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1 This rticle ws originlly pulished in the Encyclopedi of Neuroscience pulished y Elsevier, nd the ttched copy is provided y Elsevier for the uthor's enefit nd for the enefit of the uthor's institution, for noncommercil reserch nd eductionl use including without limittion use in instruction t your institution, sending it to specific collegues who you know, nd providing copy to your institution s dministrtor. All other uses, reproduction nd distriution, including without limittion commercil reprints, selling or licensing copies or ccess, or posting on open internet sites, your personl or institution s wesite or repository, re prohiited. For exceptions, permission my e sought for such use through Elsevier's permissions site t: Roe A W, Chen G nd Lu H D (2009) Visul System: Functionl Architecture of Are V2. In: Squire LR (ed.) Encyclopedi of Neuroscience, volume 10, pp Oxford: Acdemic Press.

2 Visul System: Functionl Architecture of Are V2 331 Visul System: Functionl Architecture of Are V2 A W Roe, G Chen, nd H D Lu, Vnderilt University, Nshville, TN, USA ã 2009 Elsevier Ltd. All rights reserved. Competing Locl versus Glol Views The visul world ppers to us in its entirety, coherent nd understndle. Despite our elief tht this view is unitry, it is ctully comprised of multiple competing views t the locl nd glol scles. This point cnnot e etter illustrted thn y the pintings of Slvdor Dli, the quintessentil crftsmn of depicting competing nd conflicting cues within single scene. In The Hllucinogenic Toredor (Figure 1), which is 13 foot 10 foot (4 m 3 m) pinting (exhiited t the Slvdor Dli museum in St. Petersurg, FL), different scenes ecome pprent depending on the viewing distnce. When stnding close to the pinting, in the ottom right corner smll oy is seen viewing lke with womn in ikini on pool chir nd dlmtin dog heded towrd the lke. From little frther ck from the pinting, just ove the lke ull cn e seen stuck with multiple colorful spers. Severl Venus sttues cn e seen cross the center of the pinting, one with white dress, prtly shdowed in green, nd nother with red dress. At n even greter distnce, one egins to pprecite the toredor himself, who s shirt nd green tie re formed y the fric nd shdow of Venus s white skirt, respectively, his chin y her stomch, his nose y her rest, nd his eye y the shdow of her neck. The outline of his cheek is formed y the hips of the Venus drped in red, his eret nd cpe dotted y the ptterns of flies in the stdium nd those ove the ull. Thus, depending on the scle t which this pinting is viewed, different scenes ecome pprent to the viewer. Moreover, n ttempt to tke in ll views t once my led to sense of rivlry etween locl nd glol scles: t one scle the green swth is tie, nd t nother it is the shdow of Venus s white dress. A few simple visul illusions my help rek this complex imge into simpler components. Such illusions cn e very useful tools for studying how competing cues re encoded in the rin. One exmple is shown in Figure 2(). In this wtercolor illusion, lue nd yellow dotted lines seprte regions of white ckground. Regions etween the yellow lines pper yellowish nd those etween the lue lines pper luish. In ctulity (s mesured y spectrophotometer), the white regions re ll the sme in color. This is demonstrtion of how locl cues (white) cn e overridden y distnt, glol cues (the lue nd yellow lines), leving the illusion of differently colored regions. Figure 2() is the clssic cfe wll illusion, in which prllel horizontl lines pper to e sloping. Superimposition of horizontl r demonstrtes tht these lines re indeed horizontl. Agin, the locl cues signling horizontl re overridden y the glol percept of sloping lines. In the relm of depth perception, in the rndom dot stereogrm (RDS) illustrted in Figure 2(c), the orders of the squre centrl region in the left figure re offset from tht in the right figure. When fused y the two eyes, this induces percept of squre surfce ehind (more distnt thn) four round holes in nerer surfce. This is perceived despite the fct tht the pixels within the squre re identicl nd hve no disprity. Thus, the locl disprity cues re overridden y the glol order cues of the squre. Similr illusions re used in the studies descried in this rticle to distinguish the roles of primry (V1) versus secondry (V2) visul res in the perception of contour, stereoscopic depth, nd color nd rightness (see Tle 1). Moreover, the conflicting locl versus glol cues present in these illusions re used to elicit competition etween V1 (which is locl) nd V2 (which is glol). The inherent conflict illustrted y these exmples clls for revision of the trditionl view of hierrchicl processing within the visul pthwys. In the trditionl view, erly visul stges first identify elementl fetures y mens of neurons with smll, sptilly nd feturlly restricted receptive fields. These elementl inputs re then integrted into higher-order representtions t higher corticl res. Receptive fields of neurons in higher corticl res re sptilly lrger nd tend to e less sensitive to elementl feturl specificity nd, vi some unknown invrince circuitry, ecome tuned to more-glol fetures. This integrtion process is iterted t multiple corticl levels, culminting in reltively complete sptil nd feturl representtion tht enles oject recognition. This hierrchicl view, in its strictest interprettion, rises the question of how the visul system mintins knowledge of detils when higher corticl res no longer trck these detils. It is pprent tht the detils encoded in erlier res nd the glol views encoded in higher res must e simultneously ccessile. Moreover, these different views cn (nd often do) give conflicting signls. Resolving this locl versus glol competition is likely to e context dependent nd therefore dynmic. Thus, while the hierrchicl view still crries vlidity, it lone is indequte for creting the illusion of coherence cross multiple sptil scles.

3 332 Visul System: Functionl Architecture of Are V2 Figure 1 The Hllucinogenic Toredor y Slvdor Dli (Slvdor Dli Museum, St. Petersurg, FL). This competition forms the sis for three theses presented in this rticle. Evidence supporting the first two theses is presented, nd the third thesis is discussed lrgely s future direction of study. The theses re s follows: 1. Ech corticl re processes the visul world t different sptil scle nd, in tht sense, sees different visul world. 2. Multiple views of the world which re encoded in prllel y multiple corticl res cn compete with ech other. The dominnce of one view over nother my e resolved y competitive lnce etween feedforwrd nd feedck signls etween different corticl res. 3. This competition is dynmic nd context dependent. These theses re presented in this rticle through set of studies which exmine responses of primry (V1) nd secondry (V2) visul res in the mcque monkey. In this frmework, V1 s nd V2 s views of three feturl spces re exmined: visul contours, visul color nd rightness, nd visul depth. These studies demonstrte the following: 1. V2 sees different things thn V1 sees (see Tle 1). 2. There is lnce of power etween V1 nd V2. 3. There is dynmic network of V1 nd V2 modules tht prticipte in this power struggle. Functionl Orgniztion in V2 Is Modulr V2 hs een descried s distriution center from which modlity-specific informtion feeds into the ventrl nd dorsl visul processing strems. In ddition to its role in distriution, V2 plys crucil preprtory role in midlevel vision, performing trnsformtions tht link locl detil to higher-order percepts. A gret del of ttention hs een focused on the interrel interctions nd integrtion etween corticl res. V2 holds unique position in the

