Vol 466 15 July 1 doi:1.138/nture919 Blindsight depends on the lterl geniculte nucleus Michel C. Schmid 1, Sylwi W. Mrowk 1, Jnit Turchi 1, Richrd C. Sunders 1, Melnie Wilke 1, Andrew J. Peters 1, Frnk Q. Ye 2 & Dvid A. Leopold 1,2 Injury to the primry visul cortex (V1) leds to the loss of visul experience. Nonetheless, creful testing shows tht certin visully guided ehviours cn persist even in the sence of visul wreness 1 4. The neurl circuits supporting this phenomenon, which is often termed lindsight, remin uncertin 4.Herewedemonstrte tht the thlmic lterl geniculte nucleus (LGN) hs cusl role in V1-independent processing of visul informtion. By compring functionl mgnetic resonnce imging (fmri) nd ehviourl mesures with nd without temporry LGN inctivtion, we ssessed the contriution of the LGN to visul functions of mcque monkeys (Mcc multt) with chronic V1 lesions. Before LGN inctivtion, high-contrst stimuli presented to the lesion-ffected visul field (scotom) produced significnt V1-independent fmri ctivtion in the extrstrite corticl res V2, V3, V4, V5/middle temporl (MT), fundus of the superior temporl sulcus (FST) nd lterl intrprietl re (LIP) nd the nimls correctly locted the stimuli in detection tsk. However, following reversile inctivtion of the LGN in the V1-lesioned hemisphere, fmri responses nd ehviourl detection were olished. These results demonstrte tht direct LGN projections to the extrstrite cortex hve criticl functionl contriution to lindsight. They suggest vile pthwy to medite fst detection during norml vision. We cclimted two dult mcque monkeys with chronic V1 spirtion-lesions (Methods Summry) to the fmri-testing environment. During the experiments, the nimls st upright in custom-mde chir plced in verticl 4. T mgnetic resonnce scnner, nd fixted on smll point in the centre of the screen while we recorded the eye position nd presented visul stimuli (Supplementry Methods). We estlished the oundries of the retinotopiclly orgnized visul res using stndrd functionl mpping methods 5 (Supplementry Figs 1, 2). The centre of the lesion ws locted t the representtion of the horizontl meridin, nd extended severl millimetres oth dorslly nd ventrlly into V1 (lck re in Fig. 1, re etween red rs in Fig. 1, lck re in Supplementry Fig. 2), corresponding to visul eccentricity of,2u to,u of visul ngle. Previous work hs shown tht this type of lesion in V1 does not lter the retinotopic orgniztion ssessed with fmri in severl extrstrite res 6. To ssess whether the extrstrite cortex could e ctivted in the sence of V1 input, we presented smll (2u dimeter) rotting chequerord pttern, known to effectively drive responses in the erly visul cortex, to the visul field region ffected y the lesion (scotom, Fig. 1c, top). In independent experimentl runs, we presented the stimulus to the corresponding region in the helthy hemisphere s control (Fig. 1c, ottom). As expected, the stimulus shown to the unffected hemifield elicited strong, circumscried, contrlterl responses in V1, neighouring extrstrite res V2, V3, V4, V5/MT nd FST (Fig. 2, d), nd prietl re LIP (Supplementry Fig. 3, c). When the stimulus ws presented inside the scotom region, there ws no V1 response ecuse the cortex hd een removed; nonetheless, there were stimulus-driven responses in c LS STS Scotom stimultion IOS Dorsl Posterior Anterior Ventrl Intct ed 3 9 1 stimultion LS STS Intct Anterior Left Right IOS ed Posterior 3 9 1 Time (s) Figure 1 Experimentl set-up., A side view on the right hemisphere of n inflted mcque rin. An re of, mm 2 of grey mtter in the operculr prt of V1, representing the visul field etween,2u nd u, hs een surgiclly spirted nd is shown in lck. Extrstrite res, the suject of nlysis in this study, re hidden in the sulci surrounding V1, including