rebersquire-lm1994

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10.1101/lm.1.4.217Access the most recent version at doi:1994 1: 217-229Learn. Mem.

P J Reber and L R SquireParallel brain systems for learning with and without awareness.

References

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1994 Cold Spring Harbor Laboratory Press

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Paralle l Bra in S y s t e m s for L earning w i tha n d w i t h o u t A w a r e n e s sP a u l J . R e b e r I a n d L a r r y R . S q u i r e 2 -41Department of PsychiatryUniversity of C alifornia S choo l of M edicineLa J011a, Calif0m ia 920932Department of Psychiatry and Neur0scienceUniversity of C alifornia S choo l of M edicineLa J011a, Calif0rnia 920 933Veterans Affairs Med ical Cen terSan Diego, California 92161-2002

Ab s t r a c t

A f u n d a m e n t a l i s s u e a b o u t m e m o r y a n di t s d i f f e re n t f o r m s i s w h e t h e r l e a r n i n g c a no c c u r w i t h o u t t h e d e v e l o p m e n t o fc o n s c i o u s k n o w l e d g e o f w h a t is l e a r n e d .A m n e s i c p a t ie n t s a n d c o n t r o l s u b j e c tsp e r f o r m e d a s e r i a l r e a c t i o n t i m e t a s k ,e x h i b i t i n g e q u i v a l e n t l e a r n i n g o f a ni m b e d d e d r e p e a t i n g s e q u e n c e a s m e a s u r e db y g r a d u a l ly i m p r o v i n g r e a c t i o n t i m e s . I nc o n t r a s t , f o u r t e s t s o f d e c l a r a t i v e ( e x p l i c i t )k n o w l e d g e i n d i c a t e d t h at t h e a m n e s i cp a t i e n ts w e r e u n a w a r e o f t h e i r k n o w l e d g e .M o r e o v e r , a f t e r t a k i n g t h e t e s t s o fd e c la r a ti v e m e m o r y , a l l su b j e ct s c o n t i n u e dt o d e m o n s t r a t e t a ci t k n o w l e d g e o f t h er e p e a t i n g s e q u e n c e . T h i s d i ss o c i a t i o nb e t w e e n d e c l a r a t i v e a n d n o n d e c l a r a t i v ek n o w l e d g e i n d i c a te s t h a t t h e p a r a l l e l b r a i ns y s t em s s u p p o r t i n g l e a r n i n g a n d m e m o r yd i f fe r i n t h e i r c a p a c i ty f o r a f f o r d i n ga w a r e n e s s o f w h a t i s l e a r n e d .

I n t r o d u c t i o nM e m o r y i s n o t a s i n g l e f a c u l t y b u t i s c o m -

p o s e d o f m u l t i p l e a b i l it i es s u p p o r t e d b y d i s t i n c tb r a i n s y s t e m s ( T u l v i n g 1 9 8 5 ; S c h a c t e r 1 9 8 7 ;W e i s k r a n t z 1 9 8 7 ; S q u i r e 1 9 9 2 ; S c h a c t e r a n d T u lv -i n g 1 9 9 4 ) . A k e y i d e a i s t h a t s o m e f o r m s o f le a r n -i n g a n d m e m o r y a r e i m p l i c i t ( o r n o n d e c l a r a t i v e )a n d a r e e x p r e s s e d t h r o u g h p e r f o r m a n c e w i t h o u t4 C o r r e s p o n d i n g a u t h o r .

