Extending models of hippocampal function in - Gluck

M E M O R Y , 1 9 9 7 , 5 (1 /2 ), 1 7 9 ±2 1 2

E x te n d in g M o d e ls o f H ip p o c a m p a l F u n c tio n in A n im a l C o n d itio n in g to H u m a n A m n e s ia M a rk A . G lu c k a n d B ra nd o n R . E rm ita R u tge rs U n iv er sity , U S A

L in d sa y M . O liv e r G la sg o w C a le d o n ia n U n iv ersity, U K

C a th e rin e E . M y e rs R u tge rs U n iv er sity , U S A

A ltho u gh m os t an a ly se s o f am ne si a h av e f oc u se d o n th e lo s s o f e xp lic it d e cla ra tiv e a nd e p is od ic m e m o rie s f o llow in g hip p o c a m p a l-re g io n d a m a g e, c on s id e ra b le in si g hts in to a m n e si a ca n a ls o b e re a lise d b y s tu d yin g hip p o ca m p a l fu n ctio n in si m p le pr o ce d u r a l, o r h a bit-b a se d , a ss oc ia tiv e lea r n in g tas k s . A lth ou g h m a n y si m p le fo rm s o f a sso c ia tiv e lea r nin g a re un im p aire d b y hipp o c am p a l d a m a ge , m o re c om p lex tas ks w hic h r eq u ire s en s itiv ity to un r einf o rc e d s tim u li, c on fig u r atio n s o f m u ltip le st im u li, o r c o n tex tua l inf o rm a tio n a re im p a ired by hip po c am pa l d am ag e . In se v e ra l re c e nt p a p er s w e h av e d e v elo p e d a c o m pu tatio n a l th e o ry o f h ipp o ca m p a l fu n ctio n w h ich ar gu e s th a t th is b r a in r e g ion pla y s a c ritica l r ole in th e fo rm a tio n o f n e w st im u lu s r ep r es en tatio n s d u r in g lea r nin g (G lu c k & M y e rs, 1 9 93 , 1 99 5 ; M y er s & G lu c k, 1 9 9 6 ; M y e rs , G lu c k , & G ra n ge r, 19 9 5) . W e ha v e ap p lied this th e or y to a b r o ad r a ng e o f em pirica l d a ta f ro m s tu d ie s o f c las si ca l c on d itio n in g in bo th in ta c t a nd h ip p oc a m p al-le si o n e d an im als, an d th e m od e l c o rr ec tly a c co u nts f o r the se d a ta. T h e c la s si ca l c on d itio n in g p ar a dig m c a n be ad a pte d fo r u se in h um a n s, a nd si m ila r re su lts f o r a cq u is itio n a re o bta in ed in b oth n o r m a l a n d h ip po c a m p ald a m a g e d h u m a n s. M or e re c e n tly , w e h a v e b e g un to a d d re s s a n im p o rta nt se t o f c ate go ry le ar nin g st ud ie s in b o th n o rm a ls a n d hipp o c am p a l-d am a g e d a m n e si cs . T his w o rk in te g ra te s e x pe rim e n ta l s tu d ie s o f am n e si c c a te g or y le ar nin g (K n o w lto n , S q u ire, & G lu ck , 1 9 9 4) w ith th e o re tica l a cc o un ts o f a sso c ia tiv e le a rn in g , a nd b u ild s o n p re v io u sl y e st ab lish e d b e ha v io u ra l c or re sp o n d e n ce s b e tw e e n a nim a l c on d itio n in g a nd h u m a n c a te g or y le ar n in g (G lu ck & B o w e r, 1 98 8 a ). O u r w or k to

R e q u es t s fo r re p rin ts s h o u ld b e se n t to M ark A . G lu c k , C e n t er fo r M o le c u l ar a n d B e h a v io ra l N e u ro s c ie n c e , R u t g e rs U n i v e rs it y , 1 9 7 U n iv er si ty A v e n u e , N e w a rk , N e w J e rs e y 0 7 1 0 2 , U S A . E m a i l: g lu ck @ p a v lo v .ru tg ers .ed u o r s e e w e b p a g e w w w .a rc h ty p e .c o m /g l u c k T h i s re s e a rc h w a s su p p o rte d b y a n N IM H N a t io n a l R e s e a rch S e rv ic e A w ar d 1 -F 3 2 -M H 1 0 3 5 1 -0 1 (C M ), b y a M c D o n n e ll- P e w F o u n d a tio n fo r C o g n itiv e N e u ro sc ie n ce G ran t-i n - A i d (M C & C M ), a n d b y t h e O ffi c e o f N a v a l R e s e a rch th ro u g h t h e Y o u n g In v e s tig a to r p ro g ra m (M G ) an d g ra n t N 0 0 0 1 4 8 8 -K -0 1 1 2 (M G ).

Ó

1 9 9 7 P s y c h o lo g y P re s s, an im p rin t o f E rl b a u m (U K ) T a y lo r & F ra n ci s L td

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d a te illu st ra te s s o m e in itial p r o g re s s to w a rd s a m o r e inte gr ativ e u n d er st an d in g o f h ip p oc a m p al fu nc tio n in b oth a n im a l a n d h um an le a rn in g , w hich m a y b e u se fu l in g u id in g f u r th e r e m piric al an d th eo re tic a l re se a rc h in h u m a n m e m o ry an d a m n e sia .

1. IN T R O DU C T IO N In sev e ral rec e nt p ap e rs, w e h a ve a rg u e d th a t th e h ip p o c am pa l re g io n p lay s a n e sse n tial ro le in the form atio n o f no v el stim u lus re pre se nta tio n s in the form atio n o f n e w asso c iation s a n d m e m o rie s (G lu c k & M y e rs, 1 9 9 3 , 1 9 9 5; M y er s & G lu ck , 1 99 6 ; M y er s e t al., 1 9 9 5a ). A s sh o w n in F ig . 1 .1 , the hip po c a m p al reg ion c o m p rises a gro u p o f stru c tu re s lo ca ted d e ep w ithin th e b rain , a n d in c lu d e s th e h ip po c am p us itse lf a s w e ll as the ne a rb y d en tate g y rus , su b icu lu m , a nd e n to rh ina l c orte x. T he ou term ost of th es e stru c tu re s, th e en to rhin al co rte x , re ce ive s h igh ly p ro c e ssed in fo rm a tio n fro m th e e n tire sp ec tru m of se n so ry m o da lities, a s w e ll as fro m m u ltim o da l c o rtic al a sso c ia tio n are as. In fo rm ation flo w s in a rou g h ly u n id irec tio n al fa sh io n fro m the en to rh in a l co rte x to th e d e nta te g y ru s, to h ip p o ca m pu s, to th e sub ic ulu m , an d b ac k to the e nto rhin al

F IG . 1.1 .

S c h e m a tic o f m a j o r in fo rm at io n flo w p a th w ay s i n th e h i p p o c a m p a l re g io n . H ig h ly

p ro ce s s e d , m u ltim o d al in p u ts e n te r e n to r h i n a l c o r te x , a n d p ro c e e d in a la rg e ly u n i d i re cti o n a l p at h w a y t h ro u g h t h e h i p p o ca m p a l fo rm a ti o n (d e n t a te g y r u s , h i p p o ca m p a l fi e ld s C A 3 a n d C A 1 a n d s u b ic u lu m ) b e fo r e re tu rn in g to e n to rh i n a l c o rt e x a n d th en c e b a c k to th e s a m e c o rtic a l a re a s w h er e th e y a ro s e . T h e re is a ls o a b i -d i re ct io n a l p a t h w a y th ro u g h th e fo rn ix c o n n e c tin g th e h ip p o c a m p u s w i th s u b c o rti ca l a re a s s u c h a s th e s e p ta l n u c le i . M a n y o th er c o n n e c tio n s e x i s t in ad d itio n t o t h e m a jo r o n e s s h o w n h e re .

H IP P O C AM P U S A N D A M N E S IA

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c ortex b e fo re retu rn in g to the sam e se n so ry a rea s w h ere it orig ina lly a ros e. In a dd itio n to th is b asic p ath w ay , the re a re a la rg e n u m b e r o f d ire c t co n n ec tio n s b etw ee n th e stru ctu res o f the reg io n . T h e h ip p o c am pu s h a s an o th er inp u t an d o utp u t p a th w a y th rou g h th e fo rn ix, a fib re b u n dle co n n ec tin g it w ith sub c o rtic al stru c tu re s (e.g . b asa l fo re bra in) w h ich m o d u la te h ipp o c am pa l fun c tio n in g . D am ag e to the h ip p o ca m p a l re g io n in h u m a n s p ro d uc es a ch a rac teristic a n te ro g ra d e a m n e s ia sy n d r o m e , s tro n g ly im p a irin g th e le a rn in g o f n e w inf orm atio n (S q u ire , 1 9 87 ). H u m an h ipp o ca m p al d am ag e ca n resu lt fro m a v ariety o f e tio lo gie s, ran g in g fro m isch e m ia , v ira l e n ce p h alitis, a n d a n eu ry sm / e m b o lism to th e a rte rie s th at v a scu larise th e hip p o ca m p a l re g io n . D a m a g e to o th e r re lated stru ctu re s, su c h as the b a sal fo re b ra in , c a n a lso re su lt in a n a m n e sic sy nd ro m e w h ic h sh are s fe a tu re s w ith hip p oc a m p a l a m n e sia, p re su m a bly b ec a use su ch da m ag e in d irec tly in terfer es w ith n orm a l h ip po c a m p al-re gio n p ro c e ssin g (see M y ers e t a l., 1 9 96 ). T h e an tero gr ad e a m n e sia tha t fo llo w s hu m an h ip p o ca m p a l-re g io n da m a g e is g en e rally c h ara cte rise d b y a n in a bility to ac q uire ne w e p isod ic o r d e cla rative inf orm atio n , the k ind o f info rm ation a b ou t in div id ua l ev e nts an d e xp e rie n ce s tha t is ac c essib le to co n sc io u s co n trol. T h e se p a tie nts m a y a lso sh ow so m e d eg re e o f re tro g ra de am n esia , o r d isrup tion o f p rev io us ly a cq u ire d in fo rm atio n , b ut th is is u su ally lim ited to in fo rm atio n a c qu ire d sh o rtly b efo re th e trau m a, an d ten d s to le ssen in a tim e-g ra d ed fa sh io n fo r old e r info rm a tion (R ib ot, 1 9 82 ; S q u ire , 1 98 7 ). In c o n tra st to ep iso d ic o r d e cla rativ e m em orie s th a t a re often a cq u ired in a sing le e xp o su re, o the r k ind s of m e m o ry are in cre m en tally ac q u ire d o ve r m an y e xp o su res. T he se ty p e s o f m em o ry are n ot n e ce ssarily ac ce ssib le to co n sc io u s rec o lle c tio n , an d o ften in v olv e le arn ing skills o r p ro ce d u re s rath er tha n fa cts (S qu ire , 1 98 7 ). T h is d issoc ia tio n b e tw e e n e p isod ic m em o ry a n d p ro ce d u ral m e m o ry is o fte n su m m a rise d a s a d iffere nc e b e tw e e n ``k n o w ing th a t’ ’ an d ``kn o w ing h ow ’ ’ . M an y sim ple fo rm s o f p roc e du ra l m e m ory surv ive h ip p o c am pa l-reg ion d a m ag e relativ ely in tac t. T he a n im al le a rn in g litera ture is fu ll o f stu d ie s sh ow in g ho w a nim a ls w ith h ip p o ca m p a l-re g io n d am ag e ca n sho w n orm a l a cq u isitio n o f a v a rie ty o f ta sk s su ch as th e a c qu isition o f c la ssic a lly c on d itio n ed re sp o n ses to a sing le stim u lu s (A k a se , A lk on , & D isterh o ft, 1 9 89 ; S ch m a ju k , 1 9 9 4; S o lom o n, 1 97 7 ; S o lo m on & M oo re , 1 9 7 5), th e ab ility to c h oo se the n ov e l o f a pa ir o f o b je cts w h e re o n e o bje ct w a s se en im m e d ia tely be fore (Z o laM org a n & S qu ire, 1 9 9 2) sim p le d isc rim ina tion s o f sin g ly p re se nte d o d ou r stim u li in a n o p era n t task (E ich e nb a u m , F a g an , M ath e w s, & C o h e n, 1 9 8 8), a n d lea rn in g to na v ig ate to a n e sca p e p la tfo rm w he n sta rte d from a c on sta nt lo ca tio n in a p o ol (E ic h en b au m , O tto , W ible , & P ip er, 19 9 1 ). S im ilarly , h u m a n h ip po c a m p ald am a ge d a m n e sics a re no t im pa ired at le a rn in g a c o nd itio n e d m oto r-re flex resp o n se (D a um , C h an n o n, & C an a va n , 1 9 8 9; G a b rieli e t al., 1 9 9 5 ; W o o d ruffP ak , 1 99 3 ), lea rn in g sim p le c la ssific a tio n ta sk s (K n o w lto n et a l., 1 9 94 ), o r lea rn in g n e w m o to r skills su ch a s m irro r d raw in g (C o h e n, 1 9 84 ). A ll o f th ese

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sp a red ta sks c a n be so lv e d by in cre m e n ta l fo rm atio n of h ab its o r te n d en c ie s, w itho u t re q u iring e p iso d ic m em or ie s o f a n y in div id ua l le arn in g tria l. T he re a re , h ow e v er, o th e r ta sk s th at se e m su p e rfic ia lly to be ju st as p ro ce d u ral o r im p lic it a s th o se n o te d h ere , b ut w hic h a re im p a ire d after h ip p oc a m p a l-re g io n d a m a g e. F o r e x am p le , a lth ou g h th e a c q uisitio n o f a c la ssic a lly c o nd itio n e d re sp o n se to a sin g le C S is n ot im p a ire d b y h ip po c am p al-reg io n da m ag e , th er e m ay b e se v ere im p airm en ts in cla ssica lc o nd ition ing task s th a t re qu ire lea rnin g ab o u t u nre in fo rc ed stim uli (K a ye & P e arc e , 1 9 8 7; S o lom o n & M o o re , 1 9 75 ), co n fig u ratio ns or co m b in a tio ns of stim u li (Su th erlan d & R u dy , 1 98 9 ), co n te x tu a l info rm a tio n (H irsh, 1 97 4 ), or re la tion sh ips th at sp an sho rt de la ys (E ic h en b au m , O tto , & C o h en , 1 9 9 4; M oy e r, D e y o , & D iste rho ft, 1 9 9 0; P o rt, R o m a n o & P atte rso n, 1 9 8 6; R a w lin s, 1 9 8 5; Z o la -M o rg a n & Sq u ire , 1 9 9 2). T h e se fin d ing s im p ly th at the h ip p oc a m p a lre g io n do e s in d ee d p a rtic ipa te in in fo rm a tion p ro c e ssin g du ring a pp a ren tly p ro ce d u ral task s, alth o u g h th is p artic ip a tio n m a y no t n e ce ssarily be e vid e n t fro m s tu d y in g w h e t h e r a n im a ls o r p e o p le c a n Ð o r c a n n o tÐ a c q u ire a sim p l e a sso c ia tiv e re sp o nse . In G lu ck an d M y e rs (1 9 9 3) w e p rese n ted a co m pu ta tio n al m o d el of h ip po c am p al-reg io n fu n ction in a sso cia tiv e le arn in g, w h ich su gg e sts th a t th e h ip po c am p al re g io n is in v olv ed in th e form atio n of ne w stim u lus re p re sen tatio ns d u rin g n o rm a l pro c e du ral le arn in g. L ea rnin g th a t d ep e nd s on n e w rep re sen tation s is ex p e cte d to b e h ip po c am pa l-d ep e nd e nt, w he re as le arn in g th at ca n m a k e u se of p re -ex isting rep re sen tatio ns m a y b e h ip p o ca m p a l-in d ep e n de n t. S ec tio n 2 o f this p ap e r p re sen ts this m o d e l. W e ha v e a pp lied th is m od e l to a b ro ad ra ng e of e m p irica l d a ta fro m stu d ies o f c lassic al co n d itio nin g in inta ct an d h ip p oc a m p a lle sio n e d an im a ls, a s d iscu sse d in S ec tion 3 , a nd th e m o d e l co rrec tly ac co u n ts for th ese d ata . A d d itio na lly , th e c la ssic a l c o n dition in g p a ra dig m c a n b e ad a pte d for u se in h u m a n s, a nd sim ilar re sults fo r a c qu isitio n tra in in g ap p ea r to b e ob tain e d in b o th no rm a l a nd hip p o ca m p al-d a m a ge d a m n e sic h u m a n s, m u c h as in a n im als d u rin g co n d ition in g . F in a lly , in S ec tio n 4, w e no te th at th e m od e l c an b e ea sily e x te n de d to ad d re ss a n ex a m p le o f p rob a b ilistic c a teg o ry le a rnin g in b o th n o rm a ls a n d hip p oc am p a l-d am ag e d am n esic s.