the lunte (LS), inferior occipitl (IOS) nd superior temporl (STS) sulci. To fcilitte the visul exmintion of extrstrite cortex, the occipitl loe (dshed circled re) ws cut nd flttened (inset)., Axil sections of monkey 1 s (top) nd monkey 2 s (ottom) occipitl loes t the position indicted y the green dshed line in. The outwrd orders of white nd grey mtter re highlighted y green nd ornge dotted lines, respectively. The lesions re evident y the sence of grey mtter (re etween red line mrkers). c, To compre visully elicited responses in the extrstrite cortex in the presence of V1 input to those in its sence, we sptilly restricted (2u dimeter) rotting chequerord stimuli nd presented them either inside (top) or outside (ottom) the scotom (prt of the visul field ffected y the V1 lesion, indicted here y red dotted circles; the single red dot indictes the fixtion point for the niml). 1 Lortory of Neuropsychology, Ntionl Institute of Mentl Helth (NIMH), 49 Convent Drive, Bethesd, Mrylnd 892, USA. 2 Neurophysiology Imging Fcility, NIMH, Ntionl Institute of Neurologicl Disorders nd Stroke (NINDS), Ntionl Eye Institute (NEI), 49 Convent Drive, Bethesd, Mrylnd 892, USA. 1 Mcmilln Pulishers Limited. All rights reserved 33
NATURE Vol 466 15 July 1 V1 V3 V4 MT FST 5 T-sttistic 5 15 T-sttistic 15 d e c 1 Correct trils (%) f 1 Ctch Scotom 1 1 Contrst (%) 1 Correct trils (%) Ctch Scotom Figure 2 Visul processing in V1-lesioned monkeys., Functionl ctivtion mp (t-sttistic) of monkey 1 s non-lesioned visul cortex to 85 cycles of visul stimultion outside the scotom (see Fig. 1c, ottom). The mp hs een horizontlly flipped for esier comprison with the lesioned hemisphere. White dotted nd solid lines show the position of the verticl nd horizontl meridin representtions, respectively, derived from independent retinotopic mpping experiments (Supplementry Figs 1, 2) to revel the functionl oundries of extrstrite res 5,6., Activtion mp of monkey 1 s lesioned hemisphere to 85 cycles of visul stimultion inside the scotom (see Fig. 1c, ottom). The position of the stimulus inside the scotom ws effective in tht the lesion surrounding the V1 cortex with intct grey mtter ws not ctivted. In the sence of V1 input, res V2, V3, V4 nd V5/MT continue to e visully responsive. c, Behviourl performnce of monkey 1 in detecting visul stimuli (.2u dimeter) extrstrite res V2, V3, V4, V5/MT, FST nd LIP (Fig. 2, e nd Supplementry Fig. 3, d), indicting tht stimulus informtion reched these res in the sence of V1 input. Moreover, compring the ctivtion ptterns of the lesioned nd control hemispheres reveled tht the responses within ech re were loclized to their norml retinotopic positions. One prominent difference etween the lesioned nd control conditions ws the emergence of dorsoventrl symmetry in res V2 nd V3, with only dorsl, ut not ventrl, portions of these res exhiiting V1-independent responses. This effect, which hs lso een oserved in humn lindsight, cnnot e ttriuted to the position of either the lesion or the stimulus, s the retinotopiclly mtched stimulus in the opposite visul field evoked roughly equivlent responses in the dorsl nd ventrl prts. On the ehviourl level, oth monkeys retined the ility to detect nd mke sccdic eye movement to smll (.2u dimeter) high-contrst, ut not low-contrst, visul trgets presented inside the scotom, leit with diminished performnce. Trget contrsts were djusted sed on performnce in the control hemifield, such tht there ws relile detection even t the lowest contrst level (%) (Fig. 2c, f nd Supplementry Methods). When low-contrst stimuli were presented inside the scotom, oth monkeys consistently mintined centrl fixtion, indicting tht they were unwre tht ny stimulus ws eing presented 2. By comprison, when we showed high-contrst (1%) stimuli, the monkeys were le to detect roughly hlf of the presenttions, consistent with previous reports of lindsight in humns nd monkeys 1 4,8. Finlly, direct comprison etween detection performnce nd fmri responses to the sme set of stimuli (2u dimeter) presented in the scotom t vrying luminnce contrst levels confirmed the tight reltionship etween the two mesures of lindsight (Supplementry Fig. 4). 