Efficient sensory cortical coding optimizes pursuit eye movements

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1 ARTICE Reeived Mr 26 Aepted 29 Jul 26 Pulished 9 Sep 26 Effiient sensory ortil oding optimizes pursuit eye movements Bing iu, Mtthew V. Mellio & eslie C. Osorne,2 DOI:.38/nomms2759 OPEN In the nturl world, the sttistis of sensory stimuli flutute ross wide rnge. In theory, the rin ould mximize informtion reovery if sensory neurons dptively resle their sensitivity to the urrent rnge of inputs. Suh dptive oding hs een oserved in vriety of systems, ut the premise tht dpttion optimizes ehviour hs not een tested. ere we show tht dpttion in ortil sensory neurons mximizes informtion out visul motion in pursuit eye movements guided y tht ortil tivity. We find tht gin dpttion drives rpid (o ms) reovery of informtion fter shifts in motion vrine, euse the neurons nd ehviour resle their sensitivity to motion flututions. Both neurons nd pursuit rpidly dopt response gin tht mximizes motion informtion nd minimizes trking errors. Thus, effiient sensory oding is not simply n idel stndrd ut desription of rel sensory omputtion tht mnifests in improved ehviourl performne. Deprtment of Neuroiology, The University of Chigo, 947 Est 58th Street, P45 MC928, Chigo, Illinois 6637, USA. 2 Deprtment of Orgnisml Biology nd Antomy, The University of Chigo, Chigo, Illinois 6637, USA. Correspondene nd requests for mterils should e ddressed to.c.o. (emil: osorne@uhigo.edu). NATURE COMMUNICATIONS 7:2759 DOI:.38/nomms2759

2 ARTICE NATURE COMMUNICATIONS DOI:.38/nomms2759 In rpidly hnging world, neurl systems n optimize their representtion of inoming stimuli y djusting their sensitivity s stimulus onditions hnge 4. As individul sensory neurons hve limited response ndwidth, how firing rtes re lloted ross the rnge of stimulus vlues ffets how muh informtion n e trnsmitted nd, ultimtely, how informtive ommnds for ehviour n e 2,4 6. When signl vries little over time, neuron n mximize its sensitivity y inresing its response gin, the hnge in firing rte per unit hnge in stimulus. When stimulus flututions grow lrge, lowering the gin voids informtion loss from sturtion. In theory, dpttion to vrine, lso known s temporl ontrst, is n optiml oding strtegy, euse it llows individul sensory neurons to pply their full response ndwidth to enode inoming signls 2,3. If neurons ould mintin n optiml gin ross hnges in input sttistis, the rin ould theoretilly reover more sensory informtion with whih to guide ehviour. owever, lthough the phenomenon of neurl dpttion to input vrine hs een demonstrted 7 8, its impt on informtion proessing hs only een reported in the fly visul system 3,5,6 nd the onsequene for ehviour is unexplored 9. To estlish tht gin dpttion t the neuronl level is importnt to the ury of sensory-motor ehviour, we hve nlysed the responses of sensory neurons nd movement ehviour in prllel. ere we show tht rpid gin dpttion to stimulus vrine in visul ortil neurons optimizes informtion nd movement ury in primte oulomotor system. In smooth pursuit ehviour, imge motion on the retin is trnslted into ommnd to rotte the eye long with the trget, to stilize the retinl imge 2,2. Pursuit errors lrgely tke the form of misestimtes of trget motion, whih persist for B7 ms until visul feedk ues n ltertion of the eye movement 2,22. These errors result in imge motion lur tht degrdes visul uity, impting pereption nd other visully driven ehviours Under nturl onditions where trget motion is dynmi, the qulity of feed-forwrd visul estimtes of trget motion is ritil to trking uity. The visul inputs for pursuit rise in ortil re MT (middle temporl re) where mny neurons respond seletively to visul motion nd responses re tuned for motion diretion nd speed 27,28. In theory, MT neurons ould mximize the informtion they trnsmit if they djust their response gin suh tht their dynmi rnge spns s muh of the rnge of urrent motion vlues s possile. Informtion svings t the level of individul neurons might in turn drive more urte popultion-level motion estimtes. For pursuit to enefit from n informtion svings t the ortil level, however, the dptive gin hnges must improve popultion motion estimtes nd must hppen on the B7 ms timesle of the eyes response to hnges in trget diretion. To determine whether pursuit ehviour displys the hllmrks of effiient oding, we mesured the gin of the eye s response to flututions in trget diretion for different levels of overll diretion vrine. We performed prllel set of experiments reording single units in MT to determine whether the ehviourl effets hd ortil sensory origin. We find tht oth MT neurons, nd pursuit ehviour s whole, rpidly dopt response gin tht mximizes informtion out motion diretion nd minimizes trking errors in pursuit. These dt provide diret evidene of funtionl enefit for effiient sensory oding. Results Experimentl design. Our pproh to testing for ehviourlly relevnt effiient sensory oding is inspired y nturl pursuit ehviour, whih is often lled on to trk trgets with timevrying motion profiles, suh s the flight pth of n inset evding fly swtter. We fous on diretion flututions, reting motion stimuli tht hve onstnt motion speed nd timeverged diretion, with n dded stohsti perturtion in diretion. We performed two types of experiments, illustrted in Fig. (see Methods). In the pursuit tsk, monkeys trked trgets tht trnslted ross the sreen (Fig. ). In the fixtion tsk, the sme motion stimulus ws presented within sttionry perture entred over the reeptive field of n MT unit, while we mde extrellulr reordings (Fig. ). In oth ses, stimulus diretions were rndomly hosen from uniform distriution every two frmes (2 ms) nd new sequene ws generted for eh tril (Fig.,d). We hose to seprte MT reording from the pursuit experiments, to etter ontrol visul input for repetility nd to minimize omplitions from stimulus motion within the reeptive field rising from eye movement. The ulk of our physiology dt ws olleted suh tht the entrl diretion of motion fell on the flnk of eh neuron s diretion tuning urve nd the diretion rnge remined within the neuron s response rnge (Fig. 2, inset). This onfigurtion minimized hnges in the time-verged firing rte ross step hnges in diretion vrine, llowing us to isolte dptive hnges to diretion vrine. Our emphsis on dpttion in response gin (sensitivity to flututions) rther thn mgnitude (men firing rte) distinguishes