4 Visul System: Functionl Architecture of Are V2 333 c Wtercolor effect Cfé wll illusion Disprity cpture Figure 2 Glol versus locl competing cues in visul illusions. () The wtercolor effect; see Pinn B, Brelstff G, nd Spillmnn L (2001) Surfce color from oundries: A new wtercolor illusion. Vision Reserch 41(20): () The cfe wll illusion. (c) Disprity cpture illusion. Tle 1 V1 nd V2 see different percepts V1 Brightness Luminnce Illusory rightness Depth No percept Percept Contour Rel contours Illusory contours sense tht it funnels informtion, oth feedforwrd nd feedck, etween V1 nd the lrger corticl network. To pprecite the role of V1 nd V2 in contour, color rightness, nd disprity processing, it is first importnt to recognize the modulrity of these res. In contrst to V1, which is chrcterized y oculr dominnce structure, regulr rry of orienttion domins, nd lttice of densely stining cytochrome oxidse los, V2 contins pttern of lrge (millimetersize) cytochrome oxidse stripes. Some evidence indictes these thin (cytochrome drk), ple (cytochrome light), nd thick (cytochrome drk) stripes re involved in contour, color rightness, nd disprity processing, V2 respectively. In mcques, these stripes re oriented roughly perpendiculr to the V1 V2 order nd re commonly seen in repeting thin, ple, thick, ple sequence. There re lso reports of interniml vriility nd/or vriility of stripe thickness (e.g., thin is not thin) or stripe sequence (e.g., thin, ple, thin, ple). A few studies hve hinted tht functionl differences my ccompny these differences in individul rchitecture. Within these lrger stripe structures re collections of mm domins. The presence of sustructure within stripes ws perhps first suggested y nonuniform stining in cytochrome oxidse-stined tissue nd y ptchy leling of injected trcers in V1, V2, nd V4. Studies with 2-deoxyglucose hve reveled further ptchy ctivtion within V2 stripes. Opticl imging further confirmed the presence of sudomins (e.g., color-preferring nd luminncepreferring domins within thin stripes). Although oth ntomicl nd functionl evidence support the presence of modules, the reltionship of functionl sudomins nd ntomicl ptchiness is unknown. Functionl evidence indictes tht different modules ply distinct functionl roles nd hve specific connectivities. Indeed, this is visully pprent from loclized injection of trcer into V2, which revels rrys of clusters out mmwithinv2 (Figure 3). These ntomicl dt suggest degree of intr-v2 connectionl specificity tht prllels tht of functionl networks oserved in V1. In ddition to summrizing more recent findings regrding V2, this rticle presents common frmework for understnding the different feturl modlities in V2 nd therey the common functionl trnsformtions tht V2 performs on its input, regrdless of feture spce. Are There Functionlly Distinct Domins in V2? Following the discovery of cytochrome oxidse los (lso referred to s puffs nd ptches ) in mcque monkey visul cortex, reserchers reported tht los re chrcterized y predominnce of color-selective neurons which lcked strong orienttion selectivity, wheres interlos re chrcterized y prepondernce of orienttion-selective cells lcking in color selectivity. Functionl distinctions within V2 hve lso een reported wherey thin stripes re color selective nd poor in orienttion selectivity nd ple nd thick stripes re orienttion selective nd less selective for color. This proposed dichotomy led to numer of studies, some of which supported wheres others contrdicted these findings. This controversy hs continued without pprent resolution.

5 334 Visul System: Functionl Architecture of Are V2 Figure 3 Intrinsic connections in V2 revel 200 mm modules. (, ) Boxed res indicte regions of ptchy lel (indicted y rrowheds). Arrow: site of trcer injection. Scle r ¼ 100 mm. From Amir Y, Hrel M, nd Mlch R (1993) Corticl hierrchy reflected in the orgniztion of intrinsic connections in mcque monkey visul cortex. Journl of Comprtive Neurology 334(1): The dete is fueled y two min issues. The first is whether color nd orienttion informtion re segregted in V1 (nd V2). Some studies hve found cler ssocition etween color selectivity nd lck of orienttion tuning. This finding is supported y studies which report tht color-selective cells prefer low sptil frequencies nd exhiit high contrst sensitivity. Results with 2-deoxyglucose re lso consistent with these views, indicting los in V1 re preferentilly ctivted y color stimuli nd low sptil frequency stimuli. With respect to sptil distriution, electrophysiologicl studies hve lso reched different conclusions. Some support the view tht cytochrome oxidse los re centers of color preference nd poor orienttion preference. Others hve found tht centers of los exhiit higher contrst gin nd lower sptil frequency response, which suggests tht los do exhiit responses functionlly distinct from tht of interlos. However, other studies differ. Some single-unit electrophysiologicl studies find lo nd interlo domins exhiit no significnt difference in color nd orienttion preference nd report rnge of ssocitions etween color selectivity nd orienttion selectivity within single cells of V1. Experimentl fctors my contriute to some of this controversy. Although electrode recording sites were crefully reconstructed in these studies, there is some intrinsic error ssocited with reconstruction of recording sites. Since cytochrome oxidse los re smll ( mm), smll degree of error could e significnt. There re lso differences in smpling methods nd methods of receptive field chrcteriztion (e.g., hnd plots with color filters, chrcteriztion with sinusoidl isoluminnt grtings, mpping with reverse correltion of cone-isolting stimuli). A relted ut distinct issue regrds the ssocition of color nd orienttion with los nd interlos, respectively. Studies which revel popultion responses (2-deoxyglucose nd opticl imging methods) tend to support the role of los in the processing of low sptil frequency nd color informtion. As shown y 2-deoxyglucose methodology, los re preferentilly ctivted y color-vrying grtings of low nd middle sptil frequencies nd y sptilly diffuse color stimuli. Opticl imging studies hve shown good lignment etween cytochrome oxidse los nd centers of monoculrity nd etween cytochrome oxidse los nd regions of poor orienttion selectivity. Less cler correspondence etween los nd color response hs lso een reported. Although one study reported generl correspondence etween color domins nd cytochrome oxidse los, it ws not simple one-toone reltionship: Some color-ctivted domins were irregulr in shpe nd were oserved to spn two or more los. A similr controversy exists on V2. Some reserchers found little difference in the numer of colorselective cells cross the different cytochrome oxidse stripes in V2. Some single-unit studies hve emphsized the multidimensionl spects of single cell function in V2. Others hve reported some concentrtion of color-selective responses in thin stripes of V2, in contrst to some erlier studies. In hopes of settling this dete, recent intrinsic signl opticl imging study closely exmined the lignment of lrge field views of color nd orienttion response in V1 nd V2 of the mcque monkey. As shown in Figure 4(), the V1 V2 order is well delineted y oculr dominnce imging. Opticl imges reveled the chrcteristic orienttion mps s well s regulr rry of color domins in V1 (Figure 4()). In V2, orienttion domins re lrger thn those in V1 nd re loclized to the thick nd ple stripes (white rs in Figure 4() nd 4(c)). Regions of strong color ctivtion in V1 (Figure 4(c)) re punctte nd lolike in ppernce, re ligned long centers of oculr dominnce columns, nd tend to overly regions of

6 Visul System: Functionl Architecture of Are V2 335 Oculr integrtion Orienttion Color c V2 V1 OD HV Col Figure 4 Feture mps (oculrity, orienttion, nd color) within V1 nd V2 of mcque monkey. () Oculr dominnce (OD) mp (left eye minus right eye). V1 V2 order (indicted y dotted line in () (c)). () Orienttion mp (horizontl minus verticl; HV). V2 orienttion domins re s much s severl times lrger thn those of V1. (c) Color (Col) mp (red green luminnce grting minus luminnce grting) revels V2 thin stripes nd V1 los. Note tht loctions of color ctivtions in V2 (drk rs) re complementry to loctions of oriented domins in V2 (compre () nd (c)). Scle r ¼ 1 mm. From Lu HD nd Roe AW (2007) Functionl orgniztion of color domins in V1 nd V2 of mcque monkey reveled y opticl imging. Cererl Cortex (doi: /cercor/hm081). Thin Thick Thin Thin Thick Thin Cytox Color c d Figure 5 Color domins lign with cytochrome rchitecture. Alignment of cytochrome oxidse (cytox) stripes () nd color domins () in V2, nd cytochrome oxidse los (c) nd color los (d) in V1. Tissue ws ligned using lood vessels, V1 V2 order, trcer injections, nd electrolytic lesions. Blck (() nd ()) nd white ((c) nd (d)) rrows point to corresponding structures. Scle r ¼ 1 mm. From Lu HD nd Roe AW (2007) Functionl orgniztion of color domins in V1 nd V2 of mcque monkey reveled y opticl imging. Cererl Cortex (doi: /cercor/hm081). low orienttion selectivity. In V2, color domins re complementry in loction to the orienttion-selective res nd overly the thin cytochrome oxidse stripes. An lignment of cytochrome oxidse stined tissue, nd functionl imges (using lood vessels, trcer injections, nd electrolytic lesions s guides) hve reveled good lignment of color domins with thin stripes in V2 (Figures 5() nd 5()) nd color los with cytochrome oxidse los in V1 (Figures 5(c) nd 5(d)). These findings thus support, t the level of popultion response, significnt functionl segregtion of color nd orienttion informtion in V1 nd V2 nd further strengthen their ssocition in V1 with los nd interlos, respectively. Although on the fce of it, these studies pper t odds, they re, in fct, mutully consistent. Clerly, single corticl loctions contin cells with mixture of responses nd cell types. Furthermore, ech cell displys n rry of responses in multiple feture domins. There is no question tht individul neurons re multidimensionl nd tht cells in V2 integrte informtion cross multiple feture domins, point tht is mde y numer of electrophysiologicl studies. This multidimensionlity is precisely wht leds to different views