r e q u i r i n g a c c e s s t o c o n s c i o u s m e m o r y . P e r h a p st h e m o s t f a m i l i a r e x a m p l e i s m o t o r s k i l l l e a r n i n g( M i lD e r 1 9 6 2 ; B r o o k s a n d B a d d e l e y 1 9 7 6 ; E s l in g e ra n d D a m a s i o 1 9 8 6 ) , b u t n o n d e c l a r a t i v e m e m o r ya l so i n c l u d e s p e r c e p t u a l a n d c o g n i t i v e s k il ls , h a b -i t s, adap ta t ion- leve l e f fec ts , s imple fo rm s o f cond i -t io n i n g, a n d t h e p h e n o m e n o n o f p r i m i n g ( S c h a c t e re t a l . 1993 ; Squ i re e t a l . 1993 ; Sege r 1994) . Non-d e c l a r a t i v e m e m o r y , w h i c h d e p e n d s v a r i o u s l y o nt h e s t r i a t u m , c e r e b e l l u m , a m y g d a l a , a n d n e o c o r -t e x , c a n b e c o n t r a s t e d w i t h d e c l a r a t i v e m e m o r y ,w h i c h s u p p o r t s c o n s c i o u s r e c o l l e c t i o n s a b o u tf a c t s a n d e v e n t s a n d d e p e n d s o n t h e i n t e g r i t y o fl i m b i c a n d d i e n c e p h a l i c b r a i n s t r u c t u r e s ( M i s h k i na n d P e t r i 1 9 8 4 ; T h o m p s o n 1 9 9 0 ; T u l v i n g a n dS c h a c t e r 1 9 9 0 ; S q u i r e 1 9 9 2 ; Z o l a - M o r g a n a n dS q u i r e 1 9 9 3 ) .

A n o t h e r v i e w t h a t h as e m e r g e d f r o m t h e s t u d yo f i m p l i ci t m e m o r y h a s b e e n t h a t c o n s c i o u sk n o w l e d g e i s i n v a r i a b l y a v a i l a b l e w h e n i m p l i c i tm e m o r y ( e . g . , s k i l l s a n d h a b i t s ) i s a c q u i r e d , a n dt h a t c o n s c i o u s a n d n o n c o n s c i o u s e x p r e s s i o n s o fk n o w l e d g e s i m p l y r e f l e c t d i f f e r e n t u s e s o f a c o m -m o n u n d e r l y i n g k n o w l e d g e b a s e ( D u l a n y e t a l .1 9 8 4; P e r r u c h e t a n d A m o r i m 1 9 9 2 ; P e r r u c h e t a n dG a l l e g o 1 9 9 3 ; W h i t t l e s e a a n d D o r k e n 1 9 9 3 ;S h a n k s a n d S t. J o h n 1 9 9 4 ) . B y t h i s v i e w , w h e n t e s t sa r e s u f f ic i e n tl y s e n s it i v e , i m p r o v e m e n t o f p e rf o r -m a n c e o n a n i m p l i c i t t a s k s h o u l d a l w a y s p a r a l l e lc l os e ly t h e d e v e l o p m e n t o f c o n s c i o u s k n o w l e d g ea b o u t w h a t i s l e a r n e d .

W e h a v e s t u d i e d t h e s e r i a l r e a c t i o n t i m e( S R T ) t a s k ( N i s s e n a n d B u l l e m e r 1 9 8 7 ; W i l li n g -h a m e t a l . 1 9 8 9 ) , w h i c h h a s f i g u r e d i m p o r t a n t l y i nr e c e n t w o r k o n i m p l i c i t l e a r n i n g a n d a w a r e n e s s( C o h e n e t a l . 1 9 9 0 ; H o w a r d e t a l . 1 9 9 2 ; S t a d l e r

LEARNING & M EMO RY 1 :217 -229 1994 by Co ld Sp r i ng Ha rbo r Labo rato ry Press ISSN1072-0502 /94 $5 .00

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1 9 8 9 ; C u r r a n a n d K e e l e 1 9 9 3 ; P a s c u a l - L e o n e e t a l .1 9 9 3 ; F r e n s c h e t al . 1 9 9 4 ; R e e d a n d J o h n s o n1 9 9 4 ) . T o a s s e s s t h e c a p a c i t y f o r l e a r n i n g t h i s ta s ki n t h e a b s e n c e o f t h e c a p a c i t y t o d e v e l o p c o n -s c i o u s k n o w l e d g e a b o u t w h a t i s l e a r n e d , w e s t ud -i e d a m n e s i c p a t i en t s , w h o h a v e s e l e c t i v e l y i m -p a i r ed d e c l a r a ti v e m e m o r y d u e t o m e d i a l te m p o -r a l l o b e o r d i e n c e p h a l i c b r a i n d a m a g e ( S c h a c t e r e ta l . 1993 ; Squ i r e e t a l . 1993 ; Sege r 1994) . F i na l l y ,w e a s s e ss e d c o n s c i o u s k n o w l e d g e f o r w h a t s u b -j e c t s l e a r n e d i n t h e S R T t a s k w i t h f o u r d i f f e r e n tt e s t s t h a t h a v e b e e n u s e d i n p r e v i o u s s t u d i e s o ft h i s t a s k ( v e r b a l r e p o r t , p r e d i c t i o n , r e c o g n i t i o n ,a n d g e n e r a t i o n ) .

