Visual Cortex in Humans
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- Berenice Lee
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1 Visul Cortex in Humns 251 Visul Cortex in Humns B A Wndell, S O Dumoulin, nd A A Brewer, Stnford University, Stnford, CA, USA ã 2009 Elsevier Ltd. All rights reserved. Humn visul cortex comprises 4 6 illion neurons tht re orgnized into more thn dozen distinct functionl res. These res include the gry mtter in the occipitl loe nd extend into the temporl nd prietl loes. The loctions of these res in the intct humn cortex cn e identified y mesuring visul field mps. The neurons within these res hve vriety of different stimulus response properties. We descrie how to mesure these visul field mps, their loctions, nd their overll orgniztion. We then consider how informtion out ptterns, ojects, colors, nd motion is nlyzed nd represented in these mps. Regions of cortex tht respond powerfully to retinl stimultion re clled visul cortex. In the humn rin, the visul cortex is locted in the occipitl loe nd extends into the temporl nd prietl loes (Figure 1). In mny mmmlin species, visul cortex spns s much s hlf of the entire corticl surfce re; in humns, the frction is smller pproximtely 20%. A key prolem in visul neuroscience is to understnd how informtion out ptterns, ojects, colors, nd motion is nlyzed nd represented within visul cortex. One of the gret dvnces of the pst 50 yers in our understnding of the processing of visul informtion hs een the discovery of sic functionl rchitecture. In mny species, visul cortex is divided into more thn 12 distinct functionl res. The neurons within these res differ in their stimulus response properties. New developments in the pst 15 yers hve llowed multiplicity of distinct res to e identified using functionl mgnetic resonnce imging (fmri) in the intct humn rin. The res within humn visul cortex re identified y mesuring visul field mps. These re corticl regions tht contin topogrphic representtion of the visul field; stimuli djcent in the visul field evoke responses tht re djcent in visul cortex. Visul field mps cn e identified in individul sujects with fmri experiments tht lst pproximtely 1 h. Mesurement of these mps is the most relile pproch to identifying functionl re within humn visul cortex. In this rticle, we first introduce the reder to the lrgest nd est studied visul field mp, primry visul cortex (V1). We descrie how this mp is mesured using fmri, nd we discuss the min fetures of the V1 mp. We then summrize the positions nd properties of ten dditionl visul field mps. This represents our current understnding of humn visul field mps, lthough this remins n ctive field of investigtion, with more mps likely to e discovered. Finlly, we descrie theories out the functionl purpose nd orgnizing principles of these mps. The Size nd Loction of Humn Visul Cortex The entirety of humn cortex occupies surfce re on the order of 1000 cm 2 nd rnges etween 2 nd 4 mm in thickness. Ech cuic millimeter of cortex contins pproximtely neurons so tht neocortex in the two hemispheres contin on the order of 30 illion neurons. Humn visul cortex includes the entire occipitl loe nd extends significntly into the temporl nd prietl loes (Figure 1). Visul cortex contins on the order of 4 6 illion neurons. The numer of neurons in humn visul cortex fr exceeds the numer in mny other species tht depend on vision. For exmple, the surfce re of mcque monkey visul cortex is proly no more thn 20% tht of humn visul cortex, lthough the corticl neuronl density is similr. This species difference in the numer of cells in visul cortex cnnot e explined y how these species encode the visul world. The monkey smples the retinl imge t higher resolution. There re 1.5 million optic nerve fiers from ech eye in mcque nd only 1 million such fiers in humns. The lrge size of humn visul cortex is likely not result of n increse in the supply of informtion ut, rther, due to n increse in visul processing nd the orgniztion nd delivery of informtion