A precise form of divisive suppression supports population coding in the primary visual cortex

Transcription

1 A prcis form of ivisiv supprssion supports population coing in th primary visual cortx San P MacEvoy 1,2, Thomas R Tuckr 1,2 & Davi Fitzpatrick 1 Th rsponss of nurons in th primary visual cortx (V1) to an optimally orint grating ar supprss whn a non-optimal grating is suprimpos. Although cross-orintation supprssion is thought to rflct mchanisms that maintain a istribut co for orintation, th ffct of suprimpos gratings on V1 population rsponss is unknown. Using intrinsic signal optical imaging, w foun that pattrns of tr shrw V1 activity vok by suprimpos qual-contrast gratings wr prict by th avrags of pattrns vok by iniviual componnt gratings. This priction hl across contrasts, for summ sinusoial gratings or nonsumming squar-wav gratings, an was vint in singl-unit xtracllular rcorings. Intracllular rcorings rval consistnt lvls of supprssion throughout th tim cours of subthrshol rsponss. Ths rsults inicat that ivisiv supprssion powrfully govrns population rsponss to multipl orintations. Morovr, th spcific form of supprssion that w obsrv appars to support inpnnt population cos for stimulus orintation an strngth an calls for a rassssmnt of mchanisms that unrli cross-orintation supprssion. Th rspons of a singl nuron in V1 to an optimally orint grating is markly ruc by th suprimposition of an orthogonal grating that os not vok a rspons by itslf 1 3. This crossorintation supprssion is gnrally consir to b a manifstation of a prvasiv systm of ivisiv supprssion in V1, contributing to functions such as contrast gain control an runancy ruction in th coing of natural imags 4 1. Although cross-orintation supprssion has bn wll charactriz at th lvl of singl nurons, th mannr in which ivisiv supprssion contributs to population coing in V1 is lss clar. Bcaus a singl grating activats a broa population of cortical nurons, th absolut lvl of activity of any particular mmbr of th population provis littl information about th orintation of th stimulus. Howvr, th rlativ activity of th nurons in th population provis a robust signal that faithfully rprsnts th orintation of a singl grating stimulus an, mor gnrally, th two-imnsional Fourir spctrum of any stimulus In principl, ivisiv supprssion can act to prsrv th rlativ lvls of activity among th mmbrs of th population, prvnting phnomna such as rspons saturation from istorting th istribut rprsntation 5,16,17. In this contxt, cross-orintation supprssion can b viw as a rscaling of th ntir population rspons to maintain an accurat istribut rprsntation of th orintations in th compoun grating stimulus. This viw maks th simpl priction that th population rspons pattrn in V1 to suprimpos gratings shoul approximat th scal linar sum of th rsponss to th componnt gratings prsnt by thmslvs. Although this priction is straightforwar, th availabl vinc lavs its accuracy uncrtain. Early stags of cortical procssing ar wll charactriz as linar transformations of input from th latral gniculat nuclus (LGN), but subsqunt stags introuc prominnt nonlinaritis in singl-cll rsponss (for xampl, cntr-surroun intractions), whos combin ffct on th shap of th population tuning function is ifficult to prict from singl-unit rcorings Morovr, availabl singl-unit ata on th rsponss of singl nurons to suprimpos gratings ar largly limit to scriptions of th ffct of a non-optimal grating on th rsponss of nurons to thir prfrr grating 1 3,7,23.Unrstaning th ffct of a suprimpos grating on population activity rquirs masuring nuronal rsponss to all possibl combinations of two orintations, irrspctiv of thir rlationship to ach nuron s prfrr orintation. A furthr complication in unrstaning th ffct of ivisiv supprssion on population coing is th fact that virtually all prvious stuis of cross-orintation supprssion us a singl class of stimuli: rifting sinusoial gratings whos luminanc profils sum whn two gratings ar suprimpos 2,3,7, Th mrits of using this typ of stimulus configuration ar substantial 28, but it is not known whthr th proprtis of supprssion that hav bn scrib with this stimulus st can b gnraliz to suprimpos contours whos luminanc profils o not sum linarly. This is a situation that ariss frquntly in natural scns (for xampl, as a rsult of occlusion) an prsnts no lss of a challng to a population co for orintation. In spit of this, two rcnt stuis 26,27 hav suggst that cross-orintation supprssion may aris unr stimulus conitions that ar uniqu to aitiv suprimposition of sinusoial gratings. This woul appar to limit 1 Dpartmnt of Nurobiology, Duk Univrsity Mical Cntr, Durham, North Carolina, USA. 2 Prsnt arsss: Cntr for Cognitiv Nuroscinc, Univrsity of Pnnsylvania, Philalphia, Pnnsylvania, USA (S.P.M.), an th Dpartmnt of Biology, Guilfor Collg, Grnsboro, North Carolina, USA (T.R.T.). Corrsponnc shoul b arss to S.P.M. (macvoy@psych.upnn.u). Rciv 2 Sptmbr 28; accpt 5 March 29; publish onlin 26 April 29; corrct aftr print 6 May 29; oi:1.138/nn.231 NATURE NEUROSCIENCE VOLUME 12 [ NUMBER 5 [ MAY