7 336 Visul System: Functionl Architecture of Are V2 of the sme corticl re. Different electrophysiologicl smplings nd somewht different chrcteriztion methods cn provide quite different impressions, indicting tht methodology cn strongly influence the pprent popultion response profile. (Indeed, eing le to electrophysiologiclly trget imged color domins increses the yield of color cells tremendously.) Despite vriility due to method, tht functionl imging nd functionl ntomicl studies consistently revel lo nd stripe structure suggests tht there re overll differences in the locl popultion response. The fct tht functionl responses revel stripelike structures within V2 nd tht distinct responses re recorded in different stripes in V2 suggests the presence of t lest some degree of segregtion. On verge, the cells in los nd thin stripes prefer color stimuli over chromtic stimuli. Functionl imging provides, in sense, more unised view of the verge popultion response. Perhps some of the controversy is due to the perception tht functionl orgniztion implies strict segregtion. However, this is not the cse, s ech functionl structure contins mixture of neurons with vrying selectivities. In sum, lthough single neurons re multidimensionl (hve some degree of responsiveness to oth contour orienttion nd color), s popultion, they re orgnized to some degree with respect to contour versus color. Prllel Functionl Chnnels in V2: A Useful Frmework? A frmework tht hd its roots in the 1980s mintins tht thin stripes re vehicles for processing surfce feture informtion wheres thick nd ple stripes re involved in contour nd depth informtion processing. This frmework hs een supported y ntomicl, electrophysiologicl, 2-deoxyglucose, opticl imging, nd ehviorl nd lesion study dt. This frmework is not to e interpreted s view of strict segregtion. There is mple dt to demonstrte tht functionl orgniztion within V2 is not one of strict segregtion. As noted ove, single neurons in V2 re multidimensionl nd integrte different feturl spces. Ech stripe type within V2 contins myrid of cell types. Given the extensive connectivity etween stripes in V2, cells from ech stripe type hve opportunity to influence nd integrte informtion from other stripe types. Nevertheless, the proposl tht different stripes suserve somewht different functions is still useful one. It is frmework which provides n understnding which cn e experimentlly tested nd modified. To ignore this frmework would e foolish. In the lnguge of drivers nd modultors, there my e primry functions tht cn e modified y secondry, perhps contextul, influences. A working frmework provides much greter utility nd testility thn n pproch in which every neuron is omnifunctionl. Indeed, the uiquity of functionl orgniztion in the rin whether it e t the level of glol networks, corticl res, modules nd columns, lmine, or synpses indictes tht such orgniztion is fundmentl tenet of rin orgniztion. Whether they e geneticlly determined, experientilly determined, or necessry prerequisite for specific computtions, it is likely tht functionl orgniztions er strong (nd possily predictive) link to the rin circuits tht produce function nd ehvior. The following prgrphs re thus presented in this frmework. Surfce Properties Surfce fetures, such s color, rightness, texture, glossiness, nd trnsprency, re those tht help us identify the mteril qulity of n oject. There re mple demonstrtions of the wys the perception of these surfce fetures cn e strongly influenced y lighting, locl color nd contour cues, glol context, nd experience. The humn visul system cn distinguish on the order of million different colors. However, the inputs to the visul system re confined to three types of cones, those responsive to red, green, nd lue wvelengths. How does the visul system crete the illusion of color nd trnsform tridic cone-sed representtion into perceptul continuum of slient hues? Add to this chllenge the fct tht the humn visul system cn djust to 7 orders of mgnitude of rightness (10 million to one, right sunlight to fint strlight). The visul system must lso fctor in the influence of contextul cues such s color, rightness, nd contrst of nery orders nd surfces. In ddition, the ility to see ojects through trnsprent surfces mens we not only must segregte different plnes of depth ut lso ignore fetures on the trnsprent plne. Color Representtion in V2 How do V1 nd V2 seprtely nd together contriute to these processes? The ide tht V1 nd V2 prticipte in encoding color informtion is well supported. At lest one route for color informtion rises from the prvocellulr lyers of the lterl geniculte nucleus (LGN) nd continues to lyer 4C of V1, to cytochrome oxidse los of V1, nd to the thin stripes in V2. Blue cone-driven input from S lyers of the LGN project directly to the los, with lue yellow inputs trgeting lyer 3B 4A nd red green inputs trgeting lower lyer 4C. There is lso evidence to suggest functionl segregtion of lue

8 Visul System: Functionl Architecture of Are V2 337 ON nd lue OFF inputs within lyer 4A of V1. In V2, lthough there is significnt color response in ech of the stripe types, greter concentrtion of neurons responsive to color stimuli is found in the thin stripes thn in either the ple or thick stripes. Color versus luminnce preference domins Opticl imging studies hve reveled the presence of colorresponsive domins within thin stripes. Some studies hve used preferentil response to isoluminnt red green grtings over chromtic luminnce grtings to revel color preference domins. Although there re oth color nd luminnce contrst differences etween these stimuli, experiments directly compring high- versus low-contrst chromtic responses hve reveled no structured mps in V2, indicting tht the imged sustructure is not due to luminnce contrst differences. Since sptil frequency, drift rte, nd men luminnce were identicl etween these two stimuli, the differentil response is ttriuted to the color content of the stimuli. Such stimuli elicit ctivtions tht pper more rounded nd interdigitted in some thin stripes (Figures 6() nd 6(c)) nd more elongted cross the width of the thin stripe in others (Figure 6()). It is not yet known whether there my e functionl implictions of these different rchitectures. Color: Topogrphy of hue in V2 thin stripes One of the first studies to estlish systemtic representtion of hues in V2 used isoluminnt color gry grtings of different hues nd mpped responses in mcque V2 using intrinsic signl opticl imging. These imges reveled hue-specific domins on the order of mm, which were mpped in systemtic fshion in V2. These chromtic color mps were locted within single thin stripes nd not in thick or ple stripes of V2 (Figure 7()). This ws the first demonstrtion of hue-sed mp in which topogrphic loction corresponded to hue wvelength. This study underscored three primry points: (1) lthough V1 contins color-selective cells tuned to red green nd lue yellow xes, hue representtion does not emerge until V2; (2) the topogrphic sis for this representtion is sed on mm modules, the size of which is fundmentl to other feturl representtions; nd (3) the discovery of topogrphic mps within thin stripes poses perhps the single strongest piece of evidence in fvor of the color thin stripe ssocition. Where is the lue response? Attempts t reveling lue response in V1 nd V2 with imging techniques proved unsuccessful. Similrly, compring responses to isoluminnt lue yellow grtings versus chromtic V2 V1 c Figure 6 Color domins in thin stripes. () A single thin stripe (rrow) contins severl rounded color domins. () A single thin stripe (rrow) contins color-preferring domins tht spn the width of the stripe. (c) Three thin stripes in V2, ech contining few color domins. Scle r ¼ 1 mm. () From Roe AW nd Ts o DY (1995) Visul topogrphy in primte V2: Multiple representtion cross functionl stripes. Journl of Neuroscience 15: () From Roe AW nd Ts o DY (1999) Specificity of color connectivity etween primte V1 nd V2. Journl of Physiology 82: grtings did not revel ny functionl orgniztion within either V1 or V2. However, more-recent studies hve reveled cler nd strong responses to lue stimuli. These studies exmined responses to flshing lue versus flshing gry unstructured stimuli ech t 30% luminnce nd drifting lue gry squre-wve grtings versus gry gry squre-wve grting t 30% luminnce contrst. In V2, similr to red nd green, lue stimuli preferentilly ctivte the thin stripes wheres gry stimuli exhiited preferentil thick-stripe ctivtion. Within the thin stripes, colorspecific stimuli typiclly reveled focl ctivtions. Activtions to red, green, nd lue stimuli hve een shown to shift in loction within the thin stripes. Exmintion of responses to grtings of different duty cycles reveled tht thin lue lines were surprisingly effective stimulus. Thin lue lines elicited strong lolike mps in V1 (Figure 7()). These dt suggest tht lue ctivtions, like red nd green hues, re mpped