to other prts of cortex, such s those devoted to lnguge nd reding. Given these differences in visul cortex size, it would not e surprising tht mny fetures of humn visul cortex re not present in closely relted primte systems. The Loction of Primry Visul Cortex The lrgest input to visul cortex projects from the retin vi the optic nerve to the lterl geniculte nucleus (LGN) of the thlmus nd then to primry visul cortex, commonly clled V1. V1 is locted in nd round the clcrine sulcus, which cn e found on the medil surfce of oth hemispheres (Figure 2()). The portions of left nd right V1 tht respond to signls ner the verticl meridin re
2 252 Visul Cortex in Humns connected; the xons mediting these connections pss through the posterior spect of the corpus cllosum (the splenium). The position of V1 cn e identified on histologicl grounds. There is stripe of hevy myelinted tissue in clcrine cortex tht is pprent to the nked eye. This stripe ws discovered y n Itlin medicl student, Frncesco Gennri, in 1782, nd the stripe is now clled the stri of Gennri. Consequently, V1 is lso referred to s the strite cortex, wheres other prts of visul cortex re collectively referred to s extrstrite cortex. Figure 2() is cross section through the clcrine cortex stined to revel the myelintion; note tht the white mtter is lso strongly stined. The myelintion runs through one of the corticl lyers. The stri of Gennri termintes t the order of V1. The discovery of the stri of Gennri ws one of the first indictions tht cortex could e differentited Figure 1 Humn visul cortex. The extent of humn visul cortex is indicted y the purple overly shown on the medil nd lterl views of right hemisphere. Visul cortex occupies pproximtely 20% of the surfce re of neocortex. Reproduced from Zeki S (2003) Improle res in the visul rin. Trends in Neurosciences 26(1): 23 26, with permission from Elsevier. into distinct regions. The ssocition etween this stripe nd the projection zone of the LGN ws not known t first. One hundred yers fter the discovery of the stri of Gennri, the Swedish neuropthologist Henschen showed tht it is coextensive with the LGN projection zone. Mesuring Visul Field Mps Antomicl Until recently, reserchers hve hd lmost no ccess to mesuring functionl signls in the humn rin. The development of fmri resulted in n enormous outpouring of new dt out the humn rin. One of the first pplictions of this technology ws to define the rchitecture of signls in humn visul cortex. From extensive work in niml models, prticulrly mcque, it ws known tht visul cortex could e prtitioned into set of distinct visul field mps. Hence, n erly focus in humns ws to define the loctions nd properties of humn visul field mps. The orgniztion of visul cortex is esily discernile on flttened representtion of the corticl surfce. However, in humns, the cortex is highly convoluted, msking this topogrphic orgniztion. In order to trce the orders of visul field mps, it is useful to crete representtion tht plinly exposes the signls in the sulci. This process is initited y cquiring set of ntomicl imges tht hve high contrst etween the gry nd white mtter of the rin (Figure 3()). These dt re processed to determine the loction of the white mtter (xon undles) nd the gry mtter sheet tht surrounds the white Splenium V1 Stri of gennri Clcrine sulcus Figure 2 V1 nd the stri of Gennri. () The loction of right clcrine cortex nd the splenium of the corpus cllosum re shown. Primry visul cortex flls in nd round the clcrine sulcus. Portions of right nd left primry visul cortex re connected y xons tht pss through the splenium. () Photogrph of coronl slice through the clcrine sulcus. This slice is stined for myelin (drk regions). Primry visul cortex (V1) is lso clled strite cortex ecuse it is coextensive with the densely stined stripe tht is the stri of Gennri. Reproduced from Andrews TJ, Hlpern SD, nd Purves D (1997) Correlted size vritions in humn visul cortex, lterl geniculte nucleus, nd optic trct. Journl of Neuroscience 17(8): , with permission.