2 Figur 1 Intrinsic signal optical imags of tr shrw V1 acquir uring prsntation of singl an suprimpos gratings. (a c) Singl conition pattrns vok in on animal by stationary flashing rctangl-wav gratings intifi by th icon in ach panl. () High-magnification viws of rgions of intrst (ROIs) not by yllow boxs in a c. () Th avrag optical signals in ach row of pixls in th corrsponing colorco ROI shown in. Zro on th x axis corrspons to th bottom row of pixls. (f h) Singl conition imags acquir from a iffrnt animal with gratings at 71 an 111. (i) Pattrns of activation in ach imag wr quantifi by computing avrag optical signal valus in bloo vssl fr ROIs for all pixls with th sam prfrr orintation. Pixl orintation prfrncs wr rawn from an orintationprfrnc map that was riv from a sparat atast. (j) Each PRP rprsnts th istribution of cortical activity vok by a singl stimulus, following th color co in i. A PRP gnrat from th avrag of th componnt grating ROI imags is shown in blu. Curvs ar bst-fit circular Gaussians. th rol of ivisiv supprssion in supporting population coing of natural scns. Th aim of our stuy was to provi a irct tst of th ffct of ivisiv supprssion on population rsponss in V1. Using intrinsic signal imaging tchniqus in th tr shrw, w foun that pattrns of population activity vok by suprimpos gratings wr prict with high prcision by a spcific form of ivisiv rscaling in which rsponss to qual-contrast grating pairs wr th man of th pattrns vok by ach componnt grating prsnt alon. Morovr, this outcom was unchang whthr stimuli wr compos of summ sinusois or nonsumming squar-wav gratings an hl for both high an low stimulus contrasts. Our rsults not only inicat that ivisiv supprssion has a funamntal an consistnt rol in constructing a faithful population rprsntation of multipl simultanous orintations, but also call for a rassssmnt of th factors that account for th magnitu of supprssion an th mchanisms that hav bn propos to xplain it. RESULTS Population rspons to suprimpos gratings W first sought to charactriz th pattrns of population activity that ar vok by nonsumming suprimpos gratings that iffr in orintation. To o so, w acquir intrinsic signal optical imags of tr shrw V1 uring prsntation of stationary rctangl-wav gratings that wr prsnt alon or as suprimpos pairs (Fig. 1). Unlss othrwis spcifi, componnt gratings always ha qual contrastsof.singlgratingsat1351 an 451 (Fig. 1a,b) vok complmntary pattrns of rlativly activ (ark) an inactiv (light) rgions, corrsponing to th istribution of prfrr orintation across th cortical surfac. Whn th gratings wr suprimpos, ths pattrns wr almost compltly absnt (Fig. 1c ), consistnt with th priction from singl-unit stuis that cortical rgions a b c Lat Ant 1 mm Stimulus f g h i V1 V2 R/R 1, j M Cortical istanc (mm) Prfrr orintation ( ) rsponing vigorously to on grating shoul hav much wakr rsponss whn an orthogonal grating is suprimpos. To fully charactriz th population rspons to suprimpos gratings, w construct population rspons profils (PRPs) rprsnting th istribution of cortical activity that was vok by a stimulus across cortical sits prfrring th full rang of orintation prfrncs (Fig. 1f j; s Mthos). Distributions of population activity vok by singl gratings ha pak positions that match thir stimulus orintations, confirming th accuracy of th PRP procur. In contrast, PRPs for suprimpos gratings oftn pak at intrmiat orintations, pning on th angl btwn componnts, an gnrally ha markly ruc hights compar with singl grating PRPs. Broaly consistnt with ivisiv supprssion, PRPs for suprimpos gratings closly rsmbl PRPs riv from th avrag of componnt rsponss, which w rfr to as th componnt man (Fig. 1j). Th componnt man prict rsponss to th suprimpos pair, rgarlss of th prfrr orintation of a cortical sit or of th rlativ rsponss vok by th two componnts. Changing th offst angl btwn gratings from 91 to 21 affct th shap of th PRP for th suprimpos pair, narrowing it an vntually yiling a unimoal istribution (Fig. 2a c). Nvrthlss, PRPs for suprimpos gratings Lat. 638 VOLUME 12 [ NUMBER 5 [ MAY 29 NATURE NEUROSCIENCE

3 a b c Prfrr orintation Suprimpos signal 2 1 Slop = 1 ±.2 1 Summ componnt signal Rgrssion slop closly match thir componnt man PRP for ach angl offst. Componnt mans also prict rsponss to suprimpos gratings across a rang of spatial frquncis (Supplmntary Fig. 1 onlin). To quantify this phnomnon, w compar rsponss to componnt an suprimpos gratings pool across PRPs from all imaging sssions. Rsponss to suprimpos gratings oby a strict linar rlationship to thir componnt sums (Fig. 2). Th slop of th bstfit lin rlating suprimpos rsponss to singl-grating rsponss was 1 (R 2 ¼.83); prfct priction of rsponss to suprimpos gratings by thir componnt mans woul hav prouc a slop of xactly. Rgrssions within iniviual imaging sssions yil similar rsults (Fig. 2). Ths rsults inicat that ivisiv supprssion tightly controls population rsponss to nonsumming suprimpos gratings. This rsult appars to b inconsistnt with rcnt mols suggsting that cross-orintation supprssion rsults from LGN saturation that occurs only unr conitions gnrat by rifting summ sinusoial gratings 26,27. Howvr, it is possibl that th supprssion that w obsrv with stationary nonaitiv gratings was iffrnt from th supprssion obsrv with summ suprimpos gratings. To arss this possibility, w rpat our xprimnt in thr animals using rifting sinusoial gratings. As with stationary nonsumming gratings, th PRPs for summ sinusois wr wll prict by thir componnt man PRPs (Fig. 3a,b). Th ability of th componnt man to accuratly prict rsponss to multipl orintations for both aitiv an nonaitiv stimuli suggsts that cross-orintation supprssion is not limit to a particular stimulus configuration, but rathr rflcts a mor gnraliz mchanism that rgulats ovrall lvls of population activity inuc by stimuli that contain