Experiment 1M a t e r i a l s a n d M e t h o d sSUBJECTSA M N E S I C P A T I E N T S

N i n e a m n e s i c p a t i e n t s ( s i x m e n , t h r e ew o m e n ) , w e r e t e s te d . F o r e i g h t o f t h e p a t ie n t s ,b i l a te r a l d i e n c e p h a l i c ( n - - - 6 ) o r h i p p o c a m p a l l e-s i o n s ( n - 2 ) h a v e b e e n c o n f i r m e d b y q u a n t i t a t iv en e u r o i m a g i n g ( S q u i r e e t al. 1 9 8 9 , 1 9 9 0 ; P o l i c h a n dSqu i r e 1993 ; f o r p a t i en t s N .F. , M.G ., and L .J . ( L.R.S q u i r e a n d G . A . P r e s s , u n p u b l . ) . T h e r e m a i n i n g p a -t i e n t ( H . W . ) h a d p r e s u m e d d i e n c e p h a l i c d a m a g ea s s o c i a te d w i t h K o r s a k o f f s s y n d r o m e . A l l p a t i e n t sT a b l e 1 : Cha racteristics of am nesic patients

a r e w e l l c h a r a c t e r i z e d n e u r o p s y c h o l o g i c a l l y ( T a -b l e s 1 a n d 2 ) . T h e y a v e r a g e d 6 7 . 9 y e a r s o f a g e a tt h e t im e o f t h e s t u d y ( r a n g e , 5 9 - 8 1 ) a n d h a d a na v e r a g e o f 1 3 y e a r s o f e d u c a t i o n . I m m e d i a t e a n dd e l a y e d ( 1 2 m i n ) r e c a ll o f a s h o r t p r o s e p a s s a g ea v e r a g e d 3 . 7 an d 0 s e g m e n t s , r e s p e c t i v e l y ( m a x i -m u m n u m b e r o f s e g m e n t s , 2 1 ; G i lb e r t e t al. 1 9 6 8 ) .S c o r e s o n o t h e r m e m o r y t e s t s a p p e a r i n T a b l e s 1a n d 2 . T h e m e a n s c o r e o n t h e D e m e n t i a R a t in gS c al e w a s 1 3 2 .3 [ m a x i m u m p o s s i b l e s c o r e , 1 4 4( M a t t is 1 9 7 6 ) ] . M o s t o f t h e p o i n t s t h a t w e r e l o s tw e r e o n t h e m e m o r y s u b p o r t i o n o f t h e t e st ( m e a np o i n t s l o s t = 6 . 9 ) . T h e m e a n s c o r e f o r t h e B o s t o nN a m i n g T e s t w a s 5 6 . 2 [ m a x i m u m s c o r e = 6 0 ( K a p -l a n e t a l . 1 9 8 3 ) ] . S c o r e s f o r n o r m a l s u b j e c t s o nt h e s e t e s t s c a n b e f o u n d e l s e w h e r e ( J a n o w s k y e ta l . 1 9 8 9 ; S q u i r e e t a l . 1 9 9 0 ) . T w o a d d i t i o n a l a m -n e s i c p a t i e n t s w e r e e x c l u d e d b e c a u s e o f t h e i r e x -t r e m e l y s l o w r e a c t i o n t i m e s o n t h e f i rs t b l o c k o ft h e t a s k ( > 1 0 0 0 m s e c , m o r e t h a n 2 . 0 S.D . s l o w e rt h a n t h e o t h e r s u b j e c t s ) , e v e n t h o u g h t h e y o t h e r -w i s e e x h i b i t e d g o o d l e a r n i n g o f t h e S R T t as k .