this work from fter-effet studies using exposure to onstnt stimuli, to mnipulte firing rtes nd tuning urves For oth the MT nd pursuit experiments, trils were typilly divided into two or more segments ( 2, ms) for whih the time-verged diretion remined onstnt, ut the diretion vrine stepped etween lower nd higher vlues, whih we term T (low to high) or T (high to low), to indite n upwrd or downwrd vrine step, respetively (Fig.,d). Although MT neurons showed trnsient response to motion onset, vrine steps rrely (/87) eliited seond trnsient response. Rther, the time-verged firing rte remined firly onstnt (Fig. ). Other studies employing stimuli tht lterntely exited nd inhiited spiking hve reported rte trnsients fter vrine steps, for exmple, in the fly, slmnder retin nd ortil slies 5 8, 5, In ontrst, our stimuli were onfigured to provide time-vrying firing rte without suppressing spiking ltogether (see Fig. 2). Despite the lk of firing rte or eye veloity trnsient, we find tht oth MT neurons nd pursuit shift their sensitivity to motion diretion flututions fter vrine steps. Response gin resles with stimulus vrine. ow n MT neuron or n eye movement responds to motion flutution depends on ontext. The simplest illustrtion of the vrine dependene of the neurl (or ehviourl) response is to plot the firing rte (or eye diretion) versus the stimulus diretion omputed in short 2 ms time windows. The stedy-stte input output reltionships for low- nd high-vrine diretion stimulus re shown in Fig. 2. We hve time shifted the stimulus nd response vlues y the verge response lteny throughout. For the MT neuron, Fig. 2 represents portion of the diretion tuning urve. Symol olour indites low (lk) or high (red) vrine onditions. The slope of the liner fit represents the verge hnge in response per unit hnge in stimulus nd hene the gin, g ¼ Dr/Ds (see Methods). For oth MT neurons nd pursuit, gin is high when diretion vrine is low nd low when vrine is high (Fig. 2 d). We found this to e true ross our ortil nd ehviourl smples. Resling response gin with stimulus vrine n mximize informtion trnsmission 5. If ortil nd ehviour response 2 NATURE COMMUNICATIONS 7:2759 DOI:.38/nomms2759

3 NATURE COMMUNICATIONS DOI:.38/nomms2759 ARTICE Firing rte (spikes s ) 5 MT neuron reording T, 2, 3, d Veloity (degree s ) 3 Eye trking hvel T vvel 5,,5 Stimulus (degree) 2 Dots on SD (degree), 2, 3, Stimulus (degree) 6 SD (degree) 5,,5 Figure Experimentl design nd exmple dt. () A fixtion tsk kept motion stimuli entred on the reeptive field. () ower pnel: stimuli hd onstnt drift speed nd men diretion hosen to fll on flnk of neuron s diretion tuning urve. We dded stohsti diretion perturtion, updted every 2 ms (lk) tht shifted from T (or T, not shown) vrine during the tril (red). Upper pnel: PST of n isolted MT neuron. () Pursuit tsk design. Trgets trnslted ross the sreen with identil diretion sttistis s for ut in rndomly seleted men diretion to minimize ntiiption. (d) Upper pnel: orizontl nd vertil omponents of eye veloity during single tril with T vrine shift. ower pnel: trget diretion (lk) or diretion vrine (red) over time. gin ompenstes perfetly for hnges in stimulus vrine, then if we express the stimulus in units of its s.d., the gin vlues we ompute ross vrine levels should oinide. We find this to e the se for oth MT neurons nd pursuit ehviour. Re-plotting the exmple dt in Fig. 2 in units of the diretion s.d. for oth low () nd high () vrine levels, we find lose greement etween the fitted gin vlues (Fig. 3,). ooking ross the ortil nd ehviourl smples, we lso find tht the s.d.-normlized gin vlues for nd high-vrine onditions re very similr, plotting ner the unity line in Fig. 3,d (ompre with Fig. 2,d). For the MT smple (Fig. 3), the s.d.-normlized vrine gin (2.2±2.9, men±s.d.) ws not signifintly different from the s.d.-normlized vrine gin (.5±.3; two-sided Wiloxon rnk-sum test, P ¼.35, n ¼ 92). The nine neurons in the smple with the highest firing rtes nd, therefore, the lrgest gin normliztion ftors pper to devite from the liner reltionship t the lowest normlized gin vlues (Fig. 3). Despite the pprent urvture in neurl gin sling, seond-order polynomil fit ounts for only 3% more of the vrine thn liner fit (R 2 ¼.86 liner fit; R 2 ¼.89 seond-degree polynomil fit). For pursuit, the normlized gins t high versus low vrine levels were quite similr (Fig. 3d): low gin:.53±.6; high gin:.52±., not signifintly different, two-sided Wiloxon rnk-sum test, P ¼.6, n ¼ 74 from 3 monkeys). Thus, the response gin shifts to ompenste for hnges in stimulus s.d. nerly perfetly on verge. To quntify the extent of gin dpttion in MT neurons nd pursuit ehviour, we reted n index, Dg/Sg, to pture the reltive gin differenes etween low versus high vrine onditions, tht is, Dg, in units of the sum, Sg ¼ (g þ g ). The gin indies were distriuted B.72±.3 (n ¼ 92) for MT neurons nd.4±.8 (n ¼ 74) for pursuit, inditing tht response gin is strongly vrine dependent. owever, the s.d.-sled gin index for MT neurons nd pursuit hd n verge vlue not sttistilly different from zero (neurons Fig. 3e, solid red line, one-smple t-test, two-tiled, P ¼.67; pursuit Fig. 3f, solid red line, one-smple t-test, two-tiled, P ¼.68), inditing perfet gin resling on verge ross our dt smples. Neither the neurons nor the ehviour showed lrge differene in response rnges for the stimulus vrine levels we tested. Rther, the gin shift ppers to rise from rempping of the response ndwidth onto the urrent rnge of diretion inputs, potentilly reting miguity in single-neuron diretion oding rising from the lk of fixed reltionship etween input nd response, ut mximizing sensitivity to diretion hnges 6. To ensure tht the invrine in the response rnge did not rise from sturtion, we performed ontrol. The high () vrine stimulus hs more high-frequeny power thn the low () vrine ondition. If the system is insensitive to higher frequenies, then sturtion might result in n pprent gin hnge without tul dpttion in the system 39,4. We used the response ndwidth of pursuit, essentilly low-pss filter with orner frequeny of 2 z, to filter out higher-frequeny omponents of the stimulus nd then relulted the gin vlues for nd onditions. If sturtion to high-frequeny omponents were msquerding s gin shift, the filtered nd stimuli would yield similr gin vlues. Rther, we found tht the gin vlues hnged very little with the filtered stimuli. The gin index vlues were positive for oth the rodnd (lk solid lines: neurons Fig. 3e, men±s.d..72±.3, n ¼ 92; pursuit Fig. 3f,.4±.8, n ¼ 74) nd low-pss filtered stimuli (lk dshed lines: neurons Fig. 3e,.56±.34, n ¼ 88; pursuit Fig. 3f,.44±.4, n ¼ 74). Normlizing y the stimulus, s.d. shifted the gin index distriution to ner zero men, inditing tht the response gin sled with stimulus vrine, similrly for oth the rodnd (grey solid lines: neurons Fig. 3e,.±.26, n ¼ 92; pursuit Fig. 3f, ±.7, n ¼ 74) nd low-pss stimuli (grey dshed lines: neurons Fig. 3e,.7±.33, n ¼ 88; pursuit Fig. 3f,.7±.5, n ¼ 74). NATURE COMMUNICATIONS 7:2759 DOI:.38/nomms