multipl orintations. Figur 3 Rsponss to suprimpos sinusoial gratings at iffrnt contrasts. (a,c) PRPs from on shrw that wr vok by rifting sinusoial gratings at 451 an 1351 prsnt singly an as summ pairs, color co as in Figur 2. Contrasts of both gratings wr 25% in a an 12.5% in c. Data in c wr scal accoring to maximum an minimum valus in a. (b,) Combin PRP ata from thr shrws for a contrast of 25% an 12.5%, rspctivly. (,f) Singl-animal PRPs for issimilar componnt contrasts. Numbr of imag sts 4 2 Figur 2 Th componnt man consistntly prict rsponss to suprimpos gratings. (a c) Singl animal PRPs for stimuli inicat by th color-co labls. PRPs for th man of singl grating imags ar shown in blu. Blu PRPs ar riv from th avrag of singlcomponnt imags an not th avrag of singlcomponnt PRPs. Bcaus imag avraging took plac bfor all of th othr imag-procssing stps, blu PRPs occasionally iffr slightly from th avrag of singl grating PRPs. () PRP ata collaps across 15 imag sts from ight animals, rprsnting a rang of orintation offsts. Each atum plots th activity vok by a pair of suprimpos gratings in on PRP bin with rspct to th sum of activity vok by th corrsponing singl gratings. Linar rgrssion through ths ata proucs a lin with a slop of 1. R 2 is.83. () Distribution of rgrssion slops for iniviual PRP sts. Linar rgrssions wr prform sparatly on ach of th PRP sts contributing to. Th mian slop valu across PRP sts was.48. Mols of cross-orintation supprssion that ar bas on LGN saturation also prict that supprssion shoul b absnt whn both gratings in a suprimpos pair hav low contrasts, blow th point at which thir summ contrasts woul prouc LGN saturation. Against this priction, w foun that th componnt man prict th population rspons to suprimpos gratings as wll at low contrast (Fig. 3c) as it i at high contrast. This was th cas vn though singlgrating rsponss roughly oubl whn contrast was oubl (compar PRP hights for singl gratings in Fig. 3a,c), inicating that th summ contrast of th low-contrast gratings was insufficint to saturat th rsponss of cortical nurons an, by xtnsion, thir a c Contrast = Contrast = Prfrr orintation ( ) b Suprimpos signal Suprimpos signal f Slop = 8 ±.4 Slop = 6 ±.4 1 Summ comp. signal Contrasts = an.25 Contrasts = an Prfrr orintation ( ) Prfrr orintation ( ) 1 NATURE NEUROSCIENCE VOLUME 12 [ NUMBER 5 [ MAY

4 a Spiks pr s c Spiks pr s Singl Pair Man 22.5 b Bas orintation ( ) Figur 4 Singl-unit rsponss to singl an suprimpos gratings. (a ) Tuning functions of on V1 nuron for singl stationary gratings an fix-offst grating pairs. Gray lins rprsnt th singl-grating tuning curv shift by th angular offst inicat unr th icon in ach panl. Rsponss to pairs ar plott with rspct to th orintation of a bas grating, to which a scon grating avanc in orintation by th offst valu for that panl was a. Dash lin is spontanous firing rat. Error bars rprsnt s..m. () Rlationship btwn rsponss to suprimpos gratings an summ componnt rsponss for all grating pairs across 15 nurons. Each atum rprsnts th rspons of on nuron to a singl grating pair (y axis) plott with rspct to th sum of th rsponss to iniviual componnt gratings. Units ar spiks pr scon normaliz iniviually for ach nuron to th most robust rspons across all stimuli. A rgrssion lin through ths points has a slop of.48; prfct priction by componnt mans woul rsult in a slop of. R 2 is 5. (f) Distribution of supprssion inics across all nurons. Th majority of supprssion inx valus fll in a singl clustr nar ; th ovrall man was.4. Th cll illustrat in a ha a supprssion inx of 8. Suprimpos rspons Bas orintation ( ) Slop = Summ comp. rspons LGN inputs. Combin ata from thr animals show ssntially th sam rlationship btwn suprimpos rsponss an componnt rsponss for high-contrast an low-contrast gratings (Fig. 3b,). Although th componnt man accuratly prict rsponss to suprimpos gratings whn both componnts ha th sam contrast, simpl logic ictats that th sam priction coul not hol for componnts with issimilar contrasts. At th xtrm, as th contrast of on grating gos towar zro, th PRP for a suprimpos pair shoul approach that of th rmaining grating. Consistnt with this priction, whn iniviual gratings ha iffrnt contrasts, th PRP for th suprimpos pair part from th componnt man an bgan to rsmbl that of th highr-contrast grating (Fig. 3,f). Singl-unit stuis hav shown that cross-orintation supprssion is an ssntially local phnomnon 3. Consistnt with this, w foun that th componnt man prict population rsponss to suprimpos gratings only at cortical locations that ha rcptiv fils ncompassing both componnts. Activity vok by an X consisting of a singl lin at ach orintation was wll prict by th componnt man in a rgion of cortx xtning roughly 1 mm from th rprsntation of th point of crossing btwn th two lins (Supplmntary Fig. 2 onlin). In th tr shrw, this corrspons to roughly 51 of visual angl 29, which is about th siz of th typical V1 rcptiv fil in layr 2/3 at this ccntricity 3. Rgions farthr away from th crossing point ha rsponss that wr clos to ach lin prsnt alon. In sum, our rsults inicat that ivisiv supprssion is a ubiquitous fatur of V1 procssing that oprats on a broar rang of stimulus configurations than prviously thought. W obsrv ssntially intical rscaling of th population rspons rgarlss of whthr stimuli wr summ rifting sinusois or nonsumming stationary rctanglwav gratings, or whthr thy appar at high or low contrast. Furthrmor, w foun that ivisiv supprssion taks a