimations are averaged out). Nev-ertheless, as shown in Section 5, novel approaches have been recentlyproposedthatallowacleanerassessmentofgeneralization [118,119].

4. Patternvisionandvisualshapeprocessinginrats

Theencouragingfindingsaboutratvisualprocessingabilities providedbyLashleyandhiscontemporariesinthe30sdidnot suc-ceedintriggeringasustainedinterestinthisspecies(oranyother rodentspecies)amongvision scientists.Intheensuingdecades, thevisionsciencecommunitybecameprogressivelymore inter-estedinmonkeys andsmallcarnivores(e.g.,cats) asmodelsto studythevisualsystem,andvirtuallyabandonedanysystematic attemptatstudyingvisualprocessinginrodents.Still,evenbefore theveryrecentsurgeofinterestinrodentvision(seeSection5),a fewbehavioralstudiesfurtherexploredtheperceptualstrategies underlyingratpatternvisionandobjectrecognition.Amongthese studies,themostnoteworthyarethosepublishedbySutherland andcolleaguesinthe60s[154–157]andbyGaffanandcolleagues inthe90s[147,158–160].

4.1. Insearchofthecriticalstimulusdimensionsunderlyingrat patternvision

Sutherlanddevelopedanewapparatustotrainratsinvisual dis-criminationtasks[154–156].Itconsistedinattachingtotherear wallofanoperantboxtwoshapescutoutofwhitePerspex(the discriminanda),withadrinkingnozzleforrewarddelivery protrud-ingthroughthemiddleofeachshape.Ratsweretrainedtoleavea startingbox(locatedattheoppositeendofthewallbearingthe dis-criminanda)andapproachafixedpositivepattern(whileignoring theothernegativepattern)tocollectreward.Usingthis appara-tus,Sutherlandsuccessfullytrainedpigmentedratstodiscriminate betweenaverticalandahorizontalrectangle[154].More impor-tantly,healsorantransfer(i.e.,generalization)testsinwhichrats werepresentedwithalteredversionsofthelearnedpatternsand wererewardedindependentlyoftheirchoice(i.e.,sameapproach totestgeneralizationasLashley’s;seeSection3.3.2).Thesetests confirmedand extended Lashley’searlyreports aboutrat capa-bilitytodiscriminatevisualshapesinspiteofsizevariation(i.e., bothlargerandsmallerversionsoftherectangles)andchangesto theirsurface/outline(i.e.,breakingtherectanglesinto discontinu-oussegments).

Inanotherseriesofstudies[155,156],Sutherlandand cowork-ers tried to infer the critical shape dimensions underlying rat discrimination of 2-dimensional visual patterns. They initially trained rats to discriminate between an “open” and a “close” shape(respectively,a diamond-likeandahourglass-like silhou-ette,eitherhorizontallyorverticallyoriented),andthenmeasured ratperceivedsimilaritybetweeneachof20newtransfershapes andtheoriginallytrainedshapes.Thesetransfertestswererunnot onlyusingthespatialtwo-alternativeforced-choicetaskdescribed above,butalsobypresentingasingleshapeatthetimeinthewall bearingthediscriminanda(leavingtheotherstimulusslotinthe wallempty,withjustthedrinkingnozzleprotrudingfromthebare wall).Again,beingthesetransfertests,ratswererewardedno mat-terwhethertheychosetoapproachthenozzleprotrudingfromthe testshapeorfromtheemptyslot.Noticeably,thisisoneofthe earliestattemptstoovercomethelimitationsoftwo-alternative forced-choiceprocedures(seediscussioninSection3.3.1), soas toallowamorereliableassessmentoftheperceptualsimilarity betweenthetransfershapesandtheoriginallylearned diamond-likeandhourglass-likepatterns.Theshapesthatratsperceivedas beingmoresimilartothediamond-likepatternwerethosethat, qualitatively,lookedmoreas“closed”(i.e.,morecompactand with-outprotruding elements),suchas circles,ellipses,trianglesand squares.Bycontrast,theshapesthatratsperceivedasbeingmore similartothehourglass-lookingpatternwerethose thatlooked more“open”(i.e.,morespread-out,withalotofcontourand pro-jections), suchascrosses, Hs,Us,etc.Asa waytoquantifythis

tendencyofratstorankandclassifythetransfershapesalong a “closeness–openness”stimulusdimension,theauthorscomputed theratiobetweencontourlengthandsquarerootoftheareafor eachshapeandfoundastrong,positivecorrelationbetweenthe rankingoftheshapesaccordingtotheirperceivedsimilaritytothe diamond-like(“closed”)shapeandtheirrankingaccordingtothis ratio.Sincethisratioprovidesawaytoquantifythecomplexity(in termsofopenness/closeness,i.e.,presenceorabsenceofprotruding features)of2-dimensionalpatterns(withmorecomplex, spread-outshapeshavingalongercontourthansimpler,morecompact shapes,given thesamearea), Sutherland’sand coauthors’ find-ingssuggestacapabilityofratstoabstracttheirrecognitionfrom thespecificretinalinputpatternstheywere originallyexposed to,soastobuildquiteexplicitrepresentationsofabstractshape dimensions.This conclusionis in agreementwith Krechevsky’s [143,144]andrelatedstudies[148–153]aboutratabilitytolearn thediagnosticdimensionsofverticalnessandhorizontalnessfrom discontinuousorientedpatterns bymeansofperceptual group-ing(see Sections3.2 and 4.3.2), and witha more recent study [123]aboutratcapabilityofcategorizing naturalimagesonthe baseofglobalstimulusdimensions,suchasconvexityandaspect ratio.