34 1 Mcmilln Pulishers Limited. All rights reserved 1 1 Contrst (%) presented inside (red line) or outside (lue line) the scotom t different luminnce contrst levels compred to constnt grey ckground. On one third of the trils, no stimulus ws presented nd the monkey ws rewrded for mintining centrl fixtion (green line). Dt represent men 6 s.e.m. from five experiments. d, Functionl ctivtion mp of monkey 2 s nonlesioned hemisphere to 95 cycles of visul stimultion outside the scotom. e, Activtion mp of monkey 2 s lesioned hemisphere to 95 cycles of visul stimultion inside the scotom. f, Behviourl performnce of monkey 2 for detecting visul stimuli inside (red line) nd outside (lue line) the scotom or during ctch trils (green line). Dt represent men 6 s.e.m. from five experiments. Although oth monkeys disply lrge visul deficit, they continue to process visul informtion to some extent s performnce improves with stimulus contrst. Severl controls ruled out the possiility tht scttered light ws contriuting to the oserved ehviourl nd fmri responses to stimuli in the scotom effects 9,1 : first, ehviourl responses were sptilly ccurte, s performnce ws clculted y considering only sccdes tht were within 1u of the trget. Second, when the sme high-contrst stimuli were presented monoculrly in the monkeys lindspots (the re covered y the optic disk in the retin), their performnce fell to zero (Supplementry Fig. 5). Third, no systemtic fmri modultion ws mesured in the intct V1 of either monkey djcent to the lesion (Fig. 2, e). Fourth, strong extrstrite ctivtion ws found in third monkey, in which we mde much lrger lesion, encompssing operculr V1 nd portion of the djcent V2 (Supplementry Fig. 6). As well s ruling out non-specific effects of scttering light 9,1 s responsile for the oserved effects, these experiments demonstrte vile visul pthwy tht cn operte in the sence of V1, in ccordnce with studies in humn ptients nd lesion studies in monkeys 1 8,11,12. We next investigted the components of the pthwy tht provide V1-ypssing input to the extrstrite cortex nd support visul performnce. Previous work hs shown tht direct ntomicl projections exist from the LGN, the min thlmic rely etween the retin nd the primry visul cortex, to severl extrstrite visul res 13,14. We therefore proposed tht residul ctivity in the extrstrite cortex, nd corresponding ehviourl performnce, is the result of sensory signls trnsmitted directly from the LGN. To exmine this possiility, we temporrily disrupted neurl ctivity within the LGN of V1-lesioned monkeys y loclly injecting the GABA A -receptor gonist THIP 15 (Methods Summry), nd mesured the effects on corticl fmri responses nd ehviourl performnce. Specificlly, we reversily inctivted the posterior prt of the LGN, which represents the prfovel 1