3 Visul Cortex in Humns 253 c Figure 3 Corticl surfce reconstruction nd visuliztion. () A coronl slice of n ntomicl MRI imge is shown. Regions within the right hemisphere re colored to identify white mtter (purple) nd gry mtter (green). () The white nd gry mtter segmenttion identified in multiple slices defines surfce tht cn e reconstructed. (c) The corticl surfce is inflted or unfolded to provide convenient visuliztion of the corticl sheet within oth sulci (drk) nd gyri (light). mtter. Although there re severl utomted methods tht chieve good first pproximtion for this segmenttion, creful work usully requires hnd editing. Once the gry mtter voxels re identified, mny utomted tools re ville to crete threedimensionl rendering of the oundry etween the gry mtter nd the white mtter (Figure 3()). Smoothing lgorithms crete new inflted representtion of the surfce (Figure 3(c)). In this formt, the sulci re exposed so ctivtion ptterns cn e trcked long the gyri (shown s light shding) nd within sulci (shown s drk shding). Functionl Visul field mps represent visul spce in unified, orgnized rrngement. These mps re often clled retinotopic mps ecuse their orgniztion reflects the orgniztion of the retinl imge. Visul field mps cn e identified y mesuring which stimulus position in visul spce produces the lrgest response in prticulr section of visul cortex. There re mny resonle wys to perform this experiment, ut the most widely used method is to divide the mesurements into two prts: mesurements of eccentricity nd ngle with respect to the point of fixtion. In one experimentl session, one mesures corticl responses Figure 4 Trveling wve mesurements using contrst rings. The functionl ctivtion elicited y contrst ring surrounding fixtion (red dot) is shown on n inflted representtion of cortex. The pek response shifts smoothly from posterior to nterior clcrine s the ring grows from smll centrl ring to lrge peripherl ring. to series of contrst rings, which mesures the eccentricity component of the mp (Figure 4); in second session, one mesures with series of contrst wedges t different polr ngles, which mesures the ngulr component of the mp. This pproch produces strong responses in humn visul cortex. For exmple, set of contrst rings of incresing size produce pek fmri signls t series of loctions from posterior to nterior clcrine cortex (Figure 4). The pek response shifts smoothly from posterior to nterior clcrine s the ring grows from smll centrl ring to lrge peripherl ring. By nlyzing the timing of the peks nd troughs in the dt, one cn identify the visul field eccentricity tht most powerfully stimultes ech loction in visul cortex. The informtion is commonly color coded to show the eccentricity tht most effectively drives the response t ech corticl loction (Figure 5()). In second experiment, using the rotting wedge stimulus, one cn identify the ngulr direction tht most effectively stimultes ech corticl loction (Figure 5(c)). Tken together, these two mesurements define visul field mp, expressed in polr coordintes of eccentricity nd ngle. These mesurements re comined into single visul field mp. The first three mps, V1 V3, re shown in Figure 5(d). The Humn V1 Mp There re few importnt chrcteristics to note out the V1 mesurements(figure 6). First, in the right clcrine sulcus, the most effective wedges re lwys locted in the left prt of the visul field. This confirms wellknown ntomicl projection: signls from the left visul field project to V1 in the right hemisphere. Second, stimuli in the upper visul field re
4 254 Visul Cortex in Humns most effective for neurons on the lower nk of the clcrine (lingul gyrus), wheres stimuli in the lower visul field produce the gretest response on the upper nk of the clcrine (cuneus). Stimuli ner the horizontl midline re most effective t stimulting cortex c d V1 V2 V3 V2 V3 Figure 5 Polr ngle nd eccentricity mesurements define visul field mps on the corticl surfce. () The corticl surfce of the right hemisphere is displyed from ventroposterior view, emphsizing the occipitl loe. The position mps re displyed on the enlrged prt of the occipitl loe, s indicted y the lrge lck squre. The mps for eccentricity () nd polr ngle (c) re shown. The insets indicte the color code tht defines the prt of the visul field tht most effectively stimultes ech corticl loction. Visul field mps V1 V3 re identified from these eccentricity nd polr ngle mesurements (d). ner the depth of the clcrine sulcus. Thus, the V1 mp is inverted with respect to the visul field ut consistent with the retinl imge. Finlly, the centrl portion of the visul field stimultes posterior clcrine, wheres the more peripherl visul field stimultes nterior clcrine. Note tht tht there is considerly more corticl territory in V1 responding preferentilly to