particular f Numbr of nurons Supprssion inx form in which population rsponss to any two qual-contrast gratings ar wll prict by th man of th componnt rsponss. Valiation of intrinsic signal rsults Although our imaging rsults inicat that nuronal rsponss to suprimpos gratings wr prict by th man of thir componnt rsponss, w wish to nsur that this outcom rflct nuronal activity an not non-nuronal hmoynamic factors or our imaging tchniqus. To valiat our imaging rsults, w ma singl-unit xtracllular rcorings in layr 2/3 using th sam stationary squarwav gratings that w us for imaging. Nuronal rsponss to suprimpos gratings wr wll prict by th man of rsponss to ach componnt prsnt alon (Fig. 4a ), inicating that our intrinsic signal imags faithfully rprsnt th avrag activity of V1 nurons to suprimpos gratings. To assss how rliably th componnt man prict rsponss to pair gratings among iniviual clls, w comput a supprssion inx for ach nuron by subtracting from 1 th ratio of th suprimpos rspons to th sum of componnt rsponss for ach grating pair an thn avraging th rsulting valus across all 28 uniqu stimulus pairs tst with ach cll (s Mthos). Unr this masur, a cll with rsponss to suprimpos gratings that wr th sam as th sum of componnt rsponss woul hav a supprssion inx valu of, a cll showing complt supprssion woul hav a supprssion inx of 1 an a cll with suprimpos rsponss xactly qual to componnt mans woul hav a supprssion inx of. All but 2 of th 15 nurons rcor from fiv tr shrws ha supprssion inx valus falling in a singl clustr btwn.3 an.6 (Fig. 4f), furthr suggsting that our imaging rsults rflct th bhavior of a majority of iniviual layr 2/3 nurons. Tim cours of rsponss to suprimpos gratings Our imaging an xtracllular xprimnts rval comparabl lvls of ivisiv supprssion inuc by suprimpos gratings. Howvr, both of ths masurs ar avrags of nuronal rsponss uring th stimulus prio. It is possibl that nuronal rsponss to suprimpos gratings coul show complx ynamics that la thm to part substantially from th componnt man, but that ar obscur by tmporal avraging. For xampl, if supprssion wr instantiat, at last in part, by fback mchanisms, w woul xpct to s a lay in supprssion rlativ to rspons onst. To bttr unrstan th tmporal ynamics of supprssion, w ma in vivo intracllular rcorings from layr 2/3 nurons. 64 VOLUME 12 [ NUMBER 5 [ MAY 29 NATURE NEUROSCIENCE

5 a mv from rst c mv from rst mv from rst g mv from rst Singl gratings Pair Man W obtain stabl rcorings from 15 nurons in 8 animals for a tim that was sufficint (B1 h) to collct rsponss to at last 15 prsntations of ach of th 36 stimuli in our battry. Stimulus an timing paramtrs wr intical to thos that w us uring xtracllular rcorings. Similar to our imaging an xtracllular rsults, rsponss to pair gratings rsmbl th man of thir componnt rsponss consistntly among our sampl of nurons for all grating combinations (Fig. 5). In th sam nuron, mmbran potntial an firing rats vok by suprimpos gratings wr qually wll prict by componnt mans (Supplmntary Fig. 3 onlin). To mor prcisly assss how wll this priction hl up ovr tim, w rpat th rgrssion analysis that w us for imaging an xtracllular rcors, comparing ach rspons to a suprimpos b f h Bas orintation ( ) Figur 6 Rlationship of intracllularly rcor rsponss to suprimpos an componnt gratings across tim. (a ) Main axs show combin rsponss of 15 nurons to suprimpos gratings an summ rsponss to componnts, avrag ovr th tim following rspons onst inicat in ach panl. Rgrssion slops wr.48,.49,.46 an.42 for a, rspctivly, an R 2 valus wr.72,.69, 6 an.46, rspctivly. Insts show istribution of supprssion inx valus across nurons for ach tim winow; scal bar at 1 rprsnts 5 nurons. Supprssion inx valus wr calculat as scrib for xtracllular rcorings, xcpt that w us th avrag mmbran potntial in ach tim winow. (,f) Tim-xpan viw of rsponss of two nurons shown in Figur 5a,b, using th sam color co. Figur 5 Intracllularly rcor rsponss to singl an suprimpos gratings. (a ) Rsponss of four nurons to slct grating pairs. Angl btwn gratings was in a, 451 in b, in c an 91 in. Dpolarizations following stimulus offst ar OFF rsponss. Th sha rgions rprsnt stimulus uration ( h). Population avrag tuning functions for singl an suprimpos gratings (n ¼ 15 nurons). Colors follow sam th convntion as in a. Avrag mmbran voltags uring 4 ms poststimulus wr avrag across all clls aftr aligning ach nuron s prfrr orintation to 91. Error bars ar s..m. pair to th sum of rsponss vok by its rspctiv componnts (Fig. 6a ). Rgrssion slops for avrag mmbran potntial uring th first 2, 2, 1 an 5 ms following rspons onst wr.48,.49,.46 an.42, rspctivly; as bfor, prfct priction of rsponss to grating pairs by thir componnt mans woul prouc a slop of. Ths ata inicat that ivisiv supprssion prouc by suprimpos gratings was ssntially voi of ynamics an was prsnt in clos to its matur form from th arlist masurabl rspons (Fig. 6,f). DISCUSSION W foun that pattrns of V1 population activity vok by multipl simultanous gratings iffring in orintation wr prict with high prcision by a simpl form of ivisiv supprssion. Spcifically, activity pattrns vok by two suprimpos gratings of intical contrast wr wll prict by th man of pattrns vok by ach grating prsnt alon. This priction was accurat for cortical nurons of all prfrr orintations rlativ to th stimuli an for a wi rang of orintation pairs. Morovr, th componnt man was qually ffctiv in pricting multipl grating rsponss for summ an nonsumm grating pairs an at both high an low contrasts. Singl-unit rcorings confirm that ths population masurs rflct th avrag activity of iniviual V1 nurons, that supprssion is vint at th arlist stags a Suprimpos rspons (mv from rst) c Suprimpos rspons (mv from rst) mv from rst Summ componnt rsponss (mv) Tim from stimulus onst (ms) ms 2 ms b 2 1 ms 5 ms f 1 NATURE NEUROSCIENCE VOLUME 12 [ NUMBER 5 [ MAY