C O N T R O L S U B J E C T S

F o r t y - e ig h t c o n t r o l s u b j e c t s ( 1 8 m e n a n d 3 0w o m e n ; a v e r a g e a g e , 6 4 . 3 ; r a n g e , 4 0 - 7 7 ; a v e r a g ee d u c a t i o n , 1 4 y e a r s ) w e r e a l so t e s te d . T h e y w e r ea s s i g n e d t o t h r e e d i f f e r e n t g r o u p s ( C O N - 1 , n - 1 2 ;C O N -2 , n = 1 2 ; R a n d o m , n = 2 4 ) . O n e a d d i t io n a lc o n t r o l s u b j e c t w a s e x c l u d e d b e c a u s e o f h e r s l o w

W M S - RA g e W A I S - RPa t ie n t L e s io n a ( ye a rs ) IQ a t te n t io n ve rb a l v isu a l g e n e ra l d e la yN . A . D i e n 5 5 1 0 9 1 0 2 6 7 8 9 6 8 7 1M . G . D i e n 6 1 9 7 9 2 9 7 7 7 8 9 7 2R . C . D i e n ( K) 7 7 1 0 6 1 1 5 7 6 9 7 8 0 7 2N . F . D i e n ( K) 5 8 9 4 9 1 6 2 7 3 5 3 < 5 0P.N. D ie n (K) 6 6 9 9 8 1 7 7 7 3 6 7 5 3H . W . D i e n ( K) b 7 6 1 0 9 9 7 8 4 1 0 2 8 9 5 4J . W . D i e n ( K) 5 7 9 8 1 0 4 6 5 7 0 5 7 5 7P.H . HF 7 2 1 1 5 1 1 7 6 7 8 3 7 0 5 7L .J . H F 5 6 9 8 1 0 5 8 3 6 0 6 9 < 5 0M e a n 6 4 . 2 1 0 2 . 8 1 0 0 . 4 7 5 . 3 8 0 . 4 7 1 . 3 5 9 . 6The Wechs le r Ad u l t In te l ligence Sca le -Rev ised (WAIS-R) and the Wechs le r Mem ory Sca le -Rev ised (WMS -R) ind ices y ie lda mean score o f 100 in the normal popu la t ion wi th a S.D. o f 15 . The WM S-R d oes no t p rov ide scores fo r sub jects who scorebe low 50 . There fo re , the tw o scores be low 50 were sco red as 50 fo r ca lcu la t ing a g roup mean.a(HF) Hippocampal Formation; (Dien) d iencephalon; (K) Korsakoff 's syndrome.bThe lesion site has not been co nfirm ed rad iolog ical ly but is supported by the et io logy of amnesia (see text).

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T a b l e 2 : Me mo ry test performanceW o r d W o r d

D i a g r a m P a i re d r e c a ll r e c o g n i t i o n W o r d s F a ce sP a t i en t r eca l l assoc ia t i ons ( %) ( %) ( 50 ) ( 50 )N . A . 1 7 0 - 0 - 2 4 9 9 3 3 4 4 2M . G . 6 1 - 2 -8 5 2 8 9 3 0 3 4R .C . 3 0 - 0 - 3 19 85 37 30N . F . 4 0 - 0 - 2 3 6 7 6 2 8 2 7P .N . 2 1 - 1 -1 29 83 31 31H . W . 6 0 - 1 - 0 3 1 8 5 2 3 2 2J . W . 4 0 - 0 - 2 2 8 9 6 2 9 3 4P . H . 3 0 - 0 -1 2 7 8 4 3 6 3 4L.J. 3 0 - 0 - 0 4 0 9 3 3 3 2 9M e a n 5 . 3 0 . 2 - 0 . 4 - 2 . 1 3 4 . 6 8 7 .1 3 1 . 2 3 1 . 4H e a l t h y