9 338 Visul System: Functionl Architecture of Are V2 Recording loctions L3 L2 + + L4 + + L1 Figure 7 Hue mps in V2. () Chromtic color mps locted within single thin stripe of V2 (imged with isoluminnt color/gry grtings of different hues). Outline color indictes pek response of tht loction. () Imged responses Mcque V1 nd V2 in response to thin lue oriented stimuli. In V1, lue ctivtion revels los. In V2, lue ctivtion is minly locted in thin stripes. Scle r ¼ 500 mm. () From Xio Y, Wng Y, nd Fellemn DJ (2003) A sptilly orgnized representtion of colour in mcque corticl re V2. Nture 421: () From Roe AW, Lu HD, nd Crewther D (2007) Blue Color Activtion in V1 nd V2 of Mcque Monkey. Melourne: Interntionl Brin Reserch Orgnistion. within color modules in the thin stripes of V2. The surprisingly strong response to thin lue lines my suggest some interction of color nd sptil frequency tht my contriute to contour response in V2. Dt lso suggest, counter to previous notions of dedicted red green versus lue yellow los in V1, tht lue response my reside within every lo in V1. A midlevel role in simultneous contrst nd color constncy? The color of surfce cn e drmticlly chnged y its surround, such s commonly demonstrted with exmples of simultneous color contrst. A first step in chieving simultneous color contrst response would e demonstrting chromticlly specific effect y the surround. Surround suppression of oth chromtic nd isoluminnt grtings hve een exmined on the chromtic responses of V1 nd V2 neurons. There is little evidence tht colored surrounds lter the chromtic tuning of neurons in V1 or V2 (lthough ckground color shifts chromtic tuning of V1 neurons to degree consistent with perceptul color contrst effects). However, V2 neurons, unlike V1 neurons whose surrounds exhiit little chromtic selectivity, hve chromtic signture in the surround similr to tht in the receptive field center. Thus, lthough there is no evidence of the surround shifting chromtic tuning in V2, neurons in V2 re strongly ffected y specific chromtic stimuli in the surround. Another slient spect of color perception is color constncy. This term refers to the fct tht the color of surfce remins constnt under different lighting conditions (e.g., red pple will pper red under different spectrl lighting conditions, such s right sunlight nd mient indoor lighting). This suggests tht there must e neurons somewhere in the rin tht encode redness or greenness of surfce regrdless of light condition. Do such neurons exist in V2? A few recent studies hve tried to dissect the difference etween color responses in V2 nd those in V1 or V4. Reserchers hve used isoluminnt color ptches to chrcterize the color preference of single cells in V2 thin stripes nd Mondrin stimuli to exmine the effects of color versus the illuminnt. They found tht V2 cells responded to the wvelength of the illuminnt rther thn the color of the stimulus. In contrst, the sme stimulus prdigms reveled cler color constncy in mjority of V4 neurons: these neurons exhiited shifts in their color-tuning profiles in the direction of the shifted chromtic component of the illuminnt (which ws simulted y shift in the ckground color presented on the computer monitor). In other words, V2 neurons did not exhiit ehvior consistent with color constncy. However, out third of V2 neurons studied were strongly influenced y the wvelength of the surround. Thus, these studies suggest tht V2 plys midlevel role in the genertion of color percepts such s simultneous color contrst nd color constncy. Although neurons in V1 nd even in LGN re reported to e influenced y monochromtic surrounds, shifts of the entire color tuning curve hve een reported only for V4 neurons. This is true for units recorded oth in nesthetized nd wke monkeys. Thus, computtions leding to color constncy re likely to egin t stges efore V4, ut color constncy is not represented in its full extent until V4. V2 is likely n intermedite processing stge in these computtions.

10 Visul System: Functionl Architecture of Are V2 339 Brightness Representtion in V2 With respect to V2 s role, if the primry role of thin stripes is to encode surfce properties, then in ddition to color, thin stripes my e integrl to representing surfce rightness. The chllenges of representing rightness in the visul system include representing light level (lightness nd drkness), chnge in light level (either increse or decrese), nd ility to djust to lrge rnge of light levels. Some of these chllenges my e solved y the retin nd LGN. However, other chllenges re unlikely to e resolved y erly precorticl levels. Similr to context-dependent effects in color vision, the perceived rightness of surfce cn e strongly influenced y surrounding cues. Brightness perception is influenced y multiple fctors, including luminnce, edge effects, distnt color nd rightness context (e.g., simultneous contrst, Mondrins), nd experience. Neurons in V1 of oth the ct nd the monkey exhiit response modultion to lrge field modultions in luminnce nd in ckground luminnce modultion. Reltively few studies hve exmined the representtion of rightness informtion in V1 nd V2. ON nd OFF responses Mny studies hve demonstrted tht visul corticl neurons exhiit contrst response functions which increse monotoniclly over rnge of contrsts nd sturte t higher contrsts. Most neurons in V1 respond to lrge ptch of luminnce increment or decrement in monotonic fshion. Roughly one-third of neurons re not ffected y stimultion in the surround, consistent with the type I cells which lck inhiitory surrounds. The response is often chrcterized y n initil contrstindependent trnsient, followed y sustined response which correltes with the luminnce increment or decrement. Another third of neurons re enhnced y luminnce in the surround nd pper to signl level of illumintion. And the remining third re ffected y luminnce in the surround (type II) in mnner consistent with simultneous contrst s first demonstrted in nesthetized ct visul cortex nd lter lso oserved in the lert monkey V1. In ddition to light increment (ON) nd light decrement (OFF) responses, V1 nd V2 contin cells tht exhiit ndpss chrcteristics. Tht is, they respond to n intermedite rnge of luminnce vlues (termed V-shped or gry-preferring neurons ). Some of these neurons lso exhiit color sensitivity, suggesting role for luminnce response in color encoding. ON nd OFF domins in V2 Within V2 thin stripes, there re sudomins tht exhiit luminnce increment (ON) nd luminnce decrement (OFF) responses. These domins mesure on the order of 0.5 mm nd could e the sme luminnce-preferring domins reveled in isoluminnt color versus chromtic imging experiments. Such domins hd een hypothesized sed on extended runs of tngentilly recorded of ON or OFF single unit responses within V2 thin stripes. Such ON nd OFF zones hve not een oserved in primte V1. Contrst response in V2: Thin stripes hve greter dynmic rnge One test of the hypothesis tht thin stripes re rightness-processing structures hs tken the form of exmining contrst response in V2. The expecttion ws tht if thin stripes were loci of rightness informtion processing, then they should hve contrst response ehvior consistent with such representtion. One would expect the contrst response of these stripes to exhiit sensitivity to lrge rnge of contrsts, including sensitivity to low contrsts nd nonsturting response t high contrsts. More specificlly, they should hve high contrst gin, especilly t low sptil frequencies consistent with encoding visul surfce fetures, nd they should exhiit lrge dynmic rnge for encoding visul rightness. Previous studies hd shown tht in primtes, mgnocellulr nd prvocellulr neurons in the LGN re chrcterized y distinct contrst response signtures. Mgnocellulr neurons exhiit nonliner response chrcterized y greter sensitivity to smll chnges in contrst (hve higher contrst sensitivity), especilly t low luminnce levels, nd tend to sturte t high contrsts. Prvocellulr neurons respond in liner fshion to incresing contrst nd re reltively insensitive t low contrsts (in fct, they re not responsive t contrsts lower thn round 10%). Koniocellulr neurons re heterogeneous popultion of neurons nd hve rod rnge of contrst response functions. In V1, interlos tend to e dominted y prvocellulr inputs, while los exhiit prvocellulr (color selectivity), mgnocellulr (low sptil frequency, high contrst gin response), nd koniocellulr (lue response) chrcteristics. Although thick stripes re dominted y mgnocellulr inputs nd therefore could exhiit higher contrst sensitivity thn thin stripes do, in principle oth mgnocellulr nd prvocellulr inputs rech ll the stripe comprtments in V2. The thin stripes receive oth mgnocellulr nd prvocellulr input primrily y wy of the los, nd thick nd ple stripes vi the interlo columns. Thick stripes hve the highest contrst sensitivity vlues, lthough semisturtion vlues hve shown no significnt difference etween thin, ple, nd thick stripes. Mesures of V2 response hve reveled surprisingly

