CHAPTER4 COLOUR AND THE CORTEX: WAVELENGTHPROCESSING IN CORTICALACHROMATOPSIA

CHARLESA. HEYWOOD, ROBERTW. KENTRIDGE, AND ALAN COWEY

Introduction

One of the perceptual consequencesof being able to processwavelength differences in the distribution of spectrallight is the chromatic world in which we live. The privacy of colour experienceis undisputedand is reflectedin the term'quale'coinedby C.I. Lewisin 1929to describesuch qualitative content of mental states.However, notwithstanding the philo- sophicaldebate that such a notion hasfuelled, few would deny that we live in a colourful world-never more so,perhaps, since the l8-year-old William Henry Perkin serendipitously discovereda purple aniline dye while attempting to synthesizequinine from coal tar in the mid-nineteenthcentury, and spawnedthe wealthof dyesand pigmentsthat arecommon- placetoday. What doesit mean to havecolour vision, i.e.what are its defining characteristics,and what advantagesdoes it confer on its possessor?Ascribing colour vision to an organism requiresno more, and no less,than the demonstrationthat two spectrallydifferent stimuli, made equally bright with respectto an animal's spectral sensitivity,are discriminable. Alternatively,colour vision can be demonstratedwhen discrimination remains possible when random fluctuations in brightness are introduced into two stimuli of different spec- tral distributions,i.e. the discrimination must be made on the basisof colour differences alone.Almost all vertebratesand some invertebrateshave colour vision, some in a rudi- mentary form, but differ in the number of photoreceptortypes and their spectralcharac- teristics.Trichromacy, however, is the norm for all Old World monkeys,apes, and people. But what role doescolour play in vision?One way this canbe addressedis by assessingthe variation in colour vision acrossa variety of specieswith respectto the visual environ- ments they inhabit. Good examplesare the demonstration that the spectraltuning of long- and middle-wavelengthretinal conepigments of frugivorousplatyrrhine monkeysis optimal for detecting their dietary fruits concealedagainst a variegatedfoliage (Regan et al., 1998)whereas that of African Old World monkeys and chimpanzeesis appropriatelr' tuned for detectingyoung green shoots among other and lesstasty foliage.This revealstn'o of the selectivepressures that haveoperated on primate vision during the evolutionot dichromacyand trichromacy.One role of colour vision, therefore,appears to be the rapid detectionof a particularobiect colour rvhenluminance differences alone rvould providc CULUUK AI\U TN ambiguousclues to its location. Moreover,a stationary object standsout i': ' '.rck- ground on the basisof, among others,luminance, texture, and chromati. ':.es. Spatialor temporalvariations of luminancewould maskan object'scontours ,, :Jr it invisible to a monochromatic observer,suggesting a further role for colour '. - :he segmentationof the visual scene.Finally, colour variation assistsin the rc'., - ': ,ri objects.For example,there is ampleevidence that colour playsa conspicuousr,' . ...r1 signalling,the identificationof conspecificsor, to usea much citedexample, an ..' . -:: of the ripenessof dietaryfruit from its externalappearance. However,there are attendant problems in the designof a systemwhere reflect:.. - ' differentially reflect light of wavelengthsthat constitute the visible spectrunr spectralcomposition of the illuminant can vary widely from moment to mt':- throughout the day.In the natural environment,much of the former variation dc:'. whether an object is illuminated by direct sunlight or the shorterwavelengths ot .. illumination producedby Rayleighscattering. The latter arisesfrom a combinati,': greatersusceptibility of long-wavelengthlight to atmosphericabsorption and thc :: . attenuationof shorterwavelengths as a resultof scattering,the effectof which incr..,- - ' the sun approachesthe horizon.It haseven been suggested that the principalopf,'::. axis of trichromatic vision, blue-yellowand red-green,is an adaptationto such nat..:. - occurring variation in terrestrial illumination (Shepard,1992) . Yet colours remaiIr ; . ceptuallyconstant, and suchconstancy must be a prerequisiteof a biologicalsystem rr'ir :. i-. fulfils the purported roles assignedto it, namely the facilitation of object detection. segmentationand, most notably,identification. Another clue to the role of colour vision can be derivedfrom behaviouralstudies oi peoplein whom colour vision is depleted,as in casesof retinal colour blindness,or r.'hcr. colour vision hasbeen perhaps entirely deletedas a result of a cerebralaccident. It is n,'',' establishedthat damageto human ventromedialoccipitotemporal cortex .un .J.15..;t,., '..: vision, a condition known ascerebral (Damasio et al., 1980;Kijlmcl. . " ' Heywood et al., l99l). What light can the examinationof such patientsshed on thc :'. - siblecosts and benefitsto thosewho possesschromatic vision? One consequenceof brain injury canbe a selectivedisorder of vision.f{1r\r{iii. ii - selectivityof a deficitis only asnarrow or broadas the specificitvof the bch.rvi,,.:r.,.i.,'r that is usedto studyit. Examplescome from visualagnosia (the lossoi lisu.rl l.u'.::, ': :.,- : . - orauditoryrecognitionofobjects,withoutlinguistic,sensor\-,orattentiott.tl l,'.. ..:: :' -.' agnosia,appropriate tasks can further pinpoint the impairn.rentin sontcP.rli(r::. .,\ .: \- .. tiveloss of visualrecognition of living comparedu'ith non-living,itenr:. or litL ..:. ":'i, other patients.Alternatively, the recognitionof facesmav be selectilclv J i.l .:: :'. .: ..- ' prosopagnosia,but evenin the latterdisorder deficits can be confinedto .iit:i.'.:.:.r. i . recognitionoffacialexpression,gender,oridentity(seeCorver'. 199-1.J,';;1'. 1q:. .'.l -- the refinementof behaviouraltasks can more accuratelv def-ine n'hat is lti.l.'.r::.:: ' ':' is equallyinformative about the componentProcesses of a particularI irtt.i.: -.:r.: i certainvisual functions, particularly those that arecomnronlv dc'scri[.cc .i. .' ;' might seemunlikelv that the surprisingdissociations of the sort descril'cJi:: ::'.. : * -- orderprocessing of objectand face rvill be observed. For ntnenronic or liniu:.::- .:':'-." colourprocessing, brain damage can disrupt the abiliti'to nantL'.1 it,..';.::r.i '..'- :' ' - l.t'rintto ir namedcolour, as in colouranomia iOxburv cr,l/.. 1969 . (r!-\::.:.::': :.-- .- but sparethe latter,as in disordersof short-term colour memory (Davidoffand Ostergaard, 1984).The deficit may be confined to a failure to respond correctly when askedto provide the appropriatecolour name when confrontedwith the verballabel of a common object, 'What for example, colour is a banana?'(Kinsbourne and Warrington, 1967;Lszzattiand Davidoff, 1994).However, in none of theseinstances is there any difficulty in telling colours apart and colour vision itself, that is the experienceand discrimination of colours, remainsundisturbed. Nevertheless, our experiencewith monochrome imagesreadily allowsus to imagine a world devoid of colour. This, and the evidencethat colour can be processedpreattentively (Tieisman and Gelade,1980) and may therefore constitute a visual primitive, together with the abundant physiological evidencethat colour is processedrela- tively independently,might encourageus to believethat processingof wavelengthvariation in the visual scenecan be selectivelydestroyed. The descriptionofpatients with cerebral achromatopsia,also called cortical colour blindness,where brain damageappears to have selectivelyabolished colour vision, confirms this belief (seeZeki, 1990;Cowey and He1'wood,1997, for reviews).But perhapsthe very easewith which we can (unlike, for example,the perceptionof shape)imagine a world in which colour hasbeen deleteddis- couragesexamination of the degreeto which other aspectsof wavelengthprocessing may be spared.Thus, colour vision being the phenomenalcounterpart of the processingof wavelengthvariation, the loss of the former may be held to imply an absenceof the latter. Does the absenceof colour vision preclude the use of wavelengthdifferences to determine other objectproperties? It is becoming increasinglyapparent that the preoccupationwith the discrimination paradigm to characterizethe qualities ofthe visual input, by requiring decisionsto be made about a array,neglects the nature of the responserequirements (seeMilner and Goodale,1996,for review).Conventionally, it is assumedthat whether visual choices in a discriminationtask entail a verbal,pointing, or any other motor responseis unimpor- tant. Recentreports make it is clear that certain motor output systemshave privileged accessto different visual inputs. For example, intact visual pathways can still accomplish visuomotor or other orienting responses,albeit in the absenceof consciousawareness of the properties of the visual stimuli that elicit them. And the clinical condition of blindsight is characterizedby an absenceof acknowledgedvisual awarenesspatients in patients who neverthelessperform well at forced-choiceguessing tasks. Blindsight has been considered 'unconscious an example of vision',but equally likely it is the residual motor capacitiesthat remain, but which do not contribute to the consciouspercept. This view has been used to account for visuomotor abilities in casesof visual form agnosia,notably patient DF, whose impaired discrimination of orientation and shapecoexists with accurateand appropriate visuomotor actsrequiring the coding of thesestimulus attributesfor their successful execution (Milner et al., l99l). Thus the notion, derived from the widespreaduse of the discrimination paradigm, that multiple visual inputs give rise to a single representationwhich generateswhatever responseis required, suggeststhat deletion of a single attribute merely abolishesall responsesto that attribute. However,the demonstration that there are multiple visuomotor output channelsmediating different responseswarrants an examinationof the extent to which the processingof wavelengthdifferences can mediatevisuomotor responsesin the perceptualabsence of perceivedcolour variation.If residualwavelength processing is a k.r' ture of thosewho lack chromaticvision, then to what extentcan this be considerc.i.r:: 'non-conscious'processing, exampleof asin the caseof blindsightand visual-forrnir{nr r...: (seeHeywood et al.,l998a,for review)?Perhaps judicious choiceof responserequir.'rrr.:::. could exposevisuomotor channelsthat rely on wavelengthvariation to mediater€sprr1:... Moreover,covert visual processes require that the presentationof a visual stimulusclii::. .- responsethat dependson the very property of the stimulus of which the observer.lc:'. :. - conscious,or phenomenal,awareness. Given the ubiquitousrole that colour plavsin r';.:, :: it is plausiblethat the lossof colour experience,i.e. the discrimination of thc :u::.,.. property,does not compromiseall its putativeroles, or eventhat coloursmaybe eltlc:.:::., discriminatedin achromatopsiawithout the subjectacknowledging colour awarenc\..