4 ARTICE NATURE COMMUNICATIONS DOI:.38/nomms2759 MT neuron rte (spikes s ) Pursuit eye diretion (degree) (s.d. 2 ) (s.d. 35 ) (s.d. 5 ) 2 (s.d. 5 ) Adpttion mximizes informtion in MT nd pursuit. Adpttion is enefiil for pereption nd movement if it serves to mximize informtion out the inoming signl. To quntify the impt of gin dpttion on sensory oding, we omputed the mutul informtion etween spike ounts nd stimulus diretions over time ross steps in diretion vrine. The dvntge of informtion theory is tht it yields model-independent result tht inorportes ny response nonlinerities 4. We estimted the joint stimulus-response distriutions (stimulus diretion versus spike ounts or inned eye diretion) in overlpping 6 ms time windows (see Methods). The proility of oserving stimulus-response pirings is funtion of the temporl seprtion etween the stimulus nd response windows. Being reful to orret for smpling is (see Methods) 42,43, we then estimted the mutul informtion t eh time dely etween the stimulus nd response, s funtion of time within the tril. As expeted, the dely tht mximized informtion orresponded to the time to pek of the spike-triggered verge stimulus. Similrly, the optiml dely for pursuit orresponded to the response lteny. As shown in Fig. 4,, informtion out motion diretion is onstnt throughout the tril until just fter the diretion vrine step. When the neuron egins to respond to the new diretion distriution, the informtion dips ut then rpidly reovers s the system dpts (Fig. 4). The informtion reovery ours fter the neurons hve fired, on verge, 3.8±2.5 spikes (n ¼ 23) in response to the new vrine ondition. As with MT neurons, the mutul informtion etween the eye nd trget diretion shows Gin () (spikes s degree ) d Gin () n= Gin () (spikes s degree ) n= Gin () Figure 2 Gin resles with stimulus vrine in MT neurons nd pursuit. () A single MT unit s input output funtion for low-vrine (, s.d. 2, lk irles) nd high-vrine (s.d. 35, red irles) motion stimulus. Cirles represent men vlues in 2 ms windows. Diretion flututions mesured with respet to the men (lk rrow, inset). Blk, red lines orrespond to the dominnt mode of vrition in the dt nd represent the est estimte of the response gin. () Eye movements from the sme monkey: low vrine (, s.d. 5, lk irles) nd high vrine (, s.d. 5, red irles). () MT popultion dt showing liner gin for nd vrine onditions in (pop. men : 23±27; : 3.±2., signifintly different, two-sided Wiloxon rnk-sum test, Po 28, n ¼ 92). (d) Pursuit popultion dt (pop. men :.28±.3; :.2±.4, signifintly different, two-sided Wiloxon rnk-sum test, Po 22, n ¼ 74, 3 monkeys). drop nd then rpid reovery fter step in diretion vrine (Fig. 4). The similrity in neurl nd ehviourl informtion reovery suggests tht dpttion t the neurl level llows the system s whole to mintin performne ross shifts in motion sttistis. Although the verge level of enoded informtion, I, differed ross our ortil smple, the perentge drop fter vrine step ws roughly onsistent for ll neurons suh tht DI ¼ I, where is.65 y liner regression (R 2 ¼.88, n ¼ 23; Fig. 4). As visul estimtes for pursuit rise from popultion of MT neurons 43, it is perhps not surprising tht we see less vrile informtion levels in pursuit ehviour. In pursuit, the sle of the dip is not strongly dependent on the verge level of informtion, with ¼.6 (Fig. 4d, liner regression, R 2 ¼.2, n ¼ ). To determine whether the similrity of DI vlues in pursuit ould e explined y the MT dt, we simulted popultion response y verging the informtion time ourses ross units, plotting the resultnt men nd dip vlue in Fig. 4d (red str). Although our neurl smple is modest, there is lose greement etween the predited popultion response nd pursuit dt. Units with diverse tuning will ontriute to ehviour, ut our MT smple represents supopultion with mximl sensitivity to diretion flututions nd thus might ontriute most strongly to ehviour 44, explining the result. We did not oserve informtion dips fter motion segment reks without vrine hnges 6. If the gol of dpttion is to optimize internl motion estimtes nd therey motion-driven ehviours suh s pursuit, then ltering the response gin of either MT neurons or pursuit ehviour should degrde the mutul informtion etween stimulus nd response. We tested this hypothesis y nlysing the dependene of the stedy-stte informtion on the response gin. By numerilly resling the response reltive to the stimulus, we simulted different gin levels (Fig. 5) nd reomputed the informtion for eh level (Fig. 5) 5. We found tht the true response gin (represented y the lk line, Fig. 5) lwys mximized diretion informtion, ross our ortil nd ehviourl dt sets. This indites tht the informtion svings y enoding motion effiiently t the ortil level is refleted in idel ehviour. Gin dpttion minimizes pursuit errors. Performne in trking ehviour suh s pursuit is defined y its ury: how well the eye movement follows trget movement over time. If gin dpttion optimizes pursuit, then suppressing tht dpttion should lower the trking ury. We simulted non-dptive pursuit system y re-sling the eye nd trget motions to mnipulte the response gin, holding it fixed ross rnge of motion vrine levels. For exmple, the gin vlue (G) mesured for stimulus with diretion vrine s.d. T ¼ is pproximte y the rtio G Es.d. E /s.d. T ¼.7, where the T nd E susripts represent the trget nd eye diretion, respetively, nd the s.d. desries flututions over time. If diretion vrine inreses to s.d. T ¼ 2.5 (lk tre, Fig. 6), the pursuit gin dpts to lower vlue, G 2.5 ¼.7 (green tre, Fig. 6). We simulted fixedgin (non-dptive) pursuit y multiplying the eye diretion t eh time point y ftor G /G 2.5 ¼ 2.4 suh tht the gin remined.7 (red tre, Fig. 6). It is pprent in Fig. 6 tht trking errors inrese sustntilly without dpttion. We define trking errors in the two-dimensionl plne s the differene etween the eye nd trget diretion t eh time step, ð N P ðyt ðt tþ y E ðtþþ 2 Þ =2, where y represents the eye or trget diretion, t the ehviourl lteny from the movementtriggered verge stimulus nd N the numer of time steps ross ll trils. In the exmple dt shown in Fig. 6, trking errors with dpttion (dt) hve root men squred (r.m.s.) vlue of 2.5 (green lines, Fig. 6 ), wheres non-dptive pursuit hs 4 NATURE COMMUNICATIONS 7:2759 DOI:.38/nomms2759

