Learning to see: experience and attention in primary visual cortex

Transcription

1 2 Nture Pulishing Group rtiles Lerning to see: experiene nd ttention in primry visul ortex 2 Nture Pulishing Group Roy E. Crist, Wu Li nd Chrles D. Gilert The Rokefeller University, 23 York Avenue, New York, New York 2, USA Correspondene should e ddressed to C.D.G. (gilert@rokefeller.edu) The response properties of neurons in primry sensory orties remin mllele throughout life. The existene of suh plstiity, nd the hrteristis of form of impliit lerning known s pereptul lerning, suggest tht hnges in primry sensory ortex my medite lerning. We explored whether modifition of the funtionl properties of primry visul ortex (V) ompnies pereptul lerning. Bsi reeptive field properties, suh s lotion, size nd orienttion seletivity, were unffeted y pereptul trining, nd visul topogrphy (s mesured y mgnifition ftor) ws indistinguishle etween trined nd untrined nimls. On the other hnd, the influene of ontextul stimuli pled outside the reeptive field showed hnge onsistent with the trined disrimintion. Furthermore, this property showed tsk dependene, only eing mnifest when the niml ws performing the trined disrimintion. Cortil plstiity is likely involved in the norml ognitive proessing of dult nimls, nd is importnt even in the funtioning of primry sensory res. Wheres plstiity my underlie funtionl reovery following CNS lesions, it my lso medite funtionl hnges ompnying experiene nd lerning. Severl hrteristis of pereptul lerning suggest the involvement of erly stges in sensory proessing, perhps even s erly stge s primry sensory ortex. Evidene in support of this ide hs een found in the somtosensory nd uditory systems 2 4. Primry sensory ortex is useful model for lerning euse its underlying mehnisms its iruitry, funtionl rhiteture nd reeptive field (RF) struture n e essily studied. Vrious ortil hnges oth re ssoited with improvement in pereptul performne nd our in primry sensory orties 2 4, whih suggests tht the mehnisms of lerning my e generl to the neoortex s whole. Independent studies of plstiity of RF properties nd funtionl rhiteture of primry visul ortex (V) heighten the possiility tht plstiity ssoited with pereptul lerning might our there. Wheres ertin RF properties suh s oulr dominne re mutle only during limited ritil period erly in postntl development 5, numer of other properties, most notly, visul topogrphy nd RF size, n e influened y visul experiene throughout life. In the visul system, psyhophysil evidene shows tht trining n improve disrimintion stimulus ttriutes, inluding position, depth, orienttion, motion, texture, sptil phse nd hyperuity 6. In previous study, we showed tht prtie with prtiulr visul disrimintion tsk, three-line isetion, produes sustntil improvement tht is speifi to the trined stimulus 2. The speifiity for position nd orienttion suggests tht the erly stges of visul proessing re involved in the lerning of this tsk. To determine whether V is involved in the lerning of suh visul disrimintions, we trined two mque monkeys to perform the sme isetion tsk used with humn sujets, nd we reorded from ells in re V. We exmined the RF properties nd the mp of visul spe in trined nimls for hnges tht might relte to pereptul trining. In ddition to its lssil response properties, ell s response to stimulus within the RF is modulted y the presene of dditionl stimuli round the RF, nd this modultion depends strongly on the geometri reltionship of the stimulus elements. We explored the tuning of ells to shifts in the lterl plement of two prllel lines with positions nlogous to those of lines in the isetion tsk. Furthermore, we exmined the influene of the ehviorl stte of the niml on these intertions. RESULTS Monkeys improve isetion disrimintion with trining Both monkeys showed sustntil improvement in isetion performne with trining. Over the ourse of 3 weeks of trining, monkey showed threshold redution greter thn ftor of three (Fig. ), nd monkey 2 showed 57% threshold redution (Fig. d). Monkeys were trined with series of tsks tht pproximted the finl isetion tsk. The initil threshold (Fig. ) ws mesured during the first week of trining on the isetion tsk itself, nd some lerning my hve ourred efore this time. During the reording phse, the monkey hd fewer opportunities to prtie the isetion disrimintion, ut the