stimuli within 2 or 3 of visul ngle thn responding preferentilly to stimuli in the periphery. The visul field mp in V1 is distorted version of the visul field; this mgnified forel representtion is clled corticl mgnifiction. The term is unfortunte ecuse the mgnifiction is not introduced in cortex. Rther, the mgnifiction egins t the level of the fovel cone photoreceptors in the retin, which re smller nd more tightly pcked thn peripherl cones. The numer of retinl gnglion cells crrying informtion to the LGN nd the numer of V1 neurons trnsmitting the cone signls mirror the uneven cone density. Since the density of corticl neurons is pproximtely uniform, the differentil numer of neurons needed to process fovel nd peripherl signls is mnifest y n expnded surfce re for fovel compred to peripherl representtions in V1. Extrstrite Visul Field Mps The orderly representtion of eccentricity nd ngulr responses continues eyond the V1 mp. The eccentricity representtion in the surrounding cortex prllels tht in V1 (Figure 5()). The polr ngle representtion in surrounding cortex is regulr, ut it reverses direction. At the oundry of V1, the ngulr representtion turns from the verticl meridin of the upper or lower visul field nd progresses towrd the horizontl representtion (Figure 5(c)). Visul field The visul field mp in primry visul cortex h gretly mgnified representt of the centrl prt of the visul field. Stimuli in the periphery occupy fr smller surfce re compred to stimuli in the fove. The mp is inverted compred to the visul field, consistent with the inverted imge on the retin. Visul field representtion in the rin (V1) Figure 6 Schemtic representtion of the V1 visul field mp. When one looks t the fixtion point (red dot), the left prt of the visul field evokes response in right V1. Both the visul field nd the V1 representtion of this visul field re schemticlly illustrted. The V1 mp preserves visul field topogrphy, ut reltively more corticl re is devoted to the centrl prt of the visul field; this is clled corticl mgnifiction. Also, note tht the lower visul field evokes ctivity on the upper nk of the clcrine, wheres the stimulus in the upper visul field evokes ctivity on the lower nk.
5 Visul Cortex in Humns 255 The ngulr mp reversl line is the functionl signl used to define the oundry etween the V1 nd V2 mps. The V2 mp surrounds V1 (Figures 5(d) nd 7). One section is locted on the cuneus; this section is most effectively driven y signls in the lower visul field. The other section of V2 flls on the lingul gyrus; this section is most effectively driven y signls in the upper visul field. The V2 mp is surrounded y third mp, V3. At the V2/V3 oundry, the ngulr representtion reches the horizontl nd then reverses gin into V3. Creful mpping revels the presence of t lest 10 visul field mps (Figure 7). In mny cses, these visul field mps re smll mps which contin fovel representtions distinct from the fovel confluence of the V1 V3 mps. The mps shown here re lrgely greed upon, lthough there is some dete concerning the specific orgniztion of certin mps. It cn e difficult to mesure these mps for severl resons. Some of the mps re much smller thn the V1 V3 mps nd thus re t the sptil resolution limit of conventionl fmri. Also, the size of neuronl receptive fields cn e quite lrge in mny of these res, which mkes mesurements of the internl structure of these mps more difficult. As resolution nd experimentl methods improve, new mps will e identified, nd our understnding of the known mps will e refined. The presence of so mny distinct visul field mps suggests tht the mp itself serves functionl purpose. The sptil orgniztion of the mps my fcilitte certin types of corticl computtions. The internl structure of the visul field mps my simplify the connectivity needed for sptilly loclized visul computtions etween neurons specilized for crrying such informtion s stimulus orienttion, color, or motion. The simplifiction of xonl wiring is n Visul field mps V1 V2 V3 hv4 V3 V3 VO1 VO2 LO1 LO2 hmt IPS1 IPS2 hlip Figure 7 Visul field mps on corticl surfce. Currently identified visul field mps re shown on severl views of right hemisphere (see color legend). Fove nd upper/lower visul fields re indicted y the sterisk, plus, nd minus symols, respectively. The first visul mps re termed V for visul nd numer, such s V1, V2, V3, nd V3A, following the nming of pprent homologs in monkey. Douts out the homology of the fourth visul mp etween monkey nd humn cused this mp to e identified s hv4 (for humn V4), nd similrly for hlip, puttive homolog to monkey lterl intrprietl sulcus. Historiclly, V5 is lso referred to s medil temporl. Mps in lterl occipitl cortex re numered s LOx, mps in ventrl occipitl re numered s VOx, nd mps in the intrprietl sulcus re numered IPSx.