5 NATURE COMMUNICATIONS DOI:.38/nomms2759 ARTICE MT neuron Rte (men) (s.d. 2 ) (s.d. 35 ) Diretion (s.d.) Normlized gin () n =92.. Normlized gin () e Frtion Gin index Normlized gin index Filtered Normlized filtered.5.5 Δg/Σg Pursuit Eye diretion (men) Diretion (s.d.) (SD 5 ) (SD 5 ) d Normlized gin () n = Normlized gin () f Gin index Normlized gin index Filtered Normlized filtered.5.5 Figure 3 Adpttion normlizes response gin ross vrine onditions. () Plotting the stimulus in units of its s.d., the neuron s input output reltionship is the sme for oth vrines (sme dt s Fig. 2). () Resled input output dt from the sme pursuit experiment. () MT popultion dt, showing liner gin (red nd lk lines,,) reomputed for the normlized dt (: 2.2±2.9; :.5±.3, not signifintly different, two-sided Wiloxon rnk-sum test, P ¼.35, n ¼ 92). (d) Pursuit popultion dt similr to (:.53±.6; :.52±., not signifintly different, two-sided Wiloxon rnk-sum test, P ¼.6, n ¼ 74). (e) To nlyse gin hnges ross the popultion, we defined gin differene index (see text), Dg/Sg, where n index of indites perfet resling. We plot the distriution of MT neuron gin indies efore (lk solid line; pop men±s.d.:.72±.3, n ¼ 92, signifintly different from, one-smple t-test, two-tiled, Po 3 ) nd fter normliztion (grey solid line;.±.26, n ¼ 92, not signifintly different from, one-smple t-test, two-tiled, P ¼.67). ow-pss-filtered motion stimuli (see text) yielded similr results (dshed lines). (f) Pursuit popultion dt s in e: originl dt (lk solid line, men±s.d.:.4±.8, n ¼ 74, 3 monkeys, signifintly different from, one-smple t-test, two-tiled, Po 3 ) nd the resled input output reltionship (grey solid line, men±s.d.: ±.7, n ¼ 74, 3 monkeys, not signifintly different from, one-smple t-test, two-tiled, P ¼.68). ow-pss-filtered stimuli gin yielded similr results (dshed lines). Frtion Δg/Σg muh lrger errors, s.d. err ¼ 9. (signifintly different, piredsmple t-test, two-tiled, Po 3, n ¼ 2; red lines, Fig. 6 ). The negtive impt of suppressing dpttion inreses with trget diretion vrine (red versus green lines, Fig. 6d), suh tht r.m.s. trking errors inrese more thn sevenfold for monkey Er (signifintly different, pired-smple t-test, twotiled, Po 3, n ¼ ) nd more thn ninefold for monkey G (signifintly different, pired-smple t-test, two-tiled, Po 3, n ¼ ) ompred with (dptive) dt. The simultions we performed re relisti, euse pursuit t different trget diretion vrine levels is well desried y gin resling. The differene etween trking errors in simulted (tht is, resled) versus tul dt were smll (B.2* s.d. E ) ompred with the inherent vrition in pursuit (differene etween simulted pursuit nd dt: men ¼.2, s.d. ¼.58, n ¼ 56) 22,45,46. Gin dpttion minimizes trking errors ross ll diretion vrine onditions. We used the re-sling pproh to relte gin to r.m.s. diretion errors for eh trget vrine ondition (oloured lines, Fig. 6e). By resling the eye reltive to the trget diretion, we simulted lower nd higher gin vlues, mesuring the r.m.s. trking errors for eh gin sle ftor. The error surfes re onve nd thus hve minimum vlue (oloured lines, Fig. 6e). The minimum error vlues (open irles) lie lose to the errors oserved in pursuit dt (intersetion of the dshed line with eh urve, Fig. 6e). The devitions from the minimum vlues re smll ompred with the disrimintion threshold for diretion flututions (red dshed line, Fig. 6f) 22,45,46, suggesting tht the system is in ft minimizing trking errors within the onstrint of its nturl vriility. Dynmis of ortil nd ehviourl gin dpttion. The dynmis of n dpttion proess n e suggestive of the underlying mehnism. For exmple, dpttion driven y hnges in hnnel ondutne n e slow, with time onstnt of seonds or longer 6 9,4,5, wheres ortil synpti filittion/depression ours more quikly, with time onstnts of B3 ms (ref. 47). To resolve the time t whih vrine shift n e relily deteted from the response on eh tril, we used hnge-point detetion method 48. Chnge-point detetion simultes n idel oserver who knows the distriution of responses under the two different stimulus onditions nd steps through eh time point within tril to evlute the likelihood tht the urrent response rises from the versus onditions 48,49 (see Methods). As the diretion perturtion sequene on eh tril is rndomly generted nd the responses re vrile, the time t whih the vrine step n e deteted differs from tril to tril. We found tht detetion times for T were shorter thn for T trnsitions for oth neurons nd ehviour (MT neurons: Po 3, n ¼ 3,623; pursuit: Po 3, n ¼ 6,35, two-sided Wiloxon rnk-sum test). With respet to their verge ltenies, MT neurons detet upwrd (T) vrine steps fter 45±5 ms (n ¼ 3,623, 34 neurons) nd downwrd (T) steps fter 6±3 ms (n ¼ 3,745 trils). Pursuit responds to vrine shifts slightly lter: 53±44 ms (n ¼ 6,35 trils, 9 dt sets) for T nd 7±38 ms (n ¼ 6,597) for T vrine trnsitions, gin mesured from response lteny. These times re quite lose to the erliest possile detetion times, sed on sttistil nlysis of the stimulus on eh tril (see Methods). MT neurons detet vrine steps on verge 2 ms fter n idel oserver with omplete knowledge of the stimulus distriutions ould (T.53±5.9 ms, n ¼ 3,623 trils; T, 2.2±8.2 ms, n ¼ 3,745 trils, 34 neurons) nd pursuit 4 6 ms fter (T 3.9±4.9 ms, n ¼ 5,664 trils; T 6.±5.6 ms, n ¼ 5,977 trils, 9 dt sets). The differene in detetion times for upwrd versus downwrd NATURE COMMUNICATIONS 7:2759 DOI:.38/nomms