threshold mesured severl months fter eletrophysiologil reordings egn shows tht the improved performne ws mintined over this period (Fig. ). Cortil mgnifition does not hnge with trining One of the most striking effets of pereptul trining in the somtosensory nd uditory modlities 3,4 is the rempping of the ortil representtion of the sensory surfe suh tht muh lrger region of ortex is responsive to stimultion of the trined region. To exmine whether rempping of visul spe ompnied the lerning of the isetion disrimintion tsk desried ove, we onstruted topogrphi mp of the ortex of the trined monkeys from reordings of superfiil lyer ortil ells. The lotion of the RF enter of n isolted unit ws determined y reording the response to the flshing of smll r in pttern nture neurosiene volume 4 no 5 my 2 59

2 rtiles 2 Nture Pulishing Group 2 Nture Pulishing Group Threshold (min. of r) 6 Bisetion trils Fixtion trils Fixtion point Sde trgets Bisetion stimulus Fixtion Stimulus Dely Response Lever Fixtion point Stimulus Response Rewrd Trining phse 3 66 Week of trining of eqully sped lotions oth long nd orthogonl to n xis defined y the orienttion preferene of the neuron. Reordings were mde in grid-like pttern in steps of.5 to mm. The RF lotions determined for 44 seprte penetrtion sites in monkey were used to estimte the pproprite position of isozimuth nd isoelevtion lines surrounding the representtion of the visul lotion where the isetion stimulus ws presented (Fig. 2). An estimte of ortil mgnifition of the re surrounding the trined lotion ws otined y lulting the squre root of the numer of squre millimeters representing re of visul spe 7 ; the mgnifition ftor ws 2 min/mm for the ortil region representing the visul position of the isetion stimulus. This figure mthes reported vlues for mgnifition t this ortil lotion Fig. 2. Representtion of visul spe did not hnge s result of isetion trining. () Comprison of ortil mgnifition ftor mesured t severl lotions surrounding the representtion of the trined visul lotion. () Mp of ortil re representing the region of spe where the isetion stimulus ws presented during trining (3.25 prfovel). Isozimuth nd isoelevtion lines re drwn sed on the RF positions mesured for eh penetrtion site (lk dots). () Cortil mp of untrined hemisphere of monkey 2. (d) Cortil mp of trined hemisphere of monkey 2. Light gry res in () nd (d) indite region where isetion tsk ws represented. Drk gry res in ( d) show re over whih mgnifition ftor ws lulted for pnel (). d Reording phse 6 5 ms Before trining Before trining Mgnifition ftor (mm/degree) L monkey After trining monkey After trining Fig.. Monkeys improved with trining on isetion tsk. () The tsks tht monkeys were trined to perform. Top, single isetion stimulus presenttion s it ws shown to monkey. Bottom, fixtion tsk in whih the monkey ws merely required to mintin fixtion until the fixtion point ws dimmed. Beneth the imges of the stimuli re tres inditing the time ourse of stimulus presenttion. () Thresholds mesured for monkey for eh week of trining. During the reording phse, the monkey reeived less isetion trining, ut improvement ws retined. () Before nd fter trining thresholds mesured for monkey. (d) Before nd fter trining thresholds mesured for monkey 2. in the ortex of nive monkeys 8, inditing tht no sustntil inrese ourred s result of pereptul trining. A similr mp ws mde from the trined hemisphere of monkey 2 (Fig. 2d). The mgnifition ftor t the ortil lous of the isetion stimulus ws 9 min/mm, losely mthing the vlue otined in monkey. Though the vlues for the two monkeys used in our study mth those reported for nive monkeys, the individul vrition found in the ortil representtion of spe might permit more sutle hnges to e missed in these omprisons. Therefore, we mpped the untrined hemisphere of monkey 2 (Fig. 2). The mgnifition ftors for vrious eentriities in oth trined hemispheres nd the untrined hemisphere of monkey 2 were ompred ross the ortil region surrounding the isetion tsk; the vlues in ll three hemispheres were lmost identil (Fig. 2). No hnge in reeptive field size or orienttion tuning Along with sustntil hnges in the size of the ortil representtion of the trined skin surfe, hnges in RF size hve een reported to ompny the lerning of somtosensory disrimintion tsk 3. Thus, we sked whether hnges in RF size in V ompnied lerning of the isetion disrimintion. We flshed smll right r in lotions spnning the re of the RF long the orienttion xis, nd lulted RF size s the enter-to-enter distne etween the outermost stimulus r lotions showing response ove spontneous levels. The men RF Monkey 2, left (untrined) hemisphere A P M -.5 monkey, trined hemisphere monkey 2, trined hemisphere monkey 2, untrined hemisphere distne from fove (degrees) d Monkey, right (trined) hemisphere mm Monkey 2, right (trined) hemisphere elevtion (deg) zimuth (deg) M A P L 52 nture neurosiene volume 4 no 5 my 2