(n = 8 ) 2 0 . 6 6 . 0 - 7 . 6 - 8 . 9 7 1 9 8 4 1 .1 3 8 .1A l c o h o l i c s

( n = 8 ) 1 6 . 4 5 . 1 - 8 . 0 - 8 . 8 6 2 9 7 3 6 . 2 3 6 . 2The diagram recal l score is bas ed on delayed (12 -min) rep roduc t ion of the Rey-O sterr ieth f igure (Osterr ieth 1944 ;m ax im um score = 36). The average score for cop ying the f igure was 28.4, a norm al score (Kr i tchevsky et al . 1988). Thepaired associate scores are the num ber of wo rd p airs recal led o n three successive tr ials (m ax imu m score = 10/tr ial) . Thewo rd recal l score is the percentage of words iden t i f ied co rrect ly on f ive successive stud y-test t r ials (Re y 1964). The wo rdrecogni t ion score is the percentage of words ident i fied cor rect ly by yes/no recogni t ion across f ive success ive s tudy- testt ria ls . The score for words and faces is based on a 24 -hr recogn i t ion test o f 50 w ords or 5 0 faces (modi f ied f rom Wa rr ington1984; m axim um score = 50, chance = 25) . The mean scores for heal thy cont ro l and a lcohol ic , nonam nesic sub jectsshown for these tests are f rom Squi re and Shimam ura (1986) .

r e a c t i o n t i m e s o n t h e f i rs t b l o c k o f t h e t a s k ( 9 7 9m s e c , > 2 . 0 S .D . s l o w e r t h a n t h e o t h e r s u b j e c t s ) ,e v e n t h o u g h s h e e x h i b i t e d g o o d l e a r n i n g o f t h eS R T t a s k .

MATERIALST h e S R T t a sk w a s p r e s e n t e d o n a M a c i n t o s h

C o l o r C l a s s ic I I. F o u r d a s h e s ( 0 . 4 c m i n w i d t h a n d3 . 4 c m a p a r t ) a p p e a r e d c o n t i n u o u s l y 1 .2 c m f r o mt h e b o t t o m o f t h e s c r e e n t o d e n o t e t h e p o s s i b l el o c a t i o n s o f f o u r c u e s ( A , B, C , D ) . E a c h c u e w a s a na s t er i sk 0 .4 c m w i d e a p p e a r i n g 4 . 2 c m a b o v e o n eo f t h e d a s h es . R e s p o n s e s w e r e m a d e o n t h e c o m -p u t e r k e y b o a r d , u s i n g t h e f o u r k e y s " x , " " v, " " n , "a n d " ," , w h i c h w e r e d i r e c t l y b e n e a t h t h e f o u rd a s h es . T h e s e k e y s w e r e m a r k e d w i t h r e d a s t e r is k st o i n d i c a t e w h e r e s u b j e c t s s h o u l d p l a c e t h e i r f in -g e r s. S u b j e c t s u s e d t w o f i n g e r s f r o m e a c h h a n d ,u s u a l l y t h e f ir s t a n d s e c o n d d i g i t s , a n d w e r e i n-s t r u c t e d t o m a i n t a i n c o n t a c t w i t h t h e f o u r k e y s

t h r o u g h o u t t r a i n in g . P r i o r t o t r a i n i n g , s u b j e c t s r e -c e i v e d 2 0 p r a c t i c e t r ia l s w i t h a r a n d o m s e q u e n c e .

PROCEDUREC u e s c o u l d a p p e a r s e q u e n t i a l l y in a n y o n e o f

t h e f o u r l o c a t i o n s o n t h e c o m p u t e r s c r e e n . S ub -j e c ts r e s p o n d e d t o e a c h c u e a s r a p i d l y as p o s s i b leb y p r e s s i n g a k e y d i r e c t l y b e n e a t h t h e c u e . F i v eh u n d r e d m i l l i s e c o n d s a f te r e a c h r e s p o n s e , a c u ea p p e a r e d a t a n e w l o c a t i o n . F o r a ll f o u r g r o u p s( A M N , C O N - 1, C O N - 2 , a n d R a n d o m ) , t r a i n i n g c o n -s i s t e d o f 4 0 0 t r im s w i t h ~ 3 0 - s e c r e s t s a f t e r e a c hb l o c k o f 1 0 0 tr i m s ( T a b l e 3 ) .