Overall,Sutherland’s studies suggest that therat visual sys-temiscapableofthekindofadvancedshape processingthatis thehallmark of high-level vision:the extrapolation of abstract shape dimensions. However, once again, care should be taken beforeconsideringthesefindingsasconclusiveevidencefor invari-ant object recognition in rats, because of several limitations in Sutherland’s and coworkers’ experimental approach (mostly pointed out bythe authorsthemselves). First, only few shapes weretestedandveryfewtrialswerecollectedpershape(10trials, inthetransferexperimentwithsingle-shapepresentation),thus greatlylimitingtheaccuracyofthemeasurementofratrecognition performanceand,therefore, ofratperceivedsimilaritybetween transfer and trained shapes. In addition, the single-shape pre-sentationdevisedbySutherland,whileovercomingsomeofthe issuesconcerningtwo-alternativeforced-choicetasks(seeSection 3.3.1),wasitselfaffectedbyonemainlimitation:theratsshowed aconsistentbiastoward thesideonwhichtheshape was pre-sented(nomatterwhethertheyweresupposedtoapproachitor avoidit),thus furtherreducingthepowertoestimaterat pref-erence/perceivedsimilarity[156].Morecritically,itisdifficultto understandtowhatextentotherlower-levelstimulusproperties mayhaveplayedaroleindeterminingratsimilarityjudgments. Many different feature dimensions could,potentially, correlate withtheshape–complexityratiocomputedin[156]:shapearea, averageluminosity,overallluminosity,luminosity/contrastinthe bottom/tophalvesof the shapes,etc. As shown in Section 5.2, classification image methods are arguably the bestapproaches touncoverwhatvisualfeaturesaratreliesuponwhen perform-inganobjectdiscriminationtaskand,therefore,revealthenature andcomplexityofratrecognitionstrategy[120,121].Ontheother hand,ensuringthatratsdonottriviallydiscriminatevisualobjects becauseofdifferencesinlow-levelpropertiescanonlybeachieved intwoways:either bytestingratswithavery largebattery of objecttransformationsorbycarefullymatchingasmanydifferent low-levelvisualattributesaspossible.Whiletheformerapproach wasappliedinthemostrecentstudiesofratinvariantrecognition [118–120],thelatterwasfollowedbySimpsonandGaffanintheir verythoroughinvestigationofvisualsceneandobjectprocessing inrats[147].

4.2. Evidenceofshape-basedvisualobjectrecognitioninrats Simpson’s and Gaffan’s study [147] was based on a proce-dure/apparatustotestratsinvisualtasksthatGaffanandcolleagues

haddescribedinpreviousreports[158,159],andthattheylater applied in a series of lesion studies to identify the neuronal substrates of visual object discrimination and memory in rats [160–164].TheapparatusconsistedofaYmaze,withthethreearms havingequallengthandthethreeanglesformedbyeacharmpair havingequalamplitude.Apairofcomputermonitors(jointedbya 117◦angle,soastosubtend∼94◦_{horizontally,whenviewedfrom}

themazecenter)waslocatedattheendofeacharm,wherereward wasalsodelivered.Visualscenesofvariouscomplexity(containing anumberof2-dimensionalobjects,suchasellipses,ASCIItext char-acters,polygons,rectangles,etc.)weredisplayedonthemonitors, withthescenesshownintheadjacentmonitorsattheendofanarm beingthemirrorversionofeachotheralongtheverticalaxis(each pairofmirrorscenesonadjacentmonitorsconstitutedone stimu-lusscene;seeexamplesinFig.3A).Eachratwastrainedinaspatial two-alternativeforced-choicetask,inwhichtwodifferent stimu-lusscenesweredisplayedattheendofthetwoarmsnotcurrently occupiedbytheanimal,andtherathadtolearntoeitherapproacha targetpositive-constantoravoidatargetnegative-constantscene. Thisconstantscenewaspaired,ineverytrial,toatrial-unique vari-ablescene,containingvisualobjectsthatcoulddifferfromthoseof theconstantsceneinavarietyofproperties(examplesofaconstant sceneandsomevariablescenesthatwerepairedtoitinSimpson’s andGaffan’sstudy[147]areshowninFig.3A).

Usingthisapproach,SimpsonandGaffanshowedthatratswere abletodiscriminatepairsofstimulusscenescontainingtwovisual objectspermonitor,evenwhentheseobjectsoccupiedthesame locationwithinthevisualspace(i.e.,withineachscene),thus con-cludingthat rats“mustencodemorethanjust thegrossspatial distributionofpatches(objects)thatcontrastwiththebackground” [147].Moreimportantly,theyfoundthatratsmaintainedahigh dis-criminationperformance(above80%correct)nomatterwhether position-matchedobjects in thestimulusscenes were approxi-matelyequatedintermsofarea,luminance(i.e.,graylevel,since eachobjectwasrenderedinauniformgrayintensityvalue)and luminousflux(i.e.,area×luminance).Thesethreelow-level fea-tureswerematchedindependentlyinseparatetests,thusshowing thatnoneofthemwascritical,byitself,forthesuccessful discrimi-nationofthevisualscenes(comparebarsinFig.3B).Whenallthese propertiesweresimultaneouslymatched(thusproducingstimulus scenescontainingobjectswithsimilararea,luminanceand lumi-nousflux)ratsstillsuccessfullydiscriminatedthescenes(compare barsinFig.3C),thussuggestingthattheybasedtheirrecognitionon shapeinformation.Thisconclusionwasconfirmedbyrequiringrats todiscriminatescenescontainingobjectsofthesameshape cate-goryinmatchingvisualfieldlocations(e.g.,ellipseswithdifferent aspectratioand/orslightsizedifferences;comparetheconstant scenetothelastvariablesceneinFig.3A).Thisproducedadrop inratperformance(seemiddlebarinFig.3D)thatledGaffanand Simpsontoconclude“first,thatratsperceivedtheobjectsas dis-tinctshapes,notasluminousblobs,andsecond,thattheyencoded themin termsof visualfeaturesthat arecommontoa classof shape”[147].Inaddition,whenratsweregiventhechancetobase theirdiscriminationoneithershapedifferencesorsizedifferences amongthevisualobjectscontainedinapairofstimulusscenes, theyappearedtorelyonlyontheformer(higher-level)property, whileignoringthelatter(lower-level)attribute.Thatis,rat per-formancewasequallygoodwhentheobjectsdifferedinshape(no matterwhethertheyalsodifferedinsize;seepurplebarsinFig.3E), andequallyworsewhentheobjectshadsimilarshape(nomatter whethersizedifferenceswerealsopresentthatcouldbeusedas low-levelcues;seebluebarsinFig.3E).

Overall,Gaffan’sandSimpson’sstudyprovidescompelling evi-denceaboutthecapabilityof ratstodiscriminatevisualobjects onthebaseofshapedifferences.Althoughnoattemptwasdone toinfer what shape features theanimals relied upon (as done

Fig.3.SummaryofSimpson’sandGaffan’sexperimentaldesignandresults.(A)ExamplesofstimulusscenesusedtoproberatpatternvisioninSimpson’sandGaffan’s study.Ineachtrial,ratswererewardedforavoidinganegative-constantscene(rightpanel)andapproachingatrial-specificvariablescene(examplesshownintheleft panels).Theobjectsinthevariablescenescouldbematchedtothoseintheconstantscenewithrespecttodifferentvisualproperties:luminance,area,luminousflux(i.e., area×luminance),andshapeclass.(B–E)Ratrecognitionperformancefordifferentkindsoftestedvariablescenes.Thecolorofthebarsmatchesthecolorofthecorresponding examplevariablescenesin(A).SeeSection4.2foradetaileddescription.(Forinterpretationofthereferencestocolorinthisfigurelegend,thereaderisreferredtotheweb versionofthisarticle.)