Cerebral achromatopsia ' Cerebralachromatopsia, as its name implies,refers to a lossof colour vision rvhcr.'l'.:: r r : . remark that the world is drab and devoid of colour. The severityof the deficit i: r.r:..i:' . and the lossof colour vision is most frequentlyincomplete. The hallmark of thc c()r.: :. ' is poor performanceon the Farnsworth-Munsell100-Hue test which entailsth.' chr,':::.r:.. ordering of a number of isoluminant colouredsamples and whereerror scores.r rc i: .r. - -: tiveof theseverityoftheimpairment.Achromatopsiaisfrequentlyacconrplnic.::'. -' upper visualfield lossand prosopagnosia(Meadows, 1974), reflecting the prorinritr . : " - brain damageresponsible for the colour impairment to primary visual corter .ln!i .::.-- turesinvolved in faceprocessing, respectively. A sourceof disagreementabout thc nl:.::. : achromatopsiaperhaps derives from the difficulty in sharply distinguishirlsirgl;r rr: patientswith a partialcolour loss and thosewith a denseimpairment. Tests t,t'.,'.,,..: vision can differ in the ertent to which they assesscolour detection,identit'ication. r': -r - mentation.Residual abilities may reflecteither partial damageto a brain regir'rn'p(.:.'... -' for colour perception,the putative'colourcentre' revealed by functional imasins.., ': i', to functionaldissociations revealed by differenttests. For example,in a caseot-ini,'::::' .'. colour loss(Victor et a1.,1989) the patient wasable to pick out a colour.'d.gu.r:r ..-: roundedby 39 irrelevantsquares of the complementaryopponent colour, \'c't \{r. u:.i:'.- - identifr and sort colours.The authorsproposed that intactcolour-opponent nrc.ir.i:'...:::. in striatecortex mediate colour detection,whereas identification and colour :\)rrrn- :r.; theintegrityofthe'colourcentre',i.e.theventromedialextrastriatecorticalra'gi1rr;'.r:-.-.i:. invariablydamaged in achromatopsia.Equally plausibly, the lesionnri{hl ::, : :., , - abolishedthe cortical'colourcentre'in its entiretyaccounting both tbr in.i)nrl';i:r::r.. : the achromatopsiaand the sparedperformance in an odditytask.In this rc:pcc:.i'.,i.r:.i. with completeachromatopsia are particularly informative and it is the rcsult: ,'t .\:i:-.. . - studiesofone suchcase which aredescribed here. PatientMS (Newcombeand Ratcliffe,1974), now a 5O-1'ear-oldman. sut-tcr.J .::'. .:::J-! of herpessimplex encephalitis in 1970.Repeated testing since 1971 rercals th;r n:. ., ::.: tion is stableand consistsof severeachromatopsia along rvith a leti homon\'!u(,...::.::: anopian'ith macularsparing. Using the incrementthreshold techniqu.'t,f :tlr- .'-' \lollonetal.(1980) shorvedthatthedeficitisof central originandthat\t:rc:.r:::-:''::. functional conemechanisms. Thus, his retinal trichromatic mechanismsare intact, but he lacks the processesthat compare the output of the three cone types and hence can say nothing about the colour of a visually presentedsample.