3 2 Nture Pulishing Group rtiles 2 Nture Pulishing Group Fig. 3. RF size nd orienttion tuning ndwidth did not hnge following isetion trining. RF size ws determined using the minimum response field tehnique (see Methods). () Comprison of RF size in trined nd untrined monkeys. Left r indites men RF size in monkey trined on isetion disrimintion (n = 39; monkey, 9 units; monkey 2, 2 units). Right r indites men RF size in untrined nimls (n = 5). () Orienttion tuning in trined nd untrined monkeys. Left r shows men width of orienttion tuning urves in two trined monkeys (n = 8; monkey, 87 units; monkey 2, 2 units). Right r indites the men vlue of tuning width in untrined nimls (n = 63). size ws lulted for two trined nd two untrined monkeys for neurons t eentiities ner tht of the isetion stimulus used with the trined nimls (etween 2 nd 4 ); RF size in trined nd untrined nimls did not differ (Fig. 3). Cells in V re lso prtiulrly sensitive to the orienttion of edges nd line stimuli. Seletivity for orienttion hs een proposed to e involved in hyperuity disrimintions. However, we found similr orienttion tuning ndwidth of ells in ortex of trined versus untrined nimls (Fig. 3). Tsk dependene of ontextul intertions Beuse stndrd properties suh s mgnifition ftor, RF size nd orienttion seletivity were unffeted y trining, we explored possile hnges in higher-order properties suh s ontextul tuning. Cells in V re sensitive to ptterns more omplex thn oriented line segments 9. The effet of pling dditionl lines outside the lssil RF of ell depends on the preise geometri reltionships etween the elements of the stimulus pttern. For exmple, single olliner line presented outside the lssil RF long the orienttion xis often provides filittory input to unit responding to n optimlly oriented line within its RF 2 ; when pled in side-y-side onfigurtion, the line outside the RF hs n inhiitory influene 2,22. We therefore exmined whether ontextul ptterns in the three-line isetion stimulus uniquely ffeted the responses of visul ortil neurons in trined nimls. We entered n optimlly oriented r in the RF, nd mesured the response to seond, prllel r presented in flnking position, similr to the side-y-side rrngement of lines in the isetion stimulus. Beuse the monkeys were trined to perform oth fixtion tsk nd isetion tsk, we ould exmine the responses of our units while n niml ws performing different visul disrimintions. We mesured hnges in the responses of neurons with RFs ner the trined lotion of the visul field, nd ompred the hnges sed on the tsk the RF Size (rmin) Tuning width (deg) Trined Trined Untrined Untrined monkey ws performing. Two effets ould e distinguished. First, the response rte of neuron ws slightly redued when the monkey ws instruted to perform isetion trils. This finding ws not unexpeted, s we hve oserved previously tht when dditionl stimuli (in this se, the isetion stimulus) re pled in the neighorhood of the RF, the response of the ell is inhiited. The most striking effet, however, ws tht the shpe of the tuning urve for the modultion produed y flnking r ws very different when the monkey ws performing the isetion tsk thn when it ws performing the fixtion tsk. In fixtion trils, the response of typil neuron ws redued y the presene of flnking r on either side of the RF (Fig. 4, top right). When the monkey ws performing the isetion disrimintion, the effet of the flnking r hnged drmtilly from inhiition to filittion, nd the filittory effet depended on the distne etween the two rs (Fig. 4, ottom). Furthermore, the extent of filittion ws symmetri; the filittory effet of flnking r ws stronger on one side of the RF. This effet ws even more drmti for seond ell (Fig. 4), in whih presenting flnking r on one side of the RF during isetion trils produed sustntil filittion, wheres