ModifiedfromSimpsonandGaffan[147].

bySutherlandandcolleagues[156]andby morerecentstudies [120,121,123]),thesystematic(althoughpartial)matchingof vari-ouslow-levelpropertiesconvincinglyshowsthatratscanrecognize visualpatternswithoutresortingtogrossdifferencesinarea, lumi-nosity and luminous flux. In addition, theindependence of rat performanceonthearea/sizeoftheobjectscanbetakenasa fur-therdemonstrationofthesizetoleranceofratobjectrecognition. However,tolerancetoparametricobjectvariationsalong differ-enttransformationaxeswasnotsystematicallyinvestigated,thus leavingopenthequestionofhowmuchvariabilityinobject appear-ance,andalongwhatdimensions,ratsareabletotolerate.Finally, theexperimentsofGaffanandSimpsonwerestillaffectedbythe limitationsinherentinspatialtwo-alternativeforced-choicetasks (seeSection3.3.1),althoughtoalesserextentthanotherstudies, becauseofthelargevarietyofshapesagainstwhicheachlearned targetobjecthadtobecompared(e.g.,comparetheobjectsinthe constantscenetothoseinthevariablescenesofFig.3A),which madeitmoreunlikelyfortheratstorelyonlocallow-levelcues (e.g.,luminance differences in the top orbottom halves ofthe objects,aslaterreportedbyMininiandJeffery[146];seeSection 4.4).

Gaffan and colleagues further investigated rat visual object recognitioninaseriesoflesionstudiesaimedatassessingtheroleof perirhinalcortexinobjectrecognitionmemoryandobject identifi-cation[160–164].Giventhatthisreviewismainlyconcernedwith behavioralinvestigationsofratvisualobjectrecognition,Iwillnot discusstheneuroanatomicalimplicationsof thesestudies(fora review,see[81–85]).Still,leavingasidetheneuroanatomical find-ings,someofthesestudiesprovideadditionalbehavioralevidence aboutratvisualprocessingabilities.Forinstance,in[160],ratswere testedinahighlydemandingtask,whichrequiredthemto discrim-inatetheconstantscenefromvariablescenesthatdifferedfromthe constantinfourpossibleways:(1)bothidentityandpositionofthe objectswithinthescenes;(2)onlyobjectidentity(sameposition);

(3)onlyobjectposition(sameidentity);and(4)arrangementof objectswithfixedidentityacrossfixedpositions.Sincethesefour typesofscenecomparisonswererandomlyinterleaved,thefact thatcontrol(i.e.,non-lesioned)animalsachievedanaverage per-formanceof∼70%correct(orgreater)ineachcomparisonsuggests thatratsarecapableofahighlyflexible recognitionstrategy,in whichpositionandshapecuescanbeinterchangeablyextracted, dependingontaskdemands[160].

4.3. Spatialintegrationofvisualinformationinrats

Many other lesion studies of rat recognition memory have reporteddataaboutobjectdiscriminationbehaviorinthisspecies. Unfortunately,mostofthesestudieshaveusedsolidobjectsthat ratswerefreetoapproachand touch,ratherthan purelyvisual stimuli(e.g.,see[165–167]).Inaddition,recognitionperformance hasbeentypicallymeasuredintermsofthetimespentbyan ani-malexploringagivenobject,ratherthanasthefractionofexplicit correct identifications he made. This makes extremely hard to infer anythingaboutrat visualprocessing,because,under such experimentalsettings,notonlythevisualpropertiesoftheobjects (e.g.,size,brightness,etc.)arenotcontrolled,butratscaninspect thediscriminandausingamixtureofvisual,tactileandolfactory cues[168,169].Morerecently,severalinvestigatorshavedeveloped approachesthat,similarlytotheonedevisedbyGaffanand col-leagues,allowtestingratsinpurelyvisualtasks.Theseapproaches arebasedeitheronV-shapedwatermazesequippedwithmonitors forstimuluspresentation[170–172]oronoperantboxesequipped withtouchscreens[146,173–177].Still,mostofthesestudiesare notmuchconcernedwithratvisualprocessingperse,but,rather, ratvisualbehaviorisexploitedasameantotestandunderstand learningandmemoryfunctions.Assuch,thesestudies,while pro-vidingadditionalevidenceofratcapabilitytousevisiontoextract task-relevantinformation fromvisualpatterns, do nottypically

Fig.4. Visualpatternsusedthetestconfiguraldiscriminationinrats.(A)Thestimuli usedbyEacottetal.[161],whichdidnotenforceastrictlyconfiguralprocessing strategy,becauseoftheuniquefeaturescreatedbytheintersectionoftheir con-stituentelements.(B)ThestimuliusedbyDaviesetal.[172],whichmoreproperly enforcedaconfiguralprocessingstrategy.

PanelAismodifiedfromEacottetal.[161].PanelBismodifiedfromDaviesetal. [172].

includemanipulations ofthevisualstimuli that allowinferring howadvancedratobjectvisionisintermsofshapeprocessingand invariantrecognition.

4.3.1. Configuralvisualdiscriminationinrats

Exceptionstothisruleareafewreportsabouttheabilityofrats tolearncomplexconfiguralvisualdiscriminations[161,171,172], thatisdiscriminationsthatrequiretheconcurrentprocessingof multiplefeatures(orparts)ofthevisualstimuli.Themostwidely appliedofsuchtasksisthebiconditionaldiscrimination,inwhich fourdifferentvisualfeatures(i.e.,featuresA,B,CandD)are com-binedtoobtainfourdifferentcompoundstimuli(i.e.,compound patternsAB,AC,BC,andCD)thatcanonlybedistinguishedfrom eachotherbyconcurrentlyconsideringbothconstituentelements ofeachpattern. Whileinmonkey studiesthebiconditional dis-criminationistypicallyimplementedbypresentingonecompound patternsatthetimeandthenaskingthemonkeysubjecttoreport itsidentitybymeansofsaccadesorleverresponses[178,179],in thecontextofratstudiesthisparadigmhasbeenimplementedin theformofmultipletwo-alternativeforced-choicetasks(i.e.,AB+ vs.AC−,DC+vs.DB−,AB+vs.DB−andDC+vs.AC−,withthe+ denotingtherewarded pattern),administeredtotheanimalsin interleavedtrialsorsmallblocksoftrials[161,172].