NATURE Vol 466 15 July 1 LGN inctivtion V1 V3 V4 MT 15 15 T-sttistic c 1 Correct trils (%) 1 Ctch Scotom 1 1 d LGN inctivtion e f 1 Correct trils (%) Ctch Scotom Figure 3 Role of the LGN in driving V1-independent visul processing., We inctivted the LGN y injecting the GABA A gonist THIP (Methods Summry). We co-injected the drug with the mgnetic resonnce contrstgent gdolinium (totl volume 2 ml, Methods Summry), to visulize the site in mgnetic resonnce imges. Here, coronl section through the posterior prt of monkey 1 s LGN (1 mm on the nterior-posterior xis in stereotctic coordintes) is shown. Injection of gdolinium resulted in loclized increse in the intensity of the T1-weighted mgnetic resonnce signl, with dimeter of,3 mm (red rrow). We ensured tht injections were reproducile cross experiments y permnently implnting mgnetic-resonnce-comptile cnnul (yellow rrow)., Functionl ctivtion mp of mcque 1 s left, lesioned, hemisphere to visul 1 1 Contrst (%) stimultion inside the scotom (35 stimultion cycles) during inctivtion of the LGN. LGN inctivtion results in the elimintion of V1-independent visul responses (Fig. 2). c, Monkey 1 s performnce in detecting visul trgets t different luminnce contrsts. Dt represent men 6 s.e.m. performnce from three experiments with THIP injections into the LGN. The injections eliminted the monkey s ility to detect trget inside the scotom. d, Inctivtion of mcque 2 s posterior LGN. e, Activtion mp of monkey 2 s right, lesioned, hemisphere to visul stimultion inside the scotom ( stimultion cycles) during LGN inctivtion. f, Monkey 2 s performnce for correctly detecting trgets during LGN inctivtion. Dt represent the men 6 s.e.m. performnce in three experiments with THIP injections. 1 visul hemifield nd covers the scotom-ffected region (Methods Summry), on multiple occsions vi chroniclly implnted guide tues comptile with mgnetic resonnce. The mgnetic resonnce contrst-gent gdolinium ws co-injected long with THIP, llowing us to visulize the spred of the injection in the tissue. In oth monkeys (Fig. 3, d), the 2 ml injection diffused to n effective dimeter of pproximtely 3 mm in the cudl LGN, s visulized y the gdolinium (Fig. 3, d). After we hd inctivted the LGN, virtully ll extrstrite responses in the V1-lesioned hemispheres disppered (Fig. 3, e), indicting tht the residul ctivtion to stimuli presented in the scotom hd indeed reched the extrstrite cortex y mens of direct projections from the LGN. Moreover, inctivtion of the LGN olished the nimls residul cpcity to detect high-contrst stimuli presented to the scotom region of the visul field (red line, Fig. 3c, f), demonstrting tht the LGN is the criticl thlmic link tht supports ehviourl performnce in lindsight. As control, detection of visul stimuli in the opposite hemifield (outside the scotom) ws unffected. To otin more quntittive ssessment of the mount of informtion trnsmitted directly vi the LGN, we compred the strength of fmri responses under norml visul stimultion conditions to those otined inside the scotom, with nd without dditionl LGN inctivtion, cross ll experimentl sessions (Fig. 4). On verge, cross ll monkeys nd extrstrite res, scotom stimultion with the LGN intct hd fmri ctivtion of,% of tht under norml conditions. This finding is in good qulittive greement with previously reported fmri ctivtion ptterns of humn nd monkey lindsight sujects 6,,11 nd with single-unit recordings in re V5/MT of mcque monkeys with chronic V1 lesions 12. In ddition, inctivting the LGN reduced ctivtion levels to less thn 5% of norml. Aprt from demonstrting the role of the LGN in supporting lindsight, these dt revel severl interesting fetures of V1-independent 5 Les. + inj. 3 1 1 d v V3 dv4 vv4 MT FST LIP 5 Les. + inj. 3 1 1 d v V3 dv4 vv4 MT FST LIP T-sttistic T-sttistic 1 Mcmilln Pulishers Limited. All rights reserved Figure 4 Quntittive summry of men fmri ctivtion levels. In extrstrite res under norml conditions (V1 nd LGN intct, lue rs); in the sence of V1 input (lesion, red rs); nd in the sence of input from V1 nd the LGN (Les. 1 inj., green rs)., Dt collected from monkey 1 nd corresponding to the men 6 s.e.m. t-sttistic otined during 85 visul stimultion cycles without LGN inctivtion nd 35 stimultion cycles with LGN inctivtion., Dt from experiments with monkey 2, in which the men 6 s.e.m. t-sttistic hs een computed over 95 stimultion cycles without LGN inctivtion nd stimultion cycles with LGN inctivtion. On verge cross ll res nd monkeys, fmri ctivtion in extrstrite res is reduced y,% when V1 input is missing. Additionl LGN inctivtion reduces ctivity y more thn 95% compred to norml levels. 35