pre- Fixtion trils Bisetion trils 8 Normlized response Normlized response Distne (degrees) Normlized response Normlized response Distne (degrees) - Distne (degrees) Fig. 4. Contextul intertions hnged when the monkey performed the isetion tsk. () Left, stimulus rrngement used to exmine ontextul intertions during the performne of fixtion nd isetion trils. Dotted line indites orders of RF. Upper right, tuning urve of one ell to the plement of prllel rs while the monkey ws performing fixtion tsk. Response rte of ell to ll stimuli hs een normlized y the response rte otined y pling single optimlly oriented r inside the RF. Lower right, tuning urve of the sme ell for the sme set of prllel r stimuli while the monkey performed isetion trils. () Exmple of the tuning of nother ell for prllel r stimulus. () Exmple of the tuning from third ell for prllel r stimulus. Blk lines indite responses otined when the niml ws performing the fixtion tsk. Gry lines indite tuning during isetion trils. In the tuning urves, the vertil lines represent the oundries of the reeptive fields determined y the minimum response field tehnique (see Methods). These oundries did not hnge with isetion versus fixtion trils. Error rs, s.e.m. nture neurosiene volume 4 no 5 my 2 52

4 rtiles 2 Nture Pulishing Group 2 Nture Pulishing Group isetion trined hemisphere ( = 67) fixtion senting the r on the opposite side used profound inhiition of the unit s response. The shpe of the tuning urve for flnking intertions during isetion trils vried onsiderly from ell to ell (Fig. 4 ). The wide vriety of tuning shown y different ells for flnking intertions during isetion performne hllenged us to develop method of ompring the responses over the reorded popultion. The mount of filittion or inhiition produed y the flnking r ws greter when the niml ws performing isetion trils thn when it ws performing fixtion trils. To desrie this effet for the popultion of neurons, we defined mesure of the strength of these modultory intertions. mximum normlized response minimum normlized response modultion = mximum normlized response + minimum normlized response isetion n untrined hemisphere ( n = 3) fixtion Fig. 5. Modultion depended on the tsk tht the monkey performed in trined ut not untrined hemisphere. () Modultion during isetion nd fixtion trils. Amount of modultion oserved for different units when the monkeys were performing the isetion tsk in omprison to the mount of modultion when the nimls were performing fixtion trils (n = 67). () Monkey performed isetion tsk on trined hemisphere, nd test stimuli were presented to ells in untrined hemisphere. Modultion did not depend on the ehviorl ondition for ells in the untrined hemisphere. Bisetion performne diminishes with distne from the trined lotion, suggesting tht ells in ortil res remote from the trined lotion should not show the tsk-dependent hnges in modultion. Contrry to wht we oserved in the trined hemisphere, in the untrined hemisphere, the modultion of ellulr responses y prllel line ws similr during the isetion nd fixtion tsks (Fig. 5). The differene in modultion under isetion etween the trined nd untrined hemispheres ws signifint (p <.5, t = 2.22, two-sided t-test), nd the differene in modultion in the untrined hemisphere etween fixtion nd isetion ws not signifint (t =.7, p =.29, pired t-test). Contextul intertions hve een shown to e influened y sptil ttention 23. Clerly, the fous of ttention hnged from the enter of vision to the peripherl lotion of the isetion Modultion is mesure of the influene of the prllel r on the ell s response to r entered in its RF. By definition, modultion rnges from zero (the response to single r ws not influened y the presene of the dditionl r) to one (the response ws filitted y n dditionl r in one position nd inhiited y the dditionl r in nother position). The mount of modultion oserved for 67 ells while the monkey performed isetion trils ws plotted ginst the modultion oserved under fixtion trils (Fig. 5). The differene in the distriution in modultion in the trined hemisphere etween fixtion nd isetion trils ws highly signifint (p <.2, t = 3.95, pired t-test). Most ells exmined in the experiment desried ove hd RFs ner ut not overlpping the visul lotion where the isetion stimulus ws presented during trining. The pperne of trining effets in the region