Thefirstattemptat trainingratsinsuchataskwasaffected byapossibleconfound:theconstituentelementswere superim-posedontopofeach othertoproducethecompoundpatterns, thuscreatinguniquefeaturesattheirintersectionsthataffordeda nonconfiguralsolution,inspiteofthesubstantialfeatures’overlap amongthediscriminanda(seeFig.4A)[161].Therefore,thefactthat ratssuccessfullylearnedthistasktellsmoreabouttheirremarkable abilitytoextractbehaviorallyrelevantvisualfeaturesamongvery

similarpatterns,thanabouttheircapabilitytolearnandadopta strictlyconfiguralprocessingstrategy.Alaterstudy[172]overcame thislimitationbydesigningcompoundconfiguralstimulimadeof flankingrectangularelements(eachbearingaspecificvisual pat-tern;seeFig.4B).Ratssuccessfullylearnedthistask,achievinga performancehigherthan70%correctinabout12trainingsessions, thusshowingthecapabilitytoconcurrentlyprocessmultiple con-stituentpartsof visualobjects.Thisconclusionissupportedby anotherstudy,inwhichratsweretestedinadifferentkindof con-figuraldiscrimination,knownastransversepatterning[171].The taskconsistedofthreesimultaneoustwo-alternativeforced-choice discriminations(i.e.,A+versusB−,B+versusC−,andC+versusA−), witheachofthethreestimuli(i.e.,A,BandC)appearingintwo dis-criminationsandbeingassociatedwithrewardinonecase(+)but notintheother(−).Similarlytothebiconditionaldiscrimination, transversepatterningalsorequiresthatsubjectsbuilda configu-ralrepresentationofstimuluselements.Thefactthatratslearned toperformthistaskwithhighaccuracy(>90%correct)confirms thattheycanreliablyacquireconjunctiverepresentationsofvisual patterns.

4.3.2. Perceptualgroupinginrats

Thatratscouldlearntointegratevisualinformationover mul-tiplelocationsofthevisualfieldwasalreadyamajorconclusionof Kreschevsky’sexperiments[143,144]–ratsdiscriminated discon-tinuousorientedpatternsmadeofidenticalconstituentelements, bygroupingsuchelementsaccordingtotheirproximity(see Sec-tion3.2andFig.2).Theseresultshavebeenconfirmedandextended bymorerecentstudies[148–153],thusfurtherdemonstratingthe abilityofthisspeciestointegratedistinctvisualfeaturesintoglobal percepts.Dodwell[148]wasthefirsttoreplicateKreschevsky’s findings,showingthattheyarenottheresultofanoveltyeffect, i.e.,theycannotbeexplainedbyratpreferenceforthelessfamiliar betweentwovisualpatterns.Infact,ratstrainedtochoosea posi-tivecolumnpatternoveranegativerowpattern,notonlypreferred alessfamiliarverticalgratingoverathetraining-positivecolumn pattern(asoriginallyshownbyKreschevsky),butalsopreferred themorefamiliartraining-negativerowpatternoveracontinuous horizontalgrating.Inotherwords,ratsperceivedaslessnegative theoriginallylearnednegative,discontinuouspattern,when com-paredtoanovelcontinuouspattern(thegrating)withthesame orientation.Stillmorestrikingwasthefindingofanother experi-ment,inwhichratstrainedtochoosebetweenapositivediagonal grating(D+)andanegativeverticalgrating(V−)werelatertested inadiagonal(D)vs.horizontal(H)gratingcomparison.Noticeably, someoftherats,ratherthanchoosingthetraining-positive stimu-lus(i.e.,D),chosethehorizontalgrating.Thatis,theyappearedto alwayschoosethelessverticalstimulus,whichwasD+inthecase ofthetrainedV−vs.D+comparison,butwasH,inthecaseofthe Dvs.Hgeneralizationtest.Similarresultswerefoundforrats orig-inallytrainedinaH+vs.D−comparisonandlatertestedinaDvs. Vcomparison,withsomeanimalschoosingthetraining-negative stimulusDoverV,asiftheirchoicewasbasedoncomparingthe horizontalnessofthestimuli,ratherthanavoidingarigidlylearned, negative,retinalinputpattern.

Dodwell and colleagues further explored the integration of discreteelementsintoglobalperceptsofverticalnessand horizon-talness[150],showingthatratscandiscriminateacolumnarray fromarowarray,evenwhentheseparationbetweenadjacent ele-mentsalongthehorizontaldimensionismadeveryclosetotheir separation alongtheverticaldimension(thusdrastically reduc-ingthestrengthoftheproximitycue)–columnandrowarrays witharatiobetweenthelargestandthesmallestelement separa-tionassmallas1.3:1couldstillbediscriminatedbyratswithan averageperformanceof∼74%correct.Thisisaninteresting find-ing,becauseitsuggeststhatratsmayintegratevisualinformation

overlargespansofthestimulusarrays,soastoaccumulate evi-denceaboutwhatdimension(i.e.,horizontalorvertical)hasthe shorterseparationbetweenadjacentpatternelements.However, thisstudyonlyprovidesalimitedassessmentofthedependence ofperceptualgroupingfromthepropertiesofthegroping cues, mainlybecauseitlacksincontroloverimportantstimulus proper-ties,suchasthesizeandseparation,indegreesofvisualangle,ofthe constituentelementsofthestimulusarrays.Amorerecentand rig-orousstudy[151]hasfoundthatthelargestelementseparationhad tobeatleasttwicethesmallerseparationforratstoperceiverow orcolumnpatternswithanaverageaccuracyofatleast75% cor-rect(althoughlaterstudiesbysomeofthesameauthorssuggesta somewhatsmallerseparationratiotoattainthesamecriterion per-formance[152,153]).Moreover,thestrengthoftheproximitycue thatwasnecessarytoproduceareliableperceptualgroupingwas foundtobestronglydependentontheoveralldensityofthevisual patterns–givenconstituentelementsof1.2◦ofvisualangle,the ratiobetweenthelargerandthesmallerelementseparationthat wasnecessarytoachievethecriterionperformanceincreasedfrom 2:1to4:1,whenthelargerelementseparationwasincreasedfrom 5.7◦to16.8◦ofvisualangle(thusmakingthevisualpatternsparser). Interestingly,inthisstudy,notonlyelementproximitybutalso elementalignmentwasusedasagroupingcue,withtheelements beingperfectlyalignedonly alongonedimension.Althoughthe alignmentcue,byitself,failedtoproduceanyperceptualgrouping, whenitwaspairedtotheproximitycue,itenhancedthegrouping producedbythelatter–forthesparsestpattern(seeabove),the ratiobetweenthelargerandthesmallerelementseparationthat wasnecessarytoachievecriteriondecreased to2.5:1,whenthe alignmentcuewasalsopresent.Asspeculatedbytheauthors,this findingsuggeststhat,inrats,notonlyproximitybutalso“pattern regularityinfluencestheperceptualorganizationofthestimulus” [151],althoughtoamuchlesserextentthaninhumans.