The'colour centre'

Whilst early accountsof loss of colour vision as a result of extrastriatecortical damage (Brill, 1882;Verrey, 1888) met with much scepticism,the advent of neuroimaging allowed the demonstration of increasedcerebral blood flow in an area of cortex when observersview chromatic scenes(Lueck et aI., 1989;Zeki et al., L99l). The activated 'human region, dubbed the colour centre' and invariably damagedin casesof cortical colour blindness,has now becomethe subjectof considerabledisagreement. At issue 'colour is the proposalthat the centre'is analogousor homologousto the fourth visual area,cortical areaY4,which has been identified among the two dozen or more visual areasthat occupy closeon a third of the neocortex of monkeys.It is becoming increas- ingly difficult to sustain such a view. First, the original report (Zeki, 1973) that all77 cells sampledin areaV4 werecolour selectivehas been widely contestedand the proportion of cellsassigned such a role has subsequentlydwindled (seeTootell and Hadjikhani, 1998). Second,ablation of V4 in the macaquemonkey fails to producesevere deficits in hue dis- crimination that are characteristicof the human cerebralachromatopsic (Heywood et al., 1992). Third, disturbancesin pattern vision, which accompanyY 4 removal in the monkey,are not uniformly apparentin casesof achromatopsia.The responseproperties of single cellsthus lends little support to the notion that V4 playsa principal role in the 'colour perception of colour and its deletion fails to mimic the loss of the centre'in people. A recent functional imaging study provides a clue to the discrepancyand suggeststhat the human'colour centre' is distinct from areaV4 (Hadjikhani et al., 1998).A comparison was made betweenthe location of those areasactivated more by colour than luminance variation and retinotopic areal boundaries derived from functional magnetic imaging. In addition to foveal activation of previously describedcortical areasVl, V2, V3/VR and the region suggestedto be the ventral subdivisionof V4 (V4v), a more anterior region in the middle of the collateral sulcus respondedpreferentially and robustly to colour. Moreover, unlike V4v, it was activatedfor the duration of colour-induced after-effects.The newly chartedarea has been named areaV8 and its location correspondsto the cortical'colour centre'previouslydescribed as'human V4', whoseremoval results in the completeloss of the consciousrepresentation of colour. Consistentwith the existenceof colour impair- ments affecting an entire visual half-field, V8 contains a completeretinopic map of the contralateralvisual half field. This is quite unlike V4v, VP, and inferior V2 whose represen- tations in eachhemisphere are confined to the upper visual field. Nevertheless,the discovery of a region anterior to and distinct from V4v has not resolvedthe debateas to whether the 'colour centre'is'human V4'. There remain those who staunchlydefend the correspon- denceand preferto view areaV4v,and its dorsalpartnerV4d, asinterlopers that appearto have no monkey equivalents (Zelo et al., 1998).The matter will presumably rest until the monkey counterpartto areaV8 is finally revealed.More recently,regions anterior to area COLOUR AND THE CORTE\