11 340 Visul System: Functionl Architecture of Are V2 few quntittive differences etween thin, ple, nd thick stripes, leding some to rgue for homogeneity of stripe function in V2. With 2-deoxyglucose methodology, oth thin nd thick, ut not ple, stripes hve exhiited response to low contrst (8%) grtings, suggesting tht mgnocellulr contriution could lso e prevlent in the thin stripes. A study using opticl imging methods hs demonstrted tht V2 thin stripes hve greter contrst gin thn thick nd ple stripes nd reltively nonsturting response t high contrsts. As shown in Figure 8, contrst response functions of oth los nd interlos in V1 were liner (Figure 8()), consistent with prvocellulr-dominted response in superficil lyers of V1. However, responses in V2 exhiited nonliner response, especilly t low contrsts, reminiscent of mgnocellulr input (Figure 8()). At high contrsts, thin stripes exhiited significntly stronger nd lesssturting responses thn thick or ple stripes (Figures 8(c) nd 8(d)). The response of V2 thin stripes is thus reminiscent of mgnocellulr response t low contrsts nd prvocellulr response t high contrsts. At low contrst levels, mgnocellulr inputs from V1 los my converge in V2 thin stripes, therey conferring high-contrst response t low contrsts. At higher contrst levels, prvocellulr-dominted inputs to thin stripes continue to signl chnging contrst, while those in thick nd ple stripes tend to sturte. Other contriutions to nonliner response in V2 thin stripes (such s koniocellulr input nd other thlmic inputs) my lso e t ply. In comprison with thick or ple stripes, these dt suggest lrger dynmic rnge of V2 thin stripes, consistent with preferentil role in rightness perception. Rel nd illusory rightness representtion in V2 thin stripes Perhps intermedite to locl luminnce response nd lightness nd color constncy which require rther lrge-scle integrtion re midlevel stges which re encoded in V2 (in cts). A potentil exmple of midlevel integrtion ws demonstrted in recent study reveling the equivlence of V2 response to different types of rightness stimuli. Response to sinusoidlly modulted stimuli counterphsing in dr/r ( 10 4 ) V c lo hi V Contrst d Thick/Ple dr/r (10 4 ) Figure 8 Contrst response in V2 stripes. (, ) Contrst response functions in V1 re liner, oth in los nd interlos, while those in V2 re nonliner, in thin nd thick/ple stripes. Different color lines represent response otined t different sptil frequencies (sme legend in () nd (), in cyc/deg). x-xis, visul contrst (0.2 ¼ 20%); y-xis, dr/r reflectnce chnge. (c, d) Thin stripes hve greter dynmic rnge. (c) Top: Cytochrome oxidse stin revels thin (white rrows) nd thick (lck rrow) stripe in V2. Middle nd ottom: Imged response to low (lo, 40% contrst) nd high (hi, 80% contrst) sinusoidl grtings. At high contrst, thin stripes still exhiit roust response, ut thick stripe response is wek. Green outlines indictes ctivtion res, thresholded nd outlined. (d) Thin nd thick stripe responses re similr t lower contrsts, ut thin stripe response domintes t high contrst. Thin (y-xis) nd thick/ple (x-xis) stripe responses re similr t low contrsts (lck, drk gry symols), ut thin stripe response domintes t high contrst light gry, white symols, (dr/r reflectnce chnge). From Lu HD nd Roe AW (2007) Opticl imging of contrst response in mcque monkey V1 & V2. Cererl Cortex (doi: / cercor/hl177). dr/r ( 10 4 ) Thin-dR/R (10 4 )

12 Visul System: Functionl Architecture of Are V2 341 contrst ws preferentilly loclized to the thin stripes of V2 (Figures 9() nd 9()). In fct, similr thin stripe ctivtions were otined in response to illusory rightness modultions s erly s 1970 (Figure 9(c)), when percept of rightness contrst etween the left nd right hlves ws chieved y n intervening Cornsweet order (Cornsweet eing one of the reserchers involved). This order-induced contrst illusion evokes the percept of rightness differentil where none is present. Neurons in V2 were shown to respond not only to sinusoidl modultion of the rel rightness stimulus ut lso to tht of the Cornsweet order contrst. Opticl imging of V2 response indicted tht such responsiveness ws loclized to the thin stripes of V2. Consistent with opticl imging evidence, of 89 neurons recorded in V1 los nd interlos nd V2 thin, ple, nd thick stripes, lmost ll those responsive to the Cornsweet were locted in thin Color Rel c Corn d Blnk 0.2% +0.1% 0.1% +0.1% dr/r dr/r Figure 9 Opticl imging of rightness response. () Single condition color mp revels thin stripes in V2 (lck rrowheds ove, thick/ple stripes indicted y white rrowheds). Pixels with strongest ctivtion (top 10%) indicted y red outlines. Gryscle in () lso pplies to () nd (c). () Single condition ctivtion mp in response to rel luminnce stimultion. Strongest ctivtion is seen in thin stripes with weker ctivtion in thick/ple region. (c) Single condition ctivtion mp in response to Cornsweet stimultion revels similr pttern. (d) Blnk stimulus mp. Scle r ¼ 1 mm. Ech imge sum of 50 trils. In ll single condition mps, drker pixels indicte lrger mgnitude reflectnce chnge. dr/r reflectnce chnge. stripes. These results suggest tht thin stripes re involved in not only the encoding of luminnce response ut, more generlly, the response relted to surfce rightness perception. V1 Sees Locl, V2 Sees Glol These dt re consistent with the encoding of higher-order rightness processing in V2 nd lowerorder rightness processing in V1. Tht is, responses in V1 reflect locl luminnce vlues, wheres those in V2 reflect more glol, edge-induced percepts. In the Cornsweet stimulus, V1 would report lck of luminnce modultion, wheres V2 would report slient rightness modultion. To chieve such perceptul sliency, the V2 s messge must somehow overcome V1 s. One ovious mens is vi feedck projections from V2 to V1 which led to either reltive suppression of V1 response or modultion of V1 response tht concurs with tht in V2. This possiility remins to e exmined. Stereoscopic Depth Binoculr inputs re used y the humn visul system to judge oject depth in the three-dimensionl world. This depth percept is creted y the integrtion of two views of the world received y the two eyes. Stimuli nerer or frther from the fixtion point will produce disprities from left nd right eye with negtive or positive horizontl shift. In the pthwy from retin to thlmus to cortex, oculr input remins segregted in the thlmus (the LGN) nd is first comined in V1. In V1, disprity-selective cells hve een chrcterized y their response to offset rs presented to the two eyes ( tuned excittory, tuned inhiitory, ner, nd fr cells), response to differentil phse of sinusoidl grtings, nd response to solute disprity of RDSs. In V2, disprity-selective neurons hve een descried s oligtory inoculr, selective for disprity-defined contours, nd tuned for reltive rther thn solute disprity. Despite the numer of studies on disprity responses in the visul cortex, there hve een no pulished studies ddressing ny systemtic representtion of disprity response in either V1 or V2 of the monkey. Given the known orgniztions of the other two feturl mps in V2 (color in the thin nd contour in the ple nd thick stripes of V2), this gp in our knowledge regrding disprity representtion in V2 is prticulrly conspicuous. Disprity-selective responses re elieved to e preferentilly loclized to the cytochrome oxidse thick stripes of V2, ut topogrphic representtion within these stripes hs not een exmined. Thus, t issue re the questions of whether there is