6 of cortical activation an that it continus to account for th population rspons throughout th uration of th stimulus prio. Ths rsults inicat that ivisiv supprssion an th rspons rscaling it proucs ar highly consistnt faturs of th V1 population rspons to multipl orintations unr a broa rang of stimulus typs. Th fact that suprimposition of gratings of quivalnt contrast yils a population rspons that is th avrag of th rsponss to th componnt gratings has not, to th bst of our knowlg, bn not in prvious stuis of cross-orintation supprssion in V1 (rfs. 1 3,7,24 27). In rtrospct, this is unrstanabl givn that th focus of most prvious stuis has bn on how a non-optimal grating supprsss th rspons of nurons to thir prfrr grating stimulus, rathr than on how populations of nurons rprsnt multipl orintations. In, prvious stuis hav not typically rport th rspons vok by th cross-orint grating by itslf, making it impossibl to assss whthr rsponss to suprimpos gratings coul hav bn prict by th mans of thir componnt rsponss 1,3,24,25. In aition, many stuis hav plac an mphasis on th ffct of varying th contrast of th cross-orint mask grating whil kping th contrast of th prfrr grating fix, an hav shown that th strngth of supprssion varis with mask contrast. Ths rsults ar not inconsistnt with our own, in which rsponss to suprimpos gratings ar prict by thir componnt mans only whn componnts hav qual contrast. W not, howvr, that in thos situations in which rsponss to both componnt gratings hav bn rport, rsponss of V1 nurons to suprimpos gratings of quivalnt contrast oftn appar to fall clos to th componnt avrag 7,26,27. Morovr, singl-unit stuis in macaqu xtrastriat aras hav shown that th man of th componnt rsponss gnrally pricts activity vok by multipl stimuli, such as color bars in V2 an V4 (rfs ), irctions of motion in mil tmporal an mial suprior tmporal cortx 34,35, an shaps in infrotmporal cortx 36. Howvr, as our own singl-unit ata inicat, vn with componnt gratings that ar intical xcpt for thir orintation, thr is cll-to-cll variability in th strngth of supprssion. On avrag, rsponss to suprimpos gratings ar prict by th componnt man; whthr functionally istinct subclasss of nurons show charactristic an systmatic parturs from this priction rmains an opn qustion. What maks our rsults particularly intriguing is that thy o not fit wll with th traitional viw of cross-orintation supprssion as an outcom of a contrast gain control mchanism that prvnts saturation from istorting th istribut rprsntation of stimulus faturs 2,4 7. If saturation avoianc wr th principal purpos of supprssion, thn w shoul hav foun that th amount of supprssion vari with th contrast of th componnt gratings. For xampl, th suprimposition of two low-contrast gratings rquirs littl or no supprssion to prvnt th pak of th population rspons from raching saturation. In spit of this, w foun that th componnt man prict rsponss to qual-contrast suprimpos gratings at both high an low contrasts (but s rf. 26). This consistncy suggsts that cross-orintation supprssion is ictat by factors othr than th potntial for rspons saturation. W propos insta that cross-orintation supprssion is th singl-cll manifstation of a population coing schm that maintains inpnnt cos for stimulus orintation(s) an strngth (for xampl, contrast); th orintations prsnt in a local (rcptiv fil siz) rgion of th stimulus ar nco by th rlativ activity of units tun to iffrnt orintations (that is, th shap of th population rspons), whras stimulus strngth is sparatly nco by th summ activity of th ntir local population. Spcifically, cross-orintation supprssion rsults from th ristribution of cortical activity ncssary to rprsnt th mor complx orintation spctrum of th suprimpos stimulus, without changing th total amount of cortical activity vot to its rprsntation (Supplmntary Fig. 4 onlin). Whn two gratings of th sam contrast ar suprimpos, th lvl of population activity to which thy ar ntitl by thir contrast is istribut qually btwn thm. On outcom of this ristribution is that th rsulting profil of population activity is th man of th profils vok by ach whn prsnt alon (whn ach grating is affor th full masur of cortical activity commnsurat with its contrast). A rlat outcom is that th rsponss of iniviual nurons prfrring on of th gratings ar smallr than whn that grating is shown by itslf to compnsat for incras activity among nurons prfrring th scon grating, hnc cross-orintation supprssion. Furthrmor, what w obsrv as th failur of th prictiv powr of th componnt man whn two gratings iffr in contrast simply rflcts th fact that th ristribution of cortical activity is wight by th rlativ contrast of ach grating. This wighting is ncssary to nsur that th istribution of activity across nurons with iffrnt prfrr orintations accuratly ncos th rlativ contrasts of th gratings. On notabl fatur of our rsults is th fact that th summ population rspons to a pair of suprimpos gratings was intical to th summ population rspons vok by on of th componnts prsnt alon. In othr wors, suprimposing an aitional grating of th sam