2. S T IM U LU S R E PR ES EN TA T IO N A N D H IPP O C A M P A L FU N C TIO N M a ny p rev io us ch ar ac te risatio ns o f h ip p o ca m p a l-re g io n fu nc tio n in a n im al le arn in g h a ve b e en p ro po se d w hic h are task -ce n tre d : no tin g th at a p articu lar c lass o f task is h ip p o ca m p a l-de p en d en t, an d th e n se e kin g to ch ara c te rise th e h ip po c am p us a s a p ro c e ssor tha t im ple m e n ts th at kin d of fun c tio n . T h e se ta skc e ntred d esc rip tion s h av e im p lica ted th e h ip po c am p al re g io n in spa tia l le arn in g (O ’ K e efe & N ad e l, 1 9 7 8), c on te xtu a l pro c essin g (H irsh , 1 9 74 ; N a d el & W illne r, 1 9 8 0 ), c o n fig u ra l le a rn i n g (S u th e rla n d & R u d y , 1 9 8 9 ) , a n d m o re . T h e


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h ip p o c am pa l re g io n a lso ap p ea rs to b e in vo lv e d in te m p or al pro c essin g su c h a s se qu e n ce lea rnin g (B u z sa ki, 1 9 8 9), re sp o nse tim in g (A k ase e t a l., 1 9 8 9; M o ye r e t al., 1 9 90 ) a n d inte rm e d ia te-term m e m ory (E ich en b a u m et a l., 19 9 4 ; O lto n , 1 98 3 ; R aw lin s, 19 8 5 ; Z ola -M o rg a n, S qu ire, & A m a ral, 1 9 8 9). Inste ad o f a task -sp ec ific c ha rac te risa tio n o f hip po c a m p al fu n ctio n , it m a y be p ossib le to try an d d e scrib e a n info rm ation -p ro c e ssin g ro le fo r the h ip po c am p al reg io n , a n d, from th is, d erive a w id er ra ng e o f task -sp ec ific d efic its w h ich a rise from in te rferin g w ith th is info rm a tio n -pro c e ssin g fun c tio n . F o r e xa m p le , it ha s b ee n pro p o sed tha t the hip p o ca m p a l re g io n is in vo lv ed in th e fle xib le u se o f lea rn ed info rm a tio n in n o ve l situ atio ns (E ic he n b au m & B u c k in g h am , 1 9 90 ; E ic h en b a um , C o h en , O tto, & W ible , 1 9 92 ); a tte ntio na l co n tro l th ro u g h a p ro ce ss o f in h ib itin g resp o n ses to irrele v an t cu e s (D o u gla s & P rib ra m , 19 6 6 ; S c h m a ju k & M oo re , 1 98 5 ); an d p ro v idin g ``co n tex tua l tag s’ ’ to le arn e d info rm a tio n (P en ic k & So lo m o n , 1 9 91 ; W in o cu r, R aw lin s, & G ra y, 1 9 8 7 ). In o u r w o rk , w e ha v e fo c use d o n a pu ta tiv e ro le fo r th e hip p oc am p a l re gio n in fo rm in g n ew stim u lu s re pre se nta tio n s to assist le a rn in g. T h is su g g es tio n b u ild s o n m an y o f th e e arlier in fo rm atio n -p ro c essin g c ha ra cte risa tio n s o f h ip po c a m p alreg io n fu nc tio n listed p re vio us ly , a nd also o n the psy c ho lo g ic a l id e a of stim u lu s rep re sen ta tio n s (A n d erso n , 1 9 7 7; Jam e s, 1 8 96 ; S he p ard , 1 9 5 8 ). T h e em ph a sis o n rep re sen ta tio n in p sy ch o log ic al m o de llin g h a s b e en p artic u la rly sa lie n t in rec en t y ea rs a s sim ple ru le-b a sed m o d els o f co g nitiv e fu n c tio n h av e giv en w ay to c on n ec tion ist m o de ls th a t e m p h asise h o w asso c ia tiv e ne tw o rk s re -re pre sen t stim u li w ithin a m u lti-lay er ne tw ork (H a n son & B u rr, 19 9 0 ; R um elh ar t, H in to n , & W illia m s, 1 9 86 ). T he se c o nn e c tio nist n e tw o rk s a re ge n era lly assu m e d to im p lem en t ab strac t c h ara cte risa tio n s of u nd e rly in g n e ura l p ro ce sse s, pro v id in g a fra m e w o rk fo r e xp re ssin g the o rie s ab o u t b o th a nim a l le a rnin g (B arto & S u tto n, 1 98 2 ; K e h oe , 1 98 8 ; S c h m a ju k & D iC arlo , 19 9 0 ) an d hu m a n le arn ing an d m e m o ry (G lu c k & B ow e r, 1 9 88 a ; K ru sch k e , 1 9 92 ; S h an k s & G luc k , 1 9 94 ; M cC le lla nd , M c N au g h to n , & O ’ R e illy , 1 99 4 ). In th e re m ain de r o f th is sec tio n , w e w ill b rie fly rev iew th e id ea o f stim u lu s rep re sen ta tio n w ith in th e fra m e w o rk o f c o n ne c tio n ist m o de ls, a nd th e n pre se nt o ur o w n co m p u ta tio na l m o d el o f h ip po c am p al-reg io n fu n ctio n in le a rn in g .

C o n nectio n ist M o de ls of R ep resen tatio n an d Lea rn in g W ith in a typ ic a l co n n e c tio n ist n e tw o rk (F ig . 2 .1 ), th e i nte rn a l stim u lu s rep re sen ta tio n is c ha ra cte rise d as a p attern o f a c tiv atio ns o ve r a se t o f ``h id de n n od e s’ ’ w h ich rec o d e a stim u lus in pu t. T he se h id de n no d es re pre se n t the n etw o rk’ s inte rn a l re pre sen ta tio n o f the stim ulu s p a tte rn, a n d a re ro u g hly a na lo go u s to w h a t p syc h o lo g ists refe r to a s a p sy ch o lo gic al re p rese n ta tio n (o r the ``p sy c ho lo gic a l spa c e ’ ’ ), a s d istin ct fro m a sen so ry re pre se nta tio n w h ic h p rim a rily refle cts th e p hy sic al q u alitie s o f th e stim ulu s in p ut (S h e pa rd , 19 5 8 ).

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G LU C K E T AL .

A m u l ti- la y e r n e tw o rk , w i th a ``h i d d e n ’ ’ o r i n te rm e d ia te l ay e r o f c e lls b e tw e en th e in p u t

a n d o u tp u t c e ll la y er, a n d w e i g h te d c o n n e c ti o n s b e t w ee n la y e rs. T h e h id d e n l ay e r a c tiv a ti o n s re p re s en t a re -c o d in g o r r e-r ep re s e n ta ti o n o f th e in p u ts . T h e o u tp u t l a y e r a c tiv a tio n s a re in te rp r et e d a s t h e b e h a v io u ra l re s p o n se . A l l c o n n e c t io n w e ig h ts a re a d a p ti v e .

T h e h id de n lay e r ac tiva tio n s d ep e n d on w e igh ted co n ne c tio n s b etw ee n th e in p u t a n d h idd e n lay e rs, an d th u s c h an g e s to this lo w e r lay e r o f w e igh ts are e qu iv ale nt to ch a ng ing th e stim u lus re pr ese nta tio n . T he h id d en lay e r a c tiv a tio ns fe ed th rou g h w e ig h ted c o nn e c tio ns to an o u tpu t la ye r, a n d the o u tpu t la ye r a ctiv atio n d e te rm in e s the b e h av io ura l resp o n se o f the syste m . T he n e tw o rk is train e d b y a d ap tin g th e w eig h ts in b o th la y ers u n til th e sy ste m g en era tes th e d esired o utp u t in re sp o n se to a g iv e n in p ut. T he co n n ec tio n ist n etw o rk in F ig. 2.1 c an b e tra ine d to g iv e the de sired o utp u t to ea ch o f a set o f differe nt inp u ts. H o w e a sily (qu ick ly) th is is d on e de p en d s in p a rt o n th e hid d en la ye r re p rese n tatio n s. Fo r e x am ple , su p po se th a t a p articu lar in p ut p atte rn g e n era te s th e h idd e n lay e r ac tiv atio n s sc h em atised in th e to p o f F ig . 2 .2 A . In o rd er to le arn the c o rre ct re sp on se to th e first p attern , a se t o f w eig hts w ill e v olv e m a p p in g th at hid de n la ye r re pr ese nta tio n to the c o rrec t o utp u t ac tiv a tio n s. N o w sup p o se a sec o n d inp u t p a tte rn g e n era te s th e hid d en la y e r a ctiva tion s sc h em atise d a t th e b o tto m o f F ig . 2 .2 A . N ote th at th e a ctiva tio n p attern at the top o f F ig . 2 .2 A h a s c o nsid era b le o v e rla p (sim ila rity ) w ith th e p atte rn a t th e b o tto m of F ig . 2 .2 A . T h is im p lie s tha t the n etw o rk in F ig . 2 .1 w ill ten d to g en e ra lise fro m o n e p atter n to th e o th er o r, in oth er w ord s, it w ill ge n era te o utp u t to th e sec o n d p a tte rn tha t is sim ila r to w h a t is lea rn ed fo r th e first p atte rn . If th e d esired o utp uts fo r th e tw o p attern s are the sam e , th en th is g e ne ra lisa tio n w ill b e he lp ful; if th e d e sire d ou tpu ts fo r the tw o pa tte rn s a re d iffe re nt, th is g en e ralisatio n w ill ca use u n w a nte d inte rfere n ce an d h in d er the m a p pin g of the se sim ila r re p rese n ta tio n s to d iffe re n t o utp u ts. In co n tra st, tw o inp u t p a tte rn s tha t e v ok e ve ry d iffere nt h id d e n la ye r ac tiv atio ns (a s sh o w n in F ig. 2 .2 B ) w ill e n ge n d er far le ss g e n era lisa tio n , re su ltin g in m o re fa cilita tio n fo r lea rn in g d iffe ren t o u tp uts to th ese tw o pa tte rn s, b u t le ss fac ilita tion fo r le arn ing th e sa m e o utp ut to bo th.


FIG . 2.2 .

185

S c h em a t ic o f a ct iv a tio n s e v o k e d i n t h e h i d d e n la y e r n o d e s o f a c o n n e c ti o n is t n e tw o rk

s u c h a s t h e o n e s h o w n in F i g . 2 .1 , b y p re s e n t a tio n o f fo u r d iff ere n t in p u t p a tte rn s . T h e s e a c tiv it y p at te rn s co n st it u te s ti m u l u s re p re se n ta ti o n s i n th e n e t w o rk . (A ) If th e h id d e n -l ay e r re p res e n ta tio n s e v o k e d b y t w o in p u t p a t te rn s a re v e ry s im il a r, it w ill b e d iffi c u l t t o tra i n th e n e tw o rk to re s p o n d d iffe re n t ly to e a c h . (B ) I f th e re p re se n ta ti o n s ev o k e d a re v e ry d is s im il a r, it w il l b e e a si e r to m a p e a c h to a d iffe re n t re s p o n se . C o n v e rs ely , g e n e ra lisa ti o n b e tw e en in p u t s is a i d e d b y s im il a rity in re p res e n ta ti o n an d m a d e d if fic u l t b y d iffe re n tia te d re p re s en ta t io n s .

In th is w a y , le a rn in g th e co rrec t re sp on se s to a se t of in pu t p attern s ca n be a ffec te d g rea tly by ch a ng e s in stim u lu s rep re se nta tio n s. T h e e xa ct de tails o f the se re pre se nta tio n s a re , in g en e ra l, le ss im p o rtan t th an th e v ary ing de g ree o f sim ilarity o r ov e rla p b etw ee n rep rese n tation s o f differe nt in pu t p attern s.

T he C o rtico -hipp ocam pal M od el T h e c o re id e a o f G lu c k a nd M y e rs’ (1 99 3 ) th eo ry o f c o rtic o-h ipp o c am p al fu nc tion is tha t th e h ip p o c am pa l re g io n fac ilita te s lea rn in g by co n stru c tin g inte rn al stim u lus rep rese n tatio n s tha t a re b ia sed in tw o w a y s. T h e first bia s, re du n d a nc y co m p re ssio n , is a te n de n cy to m ak e m o re sim ila r th e re p rese n ta tio n s o f stim u li th at co -o c cu r or are to b e a ssoc iate d w ith sim ilar o utp u ts; this b ia s e nsu re s h ig h g en e ralisation b e tw e e n th ese stim u li. T h e sec on d b ias, p red ictive d iffe re n tiatio n , is a te n d e n c y to d iffe re n tiate , o r m a k e le ss sim ila r, th e rep re sen ta tio n s o f stim u li th a t a re to be m a pp e d to d iffe ren t o u tpu ts; th is b ia s d ec re ase s g en e ra lisa tio n be tw ee n su ch stim u li. T h ese tw o b ia se s to co m pre ss a nd d iffe re n tiate are p a rtially o pp o sin g, an d m ay o fte n inte rac t in c o m p lex w a y s, d ep e nd in g on stim u lus±stim u lus rela tio n sh ip s w ith in th e tra in ing e n viro nm e n t. H ip p o ca m p a l P ro c essin g . H o w ca n th is p o stu late d rep re sen tatio na l ro le fo r h ip p o c am pa l-reg ion fu n ctio n b e im p le m e nte d ? G luc k an d M ye rs (19 9 3 ) sho w

186

G LU C K E T AL .

h o w a sim p le c on n e ctio nist arc hite ctu re g ive s rise to just the se so rts of re p re se n ta tio n s. T h e y m o d e l hip p o ca m p a l-re g io n pro ce ssin g as a p red ictiv e a u toe n c od e r (H into n , 19 8 9 ), as sh o w n in F ig. 2 .3 . A pre d ic tiv e a u to e nc o d er m ap s in p u t a ctiv ation s th ro u g h a h idd e n lay e r to tw o c lasse s o f o utp u ts: a re co n struc tio n o f th e in pu t p a tte rn as w ell a s a p re dic tio n fo r c la ssifyin g th e in p ut pa tte rn . S u ch a n etw o rk m ay b e train ed v ia th e e rror b ac k p rop a g atio n le arn in g a lg o rith m (P ark e r, 19 8 5 ; R u m e lh a rt e t a l., 19 8 6 ; W erb o s, 19 7 4 ); th is a lgo rithm allow s d e ve lop m e nt o f re pr ese n ta tio n s ac ro ss th e in tern a l lay e r of n o d es tha t c om p re ss re d u n da n cies w h ile e m p h a sisin g p re d ictiv e in fo rm a tio n Ð e x ac tly a s req u ire d b y o u r th e ory . T h e de tails of th e le arn ing p ro ce d u re a re n ot p a rtic u la rly c ritic a l in th at m a n y a lte rn ative le a rn in g p ro ce d u res are eq u ally a b le to a c co m p lish th e re q ui re d re pre sen ta tio n al ch a ng e s (se e M ye rs et a l., 1 9 95 a , for fu rth e r disc ussio n of th is p o int). In ta c t C o rtic o -hip p o ca m pa l P ro c essin g . T his h ip p o ca m p a l-re g io n n etw or k is a ssum ed to inte ra c t w ith o th e r co rtic a l re gio n s w hic h are th e site s o f lo n g -te rm sto rag e . O n e su c h n etw or k is sh ow n in th e inta ct m o d el o f F ig . 2.4 A . T h e co rtic al n e tw o rk o n th e left in Fig . 2 .4 A re p rese n ts a h igh ly sim p lifie d m od e l o f so m e a sp ec ts o f lon g -term m e m o ry in c ere bra l a nd c e re b ella r co rtic e s. T h is n etw or k ta ke s the stim ulu s in p u t, an d m a ps it th rou g h w e igh te d c o nn e ction s to a h id d e n n o d e la ye r an d the n to a n o u tp ut n od e ; th e ac tiv a tio n o f th is o u tp u t n od e is in te rp rete d as the sy stem ’ s b eh a vio u ral re spo n se to th e in p ut. T h is co rtic al n e tw o rk a d ap ts its w e igh ted c on n ec tion stre n gth s ac co rd ing to th e L M S le arn in g a lgo rithm (W id ro w & H of f, 1 9 60 ), w h ic h is re la te d to psy c h o lo g ic a l d esc rip tion s

F IG . 2.3 .

A p re d i c tiv e a u to en c o d e r n e tw o rk , l ik e t h a t a s s u m e d in th e c o rti c o -h ip p o c a m p a l m o d el t o

re p re s en t h ip p o c a m p a l-re g io n p ro c e s s in g . T h is n e tw o rk m a p s i n p u t s t h ro u g h a h i d d e n n o d e la y e r t o o u tp u ts th at l ea rn t o re c o n s tru c t t h e i n p u t p a tte rn a s w e l l a s c la s si fy i n g th e i n p u t. T o a c c o m p lish th is , re p re s en ta t io n s a re d e v e lo p ed in th e h i d d e n n o d e l a y e r w h ic h c o m p re s s re d u n d a n c ie s i n th e in p u t w h ile m a in ta i n i n g a n d d i ffe re n ti a ti n g e n o u g h p red ic t iv e i n fo rm a tio n t o a l lo w g e n e ra ti o n o f th e d e s ire d o u tp u ts .


187

o f le arn in g (G lu ck & B o w er, 1 9 8 8a ; R e sc orla & W a g ne r, 1 9 72 ; S u tto n & B arto , 1 98 1 ) an d a lso to b io lo g ica l m ec h an ism s o f p la stic ity su c h a s L T P (B liss & L o m o, 1 97 3 ; L e v y, B ra sse l & M o o re , 19 8 3 ; S ta nto n & S ejn o w ski, 19 8 9 ). T h e h ip p o ca m p a l-re g io n au to en c od e r, a nd a sim p ler m u lti-lay e r n e tw o rk rep re sen ting a c o rtic al m od u le, a re c o m b in ed in to th e inta ct m od e l sh o w n in F ig. 2 .4 A . W ith in th is tw o -p art m o d e l of in ta c t co rtic o-h ipp oc a m p al p ro ce ssing , n ew re p re se n ta tio n s a re d ev e lo p e d first in th e h ip p o c am p a l re g io n a n d th e n inc rem e n ta lly tra n sferre d, th ro ug h o ut the le arn in g p roc e ss, to the in tern a l-la y er n od e s o f co rtic a l (o r ce reb e lla r) n etw o rk s. T h e L M S ru le c alc ula tes th e e rror at a n od e a s th e d iffe ren ce b etw ee n the d e sire d a n d ac tu al o u tpu t a t tha t n od e , an d d istrib ute s th is e rro r am o n g th e w eig h ts fee d ing into th e n o d e. F o r th e o u tpu t lay e r n od e in th e c o rtic al n etw o rk, the d e sire d ou tpu t is sim p ly a p red ictio n o f the U S arriva l, a n d, th u s, th e L M S rule ca n b e u sed to tra in th e u p pe r la y e r o f w eig h ts in the co rtic al ne tw o rk . H ow ev e r, th e d esire d o utp u t is n o t ex tern a lly d efin e d fo r th e in tern a l lay e r n o d es of the co rtic a l n e tw o rk . H ow e v er, the a ctiv atio n s o f the in te rn al lay e r o f th e h ip p o ca m pa l-re g io n n etw o rk c an b e use d a s th e d e sired ac tiv atio ns fo r c orre sp o nd in g in te rna l la ye r n od e s in th e co rtic a l ne tw ork . T h u s, a sec o nd ap p lic a tio n of the L M S ru le c an be u sed to train th e lo w e r lay e r of c ortic a l w e igh ts. O v er tim e, th e in tern a l lay e r o f the c o rtic al n e tw o rk w ill c om e to m irro r th e rep rese n tation s de v elo pe d in the h ip p o c am pa l ne tw o rk Ð ev e n th o ug h th e c ortica l ne tw o rk alo n e, usin g th e L M S a lg o rith m , w o u ld b e in ca p ab le o f d e visin g th ese re p rese n ta tio n s. W e no te th at it is n o t n ec es sary fo r th ere to b e a o n e-to -on e m ap p in g b etw ee n th e in tern a l-la y er n od e s o f the h ipp o c am pa l-reg ion a n d co rtic al n e tw o rk s; th e co rtic a l n e tw o rk

FIG . 2.4.