Y4 havebeen implicated in colour vision (Katsuyamaet aI. 1997;Vanduffel et al., l9e' Metabolic labelling and electrophysiologicalrecording suggesta high proportion , : colour-selectivecells in anteriorand inferior portions of the temporallobe (Komatsui: .:. 1992) and,indeed, complete destruction of theseregions renders monkeys achromalt\)l'-:. (Heywood et a1.,1995). 'colour Regardlessof the terminologicaldispute, the propertiesof the centre'rnr: ::. invariableinclusion in the generallymore extensivecortical and white matter damagc...:r in achromatopsiastrongly suggests that it is a region responsiblefor our consciousp.c:.. :' tion of a colouredworld.

Processingwavelength differences

PatientMS fulfils the conditions of frank achromatopsia.His brain damageinclu.:. - " - regionof putativearea V8 (Heywoodet al., l99l), he is unableto name or sort ., ' ..- . and his scoreon the F-M 100Hue testis consistentwith random orderingof chr',:::.,' chips.What, then, can he tell us about the benefitsof possessinga perceptu.rl rc:': - - - ' tation of colours?Normal observersfind colour differencesmore effectiveth.i:r i-:: -- shapeor brightnessdifferences in guidingvisual search (Williams, 1966),retlcc::::- " . importanceofcolourvisionintherapiddetectionofobjectsinthevisua1sccIl!,.( bestowsno suchadvantage on MS. He failsto perform eventhe crudestcolour.ii..::'-' inations when presentedin an oddity task.Yet whilst MS has retainedno ..r1..r..:.. comparethe outputs of his conemechanisms there are occasionswhere his r.\i, ::.-. can be determinedby wavelength.It is commonplaceto testchromatic vision l.r :. ..' ing the conveyorof chromaticinformation, namelythe P-channelof visual pr().f\- :'- that originatesin the PB cellsof the primateretina and comparesthe out1.ut.,,i i:'- threecone classes in an opponentmanner. This canbe achievedby producin,.:c\lr::.,."' nant displaysthat contain no luminanceinformation and arethus pre\unrr\:: - invisibleto the M-channel,the broad-bandpathway which sumsthe actiritr ,'l :--::.:.:- and long-wavelengthcones. However, equiluminant chromaticcontour it..'li i,'::::'- misesthe P-channel.Colour-opponent cells receiving excitatorv and inhil.it.':',::'.:'..' from differentcone classes are antagonistic for luminancebut svnergistic.\rl(,'.::',.:-. tion. The colour-opponentpathway that conveyschromatic infornration .rl',' - :"., . spatialdetail. Real world scenesvary in both colour and luminanceand r'q11:1.:::':' -'' chromaticcontour in the naturalworld is exceptional.Thus attemprls1,r .,.:: ::- ' isolateluminance and chromaticmechanisms ignore their substanti.rlintcr-:-:: :' patternvision and may concealthe evolutionaryreason for endon'ingthq' r'i-i:.:. .'. .'.'- with the capacityto representa colouredworld. If one reasonis to dr-tr-ct.lr'..ri, ,- recognizeobjects, then the registrationof conspicuouscolour difterenc..sl\.r :::. :, :- ableguide than luminancevariation in a world whereshadorr's arg ppgl'.11.:r:.\:- ,.: .' influencewavelength distribution very little and thus colour prolidc's.r lllr\ii r r- .i - representation.Moreover, the greatersensitivitv of the p rin'ratc' r'i: r.r.r i \ i \: i ::: ' spatialfrequency colour r.ariation is ideallvsuited to the taskoi s.'snrenti::. ,,1'. - " the basisof colourdifferences. To rvhatextent. then, does cerc'bral Jchr(rln.ll(,:'.r., :': " ' ct't'icicntsccne seqnrcntation? orm from colour ne first hint that patient MS retained the ability to segmentthe visual image on the basis 'colour was the earlyreport of his ability to read the conventionaltest of retinal colour indness,the Ishiharapseudoisochromatic plates, when presentedat 2 m but not at read- g distance(Mollon et aL, 1980).This was later confirmed where it was further shown that rtical blurring had the sameeffect (Heywood et aL, I99l). The Ishiharaplates are com- lsed of discretecoloured spotsdefining a target figure, embeddedin similar spotswith Lryinglightness. The most salientcontours are thosedefining the circumferenceof indi- dual spots.The observermust readthe digit by associatingspots of the samehue over a latively large areaof the field. When the plate is viewed at a distancethe contours defin- g the spotscannot be resolvedand the dominant contour becomesthe much larger hue rundary around spotsof a particular hue. It is plausiblethat MS detectsthis chromatic rundary. In addition, MS is able to distinguishbetween boundaries composed of two abutting luiluminant colours when the salienceof the boundary is varied by selectingcolours ore or lesswidely separatedin colour space.A property of broad-band cellsin the M- rannelis that they continue to respondto a chromatic border falling in their receptive ld regardlessof the relativeluminances of the coloursof which the border is composed, :. they signal chromatic borderswithout coding information about the constituent rlours(Saito et a1.,1989). Thus an appealinglysimple view is that achromatopsiaresults om destructionof the P-channelof visual processingleaving the M-channel to mediate sidualvision. One meansby which this proposalcan be testedis to presentMS with rromatic displayswhere luminance is either spatiallyor temporally varied. With rapid rctuations of the luminance of components of chromatic visual displaysthe broad-band stem is renderedineffective in distinguishingbetween chromatic and luminance con- ast.Distinguishing the chromaticproperties of the displayis then reliant on the colour- )ponent pathway.MS was shown an achromaticchequerboard where the luminance of .chsquare was randomly assignedfrom moment to moment. When a desaturatedhue asintroduced into a single square,while maintaining luminance modulation, MS was rable to indicate its position. To him the squareswere indistinguishable. However,when ne squareswere replacedby a desaturatedcolour to form a cross,MS promptly detected i presenceand location on the screendemonstrating that he can perceptuallysegregate rromatic and luminance boundaries into figure and ground to revealthe cross(Heywood al., 1994).Thus, MS can usewavelength to extractform but lacksany phenomenal perienceof colour itself. Similar resultshave been reported for casesof incomplete achromatopsia (Barbur et al., )94).Threshold measuresof the detectionof a colour changeand for the extraction of imulus structure,whilst identical in normal observers,areyery different in casesof completeachromatopsia. This suggeststhat different and independentprocesses under- ing the generationof perceivedobject colour and the constructionof spatiallystructured ljectsfrom chromaticsignals. Deletion of the'colour centre'abolishesthe former but aresthe latter. LULUUR ANIJ 1Hh LUKI I-\ lY