contrast i not chang th total amount of cortical activity rprsnting th stimulus. Although this at first sms at os with th fact that linar summation of two gratings will prouc a nw stimulus with twic th Michlson contrast of ach componnt, it maks sns whn on nots that that this incras contrast is not rflct in th stimulus orintation spctrum. Although th spctrum of th nw stimulus is mor laborat, it contains no mor contrast at any particular orintation than th spctra of ithr of its componnt gratings. Our rsults mphasiz that th istribut coing of suprimpos gratings is funamntally a zro-sum opration. Aing lmnts of th sam contrast to a stimulus rucs th amount of nural activity that is availabl to rprsnt ach of th componnts. W prict that th aition of mor gratings at th sam contrast shoul only furthr broan th istribution of population activity without incrasing th total amount of population activity rprsnting th stimulus. Consistnt with this, w not that th componnt man has bn obsrv to prict singl-nuron rsponss to thr stimuli in infrotmporal cortx 36. By th sam tokn, changing th contrast of th stimulus without changing its orintation composition will chang th total amount of cortical activity without changing th rlativ istribution of th activity pattrn. Although th ia that th shap of th population rspons rprsnts th stimulus orintation spctrum is fairly convntional, th ia that th total population activity coul provi an inpnnt rprsntation of stimulus intnsity has not figur prominntly in prvious iscussions of population coing. Howvr, a rol for summ population activity as an inpnnt masur of ovrall stimulus strngth has bn fatur in at last on mol of population-bas probabilistic stimulus coing 37. Consistnt with this rol, w foun that plotting PRP ara vrsus contrast of a singl grating yil a contrast rspons function that was vry similar to thos of iniviual nurons (Supplmntary Fig. 5 onlin, also s rf. 38). Morovr, th consistncy of th componnt man in pricting rsponss to suprimpos gratings across contrasts inicats that a similar contrast rspons function xists for any pair 642 VOLUME 12 [ NUMBER 5 [ MAY 29 NATURE NEUROSCIENCE

7 of suprimpos gratings, allowing summ population activity to signal th contrasts of mor complx stimuli as wll. Th applicability of our rsults to combinations of stimuli iffring along imnsions othr than orintation is an opn qustion. It is important to mphasiz that w o not propos that th componnt man shoul prict rsponss to any combination of qual-strngth stimuli. Rathr, it shoul only apply whn th combin stimulus rquirs that V1 nco multipl simultanous valus along th imnsion in qustion. For xampl, whn two gratings iffring in orintation ar suprimpos, thir combin rspons rsmbls th componnt man bcaus th combin stimulus contains information about both orintations, vinc by th ual paks in th stimulus two-imnsional frquncy spctrum. On th othr han, th rspons to a stimulus riv from simpl summation of two gratings that ar intical in orintation will not b prict by th componnt man: th compoun stimulus is simply a singl grating at a highr contrast. As such, it has only a singl frquncy pak an is sn by V1 as a singl fatur. This cavat os lav opn th possibility that th componnt man may prict rsponss to othr compoun stimuli that contain information about thir sourc componnts, such as th sum of two gratings iffring in spatial frquncy. In any such cas, howvr, th xtnt to which th compoun stimulus will vok th componnt man will b critically pnnt on th componnts having qual strngths. Thus, although w might prict th sam supprssiv mchanisms to sculpt population activity for a stimulus that combins multipl spatial frquncis, th ovrall ban-pass snsitivity of V1 in th frquncy omain limits th rang of frquncy combinations unr which w woul xpct it to prouc th man spcifically. Th mchanism unrlying cross-orintation supprssion has long bn a subjct of bat. Unr th normalization mol 5,7,crossorintation supprssion was propos to b miat by inhibitory fback that is rivn by th pool activity of all orintation-tun units. Subsqunt work l to th proposal that supprssion was an outcom of activity-pnnt prssion of thalamocortical synapss, rathr than cortical inhibition 39,4. Howvr, this xplanation has bn challng by th obsrvation that synaptic prssion at th gniculocortical synaps is insufficint to xplain th amount of supprssion that is inuc by a cross-orint grating 41. Mor rcnt work has monstrat that cross-orintation supprssion of layr 4 simpl clls is accompani by a cras in both xcitatory an inhibitory currnts, ffctivly ruling out cortical inhibition as a sourc of supprssion 26.Tworcntstuis 26,27 hav propos that crossorintation supprssion ariss from nonlinaritis in th rsponss of LGN nurons, which ar furthr amplifi by th nonlinaritis of spik thrshol at th gniculo-cortical synaps. Our rsults ar ifficult to rconcil with all of th propos mchanisms of ivisiv supprssion. Consistnt with prvious rports of fast cross-orintation supprssion 25, th prsnc of supprssion from th vry onst of subthrshol rsponss sms to prclu th involvmnt of inhibitory fback. W obsrv supprssion with stationary gratings, whras th synaptic prssion mol pricts supprssion xclusivly for rifting gratings 4. Similarly, mols that attribut much of th supprssion to LGN saturation prict littl or no supprssion for gratings that o not sum linarly: that is, thos that o not prouc rgions of saturating contrast 26,27. Against this, w obsrv th sam strngth