6 256 Visul Cortex in Humns importnt spect of visul field mp orgniztion, given the remrkle oservtion tht the xons in 1 mm 3 of cortex would extend over length of more thn 3 km. Achromtopsi Prosopgnosi Akinetopsi Alexi Visul Field Mps nd Perception How informtion is processed within visul field mps nd the significnce of this processing in terms of visul perception re centrl questions in visul neuroscience. The presence of multiple mps supports view of visul cortex sed on functionl speciliztions. This view contrsts with the clssic null hypothesis tht cortex is equipotentil or the theory tht there is cnonicl corticl circuit. The dominnt thinking for the pst 30 yers ssumes tht ech extrstrite mp represents computtionl speciliztion. Furthermore, it is frequently sserted tht these computtions re ssocited with specific perceptul experiences. For exmple, mp on the lterl surfce (V5/MT) is often descried s motion center, nd set of mps on the ventrl surfce re often descried s color center. The principle of ssociting mps with perceptul experience is form of the corticl speciliztion hypothesis. This frmework hs provided scheme for scientists to discuss the significnce of these mps, lthough this frmework is fr short of computtionl theory. The sis for the reltionship etween functionl speciliztion nd perceptul experience originted in neurologicl findings: dmge to specific extrstrite regions in ventrl cortex leds to specific visul disilities. Four corticl regions in which dmge cn produce specific perceptul deficit re illustrted in Figure 8. The neurologicl deficits illustrted here re inility to recognize fces nd interpret fcil expressions (prosopgnosi or fce lindness), loss of color vision of cererl origin (cererl chromtopsi), loss of motion perception (kinetopsi), nd loss of the ility to red whole words (lexi). The neurologicl literture hs focused on cquired forms of these deficits, ut prosopgnosi lso exists in congenitl (developmentl) form; it is possile tht the other dysfunctions my e discovered in developmentl form s well. The specificity of loclized rin dmge nd perceptul deficits supports the functionl speciliztion hypothesis for extrstrite mps. In contrst, the ehviorl consequences of V1/V2 lesions re not usully functionlly specilized. Dmge to smll (<5 mm) regions of V1 degrdes vision generlly within the corresponding portion of the visul field. This suggests tht the visul signls necessry for motion, color, recognition, nd so forth re intermixed in neurl signls in V1. Extrstrite regions, either Figure 8 Regions of ventrl visul cortex ssocited with specific neurologicl deficits. Regions implicted in specific visul impirments re indicted: the inility to recognize fces (prosopgnosi; red), to detect motion (kinetopsi; lue), to red words (lexi), nd color lindness (chromtiopsi; green). fmri mesurements imed t isolting these functions typiclly yield strong ctivtions t these corresponding corticl regions. inntely or through lerning, re specilized to interpret visul informtion needed in certin tsks. Hence, the rchitecture of visul cortex supports mixed model in which certin corticl zones support mixture of functions, wheres others re highly specilized. Visul Field Mp Clusters Although the reltionship etween visul field mps nd perceptul experience is n importnt scle to understnd, the ssocition etween mp nd perceptul experience does not provide full model of visul processing, nd it is unlikely tht functionl segregtion y mps constitutes the only perceptul principle in visul cortex. For exmple, the dominnt model of visul processing in retin, LGN, nd V1 consists of severl specilized nd interleved neurl pthwys within ech structure. Strting in the retin, there re multiple prllel pthwys specilized for conveying specific informtion out different spects of the visul signl. Ech pthwy contins neurons tht form smpling mosic covering the entire visul field. The neurons within these pthwys re locted ner one nother in retin nd project to djcent loctions in the LGN nd then V1. The retin, LGN, nd V1 cn thus ech e thought of s contining multiple, functionlly distinct, superimposed visul field sumps.