13 342 Visul System: Functionl Architecture of Are V2 mp for ner-to-fr depth informtion nd whether disprity nd orienttion informtion, which re oth represented in the thick stripes, re independently represented or not. The roder issue of prllelism nd modulrity cross feturl domins in V2 is lso in question. Exmintion of these issues is further motivted y the presence of mps orgnized for disprity in the middle temporl re (MT), primry trget of V2 thick stripes. Topogrphy for Ner Fr Disprity Since it is known tht mny disprity-selective neurons in V2 include oligtory inoculr cells, previous opticl imging studies hd indicted loclized thick stripes y locting domins preferring ctivtion of two eyes over single eye. These inoculr-preferring domins were locted primrily, lthough not exclusively, within thick stripes (Figure 10). Two recent studies hve indicted the presence of topogrphic orgniztion in V1 nd V2. In one, two photon clcium imging ws used to study orgniztion of corticl responses to phse offset grtings in the ct. This study reveled eutiful pinwheels of disprity response in ct V1. In nother study, RDSs were used to proe disprity orgniztion in primte V1 nd V2. These stimuli were designed to produce the percept of surfces t different depths reltive to the ckground, rnging from 0.5 ner to þ0.5 fr. Chrcteriztion of single units in V2 reveled tht cells in V2 exhiited tuning for specific horizontl disprities (Figure 11(), RDS). It is importnt tht 1 RDS ARDS R 1mm Od c Binoc Color Figure 10 Imging V2 thick stripes. () Oculr dominnce (od) mp. () Color mp revels thin stripes (30% contrst lue/gry minus 30% contrst gry/gry grting). (c) Binoculr (inoc) versus monoculr preference mp revels thick stripes. Thick stripes (white dotted lines) nd thin stripes (red dotted lines) re in complementry loctions in V2. c Ner Zero Fr Figure 11 Topogrphy for disprity in V2 thick stripes. () Disprity tuning curves of recorded unit from imged disprity domin in V2 thick stripe. Rndom dot stereogrms (RDSs) were shifted in disprity from 0.42 to þ0.42. This cell is tuned to ner 0.4. Its response to ntirndom dot stereogrms (ARDSs) shows flt curve, indicting tht the cell s response correltes with the glol depth percept nd not simply with locl disprity cues. () Opticl imges to RDS nd ARDS stimuli. Left: RDS, differentil imge of ll ner (drk pixels) minus ll fr (light pixels) stimuli. Dotted ox, region of ctivtion in V2 thick stripe. Right: ARDS, differentil imge of ll ner minus ll fr stimuli. (c) Outlines of three disprity domins (0.34 ner, 0.34 fr, nd zero). Loction of ctivtion shifts s disprity chnges from ner disprity (red) to zero disprity (green) to fr disprity (lue). Scle r ¼ 1 mm (, c). R, reflectnce vlue. From Chen G, Lu HD, nd Roe AW (2006) Functionl rchitecture of mcque corticl re V2 for depth surfces reveled y opticl imging. Society for Neuroscience 32:

14 Visul System: Functionl Architecture of Are V2 343 these cells showed little responsiveness to stereogrms tht do not induce depth percepts; these include ntirndom dot stereogrms (ARDSs, stereogrms in which the contrst of corresponding pixels in the left nd right eyes ws reversed nd uncorrelted stereogrms) nd stereogrms in which the left nd right eye dots hve rndom reltionship to ech other (Figure 11(), ARDS). Similrly, opticl imging of such responses reveled strong responses to depth percept-inducing RDSs nd little response to ARDSs (Figure 11()). Key to the success of these studies ws rpid spot imging method tht permitted quick confirmtion of individul eye position nd mpping of the imged field of view. Consistent with previous studies demonstrting preferentil disprity response within V2 thick stripes, these ctivtions were locted within thick stripes. Furthermore, nlogous to topogrphic hue representtion within thin stripes, ner-to-fr topogrphy within the thick stripes ws oserved (Figure 11(c)). Imged disprity responses correlted well with disprity preferences of electrophysiologiclly chrcterized single unit responses. Furthermore, disprity preferences of units recorded within single verticl penetrtions were similr in disprity selectivities, suggesting the presence of columnr orgniztion for disprity within V2 thick stripes. No such topogrphies were oserved in V1. Orthogonlity of Disprity nd Orienttion It is well estlished tht thick stripes in V2 contin mps for orienttion. How, then, do disprity mps relte to orienttion in V2? Indeed, how multiple mps coexist within the sme two-dimensionl corticl spce is fundmentl issue tht hs een ddressed y numer of studies. In V1, modeling studies suggest tht competing intrcorticl influences result in oserved functionl orgniztions for oculr dominnce nd orienttion. In V2, there is n interdigittion of color, contour, nd disprity mps in single thin, ple, thick, ple stripe cycles. However, within single thick stripes, the reltive orgniztion of orienttion nd disprity in V2 hs een elusive. Is there full rnge of orienttions represented t ech disprity, nd is there full rnge of disprities represented t ech orienttion? Both psychophysicl nd electrophysiologicl evidence suggest tht representtion of horizontl disprity might e ised for verticl orienttions. Some reserchers hve found tht disprity-ctivted regions contined roughly equl representtion for different orienttions nd tht on verge, ech orienttion domin overly rnge of disprity domins. This suggests strongly n orthogonlity etween orienttion nd disprity within V2 thick stripes. Asolute versus Reltive Disprity Erly studies descried the tunings of V1 neurons in terms of solute disprity. However, depth perception is clerly dominted y reltive disprity. Tht is, if the ckground disprity moves forwrd, reltive disprity-tuned cell will shift its tuning forwrd; if the ckground moves ckwrd, reltive dispritytuned cell will shift its tuning ckwrd. The response of n solute disprity cell would remin unchnged with chnging ckground disprities. Using RDSs nd disprity clmp tht permitted stepping solute disprities without chnging ny reltive disprities within the stimulus, reserchers hve demonstrted tht V1 neurons re tuned for solute disprity. Of 253 neurons studied, roughly 20% were dispritytuned. Of these, out 80% exhiited solute disprity tuning; only two exhiited some (wek) shift consistent with reltive disprity tuning. In contrst, others hve demonstrted tht in V2, mny more neurons hve responses shifted in the direction of the ckground shift. Clerly, the influence of surround disprity on center disprity response is greter in V2 thn in V1. However, only few V2 cells exhiit shifts indictive of true reltive disprity (i.e., shifts equl to ckground shift). The distriution of these solute nd reltive disprity responses in V2 is unknown. However, given the smll numer of true reltive disprity responses in V2, such orgniztion my not ecome evident until lter processing stges (e.g., V4, MT). Although true reltive disprity mps re not expected in V2, V2 ctivtions re expected to e influenced y shifts in ckground. As shown in Figure 12(), V2 disprity tuning curve shifts towrd fr if ckground shifts fr (solid line) nd shifts ner if ckground shifts ner (dotted line). Thus, t fixed center ptch disprity (verticl red line), the neuronl response should decrese for ner shifts nd increse for fr shifts of the ckground (Figure 12()). Findings from one preliminry study hve suggested this prediction is met (Figure 12(c)). Opticl imging of thick stripe in V2 with fixed center ptch disprity (ner þ4) nd different ckground disprities resulted in predicted decresing ctivtion vlues from fr to ner (imged signl in three different disprity domins indicted y red, green, lue lines in Figure 12(c)). Thus, responses in V2 thick stripes exhiit some influence y shifts in ckground in mnner consistent with degree of reltive disprity tuning. Summry Together, these dt suggest tht topogrphic orgniztion for ner nd fr disprities my e estlished reltively erly in the visul pthwy, in V1 in the ct