The P-channel

It hasbeen suggested on the basisof colour perceptionprofiles that achromatopsiacr'r:-:. tutesa family of colour disorders(Rizzo et a1.,1993). Achromatopsic patients diffcr in :::. degreeto which cortical contributions to colour vision are preserved,e.g. the abilitr' :-.,,.: the Ishiharaplates. A possibleexplanation is that the severityof the deficit merelv rnir:. :. the extentof damagein the'colour centre'.However, neuroimaging studies shon' con.iJ.: ablevariability in the number and location of areasreported to be activatedwhen suh:r.: . perform colour-relatedtasks, depending on both the nature of the visual displ.rr'.r:'.: whetherthey entail,for example,passive viewing, activediscrimination or directc.l.r::.: tion (Corbettaet a1.,1991;Guly6s et al.,1994; Kleinschmidt et aL,1996).It is equ.rllr.:^- that the pattern of functionaldissociations depends on damageto other su.h .i:-. . engagedin the processingof wavelengthdifferences. Detection of chromaticbordcr. r:-.: . presenceof random luminancemasking in MS suggestsa contribution of colour-o[.1.,' - processesand severalother featuresof his vision support this claim. . Measurementsof spectralsensitivity (Heywood et aI., l99l) do not showa sin{lc 1...,. . approximately550 nm aswould be expectedif sensitivitywere determined bv .r l.:, .,.: band channel.Instead, MS showedsensitivity peaks at three differentwavelength.. :::.: - tive of colour-opponentmechanisms of the P-channel(Sperling and Harwerth.;'-. . addition, MS hasnormal thresholdsensitivity for the detectionof sinusoidallvrl,'.:...-,:- isoluminant chromaticgratings which elicit a visuallyevoked cortical potential Hc',.,' . et al., 1996).Itis feasiblethat gratingsensitivity is mediatedby residualbrightness rc\l( ,::-- . For example,normal observersjudge saturatedhues as being brighter than their lur':r;::.,::-. predicts(Wagner and Boynton,1972) and mixtures of red and greenlights rc.u.: .:' yellow which appearsconspicuously dimmer than would be expectedon thc lr.r.:. simplebrightness additivity (Guth, 1965).MS retainsthese residual brightnc.. rc.l., : - which are neverthelessinsufficient to accountfor grating sensitivitr'(Hevrr'orrii: .. 1998b).