Thefindingspresentedinthissection,aswellasKrechevsky’s earlyinvestigationsonperceptualgrouping(seeSection3.2),could potentiallybeaccountedbythetuningpropertiesofratV1neurons. Asfoundinothermammalianspecies,ratprimaryvisualcortex containsneuronsactingasorientation-selectivefilters,spanning thefullspectrumofpossibleorientations[62–66,74].Manyofthese orientedfiltersperformanapproximatelylinearweightedsumof thelightintensitypatternsfallingintheirreceptivefields.Assuch, aratV1neuronwithagivenorientationpreference(e.g.,vertical) wouldbeactivatedbyadiscontinuousorientedpatternmatching itspreferredorientation.Suchanactivationwouldbemoreorless strong,dependingonthedensityofthepattern,withthe maxi-malresponseachievedforcontinuousorientedgratingsmatching thepreferredorientationandspatialfrequencyoftheneuron.Itis easytoseehowcertaindecisionstrategiesrelyingontheresponse strengthoftheseorientedfilterscouldlead(e.g.)toapreferencefor anovelcontinuousverticalgratingoverapreviouslylearned dis-continuouscolumnpattern(asoriginallyreportedbyKrechevsky [143]).Forinstance,thiswouldbethecase,ifratdecision strat-egyconsistedinchoosingthestimulusthatmaximallyactivated thebankofverticallyorientedfilters(i.e.,thegrating),ratherthan choosingthestimulusthatevokedapreviouslylearned,template responsepatternacrossthefilters’bank(i.e.,thecolumnpattern). Inotherwords,thespatiallyorientedreceptivefieldsofV1neurons, whencombinedwithapreferenceforthepatternsthatmaximize theactivityofagivensetofneurons,couldeasilyaccountforrat perceptualgrouping.Thisdoesnotimplythat Krechevsky’sand Dodwell’sfindingsaretrivial,becauseotherdecisionstrategiesare possiblethatwouldleadtoadifferentbehavioraloutcome(i.e.,a differentstimuluspreference),giventhesamepatternofactivation inV1(e.g.,atemplate-matchingstrategy,aspreviouslymentioned). ThebehavioralfindingsdescribedhereandinSection3.2strongly suggestthat,amongasetofencodinganddecodingstrategies,rats

prefertorelyonanabstractrepresentationoforientationthana precisematchingofstoredtemplatepatterns.Asdiscussedin Sec-tion5.2.3,thiscanhaveprofoundimplicationsintheassessment ofhowadvancedratpatternvision is.Finally,itisimportantto mentionthatnotallKrechevsky’sandDodwell’sfindingscanbe easilyaccountedbythemechanisticargumentsdiscussedabove. Forinstance,thelackofpreferenceforacontinuousgratingover adiscontinuouspatternwiththesameorientation,inthecasea ratwastrainedtodiscriminatethediscontinuouspatternfroman Xpattern[143],confirmsthatthewaytheV1representationofa visualpatternisreadout(toleadtodecision)isnotaunique, auto-maticprocess.Whetherorientationwillemergeasthediscriminant attributewillstronglydependontaskdemands.Similarly, Dod-well’sfindingaboutthepreferenceforahorizontalgratingovera diagonalgrating,forsomeoftheratsthatwereoriginallytrainedto preferadiagonalvs.averticalgrating[148],arguesforan idiosyn-cratic,rat-dependentdecodingschemeofV1responsepatterns–a schemethatcaneitherweightmoretheactivationofagiven sub-populationofneurons(e.g.,withdiagonalpreference),orweight moretheinactivationofanotherneuronalsubpopulation(e.g.,the cellspreferringverticalstimuli).

4.4. Areratstrulycapableofadvancedshapeprocessing?

Overall,thepictureemergingfromthestudiesreviewedinthe previoussectionsindicatesthatratsarecapableofaquiteadvanced processingofvisualobjects.Tosummarize,ratshavebeenfound ableto:(1)toleratesizevariationsandothertransformationsinthe appearanceofpreviouslylearnedpatterns;(2)discriminatevisual patterns with matched low-level visual properties; (3) flexibly extractpositionandshapecues,dependingontaskdemands;(4) learncomplexconfiguralvisualdiscriminations;(5)spontaneously processcompositevisualpatternsaccordingtoperceptual group-ingcues;and (6)extract abstractstimulusdimensions(suchas verticalnessandhorizontalness)fromtrainedpatterns.However, manyofthesefindingshavebeenrecentlychallengedbyastudyof MininiandJeffery[146],whoconcludedthatrats,whentestedin asimultaneous(i.e.,atwo-alternativeforced-choice) discrimina-tiontask,donotspontaneouslyrelyonashape-basedrecognition strategy,atleastwhenotherlower-levelvisualcuesareavailable tosuccessfullyaccomplishthetask.