T h e c o r tic o -h i p p o c a m p a l m o d e l (G l u c k & M y e rs , 1 9 9 3 ). (A ) T h e in ta c t s y s te m is

a s su m e d to in c lu d e a p re d ic tiv e a u t o e n c o d e r, re p r es e n tin g h i p p o c a m p a l-re g io n p ro c e s si n g , th a t c o n s tru c ts n e w

s tim u lu s re p r es e n ta ti o n s in it s h i d d e n

la y e r w h ic h

a re b ia s ed

t o c o m p re s s

re d u n d a n c ie s w h i le d iff ere n ti at in g p re d ic ti v e in f o rm a tio n . T h e s e s t im u l u s re p re s en ta ti o n s a re a c q u ire d b y lo n g -te rm s to ra g e s ite s in th e c o rt ex , re p re se n te d a s a m u l ti-l a y e r n e t w o rk w h i ch le a rn s to p re d ic t U S a rriv a l. T h e c o rt ic a l n e tw o rk u s e s th e R e s c o r la -W a g n e r ru le t o m a p fro m i n p u ts to t h e h ip p o c am p a l-m e d i at e d in te rn al re p re s e n ta tio n s, a n d a g a in to m ap fro m t h e in te rn a l l ay e r t o o u t p u t a c tiv a ti o n s . (B ) H i p p o ca m p a l-re g i o n le s io n is a s s u m e d to d is a b l e th e h ip p o c a m p a l n e tw o rk , in w h i c h c a s es t h e c o r tic a l n et w o rk c a n n o l o n g e r a c q u i re n e w in te rn al re p re s e n t at io n s , b u t c a n a c q u ire n e w b eh a v io u ra l re s p o n se s b a s e d o n its p re -e x i st in g (a n d n o w fix e d ) i n te rn a l re p re se n ta tio n s .

188

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n o d e s c a n b e m a p p e d to a fix e d , ra n d o m lin e a r re c o m b in a tio n o f th e h ip po c am p al n etw o rk a ctiv ation s, a n d th is w ill m ain tain m o st o f th e re lev a n t in form a tio n, esp e cia lly if th e co rtic al h idd e n lay e r is larg er tha n th e h ip po c a m p al h id de n la y er. L ea rn in g in th e h ip p o c am pa l-reg ion ne tw ork , a n d in b oth la y ers o f th e lo ng te rm m e m o ry co rtic a l n e tw o rk , is a ssu m e d to p ro c e ed inc rem en ta lly an d in p a rallel. A t th is tim e , w e h av e no t m a d e an y attem p t to c larify th e rela tiv e sp e ed s o f lea rnin g in th e tw o n e tw o rk s, n o r th e tim e c o urse o f tra nsfe r of in fo rm ation f ro m o n e n e tw o rk to th e o th e r; h o w e v e r, th is g e n e r a l tw o -c o m p o n e n t a rch itec ture fo r le arn in g w ou ld c erta in ly a llo w fo r a c o nso lid ation p eriod d u rin g w h ich in fo rm a tio n is slo w ly tra n sferre d fro m hip p o ca m p a l-re gio n to lo n g-te rm m e m o ry (see A lv are z & S qu ire , 19 9 4 ; M c C le lla n d e t a l., 1 9 9 4; M u rre , 1 9 9 4; S q u ire , 1 98 7 ; W in oc u r, 1 99 0 ). A lth o u g h it is im p o rtan t to u n d erstan d the a gg re ga te fu n ctio na l role of th e h ip po c am p al reg io n, ultim ate ly w e w o u ld lik e to k no w h ow th e p ro p o se d b e h av io u ra l pro c e sses m ap o nto m o re de ta iled a n ato m ic al struc tu res. O f p a rtic u la r im po rtan c e is th e p ara hip p o ca m p a l re gio n , c om p risin g en torh ina l, p e rirh in a l, a n d pa rah ip p oc a m p al c o rtice s; the se stru c tu re s are the p rim a ry sites th rou g h w h ich sen so ry in fo rm a tion bo th e nte rs a n d lea v es the h ip po c a m p al fo rm a tio n . L a ter, in the D isc us sio n se ctio n , w e w ill b rie fly no te m o re re ce nt w o rk b y M y e rs, G lu c k, an d G ra n ge r (19 9 5 ) w h ich su gg e sts h o w G lu c k a nd M y er s’ (1 9 93 ) a g g re g ate h ip p o ca m p a l reg ion m ig h t b e d istrib ute d am o n g h ip po c am p al a n d p ara h ip p o ca m p a l reg io ns. O th er m o re re c en t w o rk o f o urs (M y e rs, E rm ita, H a rris, H a sselm o, S o lo m o n, & G lu c k, 19 9 6 ) e x te n ds th e m o d el to in c o rpo rate su bc o rtic al inp u ts, sp ec ific a lly th e ch o lin e rgic in p u ts fro m th e s e p tu m . F o r t h e m o m e n t, h o w e v e r , th i s a g g r e g a te c h a r a c t e ri s a t i o n o f h ip po c am p al-reg io n fu n c tio n w ill su ffic e fo r d e scrib in g th e re le v an t m ap p ing s fro m a n im al lea rn in g to h u m a n a m n e sia. H ipp o c a m p a l-le sion e d P ro ce ssin g. T h e le sio n e d m o de l sh o w n in F ig. 2.4 B re p re se n ts the p ro c e ssin g tha t re m a ins a fte r to tal rem o va l of all h ip p oc a m p a lre g io n m e d ia ted p roc esse s. In this c ase , th e c ortica l m o du le s a re a ssu m e d to b e u n ab le to a cq u ire n e w rep re se nta tio n s, a lth o u gh the y c an still lea rn n ew b e ha v io u ra l re sp on se s ba se d o n the ir p re -e x istin g (a n d n o w fix ed ) stim u lu s re p re se n ta tio n s. O u r lesio n e d m o de l the ref ore p re d icts th at h ipp o c am pa l-reg ion d a m a g e w ill b e m os t d ele te rio us to th o se task s th at req u ire n ew stim u lu s re p re se n ta tio n s, b u t le ss e vid en t in th o se tas k s fo r w h ic h p re -ex istin g o r ran d o m stim u lu s re p rese nta tio n s su ffic e. A s d e scrib ed in the n e x t sec tio n , th e G lu c k a nd M y ers’ m o de l o f F ig. 2 .4 c an b e a pp lied to cla ssic al co n d ition in g , a n d c ap tu re s m a n y o f the trial-lev e l asp e cts o f th e be h av io ur o f in tac t an d hip p oc a m p a l-lesio n e d a nim als. L ate r, in S e ctio n 4 , w e w ill illu strate h o w th e m o d e l c an also b e a p p lied to so m e asp e cts o f n o rm al a n d am ne sic h u m a n le arn ing .


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3. A PP LIC A TIO N O F M O DE L T O C LA S S IC A L C O N D IT IO N IN G C lassical C o nd itio ning C la ssica l P av lo via n c o nd itio n in g is o ne o f th e sim p le st fo rm s o f asso c iative lea rn in g : a pre v io u sly n eu tral c ue (th e co n ditio n e d stim ulu s o r C S ) is rep e ate d ly p aired w ith a re spo n se-e v ok in g cu e (th e u nc o nd itio n e d stim u lus o r U S ) an d c om e s itse lf to e v ok e a n an tic ipa to ry resp o nse (th e c o nd itio n e d resp o n se o r C R ). S inc e P av lov ’ s se m in a l stu d ie s, a lm o st 80 y e ars o f d etailed b e ha v io u ra l stu d ie s a nd th e o re tic a l an a ly se s o f c lassic al co n ditio n in g h av e b ee n a cc u m u la te d . T h e re n ow ex ist se v era l de tailed m ath em atic al an d c o m p u ta tio n al m od e ls for c lassic al c on d itio n in g w h ic h illu stra te h o w a w id e ran g e of c o nd ition ing b e h av iou rs c o u ld e m e rg e f ro m a sm a ll se t o f u n d e rly in g p ro ce s sin g a n d re p res e n ta tio n al a ssum p tio n s (M ac k into sh, 1 9 8 3; P e arc e & H a ll, 1 98 0 ; R e sc orla & W a gn e r, 1 97 2 ; S u the rlan d & M ac k in to sh, 1 9 7 1). N o fo rm o f a n im al o r h u m a n lea rn in g h as be e n be tte r c ha rac terise d, o r m o re suc ce ssfu lly m od e lle d , th an c lassic al c on d itio n in g . T h ese b e ha v io u ra l m o de ls p rov ide a n im p o rta nt sta rtin g po in t fo r u nd e rstan d in g an d ch ar ac te risin g w h a t is m issin g or d iffe re n t in h ip po c am p al les io n ed a nim als. P av lo v ia n co n d ition in g te ch n iq ue s h av e be e n a p p lied to sev e ral n atu ral ref le x es inc lud in g sa liv a tio n , k ne e- je rkin g , g alv an ic sk in re sp on se , a nd h ea rt ra te c on d itio n in g . T h e m ost p o pu la r a n d w id ely ad o p te d p re p ara tio n h as b ee n the e y eb link re fle x g en e rate d in resp o n se to an a ve rsiv e c o rn ea l airp u ff o r p ara o rbita l sho c k (F ig . 3 .1 A ). If th e airp uff or sh oc k U S is reliab ly p rec e de d b y a to n e o r ligh t C S , su b jec ts lea rn to ge n era te a p ro te ctive ey e blin k to th e C S, a nd tim e th e ir blin ks so tha t th e ey e is m ax im a lly c los ed a t the tim e o f e x p ec ted U S a rriva l (F ig. 3 .1 B ; G o rm e za n o , K e h o e, & M a rsha ll, 1 9 8 3). E y eb lin k c on d itio n in g h as be e n stu d ied m o st ex te n siv e ly in ra b b its, bu t a lso in fro g s, ra ts, c ats, a n d do g s. T h e n e ura l circu its u n d erly ing th e m am m a lia n ey e blin k re sp on se h av e b ee n de lin e a te d in g re a test d etail in th e ra b bit (T h o m p so n , 1 9 86 , 19 9 0 ), su gg e stin g th a t the lo n g -te rm sto ra ge o f C S ±U S asso c ia tion s oc c urs in the c ere b ellar co rtex an d u n d erly ing n u c lei. C e re be lla r le sion pe rm a n en tly ab o lishe s n ew co n ditio n e d ey e blin k le a rnin g in a n im a ls (C lark , M c C orm ick , L a vo n d , & T h om pso n , 1 9 8 4; G lic k stein , H ard im a n , & Y e o, 1 98 3 ). H ip p o ca m pa l le sio n , h o w e ve r, d o es n o t im p a ir th e a cq u isitio n o f sim p le d ela y -c o n ditio n in g in a nim als (A k a se et al., 1 9 8 9 ; B e rg er & O rr, 1 9 8 3; P ort & P atter son , 1 98 4 ; S c hm a ltz & T h e io s, 1 9 72 ; S o lom o n & M oo re , 1 9 7 5). H o w ev e r, d urin g le a rn in g o f th e c o nd itio n ed resp o n se, hip p o ca m p a l a ctiv ity d o e s c h an g e , a s in dic ate d thro u g h n eu ro p hy sio lo g ica l re co rd ing s (B e rg e r, R in a ld i, W e isz & T h om pso n , 1 9 83 ; D isterh o ft, C o u lte r & A lko n , 1 9 88 ) an d h u m a n p o sitro n e m ission to m o g rap h y (P E T ) sca n s (B la x to n e t al., 1 99 6 ; M o lch a n e t a l., 19 9 4 ). T h is im p lie s th at, a lth o u gh th e h ip po c a m p u s m a y no t b e strictly re q uire d fo r c on d itio n ed le a rn in g, it is no rm a lly a ctive d u ring suc h le arn in g. F u rthe rm o re , in

190

F IG . 3.1 .

G LU C K E T AL .

(A ) E y eb li n k co n d i tio n in g in ra b b i ts . T h e u n c o n d itio n e d st im u lu s (U S ) i s a b lin k - ev o k i n g

c o rn e a l a irp u ff o r p a ra o rb it a l s h o c k . I f th e U S is re l ia b l y p re c e d e d b y a to n e o r lig h t c o n d it io n e d s ti m u l u s (C S ), t h e a n im a l c o m e s to g e n e ra te a c o n d it io n e d b l in k t o th e C S a l o n e . C o n d it io n e d re s p o n d i n g is re co rd e d b y n o t in g t h e d i sp la c e m e n t o f a w ire su tu re d to th e s u b j ec t ’ s e y e li d . (B ) A C S ±U S p a iri n g tri al c o n s is ts o f a p re s e n ta tio n o f t h e C S , fo llo w e d b y U S p re s e n ta ti o n s ; C S a n d U S c o -te rm in at e . In i tia l ly (d a y 1 ), th e re i s b li n k res p o n d in g to t h e U S b u t n o t th e C S ; w ith re p e a te d C S ± U S p a irin g s (d a y 5 ) , a c o n d it io n e d b lin k i s e v o k e d in re sp o n s e t o t h e C S w h ic h a n t ic ip a te s U S a rri v a l. F ig u re s re p ri n t ed fro m C a rl s o n , 1 9 9 1 .

c o nd ition ing p a ra d igm s w he re th ere a re c om p le x te m p o ra l re la tio n sh ips b e tw e e n th e C S a nd U S, or co m ple x rela tio n sh ip s am on g m u ltip le C S s an d th e U S , e y eb lin k co n d itio nin g is ge n era lly disru pte d b y hip po c a m p al-re gio n d a m a g e (e .g . M o ye r e t a l., 1 9 90 ; S o lo m o n & M o o re, 19 7 5 ). G ive n th e ex te nsiv e av a ila b le d a ta o n c la ssic al c o n dition in g for b oth inta ct a n d h ipp o c am p al-le sion a nim a ls, tog e th e r w ith the ex isten ce o f fo rm al m o d els w h ich ch a ra c te rise n orm al classic a l co n d itio nin g b e ha v io u rs, it w ou ld se em th a t a m ec ha n istic in terp reta tio n o f hip po c a m p al fu n ctio n m igh t b e m o st c lea rly re v ea led w ith in this elem en ta ry fo rm o f asso c ia tive lea rn ing . A s su ch , w e be g an o u r c om p u ta tio n al m o de llin g o f h ipp o c am pa l fu n ction in a ``to p -d ow n ’ ’ fa sh io n , w ith a w ell-de fin e d c o m p u ta tio n a l m o d el th a t ac c ou n ts fo r a w ide ra n ge of b e ha v io u ra l p he n o m e n a in cla ssica l c on d itio nin g , a nd ac cu ra tely p red icts h ow b e ha v io u r sho u ld b e affe cted b y h ip p o ca m pa l-re g io n d a m a g e (G lu c k & M y e rs, 1 9 9 3; M ye rs & G lu ck , 1 9 94 ). In p a rtic ula r, w e ha v e su g ge sted th a t th e h ip po c am p us is re q u ire d to form n ew stim u lu s rep re sen tatio ns to fa cilita te le arn in g, b ut n o t n ec es sarily fo r sim p le r stim ulu s-resp o n se le a rnin g (G lu c k & M y er s, 1 9 93 ). T h e m ost sa lie n t resu lt fro m o u r an a ly se s h a s b ee n a form al c h ara c te risa tion of h ow lesio n ed an im a ls so lv e ta sk s differe ntly fro m n o rm al


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inta ct a n im a ls, e ve n if this is n o t a lw a ys ev id en t fro m c o m p arin g p erfo rm a nc e o n th e in itial le arn in g task . L ate r w e w ill n ote ho w th is ac c ou n t o f h ip po c am p al fu nc tion is b ro ad ly c o m p a tib le w ith the p re v iou s su g ge stio n b y E ich en b a um an d C oh e n tha t a n im als w ith h ip p o ca m p a l lesio ns are c h ara c te rise d b y a n in a b ility to a pp ly le arn e d k n o w le d g e fle x ib ly in a n e w situ atio n (E ic h en b au m et al., 19 9 2 ).