of supprssion for both nonsumming rctangl-wav gratings an summ sinusois. In aition, ths mols prict that supprssion shoul iminish at low contrast. Insta, w foun that th strngth of supprssion was ssntially intical for sinusoial gratings at 25% an 12.5% contrast, vn though th iffrnc in activity vok by singl gratings at ach contrast show that cortical nurons, an prsumably thir thalamic inputs, wr not nar saturation in th low-contrast conitions. Th only prvious stuy that w know of to us intracllular rcorings to xamin V1 rsponss to multipl gratings foun far gratr cross-orintation supprssion (roughly twic as much) in spik rat than in mmbran potntial, suggsting that a nonlinar rlationship btwn mmbran potntial an spik rat is important in amplifying supprssiv ffcts 26. In contrast, w foun that th componnt man prict mmbran potntials about as wll as it prict spik rats. Svral factors may xplain this iffrnc. Prviously, intracllular rsponss wr charactriz principally by masuring th magnitu of th moulation of spik rat an mmbran potntial at th funamntal frquncy of a rifting stimulus aftr iscaring ata from th first stimulus cycl 26. In our xprimnts, w us stationary stimuli an charactriz mmbran rsponss as parturs from rsting potntial avrag in iscrt tim winows following rspons onst, an spiking rsponss as avrag firing rat uring th full 5-ms stimulus poch. Anothr iffrntiating factor was th way in which w rmov action potntials from mmbran voltag rcors. Insta of using a 5-ms man filtr 26, w truncat polarizations past a manual stimat of spik thrshol. Both mthos probably istort th rlationship btwn mmbran potntial an spik rat to a crtain xtnt. Our us of a stationary stimulus, howvr, allow us to look at xtrmly arly tim points in mmbran rsponss, bfor spik thrshol was rach. Notably, w obsrv that vn at ths arlist tim points, mmbran potntials for suprimpos gratings wr wll prict by th man of th componnt rsponss. Although th iscrpancy btwn prvious rsults an our own may also b attributabl to laminar iffrncs (that is, cortical layr 4 vrsus layr 2/3) or spcis iffrncs, w conclu that cross-orintation supprssion in layr 2/3 can b xplain without th n to invok th nonlinaritis of spik thrshol. On fatur that is common to many propos mols of crossorintation supprssion is th assumption that it stms, ithr irctly or inirctly, from th sam mchanisms that miat contrast gain control 4,5,7,26,27. Our rsults challng this outlook; th ability of th componnt man to prict rsponss at iffrnt contrasts suggsts that cross-orintation supprssion shoul b viw as a sparat procss. Morovr, viw from th prspctiv of a population co that jointly rprsnts th orintation spctrum an th ffctivnss of a broa rang of stimuli, th trm supprssion itslf may b a misnomr. Th orintation spctrum of th compoun grating stimulus is funamntally iffrnt from that of th singl grating stimulus an, in this rspct, th mchanism rsponsibl for cross-orintation supprssion may b similar to th ruction in rspons that occurs in a singl nuron whn an optimal grating stimulus is rplac with a lss optimal grating, a ruction in rspons that fw woul rgar as supprssion. Of cours, rcasting th phnomnon in this way os not rval th circuitry that proucs it. Furthr stuis that prob th bhavior of intifi subpopulations of cortical nurons an thir intractions will b ncssary to gain insights into this funamntal bhavior of cortical circuits. METHODS Surgry an animal prparation. Exprimnts wr prform on juvnil tr shrws (Tupaia blangri) of both sxs. All procurs conform to US National Instituts of Halth guilins an wr approv by th Duk Univrsity Animal Car an Us Committ. Animal prparation has bn scrib in tail prviously 42. Brifly, ansthsia was inuc with a combination of ktamin an xylazin an was maintain with 2% halothan NATURE NEUROSCIENCE VOLUME 12 [ NUMBER 5 [ MAY

8 (vol/vol) in a 1:1 mixtur of N 2 OanO 2. Aftr placmnt in a strotactic vic, shrws wr paralyz an rspirat to maintain n-tial CO 2 btwn 3 an 4%. During imaging an rcoring, halothan was ruc to B1% an ajust as n to maintain a stabl hart rat. Tmpratur was maintain at 38 1C with a thrmal blankt. For intrinsic signal imaging xprimnts, th scalp was incis an th bon ovr V1 was thinn with a scalpl bla. A ntal wax chambr was mount to th skull, fill with agar an topp with a glass covrslip. Optical signals wr imag with an Imagr 31 (Optical Imaging) unr 69-nm illumination. For xtra- an intracllular lctro rcorings, a small hol was ma in th skull an th unrlying ura was rflct. Extracllular rcorings wr ma with glass-coat tungstn lctros (FHC). Signals wr ban-pass filtr btwn 3 an 3, Hz, igitiz at 1 khz an rcor for offlin analysis. Intracllular rcorings wr ma with sharp lctros (9 13 MO) fill with 2 M potassium actat. Potntials wr rcor without filtring for offlin analysis. Visual stimuli. In imaging xprimnts, th principal xprimntal stimulus consist of stationary rctangl-wav gratings compos of.251 wi lins, sparat by 31, that wr prsnt against a gray backgroun (Fig. 1a c,f h); this spacing was sufficintly clos to nsur uniform stimulation of th cortx (Supplmntary Fig. 6 onlin). Th.251 lins altrnat in unison btwn light an ark (rlativ to th fix-luminanc backgroun) at 2 Hz to maintain cortical activity uring imag acquisition. During both th light an ark phass, th Michlson contrast was. Whn suprimpos, gratings appar to b ovrlai, as if on transparnt sht with thin lins was plac on anothr transparnt sht with lins of a iffrnt orintation, an th two wr