MininiandJefferycarriedouttwodifferentexperiments,each requiringratstoapproachapositivetargetstimuluspresentedona touchscreen,whileavoidingasimultaneouslypresentednegative stimulus.Inthefirstexperiment,ratsweretrainedtodiscriminate betweenawhitesquareandawhiteequilateraltriangle(with ver-texdown)ofequalareaandequalluminance,shownsidebyside onthestimulusdisplay(i.e.,thetouchscreen)againstablack back-ground(seeFig.5A).Followingacquisitionofthediscrimination, ratsweretestedinaseriesoftransfertrials,where thetraining shapesweretransformedinavarietyofways.Ratsfailedto gen-eralizetoillusoryKanizsafiguresandtocontrast-reversedstimuli (thusconfirmingtheearlyobservationsofLashley[138]andField [140]),but succeeded atdiscriminatingthetarget shapeswhen theseweresimultaneouslyrotatedupto50–60◦,thussuggesting somedegreeofrotationinvariance.However,wheneach shape wasrotatedorverticallyshiftedofadifferentamountcompared totheothershape,soastoreversetheirbrightnessrelationshipin thelowerhemifieldofthestimulusdisplay,ratperformancefell tochanceorbelowit.Thiswasthecasewhenthetriangleandthe squarewererotated,respectively,of180◦and45◦,thusresultingin acomparisonbetweenatrianglewithvertexupandadiamond(see Fig.5B,firstbar),orwhenthesquareonlywasshiftedupward(see Fig.5B,secondbar).Asimilartrendwasfoundwhenthedifference betweenthebrightensofthetwoshapesinthelowerhemifield wasreduced,e.g.,whenonlythetrianglewasrotatedof180◦,so

Fig.5. SummaryofMinini’sandJeffery’sexperimentaldesignandresults.(A)The trianglevs.squarediscriminationinwhichratsweretrainedinoneofMinini’s andJeffery’sexperiments.(B)Ratdiscriminationperformancefordifferentkinds ofmanipulationsoftheoriginallylearnedpatterns(shownbelowtheabscissaaxis). Manipulationsalteringtherelativebrightnessofthestimuliinthelowerhemifield ofthestimulusdisplaymaderatperformancefallingtochance(dashedline)or belowit(seeSection4.4fordetails).

ModifiedfromMininiandJeffery[146].

astobringbothshapestohaveanhorizontaledgeinthelower hemifield(see Fig.5B,thirdbar). Ontheotherhand, manipula-tionsthatdidnotalterthebrightnessrelationshipofthestimuli inthelowerhemifield(e.g.,whenthetriangle onlywasshifted upward;seeFig.5B,fourthbar)producednodropin discrimina-tionperformance.Theseledtheauthorstoconcludethatrats“used, asthediscriminativecue,nottheconfigurationofedges,but dif-ferencesintheluminanceofthetwoshapesinthelowerregionof thevisualfield”[146].Whensuchadifferencereversed(compared towhat ratsexperiencedduringtraining withthedefault stim-ulusconfiguration,wherethebottomofthesquarewasbrighter thanthebottomofthetriangle;seeFig.5A),ratsfailedto discrim-inatetheshapesorevensystematicallymistookoneshapeforthe other(seeFig.5B,firstbar).However,theauthorsalsonoticedthat, whentheluminanceofthesquarewasreduced,soastomatchthe luminanceofthetriangleinthelowerhemifield,ratrecognition performancewasnotaffected(seeFig.5B,lastbar),thus suggest-ingthat“whattheratscomputedwasnotabsoluteluminanceper sesomuchastheareaofbrightpixels,irrespectiveoftheactual levelofbrightness”[146].

Obviously,thesefindingschallengetheviewthatratsare capa-ble of processing visual patters by relying primarily on shape features.Assuch,theyareatoddwithmanyearlierandlater find-ings, presented in thepreviousand next sections, aboutvisual shapeprocessinginrats,especiallythoseofGaffanandcolleagues [147,160](seeSection4.2)andZoccolanandcolleagues[118–120] (seeSections5.1 and 5.2).A waytoreconcile theseapparently conflictingconclusionsis toconsiderthecrucialrole thattask’s structure,constraintsanddemandslikelyhaveindeterminingthe complexityof thevisualrecognitionstrategyin rats,aswellas inother species(including nonhumanprimates; e.g.,see [180], discussedinSection5.2.3).Thattask’sstructurecouldaffectthe outcomeoftheirexperimentswasacknowledgedbyMininiand Jeffery,who pointedout how ratfailure to“discover shape”as thediagnosticstimulusdimension“mayreflecttheconstraintsof discriminationtasksratherthanalimitationinratvision”[146].

Specifically,inthecaseofMinini’sandJeffery’sexperiment,rats weretrainedinatwo-alternativeforced-choicediscriminationof

twogeometricalshapeswithfixedsize,positionandbrightness (thoseshowninFig.5A).Althoughduringthepre-training pro-cedurethesizeofthesquareandtriangleundergosomechanges insize[146],becauseofthenatureofthetwo-alternative forced-choicetask(seediscussioninSection3.3.1),suchsizevariations weresimultaneouslyappliedtoboththediscriminanda,thus pre-servingtheirrelativebrightnessinthelowerhemifield.Aspointed outbyZoccolanandcolleagues,underthesecircumstances, “com-putation of lower hemifield luminance was a perfectly ‘valid’ solutiontothetaskathand(i.e.,itwasoneofmanypossible strate-giesformaximizingrewardwithinthecontextoftheexperiment)” [118].Bycontrast,inGaffanandSimpsonexperiments[147],rats werepresentedineachtrialwithadifferentscenecomparison(i.e., aconstantnegativescenepairedtoatrial-uniquevariablescene; seeFig.3A),thusforcingtheanimalstorelyonthespecificshape oftheobjectscontainedinthescenes,ratherthanontheir low-levelproperties,suchasbrightnessorarea(seeFig.3C–E).Asafinal remark,itisworthnoticingthat,inspiteofthelackoftaskpressure touseshapeinformation,ratsinMinini’sandJeffery’sfirst exper-imentdidnotexclusivelyrelyonlower-levelvisualpropertiesto carryouttheirdiscrimination.Ifthiswasthecase,thena manipu-lationproducingadramaticreversalofthediscriminandarelative brightness,suchasshiftingupwardthesquare,shouldhave pro-ducedafullreversalofratstimuluspreference,while,infact,rat averageperformanceonlydroppedslightly(andnotsignificantly) belowchance(seeFig.5B,secondbar).Instead,suchastrong rever-salofthestimuluspreferencewasobservedonlyforthevertex-up trianglevs.diamondcomparison,i.e.,foramanipulationthat,in additiontochangingtherelativebrightensofthestimuli,alsomade thebottompartofthesquare(nowa diamond)very similarto theoriginallylearnedvertex-downtriangle,andthebottompartof thetriangle(nowahorizontaledge)verysimilartotheoriginally learnedsquare.Inotherwords,itlookslikeratsdidnotfullyignore shape–rather,theyreliedonastrategythatwaslargelybasedon abrightness/areacomparison,butwhereshapeinformation(for instance,edgeorientation)stillplayedarole.