surrounding the trined lotion is in greement with psyhophysil evidene from humn oservers demonstrting tht isetion disrimintion trining improves performne within ouple of degrees of the trined lotion 2. isetion fixtion. Trined hemisphere ( n = 2) fixtion. Untrined hemisphere ( n = 3) fixtion Fig. 6. Chnges in ontextul intertions re not oserved for untrined stimulus ptterns or in the untrined hemisphere. () Tsk dependene of ontextul intertions ws only seen for ptterns present in the trined stimuli. Modultion y olliner line showed no effet of ehviorl ondition. () Monkey performed fixtion tsk while test stimuli were presented in untrined hemisphere in the presene of isetion-like stimulus. The presene of isetion-like stimulus did not led to hnges in modultion. () Monkey performed isetion tsk in trined lotion while test stimuli nd isetion-like pttern were presented to ells in untrined hemisphere. Modultion of ellulr responses in the untrined hemisphere did not depend on ehviorl ondition. isetion Untrined hemisphere ( n = 3) fixtion nture neurosiene volume 4 no 5 my 2

5 2 Nture Pulishing Group rtiles 2 Nture Pulishing Group Response (spikes/s) Numer of ells Untrined hemisphere Br position (degree) N=45 < to to to to.. to.2.2 to.3 trined untrined =.3 RF position differene (degree) < to to to to.. to.2.2 to.3 tsk when our monkeys performed the isetion disrimintion. If the hnge in ontextul intertion were solely due to hnges in the fous of ttention, we would expet the modultion of ellulr responses to other ontextul ptterns. Therefore, we exmined the effet of performing the isetion tsk on the modultion produed y olliner line presented in the RF surround, ut little hnge in the modultion index ws oserved (Fig. 6). The finding tht tsk-dependent hnges were only seen for ontextul ptterns present in the trined stimulus suggests tht the differene oserved in ontextul intertions desried here ws the result of the trining the monkeys reeived. In our experiments, however, when monkey ws performing the isetion tsk, the test pttern ws presented in the RF of the ell simultneously with the isetion stimulus itself. This rises the possiility tht the hnges in ortil intertions we hve desried might e due to the differene in the stimulus pttern. If this were the se, however, the response of ell to other lol ontextul ptterns, suh s the olliner line used in the experiment desried ove, would lso hnge when the isetion pttern ws present. This ws lerly not the se (Fig. 6). Further evidene of this ft omes from reordings in the untrined hemisphere, where the modultion of ellulr responses ws unffeted y the simple presene of the isetion stimulus (Fig. 6). Finlly, to further demonstrte tht ells in untrined ortex did not show tsk-dependent hnges in modultion, we determined whether the presene of isetion-like stimulus in the untrined hemifield during isetion disrimintion in the trined lotion would indue hnges in the modultion of ells in untrined ortex. No suh hnge ws oserved (Fig. 6). The ove findings indite tht ontextul intertions, nd not the responses of ells to simple stimuli, were ffeted y trining. However, given tht the ontextul intertions show tsk dependene, one might sk whether the stndrd RF properties of size, position nd orienttion might e similrly ffeted. We mesured the RF profiles of ells under oth fixtion nd isetion trils, nd fitted these profiles with Gussin. The RF profiles were nerly identil under oth ehviorl onditions nd in oth the trined nd untrined hemispheres (Fig. 7). Between fixtion nd isetion trils, no signifint differene ws found for RF position (n = 45, t =.27, p.79), RF size (n = 45, t =.52, p.3) or orienttion preferene (n = 2, t =.67, p >.). d Trined hemisphere Br position (degree) N=45 fixtion isetion fixtion (guss) isetion (guss) =.3 RF size differene (degree) Fig. 7. Mesurement of reeptive field profiles during fixtion nd isetion trils in trined nd untrined hemisphere. () Exmple of ell from untrined hemisphere. Responses were mesured for single r stimulus pled in vrious positions long n xis orthogonl to the RF orienttion. Drk lines re fitted to the men responses, gry lines re the Gussin fits. Solid lines re mesurements tken during isetion, nd dshed lines re mesurements tken during fixtion. () Exmple of ell from trined hemisphere, sme onventions s in (). (, d) Popultion nlysis of ells from