NATURE Vol 466 15 July 1 vision. For exmple, the symmetry of visul responses in res V2 nd V3 to stimuli in the scotom, which hs previously een oserved in lindsight ptient GY, my reflect the differentil contriutions of prllel visul strems to upper- nd lower-field vision: nmely, tht lrger proportion of neurons in the retin nd the LGN respond to lower-visul-field stimultion thn to upper-visul-field stimultion 16. Psychophysicl evidence suggests tht this is is primrily relted to the mgnocellulr system 1, which, t the level of the retin, is lso the system tht is less ffected y retrogrde degenertion following V1 injury 18. Thus, one possiility for the oserved symmetry following strite cortex lesions is tht the norml visul-field symmetry of the mgnocellulr system is unmsked y post-lesionl neurodegenertion. The ner-complete drop in oth extrstrite ctivtion nd ehviourl performnce not only implictes the LGN s criticl hu for lindsight, ut lso rgues ginst the existence of pthwys tht do not involve the LGN. Blindsight functions hve een oserved for decdes in numer of different species, nd hve trditionlly een ttriuted to second visul pthwy in which retinl informtion is relyed vi the superior colliculus nd secondry thlmic nucleus, the pulvinr, to the extrstrite cortex 19. Although the role of the superior colliculus in mediting lindsight functions nd V1-independent responses in re V5/MT hs een demonstrted,21, there is presently no direct evidence tht the pulvinr is involved. On the contrry, the pulvinr my hve miniml contriution for the following resons: its ntomicl sis s first-order visul-rely is in question 22 (however, see refs 23 nd 24); its neurl responses pper to e driven more y corticl thn y colliculr inputs 25 ; there is no residul vision following LGN lesions 26 ; nd neurl ctivity in re V5/MT is eliminted during LGN inctivtion 2. Conversely, contriution of the LGN to lindsight hs sometimes een left s n open possiility 4,21, prticulrly since the neurl degenertion following V1 ltion selectively spres LGN cells tht project directly to the extrstrite cortex 28. These V1-ypssing projection neurons pper to elong chiefly to the koniocellulr system, whose neurons reside primrily in the interclted LGN lyers 13,14,22. Interestingly, it is these koniocellulr-rich lyers tht receive input from the superior colliculus 22,29. This my explin the previously descried effects of superior colliculus ltion on V1-independent visul processing,21. Finlly, recent oservtions using diffusiontensor mgnetic resonnce imging in humn lindsight ptient mny yers fter V1 lesion show significnt projections etween the LGN nd re V5/MT 3, lthough the direction of the projection could not e estlished. Our dt demonstrte tht the LGN hs cusl role in V1- independent visul function. We propose tht this residul function is medited y neurons in the interclted lyers of the LGN, whose direct projections to the extrstrite cortex my not only support residul vision following V1 lesions, ut my lso serve s shortcut to the high-level cortex during norml vision. In providing shortltency, eye-specific signls to high-level visul cortex, such shortcut could serve to fcilitte some forms of rpid ehviourl responses to visul stimuli. METHODS SUMMARY The min experiments were crried out in two helthy dult monkeys (Mcc multt): one mle (8 kg weight; monkey 1) nd one femle (5 kg weight; monkey 2). Additionl control experiments were conducted in third helthy dult