Motion from colour

The experimentaldevice of equiluminantstimuli, varying in chromaticbut not ilu:r::'..i:'- contrast,has been considered a meansof silencingthe M-channeland er'.ilu.i::::j ::: capacityof the P-channelin isolation.The assignmentof colour and motion Pr(r.u\\::'.:: the P- and M-channels,respectively, has buttressed the common beliei that tirc.r ::. attributesundergo independent processing. The substantialreduction in thc .r:.:..,:.: speedof suprathresholddrifting chromaticgrating, compared rr'ith th.'ir lu:r::::.,:'-. modulatedcounterparts, and the greatercontrast required to determinethc .iirr.:. :: motion of a drifting equiluminantgrating, compared with the thresholdtor itr .lc:r.: areboth consistentwith this view.In eachcase, chromatic motion n'asintcri.rcic.i .,. "r ' mediatedby a residualbrightness response from a luminance-basednrotion nr(.:'..,:r--- However,several instances where colour clearlyinteracts n'ith motion suSu.c.irl'.r :'.* - perhapsless independent than originallythought. The motion of a chronr.rtii!:.i::::: -., be nulled by superimposing a luminance grating moving in the opposite direction (Chichilnisky et al., L993)and prior exposureto an equiluminant stimulus can induce a motion after-effecton a luminance-modulatedstimulus (Mullen and Baker,1985). More recently,it has been firmly establishedthat the motion pathway is not colour-blind and that a colour-opponent pathway underlies judgements of chromatic motion (Cropper and Derrington, 1996).This pathwayhas a high sensitivityto colour, respondschiefly to low temporal frequencies,is sensitiveto direction of motion but does not code velocity veridi- cally (Gegenfurtner and Hawken, 1996). This pathway differs from the better known motion mechanism residing in the middle temporal area (areaMT) which respondsto higher temporal frequency hasa high sensitivityto luminance-definedstimuli and codes contrastveridically. Moreover, it treatscolour in the samemanner aslow-contrast lumi- nancevariation without signalling the colour itself. A third line of evidenceshows that MS is processinginformation about wavelength.MS was presentedwith red/green,equiluminant horizontal sine wave gratings (Heywood et al., 1994).To a normal observer,if the grating is phaseshifted by 180' at I Hz (the red bars becomegreen, and vice versa,each second), then the direction of apparentmovement of the grating is ambiguous and frequently changes.By shifting the phaseonly by 90o,either upwards or downwards,the direction of motion is now unambiguous.However, in the absenceof any information about which bar is red and which green,the ambiguity should remain. Remarkably,MS flawlesslyindicated the'correct' direction of apparent movement although he remained unable to distinguish the colours of which the grating was com- posed when they were presentedin an oddity task. Mysteriously,MS can detect the sign of colour contrast without experiencingthe colours. Functional imaging revealsthat areaMT is activatedby chromatic motion (ffytche et al., 1995)and cellsin this region of the monkey respond,not only to chromatic borders,but to colour information of the sort describedabove, i.e. 90'phase shifts (Dobkins and Albright, 1994).Is there evidencethat the parvocellular contribution to motion remains intact in achromatopsia? The'slow'chromatic motion pathwaythat is exquisitelysensitive to chromatic contrast neverthelessdoes not code velocity veridically,which presumably accountsfor the 'motion perceivedeffect of slowing' when the chromatic grating is compared with an achromatic grating drifting at the samespeed. Chromatic gratings are conventionally con- structed by modulating a red and green grating in spatial antiphase.However, colour- opponent,P-channel processing displays marked subadditivity.The combination of tlvo opponent colours,e.g. red and green,results in hue cancellationsuch that the colour mixture is perceptuallydimmer than would be expectedon the basisof the sum of their individual luminances(Guth, 1965).This is becausea colour-opponent(e.g. red+/green-) receptivefield will be maximally excited and inhibited by long and middle wavelength light, respectively.The converse occurs for cells showing opposite opponency (green+/red-). However,a mixture of middle- and long-wavelengthlight, producing yellow,will placeexcitatory and inhibitory mechanismsof the receptivefields in equili- brium and the nulling of the responseresults in a perceptuallydimmer, subadditive colour mixture. Gratingscan thereforecontain unintendedbrightness variations which are most conspicuousmidway betweenthe red and greenpeaks, i.e. at twice the spatialfrequencv of the red/greengrating where red and greenmaximally overlap.Such brightness responses COLOUR AND THE CORTI-. . may then renderthe gratingsand their motion visibleto an achromatopsicprtir':r' whom suchresidual P-channel responses are demonstrable,such as MS. Yetrr'hc:: : brightnessvariation wascorrected, by the addition of frequency-doubledluminancl. ::: , ' -. wasa further reductionin the apparentspeed of the grating (Hepvood et al., 19981.. wastrue for both normal observersand for patientMS. This finding is difficult to rc'i, : - with anlthing other than normal processingof slow equiluminant chromaticmoti(':r , when,for MS, the coloursare indistinguishable. Similar sparedmotion processesnr .:.-r" matopsiahave been demonstrated in threefurther patientswhere a strons nr, : responsewas producedby movement of high contrast,equiluminant chromatic g:.,' (Cavanaghet a1.,1998).The strengthof the preservedmotion responsewas qurlrt;::-. gaugingtheequivalentluminancecontrastrequiredtonullit.Despitegrosslvin::'.- sensitivityto chromatic contrast,comparable to that of congenitallyred-green .i.: - observers,high-contrast equiluminant gratingsproduced a robust responseequrr., -' that of normal observers.Moreover, the strengthof the responsewas some fi\'e t(r if :: ' greaterthan that expectedfrom chromatic responsesmediated by areaMT. Br' ;, ::'- congenitallyred-green deficient observers showed only a weakresponses to ci'.: : motion consistentwith their retinal conedeficiency. In addition, none of thc :'.,' - showedevidence of other residualP-channel processes, such as those described ir l. I . Colour aloneappears to be a sufficientcue for the detectionof visual motion. \":: . ' is a departurefrom the notion that colourand motion processingproceed indclr:--:-. it should come asno surprise.The luminancedifferences in the natural sceneai:..:r* :- fluctuating shadowsand highlightsintroduce ambiguitiesabout the motion rn.l -:: .:'- anobject.Theexploitationofcolourdifferencessubstantiallyreducessuchanrl.i:-:,:.. lessonto be learnedfrom achromatopsiais that the lossof the perceptualex1.g11.,--.- colouredworld neednot compromisethe ability to processwavelength diiic:.:--,,. derive form and motion information.