lai togthr on a gray backgroun. Th luminanc of pixls whr th thin lins cross was th sam as for a singl grating. A singl xprimntal run gnrally contain four stimulus conitions: two singl gratings of iffring orintations, a suprimpos conition with th sam two orintations ovrlai, an a blank. Stimuli appar for 4.5 s, with an 8-s intrstimulus intrval to allow intrinsic signals to cay to baslin (Supplmntary Fig. 7 onlin). Stimulus conitions wr ranomly intrlav an rpat 2 1 tims. In som xprimnts, w us rifting achromatic sinusoial gratings. Gratings wr.25 cycls pr gr an rift at 4 Hz. Whn prsnt as suprimpos pairs, sinusoial gratings combin linarly (that is, Michlson contrast for suprimpos gratings was twic that of ach iniviual componnt). In sparat runs, w also acquir imags uring prsntation of rifting squar-wav gratings (.4 cycls pr gr, 4 Hz) at four orintations (1, 451, 91 an 1351). W subsquntly us ths ata to gnrat orintation-prfrnc maps accoring to a vctor-sum mtho. Stimuli for both xtra- an intracllular rcorings wr intical to th stationary gratings that w us uring optical imaging. Stimuli wr prsnt for 5 ms with a 2-s intrstimulus intrval. Only th light phas of ach stimulus was us (that is, light bars on th gray backgroun). Th stanar stimulus st consist of singl gratings at ight iffrnt orintations an 28 conitions consisting of vry combination of th ight bas orintations. Stimuli wr ranomly intrlav an rsponss wr avrag ovr 15 4 rptitions. Data acquisition an analysis. W avrag imags of th cortx in 5-ms frams bginning 5 ms bfor stimulus onst. Aftr first-fram subtraction, imags wr convrt to prcnt-rflctanc-chang maps (DR/R) by iviing thm by th sam first fram. Each DR/R map was thn high-pass filtr by subtracting a 1-mm man-filtr vrsion of th sam map, an thn pass through a.5-mm man filtr to rmov high frquncis. To rlat population rsponss vok by suprimpos gratings to activity vok by singl gratings, w riv PRPs for ach stimulus conition 14.W us orintation-prfrnc maps to assign a prfrr orintation tag to ach pixl, ranging from 1 to 1791 in.71 stps. Nxt, for ach imag acquir uring prsntation of an xprimntal stimulus (for xampl, a pair of suprimpos gratings), w comput th avrag signal intnsity among all pixls with th sam orintation tag. W rbinn ths avrags at 11 incrmnts an plott thm as a function of orintation tag to prouc PRPs. Bcaus th high-pass filtring of th input imags amount to a man-valu subtraction, th rsulting PRPs no longr rprsnt DR/R an frquntly contain ngativ numbrs. To avoi confusion, w assmbl PRPs into familis compos of on PRP for a suprimpos pair an on for ach of its componnt gratings, an fin th most ngativ valu among all points in ach family as zro. W thn st th maximum valu in th family to 1 an scal all othr valus accoringly. It is important to not that nithr of ths last two stps in any way changs th rlativ valus of PRPs in a stimulus family. During xtracllular rcorings, w prform prliminary onlin spik sorting using Spik2 softwar (CED). Onc w isolat th rspons of a singl nuron, w mploy automat procurs to trmin rcptiv fil position an prfrr orintation. Only clls from which w rcor at last 15 rptitions of ach of our xprimntal stimuli wr inclu in furthr analysis. W ajust th position of gratings for ach nuron to nsur that on crossing-point of ach suprimpos pairs was locat as clos as possibl to th cntr of its rcptiv fil (this appli to intracllular rcorings as wll). Mor prcis offlin spik sorting frquntly prmitt us to xtract th rspons of mor than on nuron from ach stimulus run. During intracllular rcorings, w only analyz ata from clls with rsting potntials blow 6 mv an action potntial paks xcing mv. To analyz th volution of rsponss ovr tim, w comput rspons latncy for ach suprimpos grating pair by intifying th arlist.1-ms bin in th rspons to th mor-prfrr componnt that ha a voltag abov rst with a probability of lss than.1 on th basis of th istribution of voltags rcor uring th first 2 ms following stimulus onst. This critrion corrspon to a mian polarization of 1.8 mv from rst an intifi rspons onsts with a mian latncy of 5.7 ms, both avrag across all grating pairs from all nurons. This rlativly long mian latncy rflcts th ffct of grating pairs that vok wak an slowly-rising rsponss. Not: Supplmntary information is availabl on th Natur Nuroscinc wbsit. ACKNOWLEDGMENTS Th authors wish to thank th mmbrs of th Fitzpatrick laboratory for hlpful iscussions an assistanc with ata collction an analysis. This work was support by US National Instituts of Halth grants EY6821 to D.F. an EY16319 to S.P.M. AUTHOR CONTRIBUTIONS S.P.M. sign th stuy with D.F. an conuct all of th xprimnts. T.R.T. wrot th stimulus prsntation an ata analysis softwar, provi xprtis in intracllular rcoring tchniqus an assist with ata intrprtation. S.P.M. an D.F. wrot th manuscript. Publish onlin at Rprints an prmissions information is availabl onlin at rprintsanprmissions/ 1. Morron, M.C., Burr, D.C. & Maffi, L. 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10 rratum Erratum: A prcis form of ivisiv supprssion supports population coing in th primary visual cortx San P MacEvoy, Thomas R Tuckr & Davi Fitzpatrick Nat. Nurosci. 12, (29); publish onlin 26 April 29; corrct aftr print 5 May 29 In th vrsion of this articl initially publish, th gray curv in Figur 1j was shift to th lft. Th corrct figur is shown blow. Th rror has bn corrct in th HTML an PDF vrsions of th articl. j 9 18 Prfrr orintation ( ) natur nuroscinc