Aspreviouslymentioned,MininiandJefferyalsocarriedouta secondexperiment,inwhichratswererequiredtodiscriminate asquarefromarectangle,basedonthedifferenceintheiraspect ratio.Theanimalseventuallylearnedthetask,butonlyaftermany sessions(∼70)andonlyreachedalow,albeitsignificantlyhigher thanchance,performance(∼65%correct).Thisledtheauthorsto concludethatratsarequitepooratdiscriminatingshapesbasedon suchanabstractmetricpropertyasaspectratio.Atthesametime, thefactthattheratseventuallylearnedthetasksuggestedtothe authors“thatratsmightbesomewhatcapableofusingaspectratio, andbyimplicationshape,tosolvevisualdiscriminations”[146].

5. Invariantvisualobjectrecognitionandadvancedshape processinginrats

Takentogether,thestudiesdiscussedinSection4,strongly sug-gest that ratsare capable of processingshape information and recognizingvisualobjectsinspiteofsomevariationintheir appear-ance (e.g., becauseof size and position changes). However,till veryrecently,conclusiveevidenceaboutinvariantrecognitionand advancedshapeprocessinginratswaslacking,becauseoffourmain limitations.First,toleranceofratrecognitiontotransformationsin objectappearancehadnotbeensystematicallytested.Thatis,none ofthestudiespresentedinSection4hadmeasuredthe depend-enceofratrecognitiononthetype oftransformation anobject mayundergo,aswellasonthemagnitudeofthetransformation alongdifferentvariationaxes(e.g.,size,position,in-planeand in-depthrotation,lighting,etc.).Thesecondlimitationisthatpure generalizationofratrecognitiontonovelobjectviewshadnever

Fig.6.BehavioralrigandexperimentaldesigndevelopedbyZoccolanetal.[118].(A)Apictureofthebehavioralrig(left),showingthreeoperantboxes,eachequippedwith monitorsforstimuluspresentation,computer-controlledpumpsforliquidrewarddelivery,andtouchsensorsforacquisitionofbehavioralresponses.Ratslearnedtoinsert theirheadthroughaviewinghole,locatedinthewallfacingthemonitor(bottom-rightpicture),andinteractwiththearrayofsensors(top-rightpicture)totriggerstimulus presentation,reportstimulusidentityandcollectthereward.ThisrigiscurrentlyusedinD.D.Cox’lab(Harvard)andD.Zoccolan’slab(SISSA).Asimilarhigh-throughputrig hasalsobeendevelopedbyP.Reinagel’slab(UCSD).(B)Schematicoftheobjectdiscriminationtask.Aftertriggeringstimuluspresentationbylickingthecentralsensor,arat hadtolickeithertherightorleftsensor,dependingonobjectidentity.

PanelBismodifiedfromAlemi-Neissietal.[120].

beenproperlytested,becauseofthemethodologicalchallengeof withholdinganyfeedbacktoratsaboutthecorrectnessof their responseingeneralization/transfertrials(seediscussioninSection 3.3.2).Crucially,failuretotestpuregeneralizationpreventsarobust assessmentofwhatcomponentofratinvariantrecognitioncanbe ascribedtoaspontaneous,purelyperceptualevaluationofvisual similarity(i.e.,toatruegeneralizationprocess),andwhat compo-nent,instead,dependsonlearningarbitraryassociativerelations amongtrainedobjectviews.Thethirdlimitationisthat,inspiteof themany(ofteningenious)stimulusmanipulationsappliedinthe studiesdescribedinSection4,nodirectassessmentofthevisual featuresuponwhichratsbasedtheirrecognitionwasobtainedin theseinvestigations.Thishaspreventeda fullunderstandingof thecomplexityofratvisualprocessingstrategy,leavingopenthe questionofwhetherthisspeciesistrulycapableofadvancedshape processing(seeSection4.4).Finally,withtheexceptionof percep-tualgrouping(seeSections3.2and4.3.2),nostudyhadtestedrats inthosebenchmarkpsychophysicsexperimentsthat,inhumans, havelinkedvisualperceptiontofundamentalpropertiesofvisual corticalprocessing,suchassurroundsuppressionanddivisive nor-malization[181,182].

InSections5.1–5.3,Iwillpresentrecentexperimentalworkthat hasstartedtoaddressmany of theseopenissues. Asdiscussed inSection6,thesenewfindingsareveryencouragingaboutthe possibilityofusingtheratasamodeltoinvestigatetheneuronal substratesofhigher-levelvision.

5.1. Ratsarecapableoftransformation-tolerant(invariant) visualobjectrecognition

Thefirstsystematicinvestigationofratinvariantrecognition wascarriedoutbyZoccolanandcolleagues[118]inastudywhere ratswerefirsttrained todiscriminatethedefault viewsof two visualobjects(seeFig.6BandFig.7A,greenframes),thenrequired totoleratesomevariationintheirappearance(seeFig.7A,light blueframes),andfinallytestedwithmanynoveltransformations ofthelearnedobjects(seeFig.7A,allremainingobjectconditions).

Inthisstudy,severalratsweretrainedinparallel,usinga high-throughputbehavioralrigthatconsistedofmultipleoperantboxes, eachequippedwithaviewinghole,threetouchsensors(alsoacting asjuicetubesforliquidrewarddelivery)andacomputermonitor (seeFig.6A).Theratslearnedtoinserttheirheadintotheviewing hole,soastofacethecomputermonitor(usedasthestimulus display),andinteractwiththesensorstotriggerstimulus presen-tation(centralsensor)andreporttheidentityofthevisualobjects (leftand rightsensors). Thisrig, and the stimuluspresentation design, alloweda few importantmethodological advancesover earlierbehavioralinvestigationsofrat patternvision.First,they allowedaverytightcontroloversomecrucialstimulusproperties, suchassize,becausethestimulusviewingdistancewasconstant andreproducibleacrosstrialsandsessions.Second,itwaspossible tocarry outa veryintensive, fast-pacetraining, withcollection ofupto500behavioraltrialspersessionpersubject.Third,and more importantly,theuseofthetouchsensorsallowedtesting ratswithoutresortingtothespatialtwo-alternativeforced-choice procedureusedinthelargemajorityofrodentvisionstudies–in anygiventrial,aratwaspresentedwitha singlestimulusonly, andhadtoreportitsidentitybyrememberingitsassociationto eithertheleftorrightsensor/rewardport (seeFig.6B).Thus,it waspossibletoovercomethelimitationofprobingratinvariant recognitionwithsimultaneouslypresentedshapes,whichmakesit extremelychallengingtopreventratsfromsolvingdiscrimination tasksusinglower-levelvisualfeatures(seediscussioninSection 3.3.1andbelow).Anothermajordifferencewithpreviousstudies wasthatthevisualstimuli,ratherthanbeingsimplegeometrical shapes/patterns,wererenderingsof3-dimensionalobjectmodels madeofmultiplestructuralparts(seeFigs.6Band7A).Thisallowed transformingtheobjectsalongnaturalvariationaxes,suchas in-depthrotationsandlightingchanges,whichareimpossibletotest with2-dimensionalshapes.Therefore,thevarietyandcomplexity ofthetransformationsthestimuliunderwentinthisstudywere muchlargerthaninpreviouswork.