Colour constancy

Colour constancyrefers to the phenomenonwhereby colours appearunchans.:-.- .: - . considerablevariation in the spectralcomposition of the illuminant. Onc rr.r',::: - - achievedis for the visualsystem to comparethe spectraldistribution of light rt't.r . i - .t " disparatesurfaces in a visualscene and to attribute an overallincrease in l 1..11-11.....r,.. band asa changein the illuminant. Suchlong-range interactions across thc vi..:.r. :-- .: a featureof many computationalaccounts of colour constanc)'.Cortical arc'.r\'l l-,.,.' fore been stronglyimplicated in colour constancybecause of the report th.rt :i:c :. -:' of the cells,unlike that of cellsin areaVl, is not determinedbv the rr'avclc::-::-. wavelength "- incidenton the receptivefield, but dependson the conrl.ositior:": : surroundingareas (Zeki, 1983). Moreover, the largereceptive fields oi cell' r::\'i. .,: .: ' widespreadcallosal connections, suggest this areaas a likelv candidatelirr r::u.:-.,:" - rangeprocesses. Since areaY4 of monkeyshas been likened to the'.oloui .r:-.::. ' :' destructionof which leadsto achromatopsia,it hasbeen entir.-lv n.rlr.::.: : 'r'--. achromatopiaasadefectinco1ourconstanc\',akintoatailtrretL].()rlSi..i.: 1990,1993). It hasbeen argued above that the'colour .entre .rnLl.rr..i \ - -:'.1::- :' t2 our oF MrND rre unlikely to be homologousbecause bilateral ablation of the latter failsto renderan rnimal colour blind, i.e.colours appearto be constructedin an essentiallynormal fashion. Giventhe chromatic responseproperties of neurons in V4, most notably their ability to discountthe illuminant, it is sensibleto askwhether V4 ablationresults in a dissociationof hue discrimination and colour constancy,where the latter may be selectivelydisturbed. Severalauthors have pursued this question (Wild et al., 1985;Walsh er al., 1993)bfi reported impairments in colour constancywere accompaniedby hue discrimination impairmentsand it is difficult to ascertainwhether the latter werethe causeof the former. It is uncertain whether achromatopsiacan be interpreted as a failure to synthesizeor constructcolours, as someauthors propose. Since cerebral lesions can abolishthe percep- tual experienceof hue, it is likely that the cortex is the sitewhere colours are constructed. However,it is not clearwhether the signalsthat are usedto generateobject colour are alreadyinvariant or whetherthe rescalingrequired to achievecolour constancyis insepar- able from the processesof colour synthesis.Thus, a failure of colour constancycould expressitself at the putative early stagewhere invariancesare derived.In this casea perceivedcolour may be determinedby the wavelengthof light reflectedfrom a visually presentedobject and an objectwould changeits colour appearancewith changesin the wavelengthcomposition of the illuminant, i.e.there would be residualcolour vision but no colour constancy.This is clearlynot the casefor MS. Alternatively,if rescalingis an integral part of colour synthesis,then achromatopsiamay be viewed asa failure in the cortical,as opposedto retinal,mechanisms underlying constancy. Incomplete achromatopsia may then reflectincomplete damage to the'colour centre'and the residualtissue may mediate rudimentary hue discrimination.Testing colour constancyin suchcases should prove informative and one such study (Kennardet al., 1995)reported pronounced and pre- dictablechanges in the naming of surfacecolours with systematicchanges in the illumi- nant, demonstratinga failurein colour constancy. Thereis strongevidence to suggestthat one of the chief mechanismsof colour constancy is the computationof conecontrast. The relativeactivity of a classof coneselicited b1, reflectedlight from two different surfacesremains unaltered during a shift in the illumi- nant and conecontrasts therefore act as invariant descriptorsof surfacesin a visual scene. Colour changesthat preservecone contrast in a visualscene are interpreted by the normal observeras changesin the illuminant, whereasthose that alter conecontrast are perceived aschanges in the surfaceproperty. For isolatedpatches, viewed dichopticallyin an asym- metric matchingparadigm, MS will correctlyjudge the two patchesas identicalwhen thel' elicit different cone excitationbut appearagainst different backgroundsthat nevertheless produceidentical cone ratios (Hurlbert et al., 1998).To this extent,an important mecha- nism of colour constancycan remain intact in achromatopsia.The retention of this rudi- mentary ability,albeit with raisedthresholds, is difficult to reconcilewith the repeated demonstrationthat MS neverproduces anything other than chanceperformance in select- ing the differentpatch from neighbouringpatches which differ in chrominancein a three- choiceoddity task.The ptzzle must remain for the moment but, nevertheless,his discriminationof localcontrasts does not extendto complexscenes containing nranr surfaces,where the abilityto makeglobal comparisons of conecontrasts is abolish.'d (Hurlbert et al., 1998). Cone contrast,while resistantto shifts in natural illuminants, is by itself insufficient l, accountfor a further property of colour constancy.The surfaceof an objectmust renl.r::' unchangedregardless of its position in a visual scene.An achromatopsicpatient reportc.i by D'Zmura et al. (1998)categorized colour samplesappearing against backgrounds of .i::- ferentlightness largely on the basisof the sign and magnitudeof luminancecontrast. i.(. ., colour was assignedto a differentcategory depending on whetherit waspresented asair:-: a lighter or darkerbackground. These observations are consistent with a lossof the nrccl:.r- nism requiredto makeglobal comparisons among non-adjacentsurfaces. In sunrnrl:: destructionof a regionwhich includesthe'colour centre'in man resultsin a losso[ thc pc: ceptual experienceof colour but can leaveintact the ability to make judgementson ti: - basisof localcone contrast, the mechanismwhich providesan important contributi,'r: : the perceptualconstancy of colours. The identificationof the'colour centre'wasachieved by imagingbrain regionsr' ir:, " werepreferentially activated by passiveviewing of colour Mondrians in compari.,,rr,' ." their luminancecounterparts (Lueck et al.,1989).Most naturalvariations in the illunrir.r:'' involvechanges in chrominanceand luminanceand it would be surprisingii thc i.:.r ' regionsresponsible for colour constancyweredifferent from thoseunderlving lisi::::.-. constancy.Consequently, it may be expectedthat suchregions would be actir-atcdcllr.:.: : by luminanceand chrominanceand not readilyrevealed in imaging studiesthat cor::'.'.,:. activationas a result of passiveviewing of theseattributes. Imaging studiesusing t.r-.- .' which colour is behaviourallyrelevant have now identifiedadditional areas in rnlc:. - ventraloccipitotemporal cortex (Beauchamp et al., 1999).The role of eachof thesc.t,1, , ,.: selectiveareas has yet to be elucidatedbut a recentstudy suggestsa dissociationhcti..." achromatopsiaand lossof colour constancy.Rtittiger et aI. (1999)recentll. identitl.'.i t:r . 27 patientswith unilateralparietotemporal cortical lesions who showedcolour .()n-i.i:r, , deficitsin the absenceof impairments of hue discrimination. Significantlr-.the rcgr,':: : shareddamagewaslocateddistalandanteriortothe'colourcentre'inthesupcri{):.::: medialtemporal gyri.