A pp lication to An im al D ata E v ide n c e for R e d un d a n cy C o m p ressio n . O u r th eo ry ’ s first b ias, re d un d a n c y c o m p re ssio n , is a b ia s to c o m p re ssÐ o r m a k e m o re sim ila rÐ th e rep re sen ta tio n s o f co -o c cu rrin g or re d u nd a nt stim u li. P e rha p s th e sim p lest p ara d ig m in w hic h red u n d an c y c o m p ressio n is ex p e cte d in se n so ry p rec o n ditio n in g. C o n sid er tw o stim u lu s cu e s, A a nd B , p e rha p s a lig h t a n d a to ne . If th ese tw o cu e s are h igh ly sa lie nt, the n w e w o u ld ex p ec t th e re p re se n ta tio n s th ey e v ok e in th e hip p o ca m p a l n etw or k h id d e n lay e r to b e h ig h ly d istin ctÐ lik e the e xa m ple s sh o w n in Fig . 2 .2 A . A s suc h , th e re sho u ld b e v ery little ge n era lisa tio n b etw ee n A a n d B ; if A is sub se q u en tly p a ire d w ith th e U S (`À + train ing ’ ’ ), a tes t pre sen ta tio n o f B sho u ld e vo k e v e ry little re sp o nse . H ow ev e r, if p rior to the A + tra in in g , the re a re re pe a te d no n rein fo rce d trials p airin g A a n d B (`À B -p ree x p o s u re ’ ’ ), th e s itu a t io n c h a n g e s. R e d u n d a n c y c o m p r e ss io n m a k e s th e rep re sen ta tio n s of c o -oc c urrin g cu e s A an d B m o re sim ila r, a s in th e e x am p le o f F ig . 2.2 B . T his w ill in cre ase g e ne ralisa tio n be tw ee n A an d B , so th at su bse q u en t A + train ing w ill tra nsfe r pa rtia lly to B , a nd , th u s, a test p rese n ta tio n o f B w ill e vo k e so m e co n d ition e d resp o nd in g . F igu re 3 .2 sh o w s this se n sory p rec o n dition in g e ffe c t in th e in tac t m o de l (G lu c k & M y e rs, 1 9 93 ). S e nso ry p rec o n dition in g is like w ise se en in inta ct a n im als (T ho m p so n , 19 7 2 ). B ec a use o ur m o d e l assu m e s th a t se nso ry p rec o nd ition in g arise s from h ip po c a m p ald ep e nd e n t rep rese n tation a l c om pre ssio n du ring th e p re -ex p o su re p h a se, the e nh a nc e d ge n era lisa tio n tra nsf er is n o t se en in th e h ipp o c am p al le sio ne d m o d el (F ig. 3 .2 ). S im ilarly , h ipp oc a m p a l d a m a g e th ro u gh fo rn ix -fim b ria l les io n e lim in a te s sen so ry pre co nd itio n in g in ra bb its (P o rt & P a tterso n , 1 9 8 4). S en so ry p re co n d itio n in g illustrate s h ow the inc rea se d sim ilarity o f stim u lu s rep re sen ta tio n s c an e n h an c e stim ulu s g e ne ra lisa tio n . E a rlier w e no te d an o the r im p lica tio n o f in c rea sed sim ilarity o f stim u lus re p re se n ta tio n s: a n e x p ec ted im p airm en t fo r d isc rim in ab ility. T o the e x te n t th a t tw o stim u li h av e sim ilar rep re sen ta tio n s, w e ex p ec t th a t d iscrim in atin g b etw ee n th e se p atter ns w ill be slow e r an d m o re d iffic u lt tha n be tw e e n stim u li w ith m ore distinc t re p rese n ta tio n s. W e ca n te st this ex p ec ta tio n in th e fo llo w ing sim ple va ria tion o n se n sory p rec o n dition in g. W e e x pe c t tha t e xp o su re to th e c om p o un d A B w ill retard la ter lea rn in g to disc rim ina te A an d B in the in tac t m od e l, as g en e ralisation b etw ee n the c o m p res sed re pre se n ta tio n s w ill m ak e it h a rde r to m a p the stim u li to o pp o site re spo n ses . F igu re 3.2 B in dic ates th at th e in ta ct m od e l in de e d sh o w s th is

192

F IG . 3.2 .

G LU C K E T AL .

S im u la ti o n s re s u l ts w i th t h e in ta c t a n d le s io n e d m o d el s . (A ) S e n s o ry p r e c o n d itio n in g :

u n rei n fo rc ed p r e-e x p o su re to a c o m p o u n d o f tw o s ti m u l i, A B , fo l lo w e d b y t rai n i n g t o re s p o n d to A , re s u lts in s tro n g e r re sp o n d in g to B a lo n e th a n in a c o n tro l c o n d i tio n w it h n o p re -e x p o su re . T h e i n ta c t b u t n o t le s io n e d m o d e l s h o w s th is e ffe c t; fo r n ix le s io n s im ila rl y e li m in a te s se n s o ry p rec o n d it io n in g i n ra b b its (P o rt & P a tte rs o n , 1 9 8 4 ). (B ) C o m p o u n d p r e c o n d itio n i n g . U n r ei n fo rc e d p re -e x p o s u re t o A B s l o w s la te r tr ai n i n g to d i sc ri m in at e A a n d B , a s sh o w n b y l es s re la ti v e d iffe re n ce in re s p o n d in g t o A a n d B (D iff{ A ,B } ) a fte r, in th e in ta c t m o d e l . In ta c t ra ts s h o w c o m p o u n d p re c o n d itio n in g (L u b o w , e t al , 1 9 7 6 ); th e m o d e l p re d ic ts h ip p o c am p a l-re g i o n le s io n s s h o u l d e li m in at e th e e ffe c t.

c o m p o u nd p re co n ditio nin g effe ct: the re la tiv e d iffe ren c e in re spo n d ing to A a nd B , D iff{A ,B }, fo llo w in g 1 0 0 tra inin g blo ck s is red u c ed if pre c ed e d b y 2 0 A B p re e x po su re tria ls, rela tiv e to a c on tro l co n ditio n w ith no p re -e x p os ure (G luc k & M y er s, 19 9 3 ). In c o ntra st, th e le sio n e d m o de l, w ith n o red u n d an c y c o m p re ssio n , sh o w s n o d iffere nc e b e tw e e n th e tw o c o nd itio n s. T his e ffec t is k n o w n a s th e c o m p ou n d p re co n d itio nin g effe ct, a nd h as b e en rep o rte d bo th fo r in tac t rod e nts a n d n o rm al hu m an c h ild ren (L u b ow , R ifk in, & A lek , 1 9 76 ); th is effec t h a s n ot b e en tested in h ipp o c am p al-lesio ne d an im a ls (o r am n esic h u m a n s) a n d, th u s, th e e lim ina tio n of co m p ou n d pre co n d itio nin g b y hip p o ca m p a l d a m a ge rem ain s a n o v el p re d ic tio n o f th e m o d el. N o te th at this is a pa rtic ula rly in te restin g p re dic tio n b ec a use w e ex p ec t a re la tive e n h an c em en t o f le arn in g fo r the le sion gro u p re la tive to th e c on trol g ro up . T h is is in c o n tra st to th e p re dic tio n s o f an e x pe cte d lesio n-re la ted d e fic it in m an y o th e r task s. S uc h lesio n -relate d d eficits c an b e d ifficu lt to in terp re t b e ca u se le sio n -rela te d d eficits ca n o ften resu lt fro m o th er c on fo u nd in g fa cto rs. T h us, a pre d ic tio n o f a lesio n -relate d fa c ilitatio n is g en e ra lly m or e p o w erfu l th an a p red icted le sio n -re la te d d e fic it.


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E v ide n c e fo r P red ic tiv e D iffere n tia tio n . T h e sec o n d rep rese n tation a l b ia s a ssum e d to d e pe n d o n h ip p o ca m p a l m e d ia tio n is p red ictiv e differe n tia tio n Ð a b ia s to de c rea se th e sim ila rity of the rep rese n ta tion s of stim u li th a t are to be m a p p ed to diffe ren t o utp uts. T h e sim p le st p ara d ig m in w h ic h d iffe ren tiation is e xp e c te d is in a sim p le disc rim in a tio n ta sk in w h ich tw o stim u li, A an d B , a re a ssoc iate d w ith d iffere nt resp o n ses (e .g . A + , B ± tra inin g w he re A p red icts the U S bu t B d o es n o t). In th e inta ct m od e l, th e hip p oc am p a l-re gio n n e tw o rk c on stru cts ne w in te rn al re p rese n ta tio n s w hic h fac ilitate th is sim p le d isc rim in a tio n b y de cr ea sin g th e sim ilarity be tw e e n A a n d B . T h e se n e w diffe re n tia te d rep re sen ta tio n s a re ac q u ire d b y th e c ortica l n etw o rk ’ s h id d e n lay e r, w hic h ca n the n ea sily m a p th e se to d iffe ren t re sp o n ses, a s th e ta sk re qu ire s. Inte re sting ly , the lesio ne d m o d el sho w s n o p a rticu la r d e fic it o n th is task , a n d lea rn s a s q uic k ly a t th e in tac t m o de l (F ig . 3.3 A ; G luc k & M y ers, 19 9 3 ). T his is b ec au se , fo r th is sim p le ta sk , th e p re-e xistin g (fixe d ) hid d e n lay e r rep rese n tation s in th e lesio n ed m o d e l’ s c ortic a l n e tw o rk are like ly to at le a st p artia lly d istin gu ish A a nd B , an d so a ll th e ne tw ork m u st do is m a p th e se rep rese n tation s to th e co rrec t resp o n ses . C o n sisten t w ith th is b e ha v io u r, h ip p o ca m p a l le sio n s do n o t im p a ir le a rn in g a sim p le d isc rim in a tion in a v a rie ty o f p rep a ra tion s (e .g . G oo d & H o n ey , 1 9 91 ; Ja rra rd , 1 9 9 3; Jo n e s & M ish k in , 1 97 2 ; R oss, O rr, H o lla n d , & B erg e r, 1 9 84 ; S ilve ira & K im b le , 1 96 8 ; Z o la-M o rg an & S q u ire, 19 8 6 ; Z o la-M org a n et a l., 1 99 2 ). In so m e c ase s, h ip p o c am pa l-reg ion d am ag e h a s ev e n b ee n sho w n to fac ilita te lea rnin g (e .g . E ic he n ba u m , F ag a n & C oh e n , 1 9 86 ; E ic he n b au m et a l., 1 98 8 ; E ich e n b au m e t a l., 1 9 91 ; P ort, M ikh a il, & P a tte rso n , 19 8 5 ; S c h m a ltz & T h eio s, 1 97 2 ). T he se da ta le d to e a rly sp ec u la tion s tha t the in tac t hip p o ca m p u s im p aire d sim p le c lassica l co n d ition in g (e .g . P o rt, R o m a n o & Pa tte rso n, 19 8 6 ). In fa ct, ou r le sion e d m o d el do e s sho w a slig ht fac ilita tio n re la tiv e to the inta ct m o d e l (F ig . 3.3 A ). H o w e v e r, this p a rad o x ic a l fac ilita tio n o f sim p le d isc rim in a tio n lea rnin g in th e le sio n ed m od e l re su lts fro m the fac t tha t th e le sion e d m o d el lea rn s less tha n th e inta ct m o d el, w hic h is fo rm in g n ew stim u lu s re p rese n ta tio n s. T h e a d d ition a l tim e a nd e ffo rt sp e nt by th e in ta c t m o d e l (an d , p resu m a b ly, b y i n t a c t a n i m a l s ) i n c o n s t r u c t in g t h e s e n e w a n d d i f f e r e n t i a t e d s t im u l u s rep re sen ta tio n s c an b e v e ry h elp ful if tas k d em an d s ch a ng e in a w a y th at p rese rv es w h ich c ue s a re re le v an t, e ve n if th e asso c ia tio n s to th e se re le v an t cu e s a re d iffe ren t. A sim ple ex a m p le o f th is o c cu rs in the e asy ± h ard tra n sfe r p ara d ig m , in w h ich a nim a ls are first tra ine d on a n `è asy ’ ’ disc rim ina tio n (e.g . b la c k v s. w h ite) a n d the n tra nsfe rre d to a ``h ard ’ ’ d isc rim in ation alo n g th e sa m e stim u lu s c on tin u u m (e.g . da rk gre y v s. lig h t g re y ). T h is tran sfer fac ilita te s lea rn in g e v en m o re th an an e q u iv a le n t am o u nt o f p re-tra in in g on th e h ard d isc rim in ation itself (e .g . L a w re n c e, 19 5 2 ; R ile y , 1 96 8 ; T e rrac e, 19 6 3 ). T he inta ct m o de l c o rre ctly sh o w s this effec t (F ig . 3 .3 b ; G lu c k & M y e rs, 1 9 9 3 ): in term s o f th e diffe re n ce in re sp o nd in g , D iff(H + , H ± ), b e tw e e n th e tw o h ard stim u li in th e ha rd ta sk, p re -tra in in g o n th e e asy task le ad s to b etter p erfo rm a nc e

194

F IG . 3.3 .

G LU C K E T AL .

S im u la ti o n re s u lts w ith th e in ta c t a n d le s io n ed m o d e ls . (A ) S ti m u l u s d is c r im in a tio n :

t ra in in g to re s p o n d to A b u t n o t to B . D u rin g t h is t as k , th e in ta c t m o d e l fo rm s n e w s tim u lu s re p re s en ta t io n s, w h ic h d iff er en ti a te A a n d B , a n d th en m a p s th em t o o p p o s it e re s p o n s es . T h e le s io n e d m o d e l s im p ly m a p s fro m p re -e x i s tin g (fix e d ) re p re s e n ta tio n s in th e co rti c a l n e tw o rk to t h e c o rre c t re s p o n s e s. A s a re s u lt, t h e re is n o im p ai rm e n t in co n d i tio n e d d is c rim i n a ti o n le a rn i n g i n th e le s io n e d m o d e l . S i m ila rl y , th e re is g e n e ra ll y n o i m p a ir m e n t i n s im p le d is c rim in a t io n l e ar n in g in h ip p o c a m p ald a m a g e d a n im a ls . P l o t te d fro m d a ta p re se n te d i n M y e rs e t al ., 1 9 9 6 . (B ) E a s y± h a r d tr a n s f er : l ea rn in g a h a rd d i sc ri m in ati o n b et w ee n A a n d B i s fa c ilita te d b y p rio r tra in in g o n an e a s ie r d is c rim in a tio n a l o n g th e sa m e s tim u lu s c o n ti n u u m , i n th e in t a c t b u t n o t le s io n e d m o d e l. T h is is sh o w n b y le s s re l at iv e d iffe re n c e in re sp o n d in g to A an d B (D i ff(A ,B )) aft e r a fi x e d a m o u n t o f t ra in in g in th e l e si o n e d m o d e l t h a n i n t h e in ta c t m o d e l. I n ta c t a n im a ls s h o w t h i s e ffe c t (e .g . L aw re n c e , 1 9 5 2 ; R il e y , 1 9 6 8 ; T e rra c e, 1 9 6 3 ); t h e p r ed ic t io n o f h i p p o c a m p a l-d e p en d e n c e re m a in s to b e te s te d in a n im a l s. R e p rin te d fro m M y e rs et a l., 1 9 9 5 .

th an p re -tra inin g o n th e h ard ta sk. D u ring p re -tra inin g o n th e ea sy task , th e h ip po c am p al-reg io n n e tw o rk is assu m ed to d iffe ren tiate th e re pre se n ta tio n s of th e tw o stim u li, w h ich p red ict differe nt o u tc om es. A s th ese tw o stim u li a re a ssu m e d to d iffer o n o n ly a sin gle fea tu re d im e ns io n (su ch a s b rig h tn e ss), th a t d im e n sio n w ill be d iffe ren tiate d, so th at th ere is d e cre ase d g en e ralisatio n for stim u li w ith d iffering v a lu e s of th is fe atu re d im e n sio n . T h is d iffe ren tiatio n w ill h e lp d isc rim ina te th e stim u li in th e su b seq u e nt ha rd ta sk, b e ca u se th ey differ a lon g th e sa m e d im e ns io n . In th e c o n tro l co n d itio n, w ith p re-tra in ing o n the h a rd ta sk, th e sam e b a sic m e c h an ism s o p era te, bu t th e y a re slo w er b e ca u se th e stim u li a re h a rde r to d istin g uish , a n d th e re fo re th e p re-tra in in g is n ot so effe c tiv e. In th e le sio n e d m o d el, w ith n o d iffe ren tiatio n m e ch a n ism s, the e a sy±h a rd tra n sfer e ffec t is n o t o b ta ine d . T his lea ds us to p re dic t th at h ip p o ca m p a l-le sio n e d a n im als w ill n o t sh o w ea sy ±ha rd tra nsfe r, a no v el p red ictio n th at rem ain s to b e te ste d . C o n te x tu a l P ro c ess es. M an y o f th e lea rn ing d e fic its a sso c ia ted w ith h ip po c am p al da m a g e ca n b e d esc ribe d a s c o nte x t d eficits, as th e y sug g e st a n in ab ility to in co rp or ate info rm a tion ab o ut th e e n viro n m e nta l c o nd itio n s u n d er


195

w h ic h a n ev e n t oc c urs (c f H irsh , 1 9 74 ). In stu d ies of c lassic al c o n ditio n in g it is p ossib le to m a n ipu la te the e xp e rim en ta l se tup Ð co n sistin g o f th e sig h t, sm ell, a nd tex tur e o f th e train in g c h am be rÐ to e xp licitly test fo r th e e ffe c ts o f c on te xtu al info rm a tio n . T he sim ple st of co n tex tu al m a n ip u la tio n s in v o lv e s tra in ing a n a nim a l re sp on d to a g iv e n C S in o n e c on tex t a nd th e n te sting fo r resp o n d in g to th e C S in a n ov e l c o nte x t (F ig. 3 .4 A ). U nd e r th e se c o n ditio n s, a n orm a l an im a l w ill ge n era lly re sp o nd le ss to th e C S in th e no v e l co n tex t th an in the train ing co n te x t (e.g . H a ll & H o n ey , 1 98 9 ). T h is co n tex t-sen sitiv e d ec rem e nt in re sp o nd in g su g g ests tha t th e an im a l h a s in c lu d e d som e in form a tio n a b ou t the c on te xt in th e a sso cia tio n fo rm e d b e tw e en th e e x pe rim e n ta lly d efine d C S an d the U S . In c o n tra st, a hip p o ca m p a l-le sio n ed an im a l d o es n ot sho w th is d ec re m e nt in re sp o nd in g after a co n tex t sh ift (H o n ey & G o o d , 1 9 9 3 ; P en ick & S o lom o n, 19 9 1 ). It sh o u ld b e no ted th at th is d oe s n o t re fle c t a ge n era l in a bility to pe rce iv e co n te x tua l cu e s in th e h ip p o ca m p a l-le sio n e d an im a l, a s lesio n ed a nim a ls ca n still lea rn to d isc rim in a te c on te xts (e .g . G oo d & H o ne y , 1 9 91 ; P h illips & L e D ou x , 1 99 4 ). W h at see m s to b e d isru p ted in th e le sio n ed an im a l is the ab ility to u se co n tex t to inte rp re t th e m e an in g o f c on d itio n ed cu e s (M ye rs & G lu c k , 1 9 94 ). T h e co rtic o -hip p oc a m p a l m o de l pro v ide s a fra m e w o rk fo r un d ersta n din g w h y this p attern o f p re serv e d a n d im p a ire d co n tex tua l pro c essin g m ig h t em erg e in les io n ed an im a ls (M y e rs & G lu c k, 19 9 4 ). In pu t to the h ip p o ca m pa l-re g io n a uto e nc o de r is a ssu m e d to re p rese n t no t o n ly th e p re se nc e o f a ny C S s a n d U S s, b ut a lso th e c o m p lete set o f b a ck g ro un d o r c o n te x tua l c u es th at a re p res en t. T h ese c on tex tu al c ue s a re ``to n ic ’ ’ o r un c h an g ing th rou g h ou t th e ex p erim en t,

FIG . 3.4 .