7 Visul Cortex in Humns 257 c hmt VO1 VO2 LO1 LO2 V1,V2, V3 hv4 hmt This rchitecture is not likely to e completely ndoned in extrstrite cortex. In fct, there re lredy exmples in which single visul mp contins distinct neurl circuits tht mesure different spects of the visul signl. An erly nd importnt exmple of functionl heterogeneity cn e found in motionselective cortex (V5/MT), in which there is n orderly representtion of oth motion direction nd inoculr depth. Just s functionl speciliztions exist t resolution finer thn the mp, speciliztions my lso exist t corser scle. It ws previously noted tht the V1 V3 mps shre prllel eccentricity representtion nd re functionlly divided y reversls in the ngulr representtion. This sme mp rchitecture is present in severl other clusters of mps, locted in the ventrl, dorsl, nd lterl regions of visul cortex (Figure 9). Such orgniztion of the individul mps into visul field mp clusters my reflect corselevel orgniztion tht follows specific functionl cpilities; visul field mps my e rrnged in clusters when the neurl mosics within these mps serve similr computtionl gols. Conclusions V3B, V3A LO1 LO2 V3A, V3B The visul system is vlule model system for neuroscience reserch ecuse of the extensive informtion we hve out the retinl encoding of light, the multiple pthwys tht communicte retinl informtion to cortex, nd the distriution of the informtion from these pthwys into mps in visul hmt VO1 VO2 V1,V2, V3, hv4 VO1 VO2 LO1 LO2 V1,V2, V3 hv4 V3B, V3A Figure 9 Visul field mp clusters. () Schemtic digrm of the orgniztion of eccentricity representtions in visul cortex. This digrm is sed on mesurements of these visul field mp clusters, s shown on flttened cortex () nd on threedimensionl rendering of the inflted corticl surfce (c). Ech cluster contins severl visul field mps tht cn e delineted sed on the polr ngle mps. VO, ventrl occipitl; LO, lterl occipitl. 11 ο 3 ο cortex. This informtion mkes the visul system n excellent trget for study eyond the core of vision science, including the neuroscience of development, plsticity, nd consciousness. The orgniztion of visul pthwys, mps, nd clusters lso my hve ppliction s n rchitecturl model of generl corticl processing. The prllels for other sensory systems re ovious nd in mny wys pper to e vlid. For exmple, severl distinct uditory mps with tonotopic orgniztion hve een demonstrted. It lso my e tht cognitive functions, such s decision mking or the distriution of ffective functions, re orgnized using mixed rchitecturl model in which certin regions contin generl nd others more specilized processing. To the extent tht the corticl rchitecture of visul cortex mtches tht in other prts of cortex, we ecome more confident in results from oth fields. Functionl neuroimging, which opertes t reltively corse resolution of severl millimeters to multiple centimeters, is well suited to uncovering structures t the scle of these visul mps or groups of mps. In the ner future, there will e mny opportunities to link the functionl neuroimging mesurements in quntittive wys to mesurements t other resolutions down to smll ( few thousnd) popultions of corticl neurons. Advnces in functionl neuroimging methods hve lredy provided new informtion out the white mtter pthwys nd longdistnce connections etween corticl zones. There will e sustntil improvements in mesurements of the moleculr constituents of these corticl regions nd in trcking chnges in the moleculr composition throughout development or following dmge. Our current understnding of the rchitecture of visul cortex mkes it good system for developing these new methods nd lerning out corticl function rodly. See lso: fmri: BOLD Contrst; Vision: Surfce Segmenttion; Vision: Light nd Drk Adpttion; Visul System: Functionl Architecture of Are V2; Visul System: Multiple Visul Ares in Monkeys; Visul Attention; Visul Corticl Models of Orienttion Tuning. Further Reding Andrews TJ, Hlpern SD, nd Purves D (1997) Correlted size vritions in humn visul cortex, lterl geniculte nucleus, nd optic trct. Journl of Neuroscience 17(8): Huel DH (1988) Eye, Brin nd Vision. New York: Freemn. Huettel S, Song A, nd McCrthy G (eds.) (2004) Functionl Mgnetic Resonnce Imging. Sunderlnd, MA: Sinuer. Wndell BA (1995) Foundtions of Vision. Sunderlnd, MA: Sinuer. Zeki S (1993) A Vision of the Brin. London: Blckwell. Zeki S (2003) Improle res in the visul rin. Trends in Neurosciences 26(1):
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