monkey (femle, 5 kg weight). All procedures followed the Institute of Lortory Animl Reserch (prt of the Ntionl Reserch Council of the Ntionl Acdemy of Sciences) guidelines nd were pproved y the Ntionl Institute of Mentl Helth (NIMH) Animl Cre nd Use Committee. To immoilize the hed during experiments nd to record eye movements during ehviourl testing, we implnted hedposts nd eye coils following stndrd procedures. We cused V1-re lesions y cogulting pil vessels over the intended lesion re on the V1 operculum, nd y spirting grey mtter within this re. In oth monkeys the lesions were locted,2 u visul eccentricities wy from the fove (monkeys hd no prolems mintining fixtion), covering 36 1 Mcmilln Pulishers Limited. All rights reserved etween one-third nd one-hlf of operculr V1. We used lesion in third monkey, covering ll of operculr V1 nd lrge prts of the djcent V2 (Supplementry Fig. 6), to evlute the possiility of scttered-light effects on intct grey-mtter tissue in the first two, smller lesioned, monkeys. To rech the LGN for inctivtion, we chroniclly implnted mgnetic-resonnce-comptile fused-silic guide tues (Plstics One) in monkeys 1 nd 2, using frmeless stereotxy procedure (Brinsight, Rogue Reserch). For the experiments, we injected the GABA A gonist THIP (Tocris; concentrtion: 6.6 mg ml 21, dissolved in sterile sline, ph.4; volume: 2 ml; rte:.5 1 ml min 21 ) for LGN inctivtion together with the mgnetic resonnce contrst-gent gdolinium (Berlex Imging, 5 mm) to visulize the site nd extent of the injection in mgnetic resonnce imge. Received 1 Decemer 9; ccepted 18 My 1. Pulished online 23 June; corrected15 July 1 (see full-texthtml version for detils). 1. Weiskrntz, L., Wrrington, E. K. & Snders, M. D. Visul cpcity in the heminopic field following restricted occipitl ltion. Brin 9, 9 28 (194). 2. Cowey, A. & Stoerig, P. Blindsight in monkeys. Nture 33, 24 249 (1995). 3. Keting, E. G. Residul sptil vision in the monkey fter removl of strite nd preoccipitl cortex. Brin Res. 18, 21 29 (19). 4. Cowey, A. The lindsight sg. Exp. Brin Res., 3 24 (1). 5. Brewer, A. A., Press, W. A., Logothetis, N. K. & Wndell, B. A. Visul res in mcque cortex mesured using functionl mgnetic resonnce imging. J. Neurosci. 22, 1416 1426 (2). 6. Schmid, M. C., Pngiotropoulos, T., Augth, M. A., Logothetis, N. K. & Smirnkis, S. M. Visully driven ctivtion in mcque res V2 nd V3 without input from the primry visul cortex. PLoS ONE 4, e552, doi:1.131/ journl.pone.552 (9).. Bseler, H. A., Morlnd, A. B. & Wndell, B. A. Topogrphic orgniztion of humn visul res in the sence of input from primry cortex. J. Neurosci. 19, 2619 262 (1999). 8. Cowey, A. & Stoerig, P. Visul detection in monkeys with lindsight. Neuropsychologi 35, 929 939 (199). 9. Collins, C. E., Lyon, D. C. & Ks, J. H. Responses of neurons in the middle temporl visul re fter long-stnding lesions of the primry visul cortex in dult new world monkeys. J. Neurosci. 23, 2251 2264 (3). 1. Cmpion, J., Ltto, R. & Smith, Y. M. Is lindsight n effect of scttered light, spred cortex, nd ner-threshold vision? Behv. Brin Sci. 6, 423 44 (1983). 11. Goeel, R., Muckli, L., Znell, F. E., Singer, W. & Stoerig, P. Sustined extrstrite corticl ctivtion without visul wreness reveled y fmri studies of heminopic ptients. Vision Res. 41, 1459 144 (1). 12. Rodmn, H. R., Gross, C. G. & Alright, T. D. Afferent sis of visul response properties in re MT of the mcque. I. Effects of strite cortex removl. J. Neurosci. 9, 33 5 (1989). 13. Sincich, L. C., Prk, K. F., Wohlgemuth, M. J. & Horton, J. C. Bypssing V1: direct geniculte input to re MT. Nture Neurosci., 1123 1128 (4). 14. Bullier, J. & Kennedy, H. Projection of the lterl geniculte nucleus onto corticl re V2 in the mcque monkey. Exp. Brin Res. 53, 168 12 (1983). 