6 ARTICE NATURE COMMUNICATIONS DOI:.38/nomms2759 Pursuit MT neuron Informtion (its) Informtion (its) Dt Shuffled ΔI 2 3 Dt Shuffled 2 3 vrine steps is expeted, euse smll diretion perturtions re nerly s likely to rise from either distriution, wheres lrge diretion flutution immeditely identifies n inrese in vrine. The rpidity of resling to upwrd vrine trnsitions my e why we do not oserve n informtion trnsient for T steps essentilly the trnsients re too nrrow to detet 5,6. Gin shifts depend on the experiened diretion sequene. If the shifts in response gin do rise from dpttion, they should our only fter oserving stimulus outlier. The likelihood of oserving lrge diretion hnge goes up fter n upwrd vrine trnsition, ut in ny rndom sequene the time t whih the first outlier ppers will vry from tril to tril. As ontrol, we seleted the suset of trils from n upwrd trnsition experiment in whih the first stimulus diretion generted fter the trnsition from T vrine (time in 2, Fig. 7) hd vlue tht ould hve risen from the low diretion vrine distriution (yn tre Fig. 7; yn re Fig. 7). We then ompred the gin stte mesured from those trils with the gin stte t the preeding time step (time window, Fig. 7). The dt in Fig. 7,e show the responses of n exmple neuron nd ehviourl dt set for the time windows nd stimulus distriutions indited in Fig. 7,. The est liner fit for the response gin for the miguous T trils (yn, Fig. 7,e) ws sttistilly indistinguishle from the preeding vrine response gin (lk, Fig. 7,e) nd quite different from the post-step () gin mesured ross ll trils (red, Fig. 7,e). ΔI (its) d ΔI (its) n= n= I men (its) I men (its) Figure 4 Rpid reovery of mutul informtion fter vrine step. () Red tre: mutul informtion etween stimulus diretion nd spike ount (firing rte) for single MT neuron omputed in sliding 6 ms time window ross T vrine step (s.d. ¼ 35 to 2 ); (lk tre) shuffled dt. () Mutul informtion etween eye nd trget diretion from single dt set ross n T vrine shift (s.d. ¼ 5 to 5 ). We plotted DI, the differene etween the minimum informtion vlue t the dip nd the time-verged informtion level efore the dip, tht is, oi4, ginst oi4 for the () MT dt (n ¼ 23) nd (d) pursuit dt (n ¼, 3 monkeys). Red lines represent liner regressions. For MT, the informtion dip ws onstnt frtion of the verge informtion vlue (slope ¼.65, R 2 ¼.88, n ¼ 23). For pursuit, the dip ws less dependent on the informtion level,.2±.6 its (slope ¼.6, R 2 ¼.2, n ¼ ). The red str in d indites the simulted neurl popultion predition for pursuit, whih is quite lose to the oserved dt (see text). Normlized response Normlized stimulus /8 /4 / MT (n=94) Pursuit (n=7).25 8 Gin sle ftor Figure 5 Adpttion mximizes motion informtion in MT nd pursuit. () We rtifiilly resled the response gin y multiplitive sle ftor from /8 to 8 (oloured lines) nd re-omputed the stedy-stte mutul informtion etween neurl (or pursuit) response nd motion diretion (see text). () The mutul informtion ws lower for ll sle ftors other thn (unsled dt) ross our smple. Popultion dt for MT neurons (lk line, n ¼ 94) nd pursuit (grey line, n ¼ 7, 3 monkeys). Error rs re defined s s.d. We found no differene etween the vrine response gin nd the miguous (T) tril post-step gin ross our ortil nd ehviourl dt smples (MT neurons Fig. 7d, 22±5 for nd 7± for T, P ¼.24, pired-smple t-test, two-tiled, n ¼ neurons; pursuit Fig. 7f,.7±.8 for nd.6±.9 for T, pired-smple t-test, two-tiled, P ¼.6, n ¼ dt sets). These results llow us to onfirm tht the gin hnge we oserve is uslly relted to the experiened stimulus. Disussion The theory of effiient oding is linked to the ide tht neurl systems mximize informtion relevnt to ehviourl performne tht n influene survivl 4. Oservtions of neurl responses in mny orgnisms hve demonstrted pity for effiient oding 7 8, ut the onsequenes for motor ehviour hve not een explored 9,5. These experiments rek new ground, euse they demonstrte tht the priniple of effiient oding pplies to neurl system s whole, improving the ury of the movements it genertes nd not solely to individul sensory neurons. We hve exploited the lose onnetion etween ortil motion estimtes nd smooth pursuit eye movements 22,45,46,5 54, to demonstrte prllel dpttion effets in sensory neurons nd movement ehviour. Our experimentl design seprted the physiologil nd ehviourl reording, to rete the ontrolled repetition neessry to mesure informtion in single neurons. Although this design does men tht we nnot diretly relte flututions in eh neuron s rte to flututions in pursuit, the ft tht we oserved prllel gin optimiztion in oth neurons nd ehviour enourges us to think tht the dpttion we desrie is roust feture of sensory funtion. Adpttion is rod onept tht might inlude ny modultion in firing rte. ere we speifilly sk out dpttion to stimulus vrine sttistil feture of the environment rther thn to stimulus exposure per se suh s studies of the motion fter effet We find tht dpttion to motion vrine optimizes the enoding of motion informtion y MT neurons, with ehviourl impt of optimizing informtion in pursuit eye movements, minimizing visul trking errors nd therey improving vision of moving ojets. Pursuit ehviour rises from popultion of MT neurons 43. One ould imgine tht sensory popultion ould hve optiml sensitivity to motion flututions when individul units do not. As it hppens in the pursuit system, nd perhps generlly throughout sensory ortex, single neurons optimize gin Normlized informtion 6 NATURE COMMUNICATIONS 7:2759 DOI:.38/nomms2759

7 NATURE COMMUNICATIONS DOI:.38/nomms2759 ARTICE Error (degree) No dpt Dt Min error d e f Pursuit error (degree) Stimulus Dt No dpt No dpt model Dt Min error g er Trget s.d. (degree) r.m.s. error (degree) 8 s.d Gin sle ftor Proility ΔError (degree) No dpt Dt Min error 5 3 Diretion error (degree) er g Trget s.d. (degree) Figure 6 Adpttion optimizes pursuit y minimizing trking errors. () Exmple pursuit tril showing trget (lk) nd eye (green) over time for n s.d. ¼ 2.5 experiment. The simulted pursuit response without dpttion (red line, see text) is muh less urte. We hve sutrted the verge lteny to lign the trget nd eye dt for visuliztion. () Tril-verged diretion errors from the experiment nd simultion in : pursuit ( dt, green, stimulus s.d. ¼ 2.5, gin ¼.7) hs smller diretion errors thn simulted fixed-gin pursuit ( no dpt, red, gin ¼.7). The minimum error level from multiplitive resling of pursuit dt is very lose to the dt itself ( min error, lk, gin ¼.5). () Distriution of trking errors t eh milliseond from the sme dt (green, s.d. err ¼ 2.5 ) nd simultion: non-dpting (red, s.d. err ¼ 9. ), min. error, (lk, s.d. err ¼ 2. ). (d) Trking errors ross trget vrine levels: pursuit dt (green), fixed-gin (no dpttion) simultion (red) nd the minimum error hievle from resling gin (lk). Plots represent men vlues over ten dt sets for eh monkey. (e) Error urves generted from the