trined nd untrined hemispheres, showing men differene in RF position () nd size (d) under isetion versus fixtion. For this nlysis, the RF position nd width were otined from the pek position nd one stndrd devition, respetively, of the Gussin fits. Solid rs, trined hemisphere; open rs, untrined hemisphere. No signifint differene ws oserved in either trined or untrined hemispheres. DISCUSSION The suggestion tht pereptul lerning might rely on primry sensory ortex omes from the gret speifiity in the lerning for position nd orienttion, ttriutes to whih erly stges in sensory proessing re seletive. The speifiity of visul pereptul lerning in itself is not suffiient to indite the involvement of the erly stges of visul ortil proessing, euse even ells in inferotemporl ortex n e indued to show seletivity for suh properties 24. Moreover, ttention n redue the size of ell s RF in ertin ortil res 25 nd therefore heighten the sptil resolution of tsks involving these res. One lso hs to ount for the speifiity of pereptul lerning to the ontext within whih disrimintion is mde. Beuse ells in V show seletivity for omplex stimulus onfigurtions, it eomes diffiult to use omplexity s lue to determine the site of lerning within the ortil hierrhy. In this vein, we note tht lerning to disriminte even very omplex stimulus ptterns n show some speifiity for the lotion in whih the stimulus ws presented during trining 26. Nevertheless, the suggestion tht V might e involved in pereptul lerning is reinfored y the demonstrtion of lerning effets in other primry sensory res, nd one might expet ommon mehnisms to pply in ortil res serving ll sensory modlities. V is ple of rempping spe under ertin onditions in prtiulr, fter retinl lesions No hnges in ortil mgnifition, or ortil reruitment, were found in the urrent study to ompny trining on the isetion disrimintion, despite lrge gins in pereptul ility. Furthermore, we found the si RF properties of size nd orienttion tuning to e unffeted y isetion trining, even though nlogous properties were modified in somtosensory nd uditory ortex following trining on virtion or pith disrimintion. The pprent differene in the mehnisms operting in different ortil res my reflet the ft tht our trining involved emergent properties of ortil neurons, nd showed speifiity for ontext. In ontrst, the hnges in the somtosensory nd uditory systems resulted from disrimintion trining on the input properties to the ortex, nd therefore might not depend on intrinsi ortil iruits. Inresing the mount of modultion invoked y visul ptterns in the trined stimulus n esily e imgined to filitte pereptul performne. It is noteworthy in this ontext tht dur- nture neurosiene volume 4 no 5 my 2 523

6 rtiles 2 Nture Pulishing Group 2 Nture Pulishing Group ing isetion trils, mny ells were strongly filitted y prllel r. In study of ontextul intertions in monkeys viewing pssively, ells in untrined nimls did not show filittion for this pttern 2. The sene of suh filittion in untrined nimls strengthens the onlusion tht these intertions were the result of isetion trining. A sustrte for these intertions exists in V in the xon ollterls of superfiil lyer pyrmidl ells, whih extend over severl millimeters. These ells onnet units of similr orienttion preferene 3 33 nd re therefore well positioned to medite intertions etween the elements of the isetion stimulus used in our study. The ility of long-rnge horizontl onnetions to provide oth exittory nd inhiitory input to their trgets is lso suggestive of role in the intertions desried ove. The implementtion of pereptul lerning y seletive modultion of susets of horizontl onnetions llows for the speifiity of the lerning for the detils of stimulus onfigurtion. A mehnism of ortil reruitment would not hve this property, nd further, might e expeted to led to deline in performne in the untrined portions of visul spe represented y the djent ortil regions. This roing is not seen in the pereptul lerning experiments. The ontextul influene tht est represents the ttriute involved in the isetion tsk is the modultion in the ells responses to seond, prllel line pled t vrying seprtion from line pled entrlly within the RF. The oserved effets were speifi for this property, euse they were not seen for different ontextul influene, tht of oliner line t vrying offsets. To mke stronger onnetion etween the