In [118], ratseasily succeeded at discriminating the default viewsofthevisualobjectswitha>70%correctaccuracy,andquickly

Fig.7.ObjectconditionsandratgroupaverageperformanceinZoccolanetal.[118].(A)Thefullmatrixofsizeandazimuth-rotationcombinationsusedtotestratinvariant recognitioninZoccolanetal.[118].Thegreenframesshowthedefaultobjectviewsthatratsoriginallylearned.Thelightblueframesshowthetransformationaxesthatrats weretrainedtolerate,beforebeingbestedwiththefullsetoftransformations.(B)Ratgroupaverageperformanceforeachoftheobjecttransformationsshownin(A).The percentageofcorrecttrialsisbothcolor-codedandreportedineachcell,alongwithitssignificance.(Forinterpretationofthereferencestocolorinthisfigurelegend,the readerisreferredtothewebversionofthisarticle.)

ModifiedfromZoccolanetal.[118].

learnedtotoleratesizechangesbetween15◦and40◦ofvisualangle (seeFig.7A,verticallightblueframes)andin-depthazimuth rota-tionsovera_±60◦span(seeFig.7A,horizontallightblueframes). Followingthisexposuretosizeandazimuthchanges,ratswere testedwithalargebatteryofobjectconditions,obtainedby com-biningallpossiblepreviouslytrainedsizeandrotationvalues(i.e., allobjectconditionsshown inFig.7A).Crucially, mostofthese objectconditionswerenewfortherats(i.e.,thoseoutsidethelight blueframesinFig.7A).Ratrecognitionperformancewashighand significantlylargerthanchanceforvirtuallyalltested transforma-tions(seeFig.7B),theonlysubstantialdropbeingobservedforthe smallesttestedsizeof15◦ofvisualangle(likelybecauseofratpoor visualacuity).Thisresultshowshowratscantoleratesubstantial variationinobjectappearanceacrossverydifferentvariationaxes andtheircombination.It alsosuggeststhatthis abilityis likely rootedinageneralizationprocess,basedontheperceived simi-laritybetweenthetransformedandtheoriginallylearnedobject views.Infact,giventhelargenumberoftestedconditions(108),it wasunlikelythatratssucceededinthetaskbylearningand memo-rizingthecorrectassociationbetweeneachnewlypresentedview andthecorrespondingrewardport.

Thatratinvariantrecognitionwastheresultofpure general-izationwasalsoexplicitlyandrigorouslytested,bywithholding anyfeedbacktotheratsaboutthecorrectnessoftheirresponsefor afractionofthenewtransformations(approximately11%, cover-ingacontiguousquadrantofthesize-viewmatrix,witheachrat beingtestedwithadifferentno-feedbackquadrant).It isworth noticingthat,differentlyfrompreviousstudies,these generaliza-tiontrialswerenotjust“alwaysrewarded”(atrainingstrategythat, asdiscussedinSection3.3.2,canleadtoeitheranoverestimation orunderestimationofratrecognitionaccuracy,dependingonthe choicesofananimalonthefirstfewgeneralizationtrials).Rather, afteraratmadearesponseinageneralizationtrial,thestimulus wasimmediatelyremovedfromthedisplay,thetrialended,and theanimalwasallowedtotriggerthenexttrialrightaway.Thefact thatratrecognitionperformancefortheseno-feedbackconditions wasashighasforthe(size-matched)feedbackconditions(inboth cases,itwas∼75%correct),andbothwereashighasthe perfor-manceovertheoriginallytrainedsizeandazimuthaxes,indicates

thatratswerecapableofpuregeneralizationtonovelobjectviews. Thisconclusionwasfurthercorroboratedbyobservingthat “per-formancewashighandsignificantlyabovechance[_...],evenfor theveryfirstpresentationofeachnovelstimulus,andremained stableoverthecourseoftheexperiment”[118].Asafinal assess-ment ofrat generalizationability, Zoccolanand colleaguesalso introducedtransformationsalongtwonewaxes–in-depth ele-vationrotationandlighting(allthesenewconditions,15peraxis, werepresentedinno-feedback,generalizationtrials).Performance wasabovechanceforallbutoneofthenovellightingconditions (withanoverallrecognitionaccuracyof∼75%correct),andallthe novelelevationconditions.

Overall,theseresultsledZoccolanandcolleaguestoconclude “thatratswereabletogeneralizeacrossa widerangeof previ-ouslyunseenobjecttransformations,includingnovelcombinations of sizeand in-depthrotationsof thelearned objects[_...],new lighting/shadingpatternsovertheobjects’surface[...],andalso substantialvariationinobjectsilhouette[...]”[118].Althoughthis studydidnotexplicitlyaddresswhatobjectprocessingstrategy underlayratinvariantrecognition,severalfactorsargueinfavor ofhigher-level, shape-basedprocessing,rather thanrelianceon lower-levelvisualproperties.First,becauseeachviewofanobject waspresentedinisolation,aratcouldnotdirectlycompareittoa similarlytransformedviewoftheotherobject,asittypically hap-pensinspatialtwo-alternativeforced-choicetasks(seediscussion inSection3.3.1).Rather,theanimalhadtoimplicitlycomparethis viewtoallotherpossibletransformedviewsoftheotherobject tosucceedin thetask. Giventhesubstantialsizevariationsthe objectunderwent,thismademanylower-levelcues(suchasthe relativebrightnessorcontrastofthediscriminanda)completely unreliableaspredictorsofobjectidentity.Inotherwords,theuse ofalower-levelstrategy,suchastheonereportedbyMininiand Jeffery[146],wasruledoutbytheexperimentaldesignitself.In addition,Zoccolanandcolleaguesperformedastimulusanalysis showingthat,atthelevelofpixelorGaborfilterrepresentations (simulating,respectively,neuronalrepresentationsinretinaand primaryvisualcortex),theaverageimagevariationproducedby changingtheappearanceofanobjectwaslargerthanthe aver-agevariationbetweenmatchingviewsofthetwoobjects.Inother