(A ) In n o rm a l a n im a ls , a c o n d i tio n e d re sp o n s e to A m a y sh o w a d e c re m e n t if A i s th e n

p re se n te d i n a n e w c o n te x t (H a ll & H o n ey , 1 9 8 9 ); h ip p o c am p a l-le s io n e d a n im a l s d o n o t s h o w th is re s p o n se d ec re m e n t a fte r a c o n te x t s h if t (H o n e y & G o o d , 1 9 9 3 ; P e n i c k & S o lo m o n , 1 9 9 1 ; F ig u re re p lo t te d fro m d a ta p re s e n te d i n P e n ic k & S o l o m o n , 1 9 9 1 .) (B ) T h e in ta c t b u t n o t le s io n e d m o d e l c o r rec t ly s h o w s t h i s re s p o n s e d e c re m e n t w i th co n te x t s h i ft (M y e rs & G lu c k , 1 9 9 4 ; F i g u re re p rin te d fro m M y er s e t a l ., 1 9 9 5 a) .

196

G LU C K E T AL .

w h ile th e C S s an d U S s are ``p h a sic’ ’ an d o nly o cc u r sp o ra dic ally d u rin g train ing . A s the h ip p o ca m p a l-re g io n a uto en c o d er lea rn s to p red ict C S ±U S a ssoc iation s, it a lso lea rns to re co n stru c t its inp u t, in c lu d in g the se c o nte xtu a l c ue s (F ig . 3 .5 ). T h u s, co n tex tu al in form atio n is in c lu d e d in th e re pre se nta tio n s fo rm e d in

F IG . 3.5 .

(A ) S c h e m a t ic o f a c tiv a ti o n s in a n i n t a c t m o d e l tra in e d t o re s p o n d to th e p re s e n c e o f a

t o n e s tim u lu s in a p a rtic u la r c o n te x t (r ep re s e n te d b y t h e p a tte rn o f in p u t a c tiv a tio n s). T h e n e t w o rk h a s le a rn ed t o o u tp u t a s tro n g re s p o n se a t th e c o rt ic a l n e tw o rk o u tp u t n o d es , an d a g o o d re c o n s tr u c tio n o f th e in p u t a t th e h ip p o c am p al -re g i o n n e tw o rk o u t p u t n o d e s . T h e h i d d e n la y er re p re s en ta t io n th a t h a s e v o lv e d i n v o lv e s s t ro n g a c ti v a t io n o f o n e h id d en -la y e r n o d e , a n d w e a k a c ti v a t io n o f th e o th e r. (B ) S ch e m a tic o f a ct iv a tio n s w h e n th e t o n e s t im u l u s i s p re s en te d in a n e w c o n t e x t (re p re s e n t ed b y a d i ffe re n t p a tte rn o f in p u t a c ti v a t io n s o n th e n o d e s th a t re p re s e n t c o n te x tu al i n p u t s . T h e h id d e n la y e r a c tiv a ti o n in b o t h n e tw o rk s i s m o r e w ea k ly a c tiv a te d th an i n th e tra in e d p a tte rn s h o w n in (A ), a n d t h e b e h a v i o u ra l re sp o n s e o u tp u t fro m t h e c o rt ic a l n e tw o rk is w e ak e r a s w e ll . T h u s , th e m o d e l s h o w s a d ec re m e n te d re s p o n se w h e n a tra i n e d s t im u l u s is p re s e n te d in a n o v e l co ntext.


197

the a u to e n co d e r’ s in tern a l la y er. A s a resu lt, th e co n tex t influ e nc e s the in te rn al lay e r rep re sen tatio ns in suc h a w ay th a t, if th e C S is late r p rese n te d in a n ew c on te xt, th e re p re se n ta tio n o f th at C S w ill b e m o re w e ak ly a c tiv ate d th an it w a s in th e tra inin g c on te xt. F igu re 3 .4 B sh o w s th is re sp on se d e cre m e n t afte r c on te xt sh ift in th e inta ct v ersio n of th e m o de l, ju st a s o b serv e d in th e in ta ct a n im al d a ta o f F ig. 3 .4 A . T he m o d el a lso co rrec tly ex p e cts th a t w ith e x te n de d tra in in g the h ip p o c am pa l rep re sen tatio n w ill ex c lud e irre lev an t c o nte x tu a l in fo rm a tio n an d b ec o m e m o re a nd m o re co n tex t-de p e nd e nt (M y ers & G lu c k, 1 9 94 ); th e re is so m e ev id en c e o f th e sam e k ind o f tim e -de p e nd e n ce of c o nte x tu a l se nsitiv ity in a nim a ls (H a ll & H o n ey , 1 99 0 ; see a lso M y e rs & G lu c k, 1 9 9 4 , fo r rev iew ). In the les io n ed v ersio n o f th e m od e l, ho w e v er, n o n e w in tern al re p rese n tatio n s a re fo rm ed , a n d so th ere is no m e an s fo r in c orp o ratin g co n tex tu al in fo rm atio n into the re p re se n ta tio n s o f a C S . A s a re su lt, th e lesio n ed m od e l is rela tiv ely inse n sitiv e to c o nte x t (F ig . 3 .4 B ). T h is is c o n siste n t w ith th e stro n g resp o n d in g g en e rally sh ow n b y h ip p o c am pa l-le sion e d an im a ls in a n e w co n tex t (F ig . 3 .4 A ). T h e co rtico -h ip p o ca m p a l m o d el c an sim ila rly a c co u n t fo r re su lts fro m a ran g e o f c o n te x t st u d i e s (M y e rs & G l u c k , 1 9 9 4 ) a n d p ro v id e s a c o m p u ta ti o n a l insta ntia tio n an d ela bo ra tio n o f se ve ral e xistin g q u alita tiv e th e o rie s w h ich h av e im p lica te d th e h ip po c am p u s in c o n tex t le a rnin g (H irsh , 19 7 4 ; P en ick & S o lom o n, 19 9 1 ). A no th er c on tex t-rela te d b e ha v io ura l p h en o m e n o n is la te n t in hib itio n (F ig . 3 .6 A ) in w hic h u nre info rc ed p re-e x po su re to a cu e slo w s th e ra te o f su b seq u e nt c on d itio n in g to th at cu e (L ub o w , 1 97 3 ). W ithin th e c ortico -h ipp o ca m p a l m od e l, late nt in hib itio n ca n be u n de rstoo d a s a v a ria tio n o f c o m p o u n d p rec o n d ition in g , in w h ic h th e c on te x t is c on sid ere d a s an o th e r c u e. If w e re p rese n t the co n tex t a s a sing le, co m p o u nd cu e , X , a n d th e C S a s a no th e r cu e A , th e n c on d itio nin g is e xp re ssib le as le a rn in g th e d iscrim in atio n A X + , X ±, th a t is, re spo n d w h en A is p rese n t in c on tex t X , b u t n o t to X a lo n e. L aten t inh ib itio n in vo lv e s a p rio r p h ase o f A X ±, X ± train in g fo llo w ed by th e A X + , X ± tra inin g . In th e in itia l ph a se , w h ere n eith e r A X n o r X p red icts th e U S , red u n d an c y c o m p res sio n in the inta ct m o d e l re sults in a n in cre ase in sim ila rity b etw ee n th e rep re sen tatio n s o f A an d X , m ak ing it m o re d iffic ult to d isc rim ina te A X from X a lon e . A s a re su lt o f th is, the late r p ha se of le arn ing to resp o n d to A X b u t n o t X is m ad e m o re d ifficu lt, w h ic h is th e o b serv e d la te n t in h ib itio n effe ct. T h is is ex a ctly w h at w e see in sim u la tio ns o f th e in tac t m o de l (F ig . 3.6 B ). T he les io n ed m o d el, w ith n o re p rese n ta tio n a l c h an g es, do e s n o t p e rform re d u nd a nc y c om p ressio n d u ring th e p re -e x p os ure p h a se a nd the refo re lea rn ing in the su bse q u en t ac q uisitio n ph a se is n o t slo w ed do w n (F ig . 3 .6 B ). C o n sisten t w ith the m o d e l, b roa d h ip p o ca m pa l-re g io n d a m a ge e lim in a tes la te n t in h ibition (F ig . 3 .6 A ), a n d th ese les io n ed an im a ls lea rn a bo u t the p re -e x p os ed cu e as q uic k ly a s a n on p re -ex p os ed cu e (K ay e & P ea rc e, 1 9 8 7; S o lom o n & M o o re, 1 97 5 ). It sh o u ld b e no ted th at a sm a lle r le sio n , lim ited to th e h ip po c am p us bu t no t inc lud in g su rro un d in g co rtic es, d o es n o t elim in ate late nt in h ib itio n (H o n ey &

198

F IG . 3.6 .

G LU C K E T AL .

L a te n t i n h ib itio n , in w h i c h u n re i n fo rc ed p re- ex p o s u re t o a c u e A sl o w s la te r a c q u i si ti o n

o f c o n d itio n e d re sp o n d in g to A . (A ) In t a c t an im a l s s h o w th is e ffe c t (L u b o w , 1 9 7 3 ), re fle c te d i n l o n g e r tr ai n i n g tim e to le a rn a s tro n g re sp o n s e t o A . B r o a d h ip p o c a m p a l -re g io n le s io n e l im in a te s l a te n t in h i b i tio n (K a y e & P ea rc e , 1 9 8 7 ; S o lo m o n & M o o re , 1 9 7 5 ). F i g u re p l o t te d fro m d a t a p re s e n te d in S o lo m o n & M o o re (1 9 7 5 ). (B ) T h e i n ta c t m o d e l c o rre c tly s h o w s l a te n t in h i b i tio n w h il e t h e le s io n e d m o d e l d o e s n o t. F ig u re re p rin te d fro m M y e rs et a l. 1 9 9 5 .

G o o d , 19 9 3 ). In m o re rec en t w o rk , M ye rs e t a l. (1 9 95 ) h av e su g ge ste d th a t th is re su lt is c on sisten t w ith a m a p pin g o f fun c tio n to an a to m y in w h ich stim u lu s c o m p re s sio n m a y o c c u r in th e e n to r h in a l c o rte x w i th o u t re q u iri n g th e h ip po c am p us p ro p e r. E ich e nb a um an d B u nse y (1 99 5 ) h a v e arg u ed fo r a sim ilar fu n ctio na l in terp re ta tio n o f th e c o rtica l are as o v erla yin g th e hip p oc a m p u s, e sp ec ially the en to rh in al c o rte x , in th e ir an a lyse s o f in tac t v s. lesio ne d a n im als in olfac to ry sim p le d iscrim in a tio n le arn in g . S u m m a ry o f M o d e l P e rfo rm a n ce in A nim a l Stu die s. G iv en th e ex ten siv e a v ailab le da ta o n cla ssic al c o nd itio n ing fo r b o th in tac t a n d h ip p oc a m p a ld a m a g e d a n im a ls, to g e th e r w ith th e e x iste n c e o f fo rm a l m o d e ls w h ic h c h ara c te rise n o rm a l cla ssica l co n d itio nin g b eh a vio u rs, w e h a ve sh o w n h ow a m ec h an istic in terp retatio n of hip p oc a m p a l fu n ctio n ca n b e clea rly re v ea le d w ithin th is m o st e le m en tary fo rm o f asso c ia tiv e le arn in g. T h e m ost salien t re su lt fro m o ur a na lyse s is a fo rm a l ch a rac terisa tio n o f h o w le sio n ed an im a ls so lv e ta sks differe n tly fro m n o rm al in ta c t a n im als, ev e n if th is is n o t alw ay s e v id e nt fro m c om pa ring p erfo rm a n ce o n th e in itial le arn in g task . A n aly ses o f se n so ry p re co n d ition in g a n d c o m p o un d p rec o nd itio n in g a re in te rpre te d as re fle cting th e h ip p o c am p a l-d ep en d e n t b ia s fo r re d u n d a n c y c o m p re ssio n , w h ile stim u lu s d iscrim in a tio n an d e asy ±h ard tran sfe r are in terp re te d a s re flec tin g p red ictiv e d iffe re ntiatio n. F u rth e r ev id e nc e for th es e hip p oc am p al-d ep e n de n t rep re sen tation a l bia ses c o m e s from an a lyse s o f c o n te x tu a l e ffec ts see n in stu die s of c o nte xt sh ifts a n d la te n t in h ib itio n .


199

H um an H ip po cam pa l A m n esia and C on dition in g W h a t ca n all th e se stu d ie s o f hip p o ca m p a l-le sio n e ffe c ts in an im a ls te ll u s a b o ut h um a n m e dia l-tem p o ra l lo b e (e sp ec ially h ip po c a m p al-b a sed ) am n esia ? O n e o f the m o st im p orta nt re as on s fo r stu d yin g c la ssica l co n d itio nin g is th at th e ne u ral stru c tu re s a nd b e ha v io u ra l p ro pe rtie s a re v ery sim ilar a cro ss a w id e ran g e o f sp ec ie s, in c lu d in g h u m a n s. C la ssic a l c o nd itio n ing h as b ee n ex ten siv ely stu d ied in h u m a n s, u sin g a v a rie ty o f pre p ara tio n s (cf D au m e t a l., 1 9 9 3 ; L ye , O ’ B o yle , R a m sd en , & Sc h ad y , 1 9 8 8; S o lo m on , S to w e , & P en d leb u ry , 1 98 9 ; T o p ka , V a llsS o le, M a sa q uo i, & H a lle t, 1 9 93 ). A s w ith a nim als, th e m ost p o pu la r p re p ara tio n is th e c on d itio n ed ey e blin k re spo n se . S ub je cts ty p ic a lly w e a r a h a t-ty p e d ev ice fitte d w ith tu b in g to a llo w lig h t airp uffs to b e d ire cte d at the co rn e a; th e h at a lso p rod u c es an in fra re d be am w h ic h is ref le cte d off th e w hite o f th e ey e ba ll an d inte rrup tion o f th is b ea m b y an e ye b lin k is re c o rd e d as a re sp o n se. Just as in a nim a ls, re pe a te d p airin g of a p re v io u sly n e u tra l to n e o r lig ht C S w ith th e b lin k e vo k in g airp uff U S re su lts in a n a n tic ip a tory co n ditio n e d e y eb lin k re sp on se to the C S alo ne . A t the n eu ra l le ve l of a n aly sis, the ce re be llu m se e m s to b e the n ec e ssary su b strate for co n d ition e d e y eb lin k re sp on d in g in hu m an s a s w e ll as in inf ra -h um an sp e cie s (D a um e t al., 1 99 3 ; L y e et a l., 19 8 8 ; S o lo m o n e t al., 1 9 89 ; T o pk a e t al., 19 9 3 ).

In tact D elay C o nd itio ning in A m nesia F o u r stu d ie s h av e ex a m in ed c la ssica l co n d itio nin g an d h um an h ip po c am p al a m n e sia . W e iskra n tz a n d W a rrin g ton (1 9 7 9 ) first e x am ine d e ye b link co n ditio n in g in tw o am n e si a p a tie n ts . O n e p a tie n t h a d h ip p o c a m p al d a m a g e a s c ha ra cterise d b y an ep iso d e o f v iral en c ep h a litis, w h ile the o th e r w a s an a lc o h olic K o rsa ko ff p a tien t. A lth ou g h d eta ils in d ic atin g da m a g e sp ec ific to a n eu ro a na tom ica l fo cu s w as n ot p ro v ide d , bo th p a tie nts n eu ro psy c h o lo g ic a lly d e m o n st ra te d m e m o ry d e fe c ts th a t a re c o m m o n ly a ttri b u ta b le e ith e r to p ath o lo g y to th e m ed ial te m p o ra l lo b e o r d ie n ce ph a lic d a m ag e. B o th a m n e sic ind iv idu a ls sh o w ed c lea r ev id en ce o f co n d ition e d le a rn in g w itho ut im p airm en t. In tere stin gly , w he n la te r a sk ed to v erb alise a d ec la ra tiv e a c co u nt ab o ut the e xp e rim e nt the y w ere un a w are of the ir p erfo rm an c e . D au m e t al. (19 8 9 ) inv e stig a te d e y elid co n d ition in g in th re e am n esic p atien ts w ith b ila tera l te m p o ral d a m a ge . P a tie n t 1 h a d a h isto ry o f ep ile p sy an d a lc o h ol a bu se , p a tie n t 2 h a d a histo ry of e n ce p h alitis a n d ep ile p tic seiz u res, an d p a tie nt 3 s u f fe re d f ro m e p il e p tic s e iz u r e s . A ll th re e p a tie n t s sh o w e d s ig n if ic a n t im p a irm e n ts o n sta n d ard n e uro p sy c h o lo g ic al m e m o ry te sts an d ind ic a te d h ip p o c am pa l lesio ns as su p po rte d b y E E G o r C T m e a su re s. A s in the a m n e sic s o f W eisk ran tz an d W arrin g to n (1 9 79 ) all th re e o f th ese p a tie nt s w ere a b le to c on d itio n w itho u t im p airm e n t u sin g th e d ela y p a rad igm . H o w ev e r, w h en a ssesse d o n a m o re c om ple x tw o-C S , co n dition a l d isc rim in atio n a n d rev e rsal e xp e rim e nt, a ll th ree fa ile d to e ffe c tiv e ly lea rn th e ta sk.