modultion index nd the trined tsk, one n sk how the sle of the sensitivity to line seprtion mesured for n individul neuron ompres to the threshold in the isetion tsk. At the point t whih neurons show their gretest sensitivity (the steepest prt of the slope of the ontextul tuning urves), the mount of hnge in the distne etween the prllel lines tht gives one stndrd devition hnge in the firing rte is 9.75 minutes of r, on verge. The threshold in the tsk, fter trining, ws four minutes of r. The sensitivities re therefore roughly of the sme sle, ut the differenes rgue tht some mount of pooling in the tivity of the neurons is required to hieve the level of ehviorl performne. Perhps the most striking spet of the findings reported here is the pprent ility of the ortex to dynmilly modify the proessing of visul informtion ording to immedite ehviorl requirements. The monkeys in this study were trined to perform two different tsks: simple dimming tsk nd the threeline isetion disrimintion. Lterl intertions in trined monkeys depended on the tsk the monkey ws performing t the time. The tsk dependene of the ontextul intertion permits the sme neurons to medite entirely different pereptul funtions tht my require opposing neuronl mehnisms. The inhiition of responses y prllel lines under the fixtion tsk hs een suggested to e involved in surfe segmenttion 2. As shown here, this inhiition n swith to filittion during the performne of the three-line isetion tsk. One would not wnt to design system in whih three-line isetion trining would disrupt the sujet s ility to segment the visul sene. To llow the performne of oth tsks, one would either hve to segregte the neurons mediting the tsk into seprte funtionl omprtments, or llow the sme neurons to multiplex their funtion in tsk-dependent fshion. The results of the urrent study suggest the ltter solution. The further implition of this ide is tht t the sme time the ells hnge their RF struture, they hnge their line lel, suh tht modultion in their firing is interpreted differently y the rest of the nervous system. As mehnism underlying the improvement in the isetion tsk, we propose hnge in the strength nd exittory/inhiitory lne of suset of horizontl inputs to V neurons. This modultion of the horizontl input would then vry ording to the seprtion etween the soure nd trget neurons, therefore providing greter modultion of the tuning to the seprtion of prllel lines. The ontextul modultion would in turn e modulted y top-down influenes, presumly medited y feedk onnetions from higher-order ortil res, to generte its tsk dependene. Thus, ontextul influenes within prtiulr ortil re my ome not just from lterl onnetions within tht re, ut s n intertion etween lol iruits nd feedk onnetions from higherorder ortil res, thus providing mehnism for oth the stimulus seletivity nd tsk dependene of the ortil responses to trined stimulus ptterns. METHODS Two mque monkeys (M multt) were trined nd used to ollet the physiologil dt reported here. During reording nd trining, monkeys were seted in primte hir fing omputer monitor. The monkey s hed ws restrined using surgilly implnted stinless steel post. Eye movements were monitored using slerl serh oil system 3 (CNC Engineering, Settle, Wshington). During stimulus presenttion, monkeys were required to mintin fixtion within.75. retngulr window; trils were orted nd rewrd ws withheld if n eye movement greter thn.5 ws mde. The tul vriility in eye position from tril to tril ws muh less thn tht llowed y the fixtion window. The men position nd stndrd devition for typil experiments (sed on smple of dt otined during the reording of 2 units), reltive to the fixtion point, ws.7 ±.3 in zimuth nd.2 ±.5 in elevtion. Qulity of fixtion ws the sme during oth fixtion nd isetion trils; the men differene in eye position etween fixtion nd isetion trils for typil sessions ws.3 ±.4 in zimuth nd. ±.2 in elevtion. All proedures were onduted in ompline with the Ntionl Institutes of Helth Guide for the Cre nd Use of Lortory Animls, nd under pprovl of institutionl review ords. Trining. Monkeys were initilly trined to perform simple fixtion tsk (Fig. ). The niml ws tught to initite trils y pulling lever tthed to the primte hir. When the lever ws pulled, smll right spot ws displyed on the sreen, nd the niml ws required to mintin fixtion on the spot until it ws