15 344 Visul System: Functionl Architecture of Are V2 Firing rte (impulses) Disprity of center ptch (deg) dr/r dr/r c Fr 0 Ner Bckground disprity Bckground disprity Surround disprity(deg) Figure 12 Reltive disprity in V2. () Disprity tuning curves of reltive disprity cell in V2. Tuning curves shift in direction of ckground shift. () For fixed surfce depth, shifting ckground from fr to ner should result in decrese of neuronl firing. (c) Reflectnce mplitudes from three disprity domins (red, green, nd lue) cross shifts in ckground disprities from 0.34 to þ0.34 fr re consistent with predicted reltive disprity response. Deg, degree; dr/r, chnge in reflectnce. () From Thoms OM, Cumming BG, nd Prker AJ (2002) A speciliztion for reltive disprity in V2. Nture Neuroscience 5(5): nd in V2 in the mcque monkey. These dt lso suggest tht the prmeters of disprity nd orienttion in the thick stripes my e orthogonlly represented. Tht is, within ech orienttion domin is rnge of disprities, nd within ech disprity domin is rnge of orienttion representtion. Further computtionl modeling my suggest how orienttion nd disprity mps re mutully rrnged within V2. The overlp of orienttion nd disprity lso suggests tht orienttion-selective domins within thick stripes re distinct from those in ple stripes. It is importnt tht these dt lso rise the possiility tht t lest some spects of the disprity orgniztions oserved in MT derive from V2 nd re not estlished de novo in MT. V1 Sees Locl, V2 Sees Glol The finding tht V2 neurons re more strongly influenced y shifts in ckground disprity suggests tht V2 encodes not simply the solute disprity of surfce ut, t lest to some extent, the reltive disprity. Thus, similr to the proposed view of V2 in color nd rightness representtion, these dt re consistent with the encoding of wht cn e considered higher-order disprity processing in V2 nd lower-order disprity processing in V1. Reltive disprity signls my e importnt for figure ground segregtion, which suggests tht V2 my e involved in corse stereo vision. Another exmple of V2 s role in glol perception is the presence of neurons in V2 which chieve disprity cpture. The elements within the sujective figure re perceptully cptured nd pulled on the sme depth plne s the figure. The phenomenon hs een interpreted s the result of spreding of disprity signls from the sujective figure. In this sense, we consider disprity cpture n illusory percept, one which is induced not y true disprity of elements on the surfce ut y disprity of distnt fetures. In fct, some neurons in V2 hve een reported to shift their disprity tuning curves in mnner consistent with disprity cpture. If V2 encodes surfce depth, then it is conceivle tht such disprity cpture responses my mp to loctions similr to those of the surfce disprity responses. Agin, to chieve such perceptul sliency, the V2 s messge (the entire surfce is t the depth of the order) must somehow overcome V1 s (the ctul disprity of elements on the surfce). This could occur vi feedck projections from V2 to V1, resulting in reltive suppression of V1. This possiility lso remins to e exmined. Visul Contours There re myrid of contours in our visul world, some of which re defined y luminnce contrst nd mny more which re defined y cues without luminnce contrst. In ddition to rel luminncedefined contours (sinusoidl grting or line grting), different texture ptterns or utting line stimuli cn crete strong percepts of orders or contours. These percepts cn e perceived regrdless of the orienttion of the rel line inducers (either with cute or otuse inducers). Borders etween motion fields cn lso produce very slient percepts of contours (motion contrst contours).

16 Visul System: Functionl Architecture of Are V2 345 Cue Invrince V2 neurons exhiit responses to so-clled cognitive contours (lso termed illusory contours ). Electrophysiologicl recordings of single units in V2 hve demonstrted popultion of cells tht shre tuning for orienttions of oth rel nd illusory contours (oth utting line nd occluded contours). Opticl imging studies hve demonstrted tht orienttion domins imged in response to rel contours (rel lines or grtings) colign with those imged in response to illusory contours, suggesting the presence of higher-order orienttion domins. Recent opticl imging studies in lert monkeys hve lso extended the invrince of response in V2 to include not only rel (Figure 13()) nd illusory contours (Figure 13()), ut lso motion contrst contours (Figure 13(c)). In V1, these studies revel either very wek (wke monkey) or n orienttion-reversed (nesthetized monkey) response to illusory contours. This my e ttriuted to the difference in reltive ctivtion mgnitudes in the lert versus the nesthetized sttes: V2 ctivtion in the nesthetized monkey is typiclly weker thn tht in V1 wheres it is t lest s strong in the lert monkey. V1 Sees Locl, V2 Sees Glol The key oservtion is tht rel contours strongly ctivte oth V1 nd V2, wheres illusory contours (of severl different types) elicit ctivtion in V2 ut not in V1. Thus while the essence of the orienttion signl is similr etween rel nd illusory contours, the views in V1 nd V2 of these two contour signls re quite different. The key point is tht wheres V2 cn redily distinguish the orienttions of different types of contour stimuli, it is cler tht V1 cnnot distinguish the orienttions of illusory contours. A corollry is tht the encoding of contour type (rel or illusory) cnnot e ccomplished y either V1 lone (signls either lck orienttion contour or orthogonl orienttion) or V2 lone (V2 cnnot distinguish etween rel nd illusory). Only with pired V1 nd V2 signl cn the rel versus illusory nture of contour e decoded. Thus, oth higher V2 V1 c Figure 13 Locl nd glol V1 V2 networks inferred from cross-correltion studies. () Locl networks re those tht require sptilly overlpping receptive fields. Such interctions re typiclly seen etween orienttion-mtched cell pirs nd etween sptilly overlpped nonoriented V1 nd oriented V2 cells. () Glol networks re those tht do not require receptive field overlp. Strong interctions re typiclly seen etween nonoriented V1 nd nonoriented V2 cell pirs (surfce surfce), oriented V1 nd nonoriented V2 cell pirs (order surfce), nd nonorienttion-mtched V1 V2 cell pirs.

17 346 Visul System: Functionl Architecture of Are V2 nd lower-order signls re necessry for proper contour identifiction. Locl versus Glol Networks How Is Contour-Specific Pired V1 V2 Signl Achieved? There is roder view of V2 function which pplies to the multiple feture spces represented within V2. The view descried erlier is three-stge view of the reltionship etween V1 nd V2. It is frmework sed on oth ntomicl nd functionl connectivities etween different types of V1 nd V2 neurons. In rief, the first stge (V1) identifies elementl fetures such s locl color, orienttion, solute disprity, nd motion. The second stge (V1 V2 or intr-v2) involves surfce-order cpture, in which pproprite ssignments of surfces to orders nd orders to surfces re chieved. The third stge involves n competitive lnce of feedforwrd nd feedck interctions etween V1 nd V2. This is the stge vi which glol percepts might chieve dominnce over locl cues, perhps vi feedck from V2 to V1. Bsed on cross-correltion studies of V1 V2 interctions, two types of V1 V2 networks my e descried, one which suserves processing of locl cues nd nother which is more glol in extent. Bsed on pproximtely 250 recorded interctions etween different cell types in V1 nd V2 (e.g., oriented rodnd, oriented color-selective, nonoriented rodnd, nonoriented color-selective), two types of V1 V2 interctions hve emerged. The locl type of interction requires sptil overlp of receptive fields. We hve found tht V1 V2 orienttionmtched interctions, s well s some interctions etween nonoriented color cells in V1 nd oriented color cells in V2, re highly dependent on sptil overlp (Figure 14()). In contrst, interctions etween nonoriented color cells nd oriented cell pirs with nonmtching orienttion selectivity do not require sptil overlp (Figure 14()). The interctions without sptil overlp my e medited vi extensive intr- V2 connections (stripe-to-stripe rrows in Figure 14()). Bsed on these recordings, it is hypothesized tht the locl interctions suserve locl cue identifiction (e.g., locl contour identifiction could rise vi either Huel Wiesel-like integrtion of nonoriented input from V1 or feedforwrd of oriented signls lredy generted within V1). Glol interctions suserve surfce integrtion (integrtion nd dissemintion of surfce feture informtion) s well s pproprite integrtion of surfces nd orders. This integrtion my involve surfce cpture (feedforwrd of surfceto-order signls vi oriented V1 to nonoriented V2 interctions) or order cpture. It is proposed tht Locl V1/V2 connectivity Color Disprity/ple V2 V1 V2 V1 Glol V1/V2 connectivity Color Disprity/ple Border-order the lrger glol network within V2 is le to exert influence on the locl network, resulting in contextdependent override. Although the mechnisms y which such override occurs re unknown, one possiility is tht the strength nd/or extensiveness of the glol network in V2 results in ctivtion of suppressive feedck influence on V1. A Competitive Blnce Surfce surfce Border surfce Figure 14 Cue-invrint orienttion domins in V2. () Different types of contour stimuli: sine wve grtings, line grtings, illusory contours with cute inducers, illusory contours with otuse inducers, motion contrst illusory contours. () Orienttion mps dervied from rel lines (left) nd from illusory contours (right). () From Lu HD nd Roe AW (2007) Response to Motion nd Motion Boundry in Monkey V2. Srsot, FL: Vision Sciences Society. () From Rmsden BM, Hung CP, nd Roe AW (2001) Rel nd illusory contour processing in Are V1 of the primte: A corticl lncing ct. Cererl Cortex 11: Bsed on these studies, model of contour processing in erly visul cortex hs een proposed which comprises competitive lnce etween feedforwrd V1 V2 nd feedck V2 V1 influences (Figure 15). In this model, during rel contour processing, the feedforwrd signls dominte nd ctivte mtching orienttion domins in V1 nd V2 (Figure 15(), solid rrow). During illusory contour processing, feedck signls gin prominence nd suppress domins which encode mtching rel contour orienttions