resling simultion (oloured lines). We resled the eye movement t eh time step to simulte different response gins (from. to 2 times the tul pursuit gin), then omputed the expeted error y err (t) ¼ y trg (t t)-sle_ftor*y eye (t). The r.m.s. error level is onvex funtion of the gin sle ftor. Cirles indite minim. The dotted lk line orresponds to tul pursuit gin nd trking errors t eh vrine level (dt form monkey er). (f) The differenes etween minimum nd tul trking errors s funtion of trget diretion s.d. for two monkeys (er, red; g, lk). The differenes re well elow the pereptul threshold for diretion disrimintion (red line, see text). individully. Determining the impt of single-neuron gin hnges on popultion-level motion estimtes will require lrgesle simultneous reordings of the MT popultion, to mesure the struture of signl- nd noise-driven orreltions. Two very different mehnisms hve een proposed to explin gin dpttion to veloity vrine in fly (refs 5,6). Bilek nd ollegues 5,6,35 desried the effet s dpttion, mening resling of the system s representtion of visul motion signls. Borst et l. 39 nd Sompolinsky nd ollegues 4 proposed tht similr phenomenon ould e eliited without stte hnge from orreltion-sed (Reihrdt) motion detetor with sturting nonlinerity t high frequenies. As vrine in the stimulus inreses, the high-frequeny response sturtes sooner thn the low-frequeny response, reting n pprent drop in gin without ny tul hnge in the system prmeters. Although susequent work ultimtely supported the dpttion hypothesis, sed on the filure of the stti model to predit the mixture of dpttion timesles oserved in the fly, retin nd ortil slie reordings 3 5,55, the stti nonlinerity mehnism remins n interesting possiility. The nture of reording from ehving monkeys mkes the identifition of long dpttion timesles quite diffiult. Although ortil slie experiments ould use long sequenes of vrine hnges in injeted urrent over mny minutes, we were onstrined y the monkey s ility to mintin fixtion nd we were unle to resolve differenes in dpttion dynmis s funtion the durtion of stimulus presenttion 3. owever, two fetures of results rgue for dpttion over sturting nonlinerity model. First, we did not oserve sturtion in either MT or pursuit responses (Figs 2 nd 3). Seond, we found tht reduing the high-frequeny ontent of our stimulus to mth pursuit s frequeny response preserved gin resling (Fig. 3). We note tht Bir nd Movshon 56 did oserve hnges in MT neuron responses tht were onsistent with stti nonlinerity model, ut they mnipulted temporl frequeny ontent of the stimulus rther thn vrine, nd so our results re not diretly omprle. Severl lsses of mehnisms hve een proposed to ount for gin dpttion in other systems, inluding modultion of hnnel ondutnes, synpti filittion/depression nd iruit effets. Intrinsi ondutne hnges hve een implited in gin dpttion ourring on seonds-long timesles. For exmple, sodium hnnel intivtion in slmnder retinl gnglion ells 8, modultion of slow C 2 þ -sensitive K þ fter-hyperpolriztion ondutne in rrel ortex 37,57 nd the lne of sodium nd potssium urrents in mouse sensorimotor ortex 8 hve een implited in dpttion to input vrine. In eh of these systems, the timesles of dpttion re sustntilly longer thn the 4 7 ms timesle we oserve in the primte. Informtion flow in thlmoortil nd ortioortil pthwys is gted y dpting metotropi nd ionotropi glutmetergi synpses tht filitte or depress respetively, modulting the response gin of their trgets. In the visul system, Snzini nd ollegues 58 demonstrted gin modultion of GN tivity within B5 ms y V lyer 6 ortil projeting neurons. The reported timesle of thlmoortil nd ortioortil synpti filittion/depression is B3- ms 47, very similr to to the timesle we mesured. While synpti gin hnges lone re typilly ssoited with lrge hnges in firing rte 58 whih we did not oserve, reent studies hve identified network effets tht might produe rpid gin hnges without ffeting verge firing rte 59. For exmple, lned rrges of NATURE COMMUNICATIONS 7:2759 DOI:.38/nomms

8 ARTICE NATURE COMMUNICATIONS DOI:.38/nomms2759 MT neuron Firing rte (spikes s ) e Pursuit Eye diretion (degree) T T T exittory nd inhiitory synpti tivity rpidly inrese neuronl responsiveness on the timesle of tens of ms 6. Intertion etween lol reurrent iruit tivity nd non-liner dendriti properties hs lso een proposed s possile mehnismforortilgin dpttion tht my operte on the fst timesles we oserve 6,62. Reurrent tivity mong similrly tuned neurons ould regulte response gin, mplifying the response to thlmi input s well s shrpening the response seletivity or inresing signl-to-noise rtio whih might ount for the informtion mximiztion we oserve in individul MT neurons. Given the diversity of dptive mehnisms ville to neurl systems, it seems likely tht most if not ll sensory systems hve the pity to dptively enode the stimulus fetures to whih they re most sensitive 2,65,66. This study demonstrtes tht the impt of dptive oding rehes eyond informtion representtion of single neurons to the performne of ehvior. On longer timesles, the rin hs the ility surpss the limits of d Gin (spikes s degree ) f Gin Proility to to T T Diretion s.d. (degree) to to T n= Normlized s.d. Figure 7 Gin dpttion depends on experiened stimulus vlues. () Using n exmple neuron, we nlysed dt just efore (, grey shding) nd fter ( 2, pink shding) vrine step (T, s.d. ¼ 2 to s.d. ¼ 35 ) to determine how shifts in response gin depended on the tul stimulus diretion sequene. () We seprted trils sed on whether time in 2 diretion vlues fell in the re of overlp etween the nd stimulus distriutions (T, yn shding). () Stimulus nd response vlues in in (, lk irles) nd in 2 (, red irles) for ll trils. We hve highlighted dt from the miguous T suset of trils ( in 2 T, yn irles). iner gin vlues omputed s in text (lines). (d) MT popultion dt (n ¼ ), gins mesured in time in nd time in 2 on ll trils (red) or only on miguous T trils (yn). (e,f) Sme s,d, ut for pursuit ehviourl dt. The response gin resles with stimulus vrine only if the niml sees n outlier vlue (n ¼ ). optiml sensory oding y uilding experiene-sed models of the world 67 7 tht llow for preditive neurl responses 72,73, ntiiptory ehviours nd motor lerning The next hllenge will e to determine how neurons lne the enefits of effiient sensory representtion with other onstrints 82,83 suh s predition in guiding ehviour. Methods Eye movement reordings nd extrellulr reordings from extrstrite ortil re MT/V5 were mde in two dult mle rhesus monkeys (M multt); third monkey prtiipted in ehviourl experiments only. Animls were implnted with slerl oil in one eye, post for hed restrint nd reording hmer using sterile surgil tehnique under nesthesi. All surgil nd experimentl proedures were pproved in dvne y the University of Chigo s Institutionl Animl Cre nd Use Committee nd were in strit ompline with the US Ntionl Institutes of elth Guide for the Cre nd Use of ortory Animls. We trined nimls in si pursuit tsks efore olleting these dt. The nimls viewed right trgets ginst the drk sreen of Sony GDMFW95 fst CRT disply ( 2 fps,, pixels) in dimly lit room. Eye movements were smpled every milliseond, filtered nd digitized for future nlysis 45. Experiments were orgnized into trils lsting 2 3 s. Animls were rewrded t the end of tril for keeping the eye within severl degrees of the trget during speified periods. For pursuit tsks, nimls were required to mintin fixtion within 2 of sttionry fixtion spot t tril onset nd to e within 3 of the trget during the finl 2 ms of pursuit. Gze ury ws not penlized during time windows used for dt nlysis. During physiology experiments, nimls hd to mintin fixtion within 2 throughout the tril. orizontl nd vertil eye positions were smpled t ms intervls, low-pss filtered nd differentited. The veloity omponents were trnslted into instntneous eye diretion, to llow omprison of stimulus nd response in the sme units (degrees). Eh tril ws inspeted nd trils with links or sdes during the motion intervl were disrded from further nlysis. Mgneti resonne imgings of the monkeys were otined efore implnttion to guide hmer lotion. We reorded from visul ortex with n rry of three qurtz-pltinum/tungsten eletrodes (TREC, Germny). We lolized re MT sed on stereotti oordintes, reeptive field size, motion seletivity nd other physiologil response properties in MT nd in surrounding strutures. We smpled neurl tivity t 3 kz (Plexon Omniplex) nd stored wveforms for offline spike sorting. We performed online nlyses to mp the diretion nd speed tuning, nd the size nd lotion of eh unit s exittory reeptive field. We identified single units through prinipl omponent nlysis of spike wveforms in tndem with inspetion of interspike intervl distriutions. Visul stimuli. Stimuli onsisted of rndom dot ptterns (2 dots deg 2 )tht moved in n perture ginst the drk kground of the monitor. In physiology experiments, the dots moved within sttionry perture, while the monkey mintined fixtion, ut in ehviourl experiments oth the pttern nd perture (4 ) trnslted ross the sreen t onstnt speed. Dots moved oherently suh tht the diretion nd speed of eh dot ws identil t eh time step, ut the pttern diretion hd n dded stohsti perturtion tht ws updted every 2 ms (two frmes) from uniform distriutions with different vrines. Trget speeds were 2 25 s for pursuit nd were typilly set to the preferred speed of eh MT unit (2 96 s, men ¼ 29 s ). Some pursuit experiments used.25 spot trgets with identil motion sttistis. Trils were often onfigured to ontin one or more steps in diretion vrine t fixed times within the tril. Reeptive field mpping. Visul stimuli were tilored for eh neuron to spn the lssil reeptive field nd to fll on prtiulr portions of the diretion tuning urve. We mpped tuning urves with full-field ptterns (56 y 38 ) whose diretion spnned the irle with 5 sping nd plotted the tuning urve. We then determined the speed tuning urve using preferred diretion motion nd log 2 speed sping. Reeptive fields were lolized using 2 5 ptterns tht ppered in different sptil lotions. We seleted entre diretion for the flutution stimuli sed on eh unit s diretion tuning urve, testing on one or oth flnks. Vlues for the size of our smple (n) represent the numer of experiments rther thn the numer of neurons. We reorded from totl of 44 MT neurons (n ¼ 26 monkey ; 8 monkey 2) for this study. iner fitting. We fit liner reltionships etween input (stimulus diretion) nd output (spike ount or eye diretion), to define the response gin (see Figs 2 nd 3). We used prinipl omponent nlysis to determine the dominnt mode of vrition in the dt smple y minimizing the summed perpendiulr distne etween the dt points nd the fit. Mutul informtion estimtes. We used the diret method to ompute the mutul informtion etween stimulus nd response 4. We divided the tril into overlpping time windows of 6 ms. In eh time window, T, we dptively inned 8 NATURE COMMUNICATIONS 7:2759 DOI:.38/nomms2759

9 NATURE COMMUNICATIONS DOI:.38/nomms2759 ARTICE the vlues of stimulus, y(t), nd response (either spike ount n(t) or the eye diretion y E (T)) suh tht equl numers of exmples ourred in eh in. We then formed the joint proility distriution etween the stimulus nd response, for exmple, P(n(T), y(t t)) for neurons or P(y E (T), y(t t)) for pursuit for eh time dely, t. Informtion vlues peked t dely equl to the response lteny, whih ws somewht stimulus-vrine dependent. Simplifying the nottion to P T (n, y), the mutul informtion is defined s I T ðn; yþ ¼ X X P T ðn; yþ P T ðn; yþlog 2 ðþ P y n T ðnþp T ðyþ where I T (n, y) quntifies in its the mount of informtion tht single oservtion of spike ount of n in the time window T provides out the diretion of motion. P T (n) is the totl proility of oserving n spikes fter ounting over the time intervl, T, verged over ll stimuli. In our se, ll stimuli ourred with roughly equl proility, P T (y). The eqution is identil for omputing informtion from eye movements, exhnging P T (y E, y) for P T (n,y) nd summing over the numer of ins (2) used to disretize the eye diretion. Finite smple is orretion. We used proedure to minimize the effets of finite smple size on our estimtes of informtion, following the methods of refs 42,43. By rndomly drwing different numers of smples (N) from our totl tril set for eh neuron (or pursuit dtset), we looked for the expeted systemti ehviour s follows: I est ¼ I þ N þ N 2 þ nd extrted I N s our est estimte. The numer of repets in our dt set gve resonle liner ehviour keeping first-order terms in N only. It is noteworthy tht the extrpolted estimte of informtion for n infinite dt set is lwys smller thn the vlue mesured from finite dt set. Chnge point detetion. To quntify dpttion dynmis from the spike trins themselves, we used log-likelihood method. We time shifted the responses y the verge