200

G LU C K E T AL .

W oo d ru ff-P a k (1 99 3 ) co n d uc ted a series o f e y eb lin k stu d ies in the w e llstu d ie d am ne sic, H M . A s a re su lt of b ila tera l re m o v al o f m ed ia l-tem p ora l lo b e stru ctu res, in clu din g th e h ip po c am p u s, to relie ve th e pa tie n t’ s ep ilep sy , H M b e ca u se d en se ly a m n e sic fo r le arn in g an d re m e m b erin g n ew in fo rm a tio n . A se c on d am ne sic w ith m e d ia l-te m p o ral-lob e le sion s re su lta n t from en ce p h alitis w a s inc lud e d for c o m p ariso n , a s w ere tw o n o rm a l ad u lt c o ntro ls. It to o k H M lo n ge r (4 7 3 trials) to re a c h lea rn in g c rite rion tha n a co n trol su b je ct (3 1 5 trials). T h e en c ep h a litic am n esic too k 1 19 trials an d his c o n tro l to o k 1 5 . In th e c a se of H M , altho u g h the e xte nt o f h is h ip p o c am pa l rem o va l lesio n is w e ll k no w n , so m e c e re b ella r atro ph y in th e ve rm is a n d ce re be lla r h em isp he res h as re ce n tly b e en n o ted . D a m a g e to th e c ere b e llu m , m o re so th an h ip po c am p al d am a ge , m a y h a v e b e en m o re im p o rta n t as the ca u se o f h is slo w e r im p a irm en t (y e t no t a b olish m e n t) in co n ditio nin g . G a brie li et a l. (1 9 95 ) rec e ntly te ste d sev e n w e ll-c ha rac te rise d a m n e sic su b jec ts a nd sev e n w e ll-m a tch e d n o rm a l co n trols. In rev ie w in g th e ex p e rim en tal d e ta ils o f th e thre e p rev io us a m n e sic p ap ers, th e stud ie s m ay b e critic ised for u sin g in ferio r ey e blin k m e a sure m e n t a p pa ra tu s a n d te c hn iq u e, to o few a m n e sic su b jec ts, p o o r q u ality o f pa tie n t d ia g n ose s a n d c ha rac te risa tio n, a n d n ot in clu d ing co n trol sub je cts fo r co m pa riso ns. In th is pa p er, th e a m n e sic etio lo g ies ra n g e d fro m e n ce p h a litis (n = 2 ), a n o x ia (n = 2) , a n eu ry sm (n = 1 ), sta tu s e p ile ptic us (n = 1), a nd clo sed h e ad in ju ry (n = 1). F ive o f th e pa tie n ts h ad n e uro im a g in g d ata c o n firm in g b ila te ra l h ipp o ca m p al da m ag e . A ll w ere d en se ly a m n e sic in te rm s o f stan d a rd n eu ro psy c h olo g ic a l m e m o ry te sts. T h e su bje c ts w e re a ssesse d in te rm s o f p se ud o c on d itio n in g (no p airin g of C S a n d U S ), c o nd ition ing (C S ±U S pa irin g s) a nd e x tin ctio n c o ntin g en c ie s (C S alo n e). In su p p ort o f the th ree p rev iou s am ne sia a n d de la y co n ditio n in g stu d ie s, n o sta tistica l differe n ce s w e re fo u nd , w ith am n e sic s lea rnin g the c on d itio n ed re sp o nse as w e ll a s th e n o rm a l co n tro ls (see F ig . 3 .7 ). M o st o f th e oth e r c o nd itio n ing p ara d ig m s in w h ic h hip p o ca m p a l-lesio n ed a n im a l s a r e a f fe c t e d , s u c h a s s i m p l e d is c r im in a ti o n r e v e r s a l , s e n s o ry p re c o n d i tio n in g , la te n t i n h ib it io n , e tc ., r e m a i n to b e t e s t e d i n h u m a n h ip p o c a m p al a m n es ic s . F o r e x a m p le , n o rm a l in ta ct h u m a n s sh o w la ten t in h ib itio n o f th e co n d itio ne d e y eb link re sp o nse (H u lstijn, 1 9 7 8). It re m a in s to b e see n if h um an h ip po c am pa l am n esic s w ill sh o w a sim ilar d isru p tio n in late nt in h ib itio n as d o h ip p oc a m p a l-d a m a ge d a nim a ls. S im ilarly , w e e x pe c t th a t h u m a n h ip p o c am pa l a m n e sic s m ay sh o w d isru p tion s in o the r p a ra d ig m s (sim p le d iscrim in a tio n re ve rsa l, la te n t inh ib itio n, e tc.) th at p a rallel th o se se en in h ip po c am p al-lesio n ed an im a ls. H a vin g re v ie w e d th e e v id e n ce for o u r th e ory w ith in stu d ie s o f a n im al c o nd ition ing , a n d d esc rib e d so m e pre lim in a ry stud ie s o f its re le v an c e to h um a n e y eb lin k c o nd itio n ing in am n esia, w e tu rn n ow to co n side r a m o re c lea rly c o gn itive form of h u m a n le arn in g: c ateg o ry le arn in g.


FIG . 3.7 .

201

(A ) E y e b l in k c o n d itio n in g i n h u m a n s is n o t d i sru p te d b y h i p p o c a m p a l d am a g e in h u m a n

a m n e s ic s . F ig u re re p rin te d fro m G a b rie l i e t a l. (1 9 9 5 ) . (B ) L ik ew i se , th e le s io n e d m o d e l p re d i c ts n o d ef ic its. F ig u re re p r in t e d fro m M y e rs e t a l . (1 9 9 5 b ).

4 . A PP LIC A TIO N O F M O D EL T O C A TE G O R Y LE AR N IN G In th e p rev io us se c tio n o f th e pa p er w e d iscu sse d h o w th e p red ic tio n s o f the c ortico -h ip p o ca m pa l m o d e l h av e b ee n teste d in b o th an im a l a nd h u m an e ye b lin k co n d itio nin g stu d ies. In th is sec tio n ou r fo cu s sh ifts to h u m an c ate go ry lea rnin g , a s w e ex p lo re th e p ossib ility of e x te n din g the c ortico h ip p o c am pa l m o de l fu rthe r to aid o u r u n d ersta nd ing o f h ig he r co g nitiv e p roc e sses. C ate g ory le arn in g p lay s a p ivo ta l role in h u m a n c o gn itio n a n d ha s g en e rate d a sub stan tial b od y of e m p iric a l a nd the o retic al w o rk (E stes, 19 9 3 ). B y e x te n d in g a n e uro b iolo g ic ally ba sed m od e l o f asso c ia tive lea rnin g to a cc o u nt for c ateg o ry le a rn in g d a ta w e h op e to start to esta blish a brid ge o ve r w h ic h w e c an b e gin to in te g rate a nim a l a n d hu m a n da ta fro m stud ies o f the n eu ra l a n d b e h av iou ra l b a ses o f co g n ition . In a ty pic al ca teg o ry lea rn in g ex p erim e n t, su b jec ts a re p re se n te d w ith a se rie s o f m u ltidim en sio na l stim u li. T h e sub jec t’ s ta sk is to de term in e to w hic h o f tw o o r m ore c a te g orie s e ac h stim u lus b e lo n g s. T h e su b je ct is the n p ro vid e d w ith c orre ctiv e fe ed b ac k , in dic atin g th e c orre c t resp o n se . T h e b e ha v io ura l co rre spo n d e nc e s b etw e en an im a l c on d itio n in g a n d c ate go ry lea rn in g w e re d e scr ib e d by G lu c k an d B o w e r (1 9 8 8a ,b ) w h o d em o n stra te d th at the R e sco rla-W ag n er m o de l o f c on d itio n ing (R esc o rla & W a g ne r, 1 97 2 ), a sim p le a ssoc iativ e m o d el, c an b e e xte nd e d to a c co u nt fo r a v a rie ty o f c ate go ry lea rn in g ph e n om en a in h um a ns. G lu ck a nd B ow e r’ s c o n ne c tio n ist ex te nsio n o f the R esc o rla -W a gn e r m o d el ca n a c co u n t fo r m an y fu n d a m e nta l a spe c ts o f

202

G LU C K E T AL .

h u m a n ca teg o ry le arn in g (G luc k , B o w e r, & H ee , 1 98 9 ) in clu din g b a se- ra te n e gle c t (G lu c k & B o w er, 1 9 8 8a ,b ), th e inte rac tio n of ex e m pla r sim ilarity a nd line a r sep a ra bility in d ete rm in in g c ate go risatio n d ifficu lty (M e d in & S c h w an en flu ge l, 1 98 1 ), the re la tion sh ip b e tw e en cla ssific atio n an d re c og n itio n m em or y fo r in sta n c es (H a y es-R o th & H ay e s-R o th, 19 7 7 ), a n d the im pa c t o f c orre la te d a ttrib ute s o n c lassifica tio n (M e din , A lto m , E d elso n , & Fre k o, 1 9 8 2). T h e m o de llin g o f G luc k a n d B ow e r a s w ell a s o th er re se arc he rs w o rk in g in a sim ilar v e in (E stes, 1 9 9 3; S h a nk s, 19 9 1 ) p ro v ide u s w ith an a p riori b asis fo r be lie v in g t h a t th e re a r e s ig n if i c a n t b e h a v io u r a l c o r re sp o n d e n c e s b e tw e e n a n im a l c o nd ition ing an d hu m a n c ateg o ry lea rn ing . T his le a d s u s to ask w h e th er or n o t th ere m ig h t b e n e u rob io lo g ica l co rresp o n de n ce s, to o . S o m e p relim in a ry p ro gr ess in th is d ire ctio n w a s m a d e by K n o w lto n e t al. (1 9 94 ) w ho a dd re sse d this issue o f n eu ro b io lo gic al c orre spo n d en c es b e tw e e n c o nd ition ing an d ca te g o ry le a rn in g in a se ries o f stud ies in w h ic h a m n e sic p a tie nts a n d co n trol su b je c ts w e re g iv e n a se rie s of m ultidim en sion a l stim u li a nd to ld to c la ssify the m in to on e o f tw o ca teg o rie s. F or ex a m p le , in o n e task , th e re w e re fou r ``taro t’ ’ c ard s, ea c h w ith a u n iq u e se t o f ab strac t g e om etric pa tte rn s. T h e stim u li w ere a d raw ing o f u p to fou r o f th ese ca rd s, an d sub jec ts w ere a sk ed to p re d ic t w he th er th ere w ou ld be ``go o d ’ ’ or ``b a d’ ’ w e ath er b a sed o n th e se c a rd s. T he a ctu al w e ath e r w as de term in e d ac co rd in g to a p rob a b ilistic ru le b a sed o n th e ca rd s, an d e ac h c a rd w as th e refo re a p artial p re dic tor of th e w e ath e r. T h e p ro ba b ilistic ru le e nsu re d tha t it w as im p o ssib le fo r the sub jec ts to le arn th e p re d ic tion w ith c o m p le te c erta in ty , a lth o u g h it w as p o ssib le to u se th e p ro ba b ilistic ca rd±w e ath er relatio n ship s to a ch iev e sig nifica n tly b e tte r-th a nc h an c e p e rfo rm a n ce . T w o e qu iv ale n t task s w e re a lso u se d, w ith sim ilar u n d erly in g lo g ic . T h ese ta sk s a re e qu iv alen t to th o se u sed b y G lu ck an d B o w er (1 9 88 b ) in an in ve stiga tio n o f p rob a bilistic ca teg o ry le a rnin g in in ta c t sub je cts, w ith th e e x ce p tio n th at th e c ateg o ries u se d in th e K n o w lto n et al. stu d y o c cu rred w ith e q ua l fre q ue n c y. In e a ch task , th e a m n esic p a tie n ts in itially le arn ed to a sso cia te th e cu es w ith th e ap p rop ria te o utc o m e at th e sam e ra te a s c on tro l sub je cts, im pro v ing fro m c h an c e p erfo rm a nc e (5 0 % co rre ct) to a p pro x im ate ly 6 5% co rrec t (K n o w lto n et a l., 1 9 9 4 ). W ith e x te n d e d tra in ing , h o w e v er, co n tro l su b je c ts ev en tu a lly o u tpe rfo rm ed am n esic p atien ts (se e F ig. 4 .1 A ). T h is fin din g tha t a m n e sics o u tpe rfo rm ed co n tro ls o nly la te in tra inin g m irro rs a sim ila r fin d in g th a t h ip po c am p al am n esic s are in itia lly u nim p a ired b ut late r im p a ire d at co g n itiv e sk ill lea rn ing (S qu ire & F ra m b a c h, 19 9 0 ). A s sh o w n in F ig . 4.1 B , the c o rtico -h ip po c am pa l m od e l p rod u ce s le arn in g c u rve s an a lo g o us to tho se o b se rv e d b y K n ow lto n e t al. (G lu c k , O live r, & M y e rs, in pre ss). In th e in ta c t m od e l, th e h ip p o ca m p a l-re g io n ne tw ork d ev e lo p s n ew stim u lu s rep re sen tatio n s to aid le arn in g ; th ese re p rese n ta tio n s m ay d ev e lo p o v er m an y trials a s th e m od e l is ex p o sed to a re pre se nta tiv e su b se t o f tra in ing p a tte rn s. E arly in le a rn in g , b e fo re the se re pre sen ta tio n s d ev e lo p , the inta ct


FIG . 4 .1.

203

(A ) O n a p ro b a b ilist ic c a te g o ry le a rn in g ta s k (K n o w lto n et a l., 1 9 9 4 ), h ip p o c a m p a l

a m n e s ic s in it ia lly le a rn at th e s am e ra te a s c o n t ro l s; l a te r in tra i n in g , th e co n tro ls co n tin u e t o i m p ro v e p er fo rm a n c e m o r e th a n t h e a m n e s ic s . F ig u re re p rin te d fro m K n o w lto n e t a l. (1 9 9 4 ). (B ) T h e co rti c o h ip p o c am p a l m o d el s h o w s a s im il a r e ffe c t: th e le s i o n e d m o d el i n i tia l ly p e rfo rm s a s w e l l a s t h e in ta c t m o d e l, b u t la t er in tra in in g , th e le s io n e d m o d el s h o w s a d e fic i t. F ig u re re p ri n t e d fro m G l u c k a n d O li v e r (in p re p .).

m o d e l d ep en d s on th e p re-e xisting re p rese n ta tio n s in th e co rtic a l ne tw ork , an d m a p s th e se to (an ap p ro xim atio n of) th e c o rre c t resp o n se . L a te r in tra in in g, a s the h ipp o c am p al rep re se nta tio ns be co m e av a ila b le , th ese n ew re p rese n ta tio n s a re ac q uired by th e c ortic al n etw o rk a nd a llo w furth er im pro v e m e nt in p erfo rm a n ce . In th e le sion e d m o d el, o n ly th e p rio r c ortica l re p rese n ta tio n s a re e ve r a v ailab le. T hu s, e arly in tra inin g , pe rform an c e is sim ila r in th e le sio n e d an d inta ct m o de ls; as tra inin g p ro gre sse s, h o w ev e r, a n d n o n ew re p rese n ta tio n s b ec o m e av a ila b le to th e les io n ed c ortica l n e tw o rk , the lesio ne d m o d e l sh ow s a d eficit rela tiv e to the in tac t m o d el. T h e sim u la tion stu dy re po rted b y G lu ck , O liv er, a n d M ye rs (in p ress) sh o uld b e v ie w e d o n ly a s p re lim in a ry ev id en ce in fav o u r of th e c o rtic o-h ipp o c am p al m o d e l a s a m od e l o f h u m a n c ate go ry le arn ing . C a te g ory le a rnin g rese a rch ha s g en e rate d a c on sid era b le b o d y o f d ata w h ich m u st b e a dd resse d be fo re a m o d el c an cla im to a c co u n t fo r this p erv a siv e a sp ec t o f hu m an co g nitio n. N e v erthe less , the se p relim in a ry an a ly se s p o in t to th e p o ssib le p o ten tial o f th e c ortico h ip p o c am pa l m o de l fo r ca p turin g su b tle a sp ec ts of a m n esic le arn in g w h ic h g o b ey o n d sim p ly c lassifyin g th eir le a rn in g a s in ta c t o r im p a ire d re lativ e to n orm a ls. M o re o v er, th ey sug g e st th a t c are ful co m pa riso n s of ea rly v ersu s la te tra in ing d iffe ren c e in le a rn in g m a y b e an im po rtan t fa cto r in un d er sta n din g the d iffe ren c e s b e tw e e n in ta ct a n d a m n e sic lea rn in g .

204

G LU C K E T AL .