Covert processing

Covertprocessing is saidto occurwhen a stimuluswhich failsto elicit consciousc\lc::.:r - - neverthelessexertsinfluencesonbehaviour.Inthepresentcontext,co\'ertFr().c\\:::: colourwould entaila subjectdenying any phenomenal experience of hue dit'tcrcn;.-.-..: performing efficientlyduring forcedchoice testing of colour discrimination.Rc.i.iu:. :" cessingof wavelengthdifferences from which form and motion mav be derivc.li.. .(,::::.,- . to occasionalclaims in the literature,not covert(Heywood et a/.,l99Ea . -\chr,':::.i: :" patientsaccuratelydescribe, and arevisuallyawareof, the propertiesoicottt,,ur.:r:-i.:'. t ' by equiluminantcolour contrast despite being unable to tell the coloursrl'art. I'.i::r:'.:. not engagein guessworkabout differencesthey do not consciouslvperccir c. r.lii:r: :i . .: processingresults in a consciousperceptual change in the absenceoi cc'tlt.urqu.r,::. Testsofcovertvisualprocessingareconventionalll'conductedin.r'dirtctrri r:r.t.r--' manner.Intheformer,patientsareaskedtorespondonthebasisoithe'un.cc:r;':,':!.:'.. of visualstimuli.\/erbal report, or confidenceratinss in makingir percr'pturliu!:ir:::(:': 64 oUT oF MIND usedas a measureof awareness.An absenceof correspondencebetween ratings and performanceis the hallmark of covert processing.Alternatively,'indirect'tests gauge the influence of a stimulus that is incidentally introduced into a task which ostensiblyassesses a different ability. A brief report of a direct test of covert processingin achromatopsia (Humphreys et al., 1992) describesthe patient as being 4o-50o/ocorrect at both colour naming, or when askedto point to a named colour in a collection of coloured patches. Whether this reflectsgenuine covert processes,or resultsfrom the incomplete nature of the achromatopsia,is unclear.Certainly MS provides no such evidenceof covert ability. His performance on an oddity task, requiring him to verbally indicate the differently coloured patch concealedamong equiluminant patchesof another chromaticity, remains stubbornly at chancelevels of responding (Heywood et al., l99l). Yet when MS was askedto make an alternativebehavioural response, namely an eyemovement to the odd target,preliminary evidencesuggests that he may be more proficient (Heywood et aI., 1998a).Thus MS may indeed covertly processhue to guide his eyemovements but theseresponses appear unable to mediate performance in verbal tasks.Perhaps covert processwould be better revealedby indirect tests.Normal observersgroup non-adjacentelements of a visual display on the basisof hue and such grouping can affect performance on taskswhich are unrelatedto colour. For example,the extent to which peripheral elementsof a stimulus display interfere with identification of an elementat the fixation point dependson colour differences befiveencentral and peripheralitems (Baylis& Driver, 1992).The performanceof MS in a reactiontime task of letter identificationwas, unlike normal observers,not influencedby the chromaticity of flanking distractersand provided no evidenceof covert processing ofhue.

Conclusion

Achromatopsiareveals itself in severalguises and is likely to constitute a family of dis- orders.Nevertheless, in someinstances it doesnot precludethe processingof wavelength differencesto extractinformation about motion and form. Theseabilities appear to stem from residualP-channel processing which survivesthe completeabolition of the perceptual representationof hue. Whilst MS detectschromatic boundaries,even in the presenceof random luminance fluctuations, he lacks longer-range processeswhich allow efficient scenesegregation through perceptualgrouping on the basisof colour differences. Moreover,his discrimination of local cone contrast doesnot extend to allowing him to make the global comparisonsin complexvisual sceneswhich are a prerequisiteof colour constancy.The processingof wavelengthdifferences is not covert but is accompaniedby a changein phenomenalvision, i.e. MS will readily comment on the nature of the form or motion which results from such processing.However, the extent to which wavelength differencescan mediatevisuomotor responseis yet to be clarified.How these,and other abilities,relate to the distributed population of colour-sensitiveregions of remainsto be established.Given that many of theseregions code colour and luminance,a fruitful approachmay be a carefulassessment of luminancevision, and more particularlv its interactionwith colour,in cerebralachromatopsia. References

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