18 Visul System: Functionl Architecture of Are V2 347 Thin Thick/ple Thin Thick/ple V2 V2 V1 V1 Figure 15 Depiction of feedforwrd versus feedck forces etween V1 nd V2. Color-coded orienttion mp in V1 nd V2 (V1 V2 order nd stripe orders re indicted). () Arrow depicts orienttion-specific feedforwrd influence (locl sptil network). () Dotted rrow depicts orienttion-specific (locl sptilly loclized network) feedck influence from V2 to V1. Solid rrows depict orienttiondiverse nd sptilly extensive (glol, sptilly less restricted network) influence. Feedck ctivtion is thought to differ etween rel nd illusory contour stimultion. Rel contour stimulus preferentilly ctivtes orienttion-specific feedck (dotted rrow). Illusory contour stimultion preferentilly ctivtes orienttion-diverse feedck (solid rrows). Scle rs ¼ 1 mm (, ). (therey leding to orienttion reversl; Figure 15(), dotted rrow). In this sense, there is competitive process etween rel (feedforwrd, Figure 15()) nd illusory (feedck, Figure 15()) signls. The perception of ny contour would result from competitive lnce etween these two orienttion-selective forces. This hypothesis hs een tested using psychophysicl methods. The resoning is tht if illusory contours ctivte suppressive feedck pthwys, then dding smll mount of rel input might push the lnce in the feedforwrd direction. In other words, dding rel line on top of n illusory contour should chnge the lnce. Incresing the contrst of this rel line (from suthreshhold to suprthreshhold contrsts) should push the lnce further in the feedforwrd direction nd interfere with feedck-dependent illusory contour perception. Furthermore, since the originl oservtion ws one of orienttion reversl in V1, the feedck interction should ct in n orienttionselective mnner. In other words, it should mtter whether the rel line dded is prllel or orthogonl to the illusory contour. Results support the predictions. Prllel lines hd little effect t suthreshold contrsts ut tended to interfere with discrimintion t suprthreshold contrsts. This interference ws orienttion dependent, s orthogonl lines hd no effect on discrimintion t suprthreshold contrsts ut interfered only t suthreshold contrsts. These psychophysicl dt thus support n orienttion-specific nd contrst-specific influence of rel contours on illusory contour perception. Summry These studies provide further weight to the ide tht V1 responds to locl elements within the scene, while V2 encodes more glol spects. Reltive to V1, V2 ehves in more cue-invrint fshion. As summrized in Tle 1, wheres V1 responds only to locl luminnce cues, thin stripes encode generlized rightness percepts. Wheres V1 encodes the orienttion of only rel contours, V2 exhiits cue-invrint encoding of contour orienttion. Wheres V1 contins cells responsive to the disprity etween pixels presented to the left nd right eyes, whether they re the sme or opposite in contrst, V2 contins mp of glol coherent disprity response tht glol coherent disprity tht correltes with the perception ner nd fr percepts. This rticle (see Tle 2) hs summrized ody of evidence supporting the ide tht ech corticl re processes the visul world t different sptil scle nd, in tht sense, sees different visul world. We suggest tht these multiple views of the world compete with ech other for dominnce, perhps vi competitive lnce etween feedforwrd nd feedck signls etween different corticl res. This competition is necessrily context dependent nd therefore dynmic. Additionl studies in the wke, ehving preprtion re likely to provide dditionl insight into the dynmic spects of this proposed competition. These studies hve shown tht the sis for some glol percepts resides within mm modules Tle 2 Locl versus glol competition Why so mny corticl res? Ech re sees different view (V2 sees different things thn V1 sees) Which view domintes? Blnce of power etween res (Competition etween V1 nd V2 dominnce) Dynmic network of V1 V2 modules Correltion with ehvior

19 348 Visul System: Functionl Architecture of Are V2 Illusory contours Illusory rightness Depth from stereo com-lnk Thick/ple Thin Thick 500 µm Figure 16 Modulr sis of ehvior. Higher-order percepts such s illusory contours, illusory rightness nd color percepts, nd stereo depth re encoded in mm modules within specific V2 stripes. These modules include orienttion domins (left, ornge: horizontl; lue, verticl) in thick/ple stripes, rightless modules (middle, red: modules responsive to rel nd illusory rightness modultion) in thin stripes, nd stero depth modules (right, dotted ox: ll ner (drk pixels) minus ll fr (light pixels)). in V2 (Figure 16). Corticl modules clerly underlie not only encoding of elementl fetures such s contour orienttion nd color preference in V1, ut lso higher-order percepts such s illusory contour orienttion, illusory rightness nd color percepts, nd stereo depth percepts. In reltion to feedforwrd versus feedck competition, it is likely tht in the wke, ehving rin, the reltive dominnce of V1 nd V2 will e evident through the lnce of V1 versus V2 modulr networks. See lso: Contextul Interctions in Visul Perception; Contextul Interctions in Visul Processing; Visul Cortex: Mpping of Functionl Architecture Using Opticl Imging; Visul System: Multiple Visul Ares in Monkeys; Visul Cortex in Humns; Visul Corticl Models of Orienttion Tuning. Further Reding Amir Y, Hrel M, nd Mlch R (1993) Corticl hierrchy reflected in the orgniztion of intrinsic connections in mcque monkey visul cortex. Journl of Comprtive Neurology 334(1): Chen G, Lu HD, nd Roe AW (2006) Functionl rchitecture of mcque corticl re V2 for depth surfces reveled y opticl imging. Society for Neuroscience 32: Cumming BG nd DeAngelis GC (2001) The physiology of stereopsis. Annul Review of Neuroscience 24: Cumming BG nd Prker AJ (1999) Binoculr neurons in V1 of wke monkeys re selective for solute, not reltive, disprity. Journl of Neuroscience 19: Gegenfurtner KR (2003) Corticl mechnisms of colour vision. Nture Reviews Neuroscience 4: Goodhill GJ nd Cimponeriu A (2002) Anlysis of the elstic net model pplied to the formtion of oculr dominnce nd orienttion columns. Network 11(2): Hendry SHC nd Reid RC (2000) The koniocellulr pthwy in primte vision. Annul Review of Neuroscience 23: Huel DH nd Livingstone MS (1987) Segregtion of form, color, nd stereopsis in primte re 18. Journl of Neuroscience 7(11): Hung CP, Rmsden RM, nd Roe AW (in press) A functionl circuitry for edge-induced rightness perception. Nture Neuroscience. Julesz B (1971) Foundtions of Cyclopen Perception. Chicgo: University of Chicgo. Livingstone MS nd Huel DH (1984) Specificity of intrinsic connections in primte primry visul cortex. Journl of Neuroscience 4: Lu HD nd Roe AW (2007) Response to Motion nd Motion Boundry in Monkey V2. Srsot, FL: Vision Sciences Society Lu HD nd Roe AW (2007) Functionl orgniztion of color domins in V1 nd V2 of mcque monkey reveled y opticl imging. Cererl Cortex (doi: /cercor/hm081). Lu HD nd Roe AW (2007) Opticl imging of contrst response in Mcque monkey V1 & V2. Cererl Cortex (doi: / cercor/hl177). Prdiso MA, Blu S, Hung X, McEvoy SP, Rossi AF, nd Shlev G (2006) Lightness, filling-in, nd the fundmentl role of context in visul perception. Progress in Brin Reserch 155: Pinn B, Brelstff G, nd Spillmnn L (2001) Surfce color from oundries: A new wtercolor illusion. Vision Reserch 41 (20): Rmsden BM, Hung CP, nd Roe AW (2001) Rel nd illusory contour processing in Are V1 of the primte: A corticl lncing ct. Cererl Cortex 11: