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PLASTICITY IN THEVSTIBULOOCULAR REFLEXA NEW HYPOHESS A. Mle and G Lerge

bortory of Neurophysiology, Nton nsttute of Mentl Helth,ehesd Mrylnd

555

Eye movement recordings reveal that we do not scan our visual surroundings like the cinecamera panning across a scene, but rater take in te viewin a sequence of still-shots. isual search is a speculative business andseveal times a second throughout the waking hours we geneate rapidsaccadic eye movements tat relocate the image of he world on the retinaIn this way images that may prove to be of particular interest are positioned

in the foveate reion of most acute visionfor detailed scrutiny If thisdetailed processing of the retinal images is to proceed eectively then teeyes must be stabilized with respect to the surroundings. Indeed, visualacuity begins to deterorate appreciably when the retinal images dft atmore tan a few degrees per secod eseier McKee 1975) Headmovements pose a serous potential treat to ocular staility and are dealtwit by a reex that generates compensatory eye movements to oset tem:te vestibuloocular ree (O)

strking feature of the O is tat it operates witout te benet ofimmediate feedback The input to the system head rotation, is sensed by

the semicrcular canals whose prary aerent discharges supply the brainstem with frequencycoded information eectively describing he ead'sangular velocity A variety of diect and indirect neural patways tenconvey tese signals to te motoneurons innervating te extea eye muscles tat generate te ouput, compensaory eye rotation (see Figure )Because the output of te ree does not inuence he receptors sensing theinput the O is said to operate as an openloop control system. A majorproblem sared by all suc systems is calbration ow is te performance

+T US Govmnt t gt to tn nonluiv oyltyf lin n d to ny

copyigt coving s pap

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274 E & EGE

l so onroons o ys o n lyopns o roons o ? Alo s prol lly n y 0nn 1923 ws no lly ognz nlvy nly Th prvln ssponpl no xplws h r ws "w n prly lly sp; pol o sls n nnn pprop pon lvls ws nonlly pp Goso Mlvll Jos 1971) s osh flly o hs oon o o w hy o h h Orw sv s wh ss wo lh vs-psspls vn sow rvrs nr so rsns onsor Mlvll Jons 1976) Ts l o sson O ws so lo- lon y so vslly pv poss whosnorl on ws o kp sys pproply l T snly hnlk qly o h O n h hop h hvlly prov o ol sys or syn lll hnssnrly ory ln n h nl nvos sys

pv ply s ow os O sn n o opl ns n vy o nls Howv so spsns onn l hnss n o or o vo oso w hv srr o rvw ro

A Head Rotaion

B

i Worl

Ey oaion

a

------- w

I

l 8 1+ _LQ-L. - ---Smiircul Bri Orbi

Cana

Fue The VO a an opn-loop control sytem. A Baic neuronal orgnization (muchimplifd). B Block diagram; cuu e denote ignal ow channel withn the nervouytem dcuu line reprent extea, phyical lnk denotng head velocity withrpt to the world eye velocity with ept to the head and eye velocity withrept to the world gze eloity

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LASTCTY N VSTBULOOCULAR RFLX 5

work on he monkey n general, only passng reference s made o he workon oher anmals As ye, no bophycal or morphologcal correlaes ofhese adapve chages have been ound n ay speces a he mao

conces reman he general naure of he adapve mechansm and he seof he modable elemens. A leas nsofar as he monkey s conceed,many o he nal deas abou he adapve mechansm partcularly he roleof he cerellum, do no apply, and we shall propose a new hypohess.

ShorTerm OperatonBefore proceedng o consder he longerm regulaon of he VOR smperave o undersand he general workngs o he normal reex Insoaras he sucural orgazaon of he sysem s conceed, we need consderol he des esve rees o he erl crc d slprocessng are avalable n several excellen revews (Carpener 9, Cohen174, Prech 197, Wlson Melvl ones 197).

MACHINE-LIKE OPERATION hee noable feaures o he prmaeVOR ha ogeher gve a machnelke appearance are s hgh speed,accuracy, and conssency he combnaon of a vually nsananeous

neal recepor orga, sho cenral pahways wh ew synapc delays,and an exremely rapd plan (he eraocular muscles and eyeball) pro-duces a oa delay of only 1 mse rom head movemen o compensaoryeye movemen (F A. Mles ad S G Lsberger, n preparaon). (Noe haa car ravellng a 55 mph would manage o ravel only 1 ha me!)I s usual o assess he peromance of he reex by recordng he compensaory eye movemens resulng rom passve snusodal oscllaon o hewhole anal abou he vecal axs n he dark Over he requency rangeof 0.1 o 1 0Hz, he an of he hesus monkeys VO, dened as peak eevelocy dvded by pak hed veloy, s uslly 0 o 1 .0 wh sadarddevaons ypcally less ha 5% of he response, he sysem can be sado deserve he descrpon machnelke" (Mles Eghmy 190) n heresus monkey, hereore, preservaon o a sable renal mage durng headus can be accouned for almos enrely by he operao o he VOROher echasmspropocepon preprogrammg d vsoever mnor Bzz e al 197).

SL DBCK A OR UBSTUT OR T R n he lgh,vsual eedback mechansms n he orm of he pursu an opoknsysems are also avalable o sable he eyes wh respec o he suround-ngs. Operang he maner o neaveeedback racng sysems, hey

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276 MLS & LSRGR

pond o h ippag of ina imag by gnaing y movmn hand o duc ha ip A anima wih mobi y appa o hav anopokinic ym ha pond wid-d imag moion aco h

who ina. Sn i i poniv o movmn of h backgound mag a t tat wl r t O al t mpltly tablz ty duing had u, h opokini ym opa o du anyral rtnal imag ip and hf an b gadd a a bak-up o hO howv h opokini ym i o ow ha i man a pooubiu fo appopia O Th am tr tg prap t alr tnt t prt ytm w ar a nly bn n ngr vrtbrat T ytm pally rpnv t mall mvngmag n t val rgn an allw t anmal t trak mall bjt vn

whn hy co a faud backgound. ucc h man oviding anyopokinic ianc" ha h movmn of h y aiv o haionay bakgound woud nomay ii. Howv, fo h pn hi l n t tan t at tat wn nt bng t trakmovng bjt t pt ytm wll b avalabl t at n nrt wtt ptknt ytm t a tablatn t y wt rpt t trrnng Evn whn h wo ym opa ogh in hi ahionminima anci fom ip o on of acking y movmn a i in of 8 m Lanman t al 198) T tnv dpndn upon

viua fdbak woud ay man ha h anima woud av o nrnrabl mtn t val wr rng at a t w wlvrly mpm t val aty T mtatn t val bak mhanim obviouy mak i ll h mo impaiv ha h Ohoud b appopiay caibad.

An obviou addiiona advanag f a nonviua mhanim uh a hO r mantanng lar tably tat t ntn o ntn nlwlmnan ntn tmr t O a grat tlty n taion wh h igh v a adqua bu h nvionmn ak httral atr n r al tablzatn g t pnwatr abtatof h pagi h h iuaion phaiz h fdfowad nau of hr n t pp r obviuy nt t tablz nntnt ratrl mag bu ratr o inu ha if omhing l m ntviw i imag wi fa upon a anaby ab ina

VOR NCTONS TO SABZE RTNA MAGES BY PRESERVNG

GAZE VEOCTY Ornarly wn w rr t "y ptn w man"ptn t y wt rpt t t a Hwvr n dicuingy-had coodinaion i i ao impoan o conid poiion of h ywt rpt t t rnng wrl t w w rr a "gaz ptn Fr var ran tat wll graally bm apparnt t O


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LSCY N VSULCULR RLX 277

is most readily dealt with in he velociy domain so hat we shall mostly bereferring to eye velocity, gaze velocity, etc. Algebra denes gae velocity(abbreviaed o , o denote eye veocity with respect to the word) as thesm of he velociy of he eyes wih respect o he head (eye velociy

h) and he velocity of he head with resect to he world (head velocityGae veloiy = eh w. 1.The fnction of the VOR in simle siaions where he animal is viewing

the stationary srrondings can now be resated: to kee gae veloity(

) ero by insing that any hanges in head veloity

ae always

oset by onverse changes in eye velociy he ltimae aim of orseis to prevent movements of the head from distrbing the stability of he g g However he VOR conines o beeqally imporant when the monkey uses is prsit sysem o track sallmoving objecs a sitaion in which he monkey is now more nterested instabiliing the image of the moving targe than he image of the stationarysrrondings he animals performance in sch siations is measred byhow well it manages to ath its gae veloity (eye veloity with respetto the world) o he targe's veloity (measred with respect o the world)and this is known to be roeced by he VOR against any distrbanceresling from movements of the head (Lanman e al 17 Two systemssharing the common nal ahway are at work here (see Figre 2 thenegative-feebak psit syste wih attepts to ath ae veloity to arge velociy l, and he openloop VOR which operates toproec the gae velociy ! generated by the prsit system againstchanges n ead velocty ( he extraodinay be dea in the vestiblooclar resonse (abot 12 msec) ensres ha any distrbance of the

head will cse only brief inerrionslargely trivialin the animalsrsi of the argeOf corse the monkey may choose o prse moving targets by combin

ing smooth movements of both its eyes and head (Lanman et al 17alhogh the later will be ose b the comensatory eye movemesgeneraed b the VOR Indeed the VOR might seem o be conerrodcive here, sice in eect it cancels any conribion that he head movemenmight oherwise have made to the prsit hs a rst glance one mighthink that it wold be in the sysems nteres to rede the gain of he VOR

in hese circmsances owever any sch hange wold mean hat nforseen disrbances of the head wold be inadaeqately comensated and sowold severely compromise tracking erformance his is no only ndesirable b also contrary to eerimetal ndings (F A Miles and S

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2 MILES & ISBERGER

I I I . VOR wI

Iw +

1+w -{)

6i :

-

Fgue Blck daa f h nl O and h navfdback s acknss Cuus les dn sna w chnnls whn h nvs ssm; dscuuslines represent exteal. physcal links denoting head velocity wth rspect to the world

ye eloty wth ret to the hd 0 eye eloty with ret to the wold gzevc) and a vl wh sc h wd

b n aaon) In o em an o e monky OReem o b ed and mmabl No mae wa onon ackn

bavo o e manne n wc ben acvd e OR alwayacve

In m OR ncon away o oec n az velocywe o o oweeeby abln waev enal maae o may ne a e m e ead dbed Ony anmal wa yem ave an nee n abln e ena mae o movnae Te abb o amle doe no m abl o ack mall amovn aco a eaed backond and eoe o o lack a yem Clay va eedback n anmal alway oeae oab e nl mae o aonay ondn and nc een aze vlocy a OR ncon o oc alway zeo

Long-Term Regulation: Adaptive Gain ControlI o any eaon e an o OR devae acably om nyocl ably wll b lo dn ad and een nal mael wl el A aady oned o bca o lon laency valeedback mcanm cold ameloa b neve oally adca ocla nablyaclaly dn a ead oveen lealy vonwold b veely coomd dn ead ovemen Evn ana nec ccaon o OR wee eacly aoae ely nconcvabl a e cold man calbaed ove a wolele I O dd no o a bln adav caabl wold

b naccably vlnabe o mno da ama and an


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ASICIY IN ESIBUOOCUAR REFEX 279

G-TRM SSTTY F R T ATRD SUA PUT t simportant to raliz that th rtnal vnts during had tus provid thsystm's only truly rliabl way of dtrmining not only that a VR calibra

ton poblm ists but also th act natu of th problm, . whthrth gain is too hgh or too low Prsistnt rtinal imag slip clarly signalsth nd for a VR gain adjustmnt f th gain w too low (compnsator y movmnts fail to fully ost ad rotatons) thn th mag of thstationary surroundings would consistntly slip in a dirction contary toth had movmnt, whras th rvrs would b xprincd if th gainwr too high Th simplst dirct tst of th systm's adaptiv gan controlcapablity would b to us optical mans to induc such rtinal vntsdurng had tus and thn masur thr cts on th gan of th VR

hs has bn acvd usng magnfyng or rducng tlscopc spctacls(ils Fullr 94, Gauthir Robinson 95, ils ghmy 90).

f an animal waing say 2 X magnifying tlscopic spctacls kps itshad prfctly still, no nw dmands a placd upon ts oculomotor systmA tagt tht appas though th spctacls to b 0 o to on sid canb fovatd wth a 0 saccadic y movmnt (although n ralty th targts only o to on sd); lkwis, a targt sn movng across th ld ofvw at 0 pr sc can b trackd with a matchng y vlocty of 0 prsc (although n rality th targt s only movng at pr sc nly f th

animal movs its had will it fac a nw challng: if th had rotats at,say, 0 pr sc, th world sn through th spctacls will mov at twicthat rat Thus, n ordr to kp th mags on ts rtna stabl durng hadtus, th anmal would hav to doubl th usual vlocity of its compnsa-tory y movmnts

Wth 2 X magnfying tlscopc spctacls th gain of th monky' VR(masurd n th dark) shows a gradul incras that s roughly xponntialand achivs an asymptot about tims normal n a fw days Convrsly 05 X ducing spctacls bng about a gradual rduction in thgan ofth VR to about 0.7 tms nomal (ils Eghmy 90). causths changs always oprat to mprov stablty of th rtnal magdung had tus, th systm s sad to possss dptiv gin cotrol.

t should b apprciatd that in ordr to disturb th vsua nput associatd with had movmnts in a way that will challng th adaptivcapablity of th VR th optical dvc must mov with th had and notwith th ys anfyng contact lnss (vn assuming suc an optcalarrangmn is possibl) that mov with th ys would call for a changn th gan" of th systm that tanslats rtnal mag ccntricty intoa rapid saccadic movmnt but would not prsnt a nw challng toth VR rtinal mag stablty durng had tus would stll rqur aVR gain of unity



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20 MS & LSRGR

A ay o opcal mans ha bn mployd n a ay of dnanal spcs o donsa adapaly n h VOR all ha n coonh chaacsc of dupng h ual npu asocad wh had mo

mns and al su n gadual adap changs n h gan of h x How cla ha gan s no h ony gulad paam nh O. Fo xampl opcasa o son can c hghy compxadapon ha ac pha as wll as gan onho Mlll Jon9 Mll Jons as 9 Mls Eghy 90) ou und-sandng of h chan opang n uch uaon a pn ud-mnay

THE SYSTEM HS MEMORY Onc an appopa VOR gan has bnachd would claly b adanagous fo h sy o an h ganwhou ndng connual calbaon. A y ha odabl andha h aby o an h mod sa whou nfocmn ad ob ps ha h OR has oy and undgos changs of along nau s dn fo s ably o ndu polongd podays tot a sa fomt tota ass o hamoblaon Robnson 9 Ms Full 94 Ml Eghmy90) Th VOR paculaly abl n noa o lowgan a and

shows no gncan gan chang dung had mobzaon a la fopod up o on wk. Th hghgan sa s omwha mo abhowng om y gaua coy back owad a mo noa ganuny n h absnc o coodnad suasbua xpnc howso consoldaon pocs m o b nold h snc h coybco l s and lss apd folowng long xposus o h magnfyng spcacls

CHNGES RE "SEMIPERMNENT N NOT SIMPL N

STRTEG n h abnc o any bophycal o mophoogcal dncw can only spcula abou h chans subsng hs adap capa-by of h x How h long nau of h adap ganchangs n h VOR ncouags us o bl ha hs sym conansmodabl synapss and ha wl nualy yd nghs no somo h cllula mchansm undlyn mmoy and lang. In hs gad s paculay mpoan o y o sablh ha h adp changs a

pees ude umas (Goso & e oes 1 1, 16a, 16, Gaue& oso 15) mokeys ( & Fue 14 es & Egmy 180) cas (oso 1 evos & Daes 16, ee & 1), as (oew Gooedos 18 1,o a 14 e a 1a) ds (Ge Wama 18) ad s (ca & B1 1)

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LASCITY I VESTBULOOCULAR RFLEX 1

due to geue modicatios" i the asic reex ad are ot due to somemmedate parametrc adustmet resultg oly from some leaed strategy. Such ehavoral" ueces clearly would ot volve ay syaptc

modcatos the reex the monkey there are several peces of evdece to suggest that theadaptve gai chages assocated wth telescopic spectacle expeece reectsemipermaet" chages i the fudametal reex (Miles Eghmy190)

1 Nether he rate of adaptato to elescopc spectacles or the rate ofrecovey followg ther removal speeds up wth repeated exposures asmght have ee expected f the amals had merely ee leg some

strategy hat could e used at ay tme to adst the magude of theircompesoy eye movemets Ideed the changes ga usually pro-ceed a almost machelike way the rate eg vey smlar eve deret dviduals

. Stadard caloic tts of vstuloocular fuctio i the adapted aimals reveal chages resposveess that closely parallel the gachages see with the usual passie oscllato tests ve the vastlyderet cotextual formato avalale to the amal i these two teststuatos oe mght have expected very deret resuls f strategy

specc parametc adjustmets had ee volved3 I the head mmolatio expemets metoed earle to test for

retetio seeral days may have elapsed sce the amal last wore theadaptg spectacles yet ts VOR ga stll retas the adapted state Itseems doutful that the amal would cotue to employ a strategy forwhch there s o loger ay apparet cotug eed

4 The magtude of the shorlatecy compesatory eye movemets geerated y the VOR respose to sudde uexpected disturaces of thehead s smply a fucto of the measured ga of the reex. Eve aelevated VOR ga (followg adaptatio to magifyig spectacles suaected situatos where ero gai might seem preferale eg. itrackg a target that moves with the head reuirg that the amalattempt to keep ts eyes statoary i ts movg head (S Lsergerad F A Mles preparato Thus the short term the ga of theVOR s xed ad mmutale

Ufortuately such tests have ot yet ee carred out i ay specesother tha mokey ad the stuatio ma patcular s fa from clearThe magnitude of the compesatory eye movemets geerted y humasujects he usual VOR test situatio is kow to deped upo thestructos gve to them (Barr et l 1976) Whatever mechasm s atwork here makes t dcult to estmate the ga ofthe asc" reex maad redes the terpretato f huma adaptato data prolematcal



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282 MLS & LSBRGR

STORD TRN? s n sggsd n r VORpton nvolvs h fomton of mmo rs rprsnng spmoor ps t n mt wn t rqs smls ondons

rcr (ollwn Groonors 1979) Ths suggson ros n prt fromt nng pton lt pssv snusol oscllton of td ws rlvl spc for t osclton frqunc s n t vroccsonll t s connud to oscllt t sm frqunc vnwn nml ws sonr n totl drknss (ollwjn Groondors 99) Alog t rqncspc o dpon s lso pprnt n rsus monk (Mls Lsrgr 1980) w v on lookd forut nvr obsvdspontnous osclltons of th s followng ptton wth pssv oscllon n ths specs (F A Mls n S G Ls

rgr unpulsd osrvons 980) Ts s on on of svrlpprn drncs twn ptv gn onrol prosss n tmonk nd t rbb n ohrs wll toh upon lr

D GN ONTO NOM D NONThr s rson o lv tht th dpv gn chngs r hvthrogh h rpolon o nom phsologl procsss nd do norprsn ptholog In norml monk gn nd ps of VOR r

rtvl nsnstv to chngs n stmulus mpltud n frqunc tlst ovr th rng of 0. 1 to 1.0 Hz) bcus ths contnus to b trufollowng dptton o lscopc spctcls t sms tht th nchrrssof h pt r rlvl norm wh rnorsh h w r dlng wh pr gn cngs nd mnml sd cs(Mls Eghm 1980). In fc sms rsonl o ssum t hcllng of tlscopc spctacls s mt ultn dptv mcnsmswos norml vr functon s longtrm rgulon of olrstl w r not dng wt lborto crost It s lso clr tht

pv pl s no jus ftr of h velopng nrvos ssmnd m vn rn hroghot lf (Gonshor Mlvll Jons 197)

STE OF THE MOFL ELEMENTS N THEVOR

If th ptv gn control mchnsm n th VO s o ontbu to ournrstnng o h lllr mhnsms nrlng motor lng n th

nrl nrvos ssm r s mos rgn nd o loct th s of ts

modl lmns Lrgl s rsl of t work n wrtngs of Io1970 1972, 1974 1977)nrst s cntrd nll on th vslr prof t crllum.

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PASTICITY IN VSIBUa-OCUA FX 283

The Cerebear Hypothesisto pplied he he genel M-Als eeell model o moto leing (M 9 69, Als 1971) to the spi se of he VOR Bsed on his

knowledge of he ntomil ngemens in this sstem in the it, Itodeveloped the ide of the vestil eeellm moe pill, theolss sideloop of the VOR tht migh t s he vle ginelement in he ssem Ths, he envisged h he eeell oil newoks, ing vestil signls oiginting fom mosse inps,wold ontin modile snpses whose e ws nde liming-eontol. Fthemoe, he eognized the tilit of the etinl imge slipssoied wih eh hed s poenil eo signl th he sstemmigh se to gide dpion, nd he sggested th the liming esmight, heeoe, nsmit visl inormtion he sseqen nding tht,in he i t les, he liming es not onl eived visl inptsMw Simson 3) we dietionll sletiv Simson Alle 197), ws niel onsistent with he hpothesis. Howev, he mjoevidene tht sstined he plsiilit o his hpothesis ws the eet oeeell lions in ll o the speies emined, lesions of h eeellmht inlded the vestil portion eslted in loss o sevee deit indptive gin onol in the VOR (Io e l 1974, Roinson 197, Shie

nnt 98 Optn l 98) Howev en singl nit sdis inthe monke ols ge stongl ginst this hpohesis in his speiesnd sggest letive eplntions fo the lesion dits

THE PRIMATE FLOCCULUS: NORL PHYSOLOG In ode to eview this eent videne sisftoil i is st neess to stlish thenorml phsiologil ole o the ols In the monke, the ols ismh moe thn sideloop of he VOR. Single ni sdies o the ivitht origines om mosse inpts (isege hs 198, Miles etl 1980), vel tht, in ddition o ing vestil signls enodingngl hed veloi (mesed with espe to the sondings), isPinje otpt ells (P-ells) lso dishge in eltion to ee veloit(mesed wih espe to he hed) In t, these wo omponents o Pelldishge e, on the vege, of simil sengh, hve the sme dietionlpfn, nd sm lgeill to eeivel node ge vloi (movemen of he ees with espe to he ondings)

Sine the monke's VOR gin is noll lose to nit, its gze veloitdng hed ts is lose o zeo nd he P-ells in he ols show litle

ifn modlion of hei dishge. hs, these P-ells noll melitle o no onion o the VOR. In f, ppeile modlion of heivi of hese ells is vident onl wn he niml tks moving tges;rhermoe, eing eled o ge veloit, this modltion is elivel



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284 IE EGE

ndpndn o whv omnon o y nd hd movmns hmonky ops o s Lsons o h pm os s n g dsn ps h oghy y sv whh h nm mps o

mpoy movmns o s ys on o n omnon w hd movmns 178; s s onssn wh d h hs P-snomy non o oos h pomn o h smooh kng sysmy onng gz voy sgn

In Fg 3 w hv nopod hs gzvoy Ps no hsgn ow mod o h O nd ps sysm psnd hhd voy omponn o P- dsg sms o vs n onnd s ongd n h mod s p of n nhoy sdoop o hvsoo phwy whs h y voy omponn s ssmd

o d o h moo ommnd o mov h ys hogh my som n np nd s ongd s p o posvdk ooph sn o h hs ong n pdd y hons nnpon odng h ps sys Fnd Ny 1 61 Fnd 6Yong 1 68 onson 11) nd posvfdk s ommony

mpoyd y ngns o oos h gn o ngv-dk ono sysms Howv s dsssd monkys on ompsh pssks wh omnd yhd movmns ssng p o h ymovmn wh hd movmn I s n hs son wh h o

omponn o ps nd n y-voy posv-dk ooshogh h os) s dmnshd h h vs hd voyomponn o P dshg pys o n h poss mksp o h dop n h y voy omponn Ths nss h h opom h os onns o povd h sm g voy sgn nsppo o kng whh h hd s sony o movng I w so ppn fom Fg 3 h vs omponn of P- dsgvy ops o on-n h nsm vs dv gnd y h hd omponn of h kng gs

In smmy h pm os dos no nomy on sgnny o h gn o h O s ond h wh oosng h gnof h ps sysm sn hs oos s n h fom o gz voy sn ps sys ds n no wh onon of ynd hd movmn h nm hooss o dpoy

HE PRIMAE OCCUUS VOR ADAPAION Ahogh hsom h pm os dos no op n h shon

nvsgd y Io 2 o h mg s onn modmns ssvng dpv gn ono n h O In h sgn owdgm n Fg 3 s vdn h gn o O s ydpndn pon h gns of sv mns dsgnd A nd


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LASICIY IN VSIBULOOCULAR RLX 28 5

II

I'

e!+ --- Eye _;

IIII

Fu Bo daga o e VO and pus sysem ncorpoang e gaze eoyPces n e occs Cuu denoe sgna ow cannes wn e nevossysem; diiuu i epesen eea, pysca ns denong e eoc wspc o e wod (w) eye veocy w espec o e ead eye oc w spc h wld a vlc) and a vc wh sc h wod A B Cand D epesen gan eemens and 'b denoe e ead veocy and eye veocy npsespcvy h Pces n h ccs whs dscha dlans cvl ncd avlc ).

n e re an one or more o wc m be "modabe e oown sme eression dsrbes e ain o e O

an RCD A

- B 2.

n nceae n e an e R be aceed b nceae n D, B and/ a deceae n (Ne a e an e eex a aneae ae snce s op oppoed n decon o s np)

Sne n ecdn n e pae cc (e e a 80a) aeeeaed a e aeae en e ead ec (eba sncarred b e Pces ares w e an o e O Adaaon oann pecace nsance was asocaed w an ncease n eaeae an cpnen wc wa e cpaabe n ando e nceae n e an o e R. In Fe e en o eeba na ecded a e Pce depend pn e an eeen and Hwee . w a an nceae n e an eeenA n e ocs wod operae o decrease e R an; wod benecessa o noke addna canes de e occsn eeen



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28 6 IE & IBERGER

to achieve the obseved increase in VOR gain n that case element Dwould be popey egaded as the modiable element subseving adaptivegain control in the ee f on the othe hand the changes ecoded at the

-cell wee due to modications in element thn the occulus and thebrainstem relay would both receive a vestibular signal of changed gan;such modcations would therefore account for the observe increasesin the gain of both the VOR and the vestibula component of celldischage lthough the available data do not distinguish between the twopossibilities it is nonetheless clea that the modiable elements subseving VOR gain changes lie outside the occulus (elements and/or D inigure 3).

t will be ecalled that these cells nomally conribute little to the VOR

thei acivity being only vey wealy modulated duing head tus and unitecordings reveal that this remains true in the adapted animals at least inthe high-gain state he incease in the magnitude of the comensatory eyemovements couped to head tus in the high-gain animal means that theeye velocity input to the -cell associated with a given head tu will beproportionately higher than normal however this potential threat to theusua aance eeen ea an eyeeocy sgnas a e ce s oseby the aboveentioned concomitant increase in the Pcells' sensitivity tohead velocity hus the inceased eye velocity input to the occulus which

is due diectly to the increase in the gain of the VOR is countebalancedby a roortional increase in the hea velocity inut he net result is thatthe P-cells continue to show little dischage modulation during head tusin the adapted animal and hence continue to make little contribution to theVOR

f the obseved changes in the cells vestibula signals ae not esponsible for the change in the gain of the VOR then it is pertinent to ask whatupose hey accomlish n fc fsuch changes dd not occu the occulus would be less eective in cayng out its important supporing role

in combined eyehead tracking t wa pointed out above that the vestibularcomponent of Pcell discharge is imortant in countebalancing the vestibula dive geneated in the baintem by the head component of thetacking maneuve ccodingly ay changes in the "gain of the brainstem vestibular signal should be mathed by coresonding changes in the"gain of the occulu estibular sinal: the one should be regulated inharony with the other n summary the changes in the vestibular sensitivity of the cells ae a seconday consequence athe than a pimaycause of the change in VOR gain ad these changes enable the occulusto continue to provide appopiate suppot fo the pusuit system duinghead movements in the adapted anial


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LAICIY IN VIBULOOCULAR RFLX 287

OCCUUS RECORDINGS IN OHER SECIES It ha bn rortdthat th c in th rabbit' occulu chan thir dichar odulationdurin ocilation in th dark in aociation with han in th ain of th

VOR Dufo t al 1978a Ito 1977) nforunatly th inal ontnt ofth ll in th rait oulu ha not n dtrmind hn thtioloy of th rcordd chan i uncrtain In particular, it i not knownif th l ar lik tho in th riat and arry an yvloity inalAt th rnt ti, thrfor it i not oibl to artain th funtionalinican ofth ndin

WH DO OCCUUS ESIONS COROISE ADAIVE GAIN CON-

RO? It i rtinnt at thi point to ak why oculu lion, vn in

th at, liinat adativ ain control in th VOR o ctivly if aw art abov th inl unit rcordin vidnc i aaint th viw thatth occulu of onky contain th modiabl lmnt On poiilityi that th known dit in th anmal' uruit ytm undrin itaility to taili th rtinal ima n throuh th tlop ptalo vrly a to ctivly dirut th adativ chani In thi vnt,th lo of adativ capability i condary to an oculootor inucincyA cond, and in our vw or lik, xlanaton i that th output froth occulu i iortant in th induction of th modiations undrlyin

adativ an ontrol in th VOR pathway i it provid al or part ofth rror inal uidin raliration of th r Mil t al 18a). Whall rtu to thi point in o dtail blow

iilar planation iht b advancd to xplain th liination ofadativ ain control in th VOR by olivary lion that dtroy th limin br input to th occulu Ito Miyahita 17 5 Haddad t a198)It ha rntly bn hown that dtrution of th limbin br in th

rabit ha a draatic t on th tart 1l, whih lo thir utoaryinhiitory ation on th vtiular ray l in th raintm Dufo t

al 178b, Ito t al 1978, 1979b) Thu, lion of th oliv ay b xctdto iic lion of th oulu

The Brainsem ypohesisIn th onky all of th rtinnt vidnc ut that th modiallmnt undrlyin ain han in th VOR ar not in th oulu Milt al 198a). Thi and th fat that VOR ain han ar vidnt in vnth hottlatncy vtibuloocular ron that follow uddn diturbanc of th had S. G Librr and A Mil, n rparation) focu

nw attnton on th brant an ut that th odabl lntihtvn b found in th dirct VOR pathway havin only two or thr

Annu.

Rev.Neurosci.1981.4:273-299.



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288 MLES & LSBERGER

ynap hmo h adapaon p o h VOR hn onmgh p ha n gnal h nal hang wold o a an aly

sg n pw or pons w or sgnls rld o

gnaon o oh knd o y movmn a nodd I wold mponally mo dpv o h modabl lmn o b load n hopa o h pahway ha a had wh oh ym W am aall ha h oh ym dd no om nd any adapv powv ompllng hogh h agmn may m n vdngg ha om nonvbla olomoo onol gnal a odrog s modl gn lmns (Lsrgr al 180) Indd o VOR gn ngs on os qn msrs o olomoorpoman ha vald om nw ap o h nal oganaon o

h olomoo ym

ONVRGN O OOMOTOR ONTRO GN BVO NTOMY Poplaon d amnng h vbla nvy o mla anal pmay an and o ll n h malslr nl r nps rom s rns ld oval any vdn o gnan nal hang aoad wh ooldhang n h gan o h VOR (Ml Baman 180 bg Ml180) s mpls modl lmns ms l ond rs

nrl snps n VOR pahway owv gnally amd hah opokn and vbloola ahway onvg a h lvl o hondod non and dhag lad o opokn maonhav bn nvly domnd n h v ll o h mdal vblanl ha w nad by VOR adapaon (Wap & nn 177) Iollow ha h gnal ponbl o all o pa o h opokn rspons

sold sr h modl lmn nd ngs n VOR gn sold ompnd prlll ngs n gn oh opon rsponss

omplaon h ha a alady mnond n an al on

h pma ha wo val ablaon mhanm h p and opon ssms o r og o opr n sl opons son whn omay o od h y movmn ld bya onnolymovng val ld ahvd ondng h anmalwh a oang pd ylnd h lng opokn nyagm on o mooh akng y movmn n h don o h n movmn npd a nval by a, ng aad n h oppodon Smooh y vloy how an nal apd ha la o a whndd mllond ollowd by a m mo gadal na ha m

10 o 15 s o r smpo on 1 177 Rpn 17)I hogh ha h apd hang a d manly o h p ymwha h bqn low hang a d o bldp n a vloy

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.Rev.Neurosci.1981.4:273-299.Downloadedfromwww.annualreviews.org

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PASY N ESBUaOUA EFEX 28

toage ecan tat epeent te optoknetc yte pope (Zee et a1 6, begeet a1 80. If te gt ae extngue afte t buupa ommene ten te ntagmu t a otoknet aftetagmu

(OKAN te nta ntenty of wc ume to be a ect nex ofte "optoknetc comonent of te o epone (Rapan et a 1 bege et a 1 80.

Cange n te gan of te VOR ave been own to eut n aatcan aot opotona cange n te ntenty of te ow "otoknetccoponent a ncate b te nta OKAN veocty but not n te fat"uut eone (bege et a 1 80. Tat te cange n te "otoknet oonent o nea moe toe n te ga of e VOR content wt te vew tat tey ae a econay coneuence of te atte

an tat te oabe eeent ae o te ot pat ocate n te atetage of te vetbua patway tat ae ae wt te optoknetc yte.e fae to ee cane n te "uut omonent of te otonetceone uggst tat te a vng t o not ae te na ocuomoto patwa toug te oabe eement

Tee new ata ave been ncopoate nto ou gna ow aga nFgue 4 In keeng w e auent ae n te evou ecton teptatve oabe eeent ae ocae at C an D n te bante Teoptoknetc gna ut convege on te vetbuo-ocua patway above te

eve of tee eement an te puut gna at ome ate tage Howevene ouu son ave a evatatng eet uon te gan of ursut (Zeeeta11 8 an te "uut coonent of te optoknetc eone (Otcan et a 1 80 tee eye oveent ut be eate by nput tatconvee on te VOR atway befoe te eye veocty na fe backto te occuu.

OER SPECES ata fom ote pee peent a omewat eenttue. Kee & Pet (1 ave eote gncant cnge n tevetbua entvty of ce n te cat ea vetbua nuce n aocaton wt cane n te gan of te eex At eent t not cea f tappaent eence between cat an onkey eect a genne peceeence o ome etooogca ncontency urteoe atougange ave been eorte n te otoknetc eone of te abbt naoaton wt aatve ange n te gan of te VOR (oewn &Kenct 1 5 oewjn & Gootenot 1 tey apea to avea vey eent etoogy fo toe n te onkey Weea te cangen te ate otoknetc eone wee vewe eey a a eonaryconeuence o te vaabe gan eeent beng n te ate e oonof te optoknetc an vetbua patway te cange n te abbtotoknet eone wee vewe a nepenent of te gan ange n te



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290 IS & ISBRGR

'

-'

--l.-L_ iure 4 Block diagram of the R together with the "pursuit and "optokinetic visualfback systems. Ciuu e denote sinal ow channels within the nervous system;uu repren exern phycl ink denin hed veli h ec the world , eye velity with rpt to the head eye velocity with rpt to the worldi gz velcity), target velity wth rpt to the world ) and vety o the vsualsuound wth rpt to the world ()

etbul ytem u, n te bbt egdle of ete te gn of teVOR ineed o deeed, te optokineti ytem lwy owed ignint inee in gin ine te optokineti yte i negtiveeedbkmni, u ineae in gin ould ly opete to impove teyte' peorne nd ene old be egded "dptive. t idult to genete onnng tellogl gument to jutfy te needfo u "dpte mpoement ne it not le y u ytemwould not be libted optimlly ie mimlly) t te outet of te

epeiment Hoeve, befoe eptig tee dt yet ute doumenttion o peie dieene, it old be noted tt, in te pite tudie,optokineti epone wee eed uing polonged unidietionl timultion wee in te bbit tudie, iuoidl tiuli wee ued. urteomplition i tt wen oionly bot teting teniue polongedunidietionl nd inuoidl) wee ed in te bbit tudie, tey geonty nwe ollewin & ooendot 1979)

NTUE OF THE VO GN O SGNL

ute libton of te VOR ue elble "eo nfomtionbout it peorne aledy poited out, any otoing in te gin


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AICIY IN VIUOOCULA RF 29

f e VO reu n eren rena urng ea u Of curee ye cann ane an er fr rena ane an reae n e ay e ngng ea veen T recna

rean beeen e an e ea veen eay ncae erecn n c e VO gan nee cange aceve beer ageaban and e f e aave ecan erve er errrnfran fro a carn f vua an vebuar u I 2Rbnn 6 nr & Mev Jne 6b. e uae eenencyn vua an vebuar nu ceary bgae nce ey ane rvenfan e cenra nevu ye a eae recy e exerna eference uunn eve nee n ean ae ye neceary ue vua an veuar nu er e guecabran: any reabe cenra crreae f e ae g eve euaye.

Sbsttts for Vstblar (Had Vlocy) Snals?In an ana ke e rabb a never rack vng bjec eyevece are ue ey cenae fr ea veen an eraeaay abe e eye reec e anary urrunng Inuc a ye eye vecy gna cu ubue f ea vecy (vebuar gna aceve aave VO gan cange Wen e rena n e ae recn a e eye veen u ncae a e eyevecy a n arge enug a uan a cu be reee y ncreang e gan f e VO cnvere f an eye vecy are n ngrecn u ndcae e nee fr a ecreae n e an f e VOere evdene a nee e u ean n e abb .e.e reguae varabe an eye vecy gna raer an a ea vecygna. ca uan can erey an ncreae ecreae n an e VO (e.. anfn r reucn eecc ecace

ecan u eae araey an be nnguabe fr neervng errr nfran fr rena an ea vecy gna. ever ca uan rducng ef-rg rrr revea f e vuanu ave rve be reveang. Wen e rabb a aveycae en & ren ( berve a fr e r ur e an f e VO ecreae bu eeae e a graua an

cnen ncreae Un exang e gna eye veen recrey berve a fr e r ur e ana' cenar eeveen n e g ee aenuae an nay rece bu ereaf

er e revera u ag e ecna rean beeenrena an ea veen reane uncange rugu e recna rean beeen rena an eye veen uneren arevera a cnce e evea n e ecn f e VO gan



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9 & BRGR

ag W slip ad y moms w i opposig diios hV gai dasd wh h wo w i sm diio i iasdFu id ha h loiy of ys a a of h ad was

h a paam was h dmosaio ha h ga of h abbisV old b id mly by pologd po o siuoidal opokii imlaio wih ad xd poiio i ad mom ao ay ollwi Goodo 199)

Pologd opoki simulaio is also kow o ias gai ofh V i s Sai & 198) bu is ii i mokyMils & isbg 1980) umo passi osillaio of moky lfigh sig pism uls i a das i V gai oug ompsao y mom sow ois al" i ligMils Eigmy 1980) Ts h adapi maism i mokyspods o sdisio siuaio i sam way a i spodso duig spals; a bo opial siuaios sa h sam kid oflaioship isofa as slip ad ad loiy a od, wil diigi gad o lp ad y loiy ida o o a y omp a ila I h mok hfo all of h aailab idi ois wi iw a ym s so di masu of adloiy o ddu os i h ai

utitute or Retinl lip inlspi ou oio a h oulus is pobably o si of hmodiaios udlyig hags i gai, lio daa bli olu-io a h pima oulu ha o ol i adapaio Idd lsios of ols ha a fa mo pooud o h adapi apabiliyof h pima pia al 180) a was pod i ogialsudi i h a a a so widly id i fao of blla yposis obiso 976) his lads o h oposiio ha h pma oulusg play a idi ol i poduig ags i V gai hispoi i boms say o ask w adapi gi ool maism uss ial slip sigals p s o guid alibaio o subsius somliabl al ola paiula ould a gaz loiy sigal su asha odd by Plls i pima oulus poid suh a olad so fuio o gua VR ga?

W suddly ofod wih sy magifyig lopi spals omal moky m a pi ysm dig ad o supplm is ow iadqua V i amp o abili shifig imags s ough spals Tu allg of l

sopi spals is iiiall m by pusui sysm a impoa paof wi is ga loiy sigal oibud by h oulus Plls Z a1 198 isbg & uhs 978, ls a 980b) So log as h

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AIIY I EIBOOAR REFEX 2

gain is inapproprae for he new visual condiions, reinal slip will pesisduing head us and wih i reliance upon he pursui sysem and hemodulaion of he occulus P-cels' discharge. Indeed he exen o which

pusu is consisenly used durng head us is iself an index of he"eo in he O nd he ssocied dischge modulaion of the gazevelociy Pcels migh be used by he adapive mechanism as subsiuefor frank visual signals

An undeying ssumpion hee is ha so long s he nimal mus employpursui durng head us, hen is O gain mus be in need of adjusmenIn some as e undened way, he resulan modulaion of Pcel discharge,if persisen nd associaed wih vesibula siulion is ssumd o induceappopiae changes in he modiable gain elemen I will be ecalled ha

he discharges of he gaevelociy Pcells modulae consisenly durnghead us only when he O is inappopiae fo he visua condiionsn cese when dion is complee (Miles e l 1980a) Suh ehaoris enirely consisen wih he view ha hese ells signal O gain error

The idea ha he modulaion of gae velociy Pcell dischrge duinghead movemens may be sucien o induce O gain changes eceivessome indirec suppor from ecen expeimens involvng only foveal pusuiages (Miles Lisberger 80 Wae-depived monkeys wee einfocedwih uids for xaing a small dim arge presened agains ohewise oally

dar surrundings aers wee aranged so ha durng he perods ofxaion, he money and he arge wee moved eihe inphase or 80 ouof phase o mimic he gae veloiy evens, and presumably also he Pcelldishage modulaion, nomally associaed wih weaing mgnifying oeducing elscopic speccles his esuled in adapive chnges in hegan of he VO equ o muh 50% of he hanges pduced y anequivlen amoun of expeience wih elescopic speccles hese nngsae consisen wihhough hrdly pure es ofhe hypohesis ha heerror signal guiding ecalibaion of he O is in par he modulaion ofgaevelociy Pcell dischage; i is ceainly clea howeve, h appeciable gain changes ca be obseved in he absence of peiphel einl slip

Noneheless, some inuence of visual inpus clearly seems o be indicaedand he "eror in he O would seem o be a combinaion of einl slipand gae velociy signals In fac, i is possible ha he occulus Pcellsprovide boh signals, especially since here is evidence ha some of hesecells discharge in elaion o moion ofhe visul suoun (o uuki7 Wai e al 7) his would lso help o explain he exemesevery of he decis in adapaion following oulus lesions ll of heavailable evdence conceing he role of he occulus in he adapiveconol of he primae O including single uni ecodings, lesion daa,and even he abovemenioned longem eecs of pursui on he reex, are

Annu.

Rev.Neurosci.1981.4:273-299.



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24 MLS & LSBRGR

onsistent with the notion that the oulus proides the error signal thatregulates the gain

Adpe Gn Conrol n he Prme OR A NewHypoheWe hae proposed that the modiable elements mediating adaptie gainontol in the pimate VOR ae a loated in the bainstem pathway and(b) reulated by error sinals eneated at least in part by the oulusPells t remains to link these two ideas into a plausible single hypothesis

n our sheme (igure 5) the aze-eloity P-ells hae been assignedtwo quite separate untions with but one pupose to improve the stabilityothe retinal image. s a part o the pursuit system their disharge modula

tion has an immediate inuene upon their target neuons through onentionl (inhibitoy) synapti mehanisms s a pat o the system egulatinVOR in their pesistent dishare modulation duin head tus indiates errors in the VOR and has a longterm inuene on the eay osynapti transmission in the estibuo-oular pathway

impotant eature o ou hypothesis is that the Pells exet thei twodierent inuenes at two dieent points in the vestibular pathway inethe gain o the pursuit system is vey sensitie to lesions o the oulus butnot to VOR ain hanes we assume that the Pells shottem synapti

ation in support o pursuit is exerted down-stream o their long-termmodulatory ation n at in our seme the Pells longterm inuenemust be exerted aboe the point o whih the P-ells derie their ownvestibular input his is assumed to be at C in iue 5 though parallelhanges at and D whih would be operationally equialent albeit moreomplex nnot be ruled out. t is vital o the untioning o ou modelthat thee be reipoal onnetions between the Pells and the vestibularrelay ells in the brainstem and that they be oranied in essene as aninteal negatieeedbak loop that i oneed with longtem regulation

rather than with shortterm ompenstion hus we enisage a loal eedbak loop opeating (vey slowly) t ahieve eo modulation o P-elldisharge duing head tus persistent modulations o Pell dishare("errors) indue hanges in the gai o the estibular input that in tuoperate to redue those modulations he sinle unit data show that theoutput o the Pells is indeed reglated in this manner and produsinimal disharge modulation during head tus in the ully adapted state.he problem now is to eplai how a ontrol loop that is entiely intealand untions to eulate P-ell dishae an at the same time eetiely

ahiee an appropiate VOR gainn the example that ollows it will be seen that the ruial ator is the

eye-veloity input to the Pell this sinl is assumed to etain a eliable


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LASICIY IN VSIBULOOCULAR RFLX 2 5

r--- - -- --- ---- ---- ---,

: hwI

+ ,t _"

Figue Block diagram of the VR and the pursuit system, indiatng the hypothesizedlong-tem reguato nuene of the gaevelity P-ells (broad stippl aow) on thepostulated modiable gain eements in the etibular pathway (element C Cuu liedente signal ow hanes within the neous system; diiuu le epent exteaphysial Jns denoting head eloity with rspet to the world eye eloty wth resptto h had (eJ ye eloit with rpt to te world gaze eoity) and target eloiywth rpet to he word

cnan en eye vecy (en a cu be aceve byan nea neave-feeback newk wn e ceeea cex an ve e nea ana aan wc eveyn ee u be cabae

Cne e can f even e n n wen e na nkey wea anfyn eecc ecace. nay ee cneae e

na un ea u an e uu ye ake n e eaeenby f auenn e cenay eye veen eneaey e nw-naeuae VO. In e ccuu ee a an eevaeeye vecy na nu e Pce we cae a a cneuencenw uae n ea u n eec eye vec na ePce exena efeence an ee w any vua nu a eyay a eceve (n ncae n Fue 5 ve e P-ce ny nk(abe nec va e uu ye w e exea vua w. If enkey cnnue wea e ecace e een uan f P-ce

cae ue e eevae eye vecy na nu aue nucea aua nceae n e an f eeen T wu eu n ( anneae n e an f e VOR wc wu auay anfe e buenf enean aecena eye veen f e uu ye



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6 IES & SERGER

o h V and (b) an nra n h had voy gna nu o houu P, whh woud ora o o h augmnd voygna and, hn graduay rdu h P dharg moduaon W

aum a h ro woud onnu un vnuay h P arrvng hadvoy nu ha on mor baan hr y voynu dung had u n h g No ha a a m dung hadaaon, P dharg moduaon w b mnma dung had un h dar Whn VO gan bom arora for h vua ondon,had u n h gh w b aoad wh h am omnao yvo a had u n dar ad moduaon of P darg wb mnma on, w hav om fu r: h ronb forgnrang h nowargr omnao y movmn ha hfd from

h uru ym ba o h vbuar and h rror ga (Pdharg moduaon) ha rud o ro

SURY

vuoouar r unon o rvn had movmn rodurbng rna mag by gnrang omnaor y movmn oo h had movmn n h mnyh many undr on

draon hrh r mahn and vry v n h horm, h VO ora a an ono onro m whou h bnof fdba and oman d and mmuab No mar whaa of had oordnaon h anma u o vw a obhr a onnung nd for h VO and onnu o ora howv,houd h VO onny fa o ab h rna mag durng hadu, w graduay undrgo ongrm adav gan hang ha ror ha aby h adav aab uma dndn uonvon, and a vay of oa dv ha durb h vua nu nomay

aoad wh had u hav bn ud o ndu arg hang n hr nofar a h mony ond, a of h avaab vdnugg o u ha h modab mn undryng h ongrmadumn ar oad n h branm vbuar ahwa and no, arvouy uggd by ohr n ouar ob of h rbumHowvr h ouu do aar o hav an moan nduv ro nh adav ro rovdng a a ar of h rror gna gudng hongm admn n h bran n our vw, h VOR a auary wdnd am of a a ym and rom o b a mo

ufu mod for udyng h uar mhanm undryng mmory andang n h nra nrvou y


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