5. D IS C U S S IO N A ltho u g h m o st a n aly ses o f a m n esia h a ve fo c us ed o n th e loss of ex p lic it d e cla ra tive an d ep iso dic m e m o ries fo llo w in g h ip p o ca m p al -re g io n da m ag e , w e h a ve trie d to sh ow h e re h o w in sigh ts into am n esia ca n also be rea lise d b y stu d y in g hip po c am p a l fun c tio n in sim p le pro c e du ral, o r ha b it-b ase d , a ssoc ia tiv e le arn ing tas ks. A ltho u g h m a ny sim p le fo rm s o f a sso c ia tiv e le arn in g a re u n im p aire d by h ip po c a m p al d a m a g e, m o re co m p le x task s th at re q uire sen sitiv ity to un re in fo rce d stim uli, co n fig ura tio n s of m u ltip le stim u li, or c on tex tu a l in form a tio n a re im p aired b y hip p o ca m p a l d a m a g e. W e h av e re v ie w e d h e re th e re su lts o f se v era l o f o ur re ce n t p ap e rs in w h ic h w e h av e arg u ed tha t th e se a n im al c on d itio nin g da ta im p ly th at th e h ip po c a m p al reg ion p lay s a c ritica l ro le in th e fo rm a tio n o f n e w stim u lus rep rese n tation s d urin g lea rn ing (G lu ck & M y er s, 19 9 3 , 1 9 95 ; M ye rs & G luc k , 1 9 9 6; M ye rs e t a l., 1 9 95 ).

D iss o ciatin g H ipp ocam pa l an d Pa rah ip po cam pal F un ction M o re rec e ntly w e h a ve be g u n to ex te n d o ur m o d e lling effo rts to se ek a clo ser ra p pro ch e m en t w ith th e u n d erly in g bio lo g y . A lth o ug h th e in ta ct m o de l o f F ig . 2 .4 A ad o p ts th e sim plify in g a ssum p tio n th at th e h ipp o ca m p al re gio n fu n ction s a s a u nitary pro ce sso r, th e h ip p o ca m p al reg ion is, in fa ct, an a to m ica lly d ivid ed in to se v era l d istinc t stru c tu re sÐ in clu d in g h ip p o ca m pa l fie ld s C A 1 th ro u gh C A 4 , d e nta te g y ru s, sub ic ulu m , an d e nto rh in a l co rte x . T h ere are a lso se ve ral in p uts to th e h ipp o c am p al reg io n , in c lud ing p e rirh ina l an d pa rah ip p oc a m p al c o rtic es, w h ich p rov ide h ig h ly p roc e ssed p oly m o d a l se nso ry in fo rm a tio n, as w e ll as a dire ct co n ne c tio n fro m un im o d a l piriform (o lfa c to ry ) c ortex (see F ig . 5 .1 ). In M y e rs e t a l. (1 9 95 ) w e h yp o th e sised th a t th e rep re sen tation a l fu n ctio n c o m p u ted in o u r in tac t m od e l’ s h ip p o c am pa l re gio n m ay be sub d ivid e d, an d th e su b fu nc tio n s loc a lised in differe nt a n ato m ica l sites a ro un d the reg ion ; in p a rtic u la r, w e pro p o sed tha t stim u lu s±stim u lu s re du n d a nc y c o m p res sio n co u ld e m e rg e fro m th e an a to m y an d p hy sio lo g y o f su p e rfic ial en to rh in a l c o rte x . T h e n e t re sult o f b o th e nto rh in a l a n d h ip po c a m p al p roc e ssing w ou ld th e n b e a n ew stim u lu s rep rese n tatio n co n stra in ed b y b o th co m pre ssio n an d d iffe ren tiatio n b iase s w h ic h co u ld b e tra nsfe rred to lo ng -te rm sto ra ge site s in th e c o rte x . T his hy p o th e sis a ssum es tha t a se le ctiv e h ip p o ca m p a l-le sio n (th e H -le sio n ), w h ich do e s n o t oth e rw ise d am ag e e n to rh in al c o rte x (cf Jarrar d & D a v id so n , 1 9 9 1), m ig h t a llo w red u n da n cy c o m p ressio n pro c e sses to surv ive . B e h av io urs th at d e pe n d m a in ly o n th ese p roc e sse s sho u ld co n tin u e to b e e x hib ite d afte r H le sio n , w he re as b eh av io ur s tha t req u ire o th e r rep rese n tatio n al p roc e sse s su ch as p re dic tiv e diffe re n tia tio n sh ou ld b e d isrup te d. W e c an stu d y th is situ atio n b y c o nstru c tin g a ``S e lec tiv e H -lesio n ed ’ ’ m od e l, in w hic h th e fu ll h ip p oc a m p a lre g io n ne tw ork o f Fig . 2 .4 is re d uc e d to an e nth o rh in a l n etw o rk o n ly. T h e lo ng -


FIG . 5.1.

205

S ch e m a tic o f m a jo r in f o rm a ti o n fl o w p a t h w a y s in th e h ip p o c a m p a l re g i o n . In p u ts a re

p ro v id e d d i re c tly fr o m

u n im o d al o lfa c to ry c o r te x , a s w el l a s p o l y m o d al c o rtic e s i n c l u d in g

p ar ah ip p o c a m p a l an d p e ri rh i n a l c o rt e x . In fo rm a tio n tra v el s th ro u g h s u p e rfi c ia l e n to rh i n a l co rte x , th ro u g h th e h ip p o c am p a l fo rm at io n (in c lu d i n g h i p p o c a m p a l fie ld s C A 1 ±C A 4 , d e n t at e g y ru s , a n d s u b ic u lu m ), a n d re tu rn s th ro u g h d e ep en to rh in a l c o rte x to o t h e r c o rt ic a l a re a s fo r lo n g -t er m s to ra g e . T h e re is a l so a b i-d ire c ti o n a l p a th w a y th ro u g h t h e f o rn ix w h i c h p ro v id e s co n n e c ti o n to s u b c o rtic a l s tru c tu re s. M a n y o t h e r c o n n e ct io n s e x i st , w h ic h a re n o t s h o w n h e re fo r s im p l ic it y .

term m e m o ry n e tw o rk c on tin u e s to o pe ra te as in th e in tac t m o de l, e x ce p t th at the n ew rep rese n tation s pro v id e d b y the e n to rh ina l n etw o rk are b iase d o nly b y stim u lu s±stim u lu s red u n da n cy co m pre ssio n, b u t n ot by the o th er re p rese n ta tio n al b iase s attrib u ted to th e h ipp o c am p al reg ion a s a w h o le . A sim p le e x am p le o f a co m pre ssio n-b ase d task is la te n t in h ibitio n , in w h ic h u nre in forc ed p re -ex p o su re to a cu e slo w s later ac q uisitio n o f a c on d itio ne d resp o n se to th at c u e (L u bo w , 1 97 3 ). In o u r in tac t m o d e l of F ig . 2 .4 A , laten t inh ib itio n is c au se d b y c o m p ressio n o f th e pre -ex p o se d c ue w ith c o-o cc u rrin g a nd eq u ally n o n re in forc e d c on tex tu al cu es. T h e su b seq u e nt in c re a se in lea rn in g tim e resu lts b ec a u se th e m od e l m u st first red iffe re ntiate th e cu e fro m th e c on te xt b efo re a resp o n se ca n b e sele ctiv ely a sso cia te d w ith th e c ue (F ig . 3 .6 ). B ec a use this effec t is assu m ed to d ep e n d prim a rily o n re du n d an c y co m pre ssion , the e nto rh in a l n etw or k in th e H -le sio n e d m o d el is sufficie n t to p ro du c e laten t inh ib itio n. C o n siste nt w ith th is m o d e l b eh av io ur , ra ts w ith sele ctive h ip po c a m p al le sion s bu t n o e n to rh ina l d a m a g e sho w no rm a l o r ev en en h an c e d laten t inh ib itio n (H o n e y & G o o d , 1 9 9 3; R e illy , H a rle y & R e v usk y , 19 9 3 ). O b v iou sly , m o re e x pe rim en ta l tests n e ed to be p e rfo rm ed , b ut th is is a t lea st initia l su p p ort fo r the M y e rs e t al. (1 99 5 ) p rop o se d d iss o ciatio n o f h ip p o ca m p a l a nd en torh in al fu nc tion . E ic he n b au m a nd B u n sey (19 9 5 ) h av e re ce n tly a dd re sse d th is sa m e issu e an d h av e sug g es te d th at th e pa ra hip p oc a m p al re gio n m ed iate s th e ``fu sio n ’ ’ o f co o cc u rrin g o r n ea rly co in cid en t stim u li; th is pro c ess is e sse ntially id en tic al to the red u n d an c y c om p re ssio n fun c tio n w e h av e p ro po se d . It is in te re stin g to n ote th at w h ere as th eir fu sio n th eo ry de riv e s fro m b e h av io ura l o b serv a tio n s c o m p a rin g

206

G LU C K E T AL .

p a ire d -asso c ia te le arn in g in in ta ct, hip p o ca m p a l-le sio n ed a n d pa ra h ip p oc a m p a lle sio n e d an im a ls, o u r sim ila r co m pre ssion th e o ry a rise s fro m a n inte g ra tio n of b o th p hy sio lo g ica lly ba se d a nd be h av io u ra lly ba se d c o m p uta tio n al m o d e ls of h ip po c am p al-reg io n fu n ctio n . W e h op e the c o nv e rg e n ce o f th e se tw o w id e ly d iffe re n t a pp ro ac h es to the o ry d ev e lo pm en t is a sign tha t stim ulu s co m pre ssio n is a u se ful a nd a cc u rate d e scrip tio n of p a ra h ipp o c am pa l-reg ion fu n ctio n .

M o de lling C h olin erg ic M od u latio n in S ep to hipp o ca m p al P ath w ay s In oth er, m ore re c en t w o rk , w e ha v e a lso sh o w n th at a sim p le ex ten sio n o f th e m o de l ca n suc ce ssfu lly a cc o un t for th e re tard ed c la ssica l co n ditio nin g th a t o c cu rs a fte r se pto h ipp o ca m p a l d isru p tio n v ia a n tic ho line rg ic d ru gs (M y e rs et a l., 1 9 9 6). T his la st is im p o rtan t b e ca u se sep to hip p o ca m p a l p ath w ay s m a y b e d a m a g ed in a va rie ty o f w a y s. B a sa l fore b rain d am a g e m a y o cc u r in c ase s of A lzh e im e r’ s D em en tia, b ut m o re c o m m on ly o cc u rs in ca se s o f an e ury sm rup tu re o f the a n te rio r c om m un ica ting a rte ry (A C o A ). T h e A C oA a n eu ry sm surv ivo rs a re an esp e cia lly in te restin g g ro u p b e ca u se the y o fte n m an ifest an a nte rog ra d e a m n e sia sy n d rom e w h ic h is su pe rficia lly v ery sim ila r to th at sh o w n b y h ip po c am p al a m n e sic s (D eL uc a & D iam on d , 1 9 9 5)Ð a lth o ug h the A C o A a m n e sics h av e n o direc t le sion to the h ip p o ca m p u s. T h e pro b le m in th e se p a tie nts m ay re sult from b asa l fo re bra in d a m a g e, in d ire c tly inte rfe ring w ith p ro p e r h ip p o c a m p a l f u n c ti o n i n g . N e u r o im a g in g to d ire c tly a ss e s s b a sa l fo reb ra in le sion e x te n t is diffic u lt be ca u se A C o A a n eu ry sm is often tre ate d b y su rg ic a l p la c em en t o f fe rro m a gn e tic c lip s o n the ru p ture d a rte ry . M R I is th ere fo re co n train dic ate d in th es e ca se s a s it m a y re su lt in d isp la ce m e n t a nd h e ating of th e m e tallic c lip w h ich co u ld kill th e p atien t (K luc z nik , C a rrier, P yk a , & H a id, 19 9 3 ). A lte rn a te n e uro im a gin g te ch n iq ue s su ch as an g io gra p h y a nd c o m p u terised to m o g rap h y (C T sc an ) m a y b e u se d in th es e a m n e sic p a tie n ts re co v e rin g fro m strok e ; h o w e v er , th e p la c em e nt o f the m e ta llic c lip often o b scu re s p rec ise im ag in g of th e b asa l fore b rain reg io n. T he re fo re , a n inte re sting p o ten tia l a pp lica tio n o f this w o rk is to d e ve lo p be h av io ura l te sts th at a re se n sitiv e to th e d a m a g e o f p articu lar n eu ra l struc ture sÐ th u s a id in g in th e a sse ssm e n t o f le sion e xte n t in th e se p a tie nts.

S um m ary O u r lon g -term go a l is to u se co m p u tatio na l m o d els to d ev e lo p a co m pre h en siv e v iew of h ip po c a m p al-re gio n fun c tio n tha t illu m in ate s c om m o n b eh a v iou ra l fu n ctio ns, an d u nd e rly ing n e ura l m e ch an ism s, in b o th a nim al an d h um a n m em o ry. O u r w ork to d ate illu stra te s som e in itia l p ro g re ss to th is e nd , a nd m ay h e lp pro v id e p red ictio ns an d d ire ctio n s to g u ide fu rth e r em p iric al a n d th eo re tic al re sea rc h in h um an m e m o ry a n d am n esia . O u r ho p e is th at th e in sig h ts g ain e d fro m th e se in itia l a na lyse s o f a sim ple le arn in g be h av iou r w ill lea d to a d ee p er


207

u nd e rstan d in g o f th e h ip p o ca m pa l re g ion in m o re c o m p lex fo rm s o f lea rn in g an d m e m o ry , in bo th an im a ls a n d h u m a n s.

R E FER EN C E S A k a s e , E ., A lk o n , D .L ., & D is t er h o ft, J .F . (1 9 8 9 ). H ip p o c a m p a l l e si o n s im p a ir m e m o ry o f s h o rtd e l a y c o n d itio n e d e y e b li n k in ra b b it s. B e h a v io ra l N e u ro s c ien c e , 1 0 3 (5 ), 9 3 5 ±9 4 3 . A lv a re z, P ., & S q u ire , L . (1 9 9 4 ). M e m o r y c o n s o lid a tio n a n d th e m e d i al te m p o ra l l o b e : A s i m p le n e t w o rk m o d e l. P ro c e e d in g s o f th e N a tio n a l A ca d e m y o f S c i en c e s, 9 1 , 7 0 4 1 ±7 0 4 5 . A n d e rs o n , J . (1 9 7 7 ). N eu ra l m o d e ls w it h c o g n it iv e im p li ca t io n s . In D . L a B e rg e & S . S a m u e l s (E d s .), B a s ic p r o ce s s e s in re a d in g : P e r ce p ti o n a n d c o m p re h e n s io n (p p .2 7 ±9 0 ). H il ls d a le , N J : L a w re n ce E r lb a u m A ss o c ia te s In c . B a rto , A ., & S u tt o n , R . (1 9 8 2 ). S im u l a tio n o f a n ti c ip a to r y re s p o n s es i n c la s si c a l c o n d itio n in g b y a n e u ro n -l ik e a d a p ti v e e le m e n t. B e h a v i o r a l B r a i n R e s e a r c h , 4 , 2 2 1 ±2 3 5 . B e rg e r, T ., & O rr , W . (1 9 8 3 ). H ip p o c a m p ec to m y s e le c ti v e l y d is ru p ts d is c rim i n a tio n re v e rs a l le a rn in g o f th e ra b b i t n ic ti ta ti n g m e m b ra n e re sp o n s e . B eh a vi o r a l B r a in R e s e a r c h , 8 , 4 9 ±6 8 . B e rg e r, T .W ., R in al d i , P ., W e is z , D .J ., & T h o m p s o n , R .F . (1 9 8 3 ). S in g l e -u n it a n a ly s is o f d iff ere n t h i p p o ca m p a l c e ll ty p e s d u ri n g c la s s ic a l c o n d itio n in g o f t h e ra b b it n i ct ita t in g m e m b ran e re s p o n s e . J o u r n a l o f N e u ro p h y s io l o g y , 5 0 (5 ), 1 1 9 7 ±1 2 1 9 . B la x to n , T .A ., Z e ffiro , T .A .,G a b rie li, J .D .E ., B o o k h e im e r, S .Y ., C a rril lo , M .C ., T h eo d o re , W .H ., & D is te rh o ft , J .F . (1 9 9 5 ). M a p p i n g th e n e u ro a n a to m ic a l c o rre la te s o f h u m a n le a rn in g : A P E T a c tiv a tio n s tu d y o f e y e b li n k c o n d it io n i n g . M a n u s c rip t s u b m it te d fo r p u b lic a ti o n . B li s s, T ., & L o m o , T . (1 9 8 3 ). L o n g -la s tin g p o te n t ia ti o n o f s y n a p tic tra n s m is sio n in th e d e n t at e are a o f an a e s th et iz ed ra b b i t fo l lo w in g s tim u la ti o n o f t h e p e rfo ra n t p a th . J o u r n a l o f P h y s io lo g y , 2 3 2 , 3 3 1 ±3 5 6 . B u z sa k i, G . (1 9 8 9 ). T w o -s ta g e m o d e l o f m em o ry -tra c e fo rm a ti o n : A ro le fo r ``n o is y ’ ’ b ra i n s ta te s . N e u r o s c ie n c e , 3 1 (3 ), 5 5 1 ±5 7 0 . C a rls o n , N .R . ( 1 9 9 1 ). P h y si o l o g y o f b e h a v io r (4 th e d n .). N e e d h a m H e ig h ts , M A : A lly n & B ac o n . C la rk , G .A ., M c C o rm i ck , D .A ., L av o n d , D .G ., & T h o m p so n , R .F . (1 9 8 4 ). E ff ec t s o f le s io n s o f c e re b e ll a r n u c le i o n

c o n d it io n e d

b e h a v io ral a n d h ip p o c a m p a l n e u ro n a l re sp o n s e s . B ra in

R es e a r ch , 2 9 1 , 1 2 5 ±1 3 6 . C o h e n , N . (1 9 8 4 ). P re s erv e d le a rn in g c a p a c it y in a m n es i a: E v i d e n c e fo r m u lt ip le le a rn in g s y s te m s . In L . S q u i re & N . B u tt er s (E d s .) , N e u r o p s y c h o lo g y o f m e m o ry (p p .8 3 ±1 0 3 ). N ew Y o rk : G u i lfo rd P re s s . D a u m , I., C h an n o n , S ., & C a n a v a n , A . ( 1 9 8 9 ). C la s s ic a l c o n d itio n in g in p a t ie n t s w ith s e v e re m e m o ry p ro b le m s . J o u r n a l s o f N e u r o l o g y , N e u r o s u r g er y a n d P s yc h ia tr y , 5 2 , 4 7 ±5 1 . D a u m , I., S c h u g e n s , M .M ., A c k e rm a n n , H ., L u t z en b e rg e r, W ., D ic h g an s , J ., &