lteny, found the totl spike ount or time-verged eye diretion nd the stimulus diretion in suessive 2 ms time windows. We pooled windows over eh motion segment to mesure the joint distriution of inned ounts nd trget diretions, P(r, y), or inned eye nd trget diretions, P(y E, y T ), for low- nd high-vrine onditions. We then stepped through the response on eh tril nd omputed the umultive likelihood tht the series of response vlues me from low-vrine or high-vrine stimulus ondition. We defined the umultive likelihood t time T, C(T), for n T vrine step tril s CðTÞ ¼ XT logð PðrðÞ; t sðtþþ Þ ð3þ PðrðÞ; t sðtþþ t¼ where r(t) represents the response in time window t, s(t) the stimulus in the sme time window, the susript indites low-vrine ondition nd represents high-vrine ondition. For eh dt set, we defined threshold from the s.d. of C(T) over ll time steps (nd ll trils) efore the vrine shift. We then strted integrting the likelihood from the time of the shift nd omputed the umultive likelihood over time for eh tril 48. Negtive C-vlues were reset to. We defined the hnge point s the time t whih C exeeded the threshold. Dt vilility. The dt tht support the findings of this study re ville from the orresponding uthor upon request. Referenes. Attneve, F. Some informtionl spets of visul pereption. Psyhol. Rev. 6, (954). 2. Brlow,. B. in Sensory Communition (ed. Rosenlith, W. A.) (MIT Press, 96). 3. ughlin, S. A simple oding proedure enhnes neuron s informtion pity. Z. Nturforsh. C 36, 9 92 (98). 4. Winwright, M. J. Visul dpttion s optiml informtion trnsmission. Vision Res. 39, (999). 5. Brenner, N., Bilek, W. & de Ruyter Vn Stevenink, R. R. Adptive resling mximizes informtion trnsmission. Neuron 6, (2). 6. Firhll, A.., ewen, G. D., Bilek, W. & de Ruyter Vn Stevenink, R. R. Effiieny nd miguity in n dptive neurl ode. Nture 42, (2). 7. Kim, K. J. & Rieke, F. Temporl ontrst dpttion in the input nd output signls of slmnder retinl gnglion ells. J. Neurosi. 2, (2). 8. Kim, K. J. & Rieke, F. Slow N þ intivtion nd vrine dpttion in slmnder retinl gnglion ells. J. Neurosi. 23, (23). 9. Rieke, F. Temporl ontrst dpttion in slmnder ipolr ells. J. Neurosi. 2, (2).. Den, I., rper, N. S. & MAlpine, D. Neurl popultion oding of sound level dpts to stimulus sttistis. Nt. Neurosi. 8, (25). ð2þ. Mrvll, M., Petersen, R. S., Firhll, A.., Arzdeh, E. & Dimond, M. E. Shifts in oding properties nd mintenne of informtion trnsmission during dpttion in rrel ortex. PoS Biol. 5, (27). 2. Mrvll, M., Alend, A., Ble, M. R. & Petersen, R. S. Trnsformtion of dpttion nd gin resling long the whisker sensory pthwy. PoS ONE 8, e8248 (23). 3. Wrk, B., undstrom, B. N. & Firhll, A. Sensory dpttion. Curr. Opin. Neuroiol. 7, (27). 4. undstrom, B. N., iggs, M.., Spin, W. J. & Firhll, A.. Frtionl differentition y neoortil pyrmidl neurons. Nt. Neurosi., (28). 5. undstrom, B. N., Firhll, A.. & Mrvll, M. Multiple timesle enoding of slowly vrying whisker stimulus envelope in ortil nd thlmi neurons in vivo. J. Neurosi. 3, (2). 6. Shrpee, T. O. et l. Adptive filtering enhnes informtion trnsmission in visul ortex. Nture 439, (26). 7. Ngel, K. I. & Doupe, A. J. Temporl proessing nd dpttion in the songird uditory forerin. Neuron 5, (26). 8. Mese, R. A., Fmulre, M., Gjorgjiev, J., Moody, W. J. & Firhll, A.. Emergene of dptive omputtion y single neurons in the developing ortex. J. Neurosi. 33, (23). 9. Wester, M. A. Visul dpttion. Annu. Rev. Vis. Si., (25). 2. Rshss, C. The reltionship etween sdi nd smooth trnking eye movement. J. Neurophysiol. 59, (96). 2. iserger, S. G. & Westrook,. E. Properties of visul inputs tht initite horizontl smooth pursuit eye movements in monkeys. J. Neurosi. 5, (985). 22. Osorne,. C., iserger, S. G. & Bilek, W. A sensory soure for motor vrition. Nture 437, (25). 23. Kruzlis, R. J. Resting the smooth pursuit eye movement system. J. Neurophysiol. 9, (24). 24. iserger, S., Morris, E. & Tyhsen,. Visul motion proessing nd sensory-motor integrtion for smooth pursuit eye movements. Annu. Rev. Neurosi., (987). 25. Collewijn,. & Tmming, E. P. umn smooth nd sdi eye movements during voluntry pursuit of different trget motions on different kgrounds. J. Physiol. 35, (984). 26. Westheimer, G. & MKee, S. P. Visul uity in the presene of retinl-imge motion. J. Opt. So. Am. 65, (975). 27. Munsell, J.. & Vn Essen, D. C. Funtionl properties of neurons in middle temporl visul re of the mque monkey. I. Seletivity for stimulus diretion, speed, nd orienttion. J. Neurophysiol. 49, (983). 28. Groh, J. M., Born, R. T. & Newsome, W. T. ow is sensory mp red Out? Effets of mirostimultion in visul re MT on sdes nd smooth pursuit eye movements. J. Neurosi. 7, (997). 29. Kohn, A. Visul dpttion: physiology, mehnisms, nd funtionl enefits. J. Neurophysiol. 97, (27). 3. Kohn, A. & Movshon, J. A. Adpttion hnges the diretion tuning of mque MT neurons. Nt. Neurosi. 7, (24). 3. Drgoi, V., Shrm, J. & Sur, M. Adpttion-indued plstiity of orienttion tuning in dult visul ortex. Neuron 28, (2). 32. Glsser, D. M., Tsui, J. M. G., Pk, C. C. & Tdin, D. Pereptul nd neurl onsequenes of rpid motion dpttion. Pro. Ntl Ad. Si. USA 8, E8 E88 (2). 33. Grdner, J.., Tokiym, S. N. & iserger, S. G. A popultion deoding frmework for motion ftereffets on smooth pursuit eye movements. J. Neurosi. 24, (24). 34.deRuyterVnStevenink,R.R.,Bilek,W.,Potters,M.&Crlson,R.in Proeedings of IEEE Conferene on Systems, Mn nd Cyernetis (994). 35. Smirnkis, S. M., Berry, M. J., Wrlnd, D. K., Bilek, W. & Meister, M. Adpttion of retinl proessing to imge ontrst nd sptil sle. Nture 386, (997). 36. Kvle, M. N. & Shreiner, C. E. Short-term dpttion of uditory reeptive fields to dynmi stimuli. J. Neurophysiol. 9, (24). 37. Díz-Quesd, M. & Mrvll, M. Intrinsi mehnisms for dptive gin resling in rrel ortex. J. Neurosi. 28, (28). 38. Díz-Quesd, M., Mrtini, F. J., Ferrti, G., Bureu, I. & Mrvll, M. Diverse thlmoortil short-term plstiity eliited y ongoing stimultion. J. Neurosi. 34, (24). 39. Borst, A., Flngin, V.. & Sompolinsky,. Adpttion without prmeter hnge: dynmi gin ontrol in motion detetion. Pro. Ntl Ad. Si. USA 2, (25). 4. Sfrn, M. N., Flngin, V.., Borst, A. & Sompolinsky,. Adpttion nd informtion trnsmission in fly motion detetion. J. Neurophysiol. 98, (27). 4. Bilek, W., de Ruyter vn Stevenink, R., Rieke, F. & Wrlnd, D. Spikes: exploring the Neurl Code (MIT Press, 997). NATURE COMMUNICATIONS 7:2759 DOI:.38/nomms