15. Cope, D. W., Hughes, S. W. & Crunelli, V. GABA A receptor-medited tonic inhiition in thlmic neurons. J. Neurosci. 25, 11553 11563 (5). 16. Curcio, C. A. & Allen, K. A. Topogrphy of gnglion cells in humn retin. J. Comp. Neurol. 3, 5 25 (199). 1. McAnny, J. J. & Levine, M. W. Mgnocellulr nd prvocellulr visul pthwy contriutions to visul field nisotropies. Vision Res. 4, 232 2336 (). 18. Cowey, A., Stoerig, P. & Perry, V. H. Trnsneuronl retrogrde degenertion of retinl gnglion cells fter dmge to strite cortex in mcque monkeys: selective loss of P cells. Neuroscience 29, 65 (1989). 19. Dimond, I. T. & Hll, W. C. Evolution of neocortex. Science 164, 251 262 (1969).. Mohler, C. W. & Wurtz, R. H. Role of strite cortex nd superior colliculus in visul guidnce of sccdic eye movements in monkeys. J. Neurophysiol., 4 94 (19). 21. Rodmn, H. R., Gross, C. G. & Alright, T. D. Afferent sis of visul response properties in re MT of the mcque. II. Effects of superior colliculus removl. J. Neurosci. 1, 1154 1164 (199). 22. Stepniewsk, I., Qi, H. X. & Ks, J. H. Do superior colliculus projection zones in the inferior pulvinr project to MT in primtes? Eur. J. Neurosci. 11, 469 4 (1999). 23. Bermn, R. A. & Wurtz, R. H. Functionl identifiction of pulvinr pth from superior colliculus to corticl re MT. J. Neurosci. 3, 6342 6354 (1). 24. Lyon, D. C., Nssi, J. J. & Cllwy, E. M. A disynptic rely from superior colliculus to dorsl strem visul cortex in mcque monkey. Neuron 65, 2 29 (1). 25. Bender, D. B. Visul ctivtion of neurons in the primte pulvinr depends on cortex ut not colliculus. Brin Res. 29, 258 261 (1983). 26. Schiller, P. H., Logothetis, N. K. & Chrles, E. R. Functions of the colour-opponent nd rod-nd chnnels of the visul system. Nture 343, 68 (199). 2. Munsell, J. H., Neley, T. A. & DePriest, D. D. 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NATURE Vol 466 15 July 1 29. Hrting, J. K., Huert, M. F., Hshikw, T. & vn Lieshout, D. P. Projection of the mmmlin superior colliculus upon the dorsl lterl geniculte nucleus: orgniztion of tectogeniculte pthwys in nineteen species. J. Comp. Neurol. 34, 25 36 (1991). 3. Bridge, H., Thoms, O., Jdi, S. & Cowey, A. Chnges in connectivity fter visul corticl rin dmge underlie ltered visul function. Brin 131, 1433 1444 (8). Supplementry Informtion is linked to the online version of the pper t www.nture.com/nture. Acknowledgements We thnk A. Mier nd D. McMhon for comments on the mnuscript; S. Smirnkis, R. Bermn, R. Wurtz, B. Richmond, S. Guderin nd M. Fukushim for discussions; C. Zhu nd H. Merkle for mgnetic resonnce coil construction; K. Smith, N. Phipps, J. Yu, G. Dold, D. Ide nd T. Tlot for technicl ssistnce; D. Sheinerg for developing visul stimultion softwre; nd memers of the Brin Wndell lortory for developing nd shring mrvist softwre. This work ws supported y the Intrmurl Reserch Progrmme of the NIMH, the NINDS, nd the NEI. Author Contriutions M.C.S. took the primry led for ll spects of this work nd wrote the pper; S.W.M. helped with experiments nd nlysis; J.T. helped with the experiments nd developed the inctivtion method; R.C.S. creted the lesions; M.W. developed the inctivtion method; A.J.P. helped with experiments nd nlysis; F.Q.Y. developed pre-processing softwre nd optimized mgnetic resonnce sequences; nd D.A.L. provided resources, cted in supervisory role on ll spects of this work nd wrote the pper. Author Informtion Reprints nd permissions informtion is ville t www.nture.com/reprints. The uthors declre no competing finncil interests. Reders re welcome to comment on the online version of this rticle t www.nture.com/nture. Correspondence nd requests for mterils should e ddressed to M.C.S. (schmidmich@gmil.com) 1 Mcmilln Pulishers Limited. All rights reserved 3