B irb a u m e r,

N . ( 1 9 9 3 ). C la s s ic a l c o n d i tio n i n g a ft er c e re b e lla r le s io n s in h u m a n s . B e h a v io r a l N e u ro s c ien c e , 1 0 7 (5 ), 7 4 8 ±7 5 6 . D e L u c a, J ., & D i a m o n d , B . (1 9 9 5 ). A n e u ry sm o f th e a n t e rio r c o m m u n ica t in g a rte ry : A re v ie w o f n e u ro a n a t o m ic a l a n d

n e u r o p h y s io lo g ic a l s e q u e l ae . J o u r n a l o f C l in i c a l a n d

E x p e r im e n ta l

N e u r o p s y c h o lo g y , 1 7 ( 1 ), 1 0 0 ±1 2 1 . D is te rh o f t, J.F ., C o u l te r, D .A ., & A lk o n , D .L . (1 9 8 8 ). C o n d i tio n in g - sp e c ific b i o p h y s ic a l a l te ra tio n s in ra b b it h ip p o c a m p u s. In C .D . W o o d y , D .L . A lk o n , &

J .L . M c G a u g h (E d s .), C e l lu la r

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o rien tin g

rea ctio n

d u rin g

hum an

ey e lid

c o n d itio n in g

fo llo w in g

p re c o n d it io n in g e x p o s u r es to th e C S . P s yc h o lo g ic a l R es e a rc h , 4 0 , 7 7 ±8 8 . J a m es , W . (1 8 9 6 ). T h e p r in c ip l e s o f p s y c h o lo g y . N e w Y o rk : H e n ry H o l t & C o . J a rra rd , L . (1 9 9 3 ). O n t h e r o le o f t h e h ip p o c a m p u s i n l e arn in g an d m e m o ry in th e ra t. B e h a v io ra l a n d N e u r a l B i o lo g y, 6 0 , 9 ±2 6 . J o n e s , B ., & M is h k i n , M . (1 9 7 2 ) . L im b i c l es i o n s a n d th e p ro b le m o f s tim u lu s -re in fo rc e m en t a ss o c ia ti o n . E x p e ri m en ta l N e u ro lo g y, 3 6 , 3 6 2 ±3 7 7 . K a y e , H ., & P e a rc e , J . (1 9 8 7 ). H i p p o c a m p a l le s io n s a tte n u a t e la t en t i n h ib itio n a n d th e d e c lin e o f t h e o ri e n t in g re s p o n s e in ra ts . Q u a r te r ly J o u r n a l o f E xp e r im e n ta l P sy c h o l o g y , 3 9 B , 1 0 7 ±1 2 5 . K e h o e , E .J . (1 9 8 8 ). A la y e re d n e t w o rk m o d e l o f a s so c ia tiv e le a rn in g . P s y ch o lo g ic a l R e vi e w , 9 5 (4 ), 4 1 1 ±4 3 3 . K lu c z n ic k , R .P ., C a rri e r, D .A ., P y k a , R ., & H a id , R .W . (1 9 9 3 ) . P l a c em e n t o f fe rro m a g n et ic in tra c e re b ra l a n e u ry s m c lip in a m a g n e ti c fi e ld w i th a fa ta l o u t c o m e . R a d i o l o g y, 1 8 7 , 8 5 5 ± 85 6 . K n o w lt o n , B ., S q u ire , L ., & G lu ck , M . (1 9 9 4 ) . P r o b a b i listic c la s si fic a tio n le a rn in g i n a m n e s ia . L e a rn in g a n d M e m o r y , 1 , 1 0 6 ±1 2 0 . K ru sh k e, J.K . (1 9 9 2 ). A L C O V E : A n e x e m p la r-b a se d c o n n e c tio n ist m o d e l o f c a te g o ry le a rn in g . P s y c h o lo g ic a l R e v ie w , 9 9 (1 ), 2 2 ±4 4 . L a w r e n c e , D .H . ( 1 9 5 2 ). T h e

t ra n s f e r o f a

d i s c r im in a ti o n

alo ng

a

co n tinu u m . Jo u rn a l o f

C o m p a ra ti ve a n d P h y si o l o g ic a l P s y c h o lo g y , 4 5 , 5 1 1 ±5 1 6 . L e v y , W .B ., B ra ss e l, S .E ., & M o o re , S .D . (1 9 8 3 ). P a rti a l q u a n ti fica ti o n o f th e a s s o c ia t iv e s y n a p tic le a rn in g ru le o f t h e d e n t at e g y ru s . N e u r o s c ie n c e, 8 (4 ), 7 9 9 ±8 0 8 . L u b o w , R . (1 9 7 3 ). L a te n t in h i b itio n . P sy c h o l o g ic a l B u lle t in , 7 9 , 3 9 8 ±4 0 7 . L u b o w , R .E ., R if k i n , B ., & A l e k , M . (1 9 7 6 ). T h e co n te x t e ffe c t: T h e re l at io n s h ip b e tw e e n st im u lu s p re -e x p o s u re a n d e n v i ro n m e n t al p re -e x p o s u re d et e rm in es s u b s e q u e n t l e ar n in g . J o u r n a l o f E x p e ri m en ta l P s y c h o lo g y: A n i m a l B e h a v io r P r o c e ss e s , 2 ( 1 ), 3 8 ±4 7 . L y e , R .H ., O ’ B o y le , D .J ., R a m s d e n , R .T ., & S c h a d y , W . ( 1 9 8 8 ). E ffe c ts o f a u n ila t era l c ere b e lla r le s io n o n t h e a c q u is it io n o f e y e -b lin k c o n d it io n i n g i n m a n . J o u r n a l o f P h y s io lo g y (L o n d o n ), 4 0 3 , 58 P. M a c k in to sh , N . (1 9 8 3 ). C o n d itio n in g a n d a s s o c ia t iv e le a r n in g . O x fo rd : O x fo rd U n i v e rs ity P re s s . M c C l e lla n d , J., M cN a u g h to n , B ., & O ’ R ei lly , R . (1 9 9 4 ). W h y w e h a v e c o m p le m e n ta r y le a r n in g s ys t e m s i n th e h ip p o c a m p u s a n d n e o c o r t ex : In s ig h ts fr o m th e s u c ce s s e s a n d fa il u r e s o f c o n n ec t io n is t m o d el s o f le a rn in g a n d m em o r y . T e c h n ic a l R e p o rt N o . P D P .C N S .9 4 .1 . C a rn e g i e M e ll o n U n i v e rs it y , P ittsb u rg h . M e d in , D .L ., A lto m , M .W ., E d e l so n , S .M ., & F re k o , D . (1 9 8 2 ) . C o rre la te d s y m p t o m s a n d si m u l at e d m e d i ca l c la s s ific a tio n . J o u r n a l o f E x p er i m e n t a l P s y c h o lo g y: L e a r n in g , M e m o ry , & C o g n itio n , 8 , 3 7 ±5 0 . M e d in , D .L ., & S c h w a n en flu g e l, P .J . (1 9 8 1 ). L i n e a r s e p a ra b ility in cl a ss i fic a tio n l e a rn i n g . J o u r n a l o f E x p e ri m en ta l P s y c h o lo g y: H u m a n L e a r n in g a n d M e m o r y, 7 , 3 5 5 ±3 6 8 . M o lc h a n , S .E ., S u n d e rla n d , T ., M c In to s h , A .R ., H e rs o v i tc h , P ., &

S c h re u s , B .G . (1 9 9 4 ) . A

fu n c ti o n a l an a to m ic a l st u d y o f a s s o ci a tiv e l ea rn in g in h u m a n s . P r o c ee d in g s o f t h e N a tio n a l A c a d e m y o f S c ie n c e s o f t h e U n i te d S ta te s o f A m e r ic a , 9 1 , 8 1 2 2 ±8 1 2 6 .

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G l u c k , M . (1 9 9 4 ). C o n t e x t, c o n d i t io n i n g a n d

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&

S o lo m o n , R . (1 9 9 1 ). H ip p o c am p u s , co n tex t an d

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N e u r o s c ie n c e , 1 0 5 (5 ), 6 1 1 ±6 1 7 . P h i llip s , R . & L e D o u x , J . (1 9 9 4 ). L e s io n s o f th e d o rs a l h ip p o c a m p al fo rm a tio n in te rfe re w i th b a c k g ro u n d b u t n o t fo re g ro u n d c o n t ex tu a l fe a r c o n d i tio n i n g . L e a r n i n g & M e m o r y , 1 , 3 4 ±4 4 . P o rt , R ., M ik h a il , A ., &

P a t te rs o n , M . (1 9 8 5 ). D i ffe re n t ia l e ffe c ts o f h ip p o c a m p e c to m y o n

c la s s ic a ll y c o n d it io n e d ra b b it n i c tita tin g m e m b ra n e re s p o n s e re la te d to i n t ers t im u lu s i n t er v a l. B eh a v io r a l N e u ro s c ie n c e , 9 9 (2 ), 2 0 0 ±2 0 8 . P o rt , R ., R o m a n o , A ., & P a tte rs o n , M . (1 9 8 6 ). S t im u lu s d u ra tio n d is c rim in a t io n in th e r ab b it: E ffe ct s o f h ip p o c a m p e c to m y o n d i s cri m in a ti o n an d re v e rs a l l ea rn in g . P h y s io lo g i ca l P s y c h o lo g y, 4 , 1 2 4 ±1 2 9 . P o rt , R ., &

P a tte rs o n , M . ( 1 9 8 4 ). F im b ria l le s io n s a n d s e n s o ry p re c o n d i tio n i n g . B e h a v io r a l

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W a g n e r, A . (1 9 7 2 ) . A

th e o ry o f P a v lo v ia n co n d i tio n in g : V ar ia tio n s in th e

e ffe c ti v e n es s o f re in fo rc e m en t a n d n o n -re in fo rc e m en t. In A . B l a ck & W . P ro k a s y (E d s .), C l a s s ic a l c o n d it io n in g II: C u r r e n t r e s e a r c h a n d t h e o ry (p p .6 4 ±9 9 ). N e w Y o rk : A p p le to n C e n tu ry -C ro fts . R i b o t, T . (1 8 8 2 ). T h e d i se a s e s o f m e m o r y . N e w Y o rk : A p p le to n .


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D . R u m e l h a rt &

J . M c C le l la n d (E d s .), P a r a l le l d i st r ib u t e d

p r o c e ss i n g :

E x p lo ra ti o n s i n t h e m ic r o s t ru c tu r e o f c o g n itio n (p p .3 1 8 ±3 6 2 ). C am b rid g e, M A : M IT P re s s . S c h m a ju k , N . ( 1 9 9 4 ). S tim u lu s c o n fi g u ra tio n , c la s s ic a l c o n d it io n in g , a n d s p a ti a l l ea rn in g : R o le o f th e h i p p o c a m p u s . In W o r ld C o n g r es s o n N e u r a l N et w o r k s , 2 (p p .II 7 2 3 ±II 7 2 8 ). S a n D i e g o : IN N S P re s s . S c h m a ju k , N ., & D i C a rlo , J . (1 9 9 0 ). B a c k p ro p a g a ti o n , c la ss i ca l c o n d i tio n in g a n d h i p p o ca m p a l fu n c t io n (T ec h n i ca l R ep o rt, N o rth w es t er n U n iv e rs ity ). S c h m a ju k , N ., &

M o o re , J . (1 9 8 5 ) . R e a l-t im e a tt e n t io n a l m o d e ls fo r c l as s ic a l c o n d i ti o n i n g .

P h y s io l o g ic a l P s y c h o lo g y , 1 3 (4 ), 2 7 8 ±2 9 0 . S c h m a lz , L ., & T h e io s , J . (1 9 7 2 ). A c q u i s itio n a n d e x t in c tio n o f a c la s s ic a ll y co n d i tio n ed r es p o n se i n h i p p o ca m p e c to m iz e d r ab b its (O r yc t o l a g u s c u n ic u lu s ). J o u r n a l o f C o m p a r a tiv e a n d P h y s io lo g i c a l P s y c h o lo g y, 7 9 , 3 2 8 ±3 3 3 . S h a n k s , D .R . (1 9 9 1 ) . C a t e g o ri z a t io n

by

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P s y c h o lo g y: L e a r n i n g , M em o r y , & C o g n itio n , 1 7 (3 ), 1 ±1 1 . S h a n k s , D .R ., & G lu ck , M .A . ( 1 9 9 4 ). T e s ts o f a n a d a p tiv e n e t w o rk m o d el fo r t h e id e n tifi ca t io n , c a te g o riz a ti o n a n d re c o g n i tio n o f c o n t in u o u s -d i m e n s io n st im u li. C o n n e c tio n S c i en c e , 6 (1 ), 5 9 ±8 9 . S h e p a rd , R . (1 9 5 8 ). S tim u lu s an d re s p o n se g e n e ra li z ati o n : D e d u c t io n o f th e g en e ra li za t io n g ra d i en t fro m a t ra c e m o d e l . P s y c h o lo g i c a l R e v ie w , 6 5 , 2 4 2 ±2 5 6 . S i lv ei ra , J ., & K im b le , D . (1 9 6 8 ). B rig h t n e s s d i s cri m in a ti o n a n d re v e rs a l i n h i p p o c a m p a ll y -l e si o n e d ra ts . P h y s io lo g y a n d B e h a v io r, 3 , 6 2 5 ±6 3 0 . S o lo m o n , P . (1 9 7 7 ) . R o le o f t h e h ip p o c am p u s in b lo c k in g a n d c o n d it io n e d i n h ib itio n o f th e ra b b it ’ s n i c tita tin g m e m b ra n e . J o u r n a l o f C o m p a r a ti ve a n d P h y s io lo g ic a l P s y c h o lo g y, 9 1 (2 ), 4 0 7 ±4 1 7 . S o lo m o n , P ., & M o o re , J. (1 9 7 5 ). L a te n t in h ib itio n a n d st im u lu s g e n e ral iz a ti o n o f th e c l as s ic a ll y c o n d itio n e d n i c titat in g m e m b ra n e re s p o n se in ra b b it s (O r y ct o l a g u s c u n ic u lu s) fo llo w in g d o rs a l h i p p o ca m p a l a b la t io n . J o u r n a l o f C o m p a r a tiv e a n d P h y s io lo g ic a l P s yc h o lo g y, 8 9 , 1 1 9 2 ±1 2 0 3 . S o lo m o n , P .R ., S to w e , G .T ., & P e n d le b u ry , W .W . (1 9 8 9 ). D i sru p te d e y el id c o n d itio n in g in a p a tie n t w ith d am a g e to c e re b e lla r a ffe re n t s. B e h a v io r a l N e u r o s c ie n ce , 1 0 3 (4 ), 8 9 8 ±9 0 2 . S q u ire , L . (1 9 8 7 ). M e m o r y a n d b r a i n . N e w Y o rk : O x fo rd U n i v e rs it y P r es s . S q u ire , L ., & F ra m b a ch , M . (1 9 9 0 ). C o g n it iv e s k ill l e a rn i n g in a m n e s ia . P s y c h o b io lo g y, 1 8 (1 ), 1 0 9 ± 11 7 . S t a n to n , P ., & S e jn o w s k i, T . (1 9 8 9 ). A s s o c iat iv e lo n g -te rm d e p re s s io n i n t h e h ip p o c a m p u s in d u c e d b y H e b b ia n co v ar ia n c e . N a tu re , 3 3 9 , 2 1 5 ±2 1 8 . S u th e rla n d , N ., & M a c k in to sh , N . (1 9 7 1 ). M e ch a n i sm s o f a n im a l d is c r im in a t io n l e a r n in g . N ew Y o rk : A c a d e m i c P r es s . S u th e rla n d , R ., & R u d y , J . (1 9 8 9 ). C o n fig u ral a ss o c ia ti o n th e o ry : T h e ro le o f t h e h ip p o c a m p a l fo r m at io n in le a rn in g , m e m o ry a n d a m n es i a. P s yc h o b io lo g y , 1 7 (2 ), 1 2 9 ±1 4 4 . S u tt o n , R ., & B a rt o , A . (1 9 8 1 ). T o w a rd a m o d e rn th e o ry o f ad a p tiv e n e t w o rk s : E x p e c t at io n a n d p re d ic t io n . P s y c h o l o g ic a l R e v ie w , 8 8 , 1 3 5 ±1 7 0 . T e rra c e , H . (1 9 6 3 ) . D is c rim i n a tio n le a rn i n g w ith a n d w it h o u t `è rro rs ’ ’ . Jo u rn a l o f E x p e r im e n t a l A n a l y si s o f B e h a v io r, 6 (1 ), 1 ±2 7 . T h o m p s o n , R . (1 9 7 1 ). S e n so ry p re c o n d i tio n in g . In R . T h o m p s o n & J . V o s s (E d s .), T o p ic s i n le a rn in g a n d p e rf o r m a n c e (p p .1 0 5 ±1 2 9 ). N e w Y o rk : A c a d e m ic P re s s . T h o m p s o n , R . (1 9 8 6 ). T h e n e u ro b i o l o g y o f le a rn i n g a n d m e m o ry . S c i e n c e , 2 3 3 , 9 4 1 ±9 4 7 . T h o m p s o n , R . (1 9 9 0 ). N e u ra l m e ch a n i sm s o f cl a ss i ca l c o n d it io n in g . P h ilo s o p h i ca l T ra n sa c tio n s o f th e R o y a l S o c ie ty , L o n d o n [B io lo g y ], 3 2 9 1 6 1 ±1 7 0 .

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G LU C K E T AL .

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