dimmed. If the monkey relesed the lever within rief period of time following the dimming of the fixtion spot, smll drop of juie ws given s rewrd. To teh the monkeys to perform the isetion disrimintion, we first trined them to perform series of tsks designed to led to isetion performne. The initil thresholds for isetion performne refleted the first thresholds mesured for the finl isetion tsk. In the isetion tsk, the monkey ws presented with set of three prllel horizontl lines (Fig. ). The monkey s tsk ws to determine whether the entrl line ws nerer to one or the other flnk. During the presenttion of the stimulus, the monkey ws required to mintin fixtion on smll spot. Following the presenttion of the isetion stimulus, the fixtion spot ws extinguished nd the monkey indited its response y mking n eye movement to one of two smll spots presented t the top nd ottom of the sreen. Corret responses were rewrded with drop of juie. The responses of the monkey to the isetion tsk were reorded nd used to lulte the threshold of performne using the method of proits. Eletrophysiologil reording. After trining ws omplete, monkeys were surgilly implnted with steel hmer (inner dimeter, 22 mm) enlosing rniotomy over portion of V. Surgil proedures were done under septi onditions with pentoritl sodium nesthesi. Reordings were mde with glss-oted pltinum iridium miroeletrodes 4 with impednes etween. MΩ nd 3. MΩ. Using stepping motor mirodrive (Nrishige, Tokyo, Jpn), penetrtions were mde t typil intervls of.5 mm through the dur. 524 nture neurosiene volume 4 no 5 my 2

7 2 Nture Pulishing Group rtiles 2 Nture Pulishing Group Reordings from single units were onduted dily in 2 to 4 hour sessions. After penetrting the dur, rough RF mp ws otined while the niml performed fixtion tsk. All reordings were mde from the operulr surfe of V t RF eentriities rnging from.5 to 5.. Grnule lyers were identified y the hrteristis suh s high levels of spontneous tivity nd risk on/off response 5,6. When suh tivity ws enountered, the eletrode ws retrted to restrit reording to the superfiil 6 µm of the ortex. Neuronl tivity ws reorded over 6-ms epohs spnning the presenttion of the stimulus. The level of kground tivity ws mesured for 2 ms, nd stimulus ws then presented for ms. During eh tril, three to five 6-ms reording periods were onduted. For eh ell, time window ws set within rnge of 5 25 ms fter stimulus onset depending on the lteny nd length of the response. The men firing rte within this response window minus the spontneous firing rte, lulted from the numer of spikes otined in the first 2 ms of the reording epoh, ws used to determine the mgnitude of the evoked response. The t-test ws used to evlute the signifine of the evoked response. Eh reording session egn y hrterizing the RF extent nd orienttion preferene while the monkey performed fixtion trils. RF extent ws determined y the minimum response field tehnique in whih smll r (typilly.2.25 in length nd 3 inhes in width) ws presented in steps (..25 prt) either long the prinipl orienttion xis of the ell to determine its length, or orthogonl to the orienttion xis to determine its width. The distne etween the outermost points tht eliited signifint response ws defined to e the size of the RF. For the omprison etween RF profiles during fixtion nd isetion trils in trined nd untrined hemisphere (Fig. 7), RF extent ws determined y fitting the responses otined t eh position with Gussin nd tking the stndrd devition to e the size of the RF. Susequently, ontextul intertions were exmined while the niml performed either fixtion or isetion trils. During isetion trils, experimentl stimuli were presented simultneously with the isetion stimulus. The fixtion nd isetion trils were olleted in seprte loks, nd we olleted trils per stimulus ondition. The tuning urves were lulted, nd re shown long with stndrd error rs. ACKNOWLEDGEMENTS This work ws supported y NIH grnts EY7968 (C.D.G.) nd GM7524 (R.E.C.). RECEIVED 2 OCTOBER 2; ACCEPTED 28 FEBRUARY 2. Gilert, C. Adult ortil dynmis. Physiol. Rev. 78, (998). 2. Weinerger, N. M. et l. Retuning uditory ortex y lerning: preliminry model of reeptive field plstiity. Conepts in Neurosiene, 9 32 (99). 3. Renzone, G. H., Merzenih, M. M., Jenkins, W. 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Neuron 5, (995). nture neurosiene volume 4 no 5 my 2 525