S E Q U E N C E L E A R N I N G IF o r t h e a m n e s i c p a t i e n t s ( A M N , n = 9 ) a n d

o n e g r o u p o f c o n t r o l s u b j e c t s ( C O N - l , n = 1 2) , as e q u e n c e o f 1 0 l o c a ti o n s ( D B C A C B D C B A ) re -p e a t e d e v e r y 1 0 t r im s t h r o u g h o u t t r a i n i n g (i .e . , 4 0

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T a b l e 3 : Te st order for Exper iment 1T es t A M N C O N - 1 C O N - 2 R a n d omS R T ( S eque nce I) x xV e r b a l r e p o r t x xP r e d i c t i o n x xSRT (Se que nce I I) x xV e r b a l r e p o r t x xR e c o g n i t i o n x xG e n e r a t i o n x x

XX XX a XX X

(x) Each test taken by subjects in each group . (A MN ) 12amnesic patients ; (C ON - l , CO N-2) 12 cont ro l sub jectseach; (Random) 24 subjects given a random sequence.Ha lf of the Random subjects were given the tests in thetop panel; the other half were given the tests in thebot tom panel .aThe CO N-2 group wa s g iven a d i fferent recogni t ion testthat d id not measure exp l ic i t knowledge successfu l ly(see text).

repetitions of a l O-trial pattern). Subjects were nottold that the training trims contained a repeatingsequence. The subjects assigned to the Randomgroup (n = 24) received 400 training trims with arandom sequence, constructed such that each ofthe four cue locations appeared equally often ( 1O0times each during the 400 training trials).

Immediately following the SRT task, the am-nesic patients, th e CON-1 group, and 12 of the 24Random subjects were given two tests of explicitknowledge: verbal report and prediction. (The re-maining 12 Random subjects were given threetests of explicit knowledge; see Sequence LearningII, below).

VERBAL REPOR T

Subjects were first asked three questions todetermin e thei r appreciation of the repeating se-quence: "Do you think the asterisks appeared ran-domly, or did you think there was some pattern tothe sequence?"; "Did the asterisks appear moreoften in some positions than in others?"; "Did younotice a pattern or repeating sequence?" Subjectswho answered the latter question affirmativelywere then asked to report the sequence eitherverbally or by pointing to the screen. Subjects whoanswered negatively wer e told, "Suppose for a mo-ment that the asterisks did follow a sequence.Please show me as much of that sequenc e as youcan, even if you have to guess."

PREDICTION TASKS

The first target location of the sequence waspresented, and subjects were asked to predict thenext target location. Subjects responded at theirown pace by pressing the key under the locationwhere they thought the cue would appear next.Subjects were instructed to make their predictionsbased on how the cues appeared during training. Ifthey guessed correctly, the cue appeared in thatlocation. Otherwise, subjects continued to guessuntil they were correct. This procedure continueduntil 200 trials of the training sequence had beenpresented (i.e., 20 repetitions of the lO-trial pat-tern).

SEQUENCE LEARNING IIIn a second session (mean = 73 days later), the

same amnesic patients (AMN), the same controlsubjects (CON-l), and 12 new control subjects(CON-2), completed 400 training trials with a dif-ferent repeating sequence (blocks 1-4, BADCD-ABDAC), followed by three tests of explicit knowl-edge: verbal report, a recognition memory task,and a generation task. The verbal report task wasidentical to the one used for Sequence Learning I.

RECOGNITION MEMORY TASKSubjects saw five lO-item sequences pre-

sented according to the procedure used for train-ing. One of the sequences was the one presentedduring training. The other four sequences (foils)were constructed such that within each sequencetwo cue locations appeared twice and two ap-peared three times, for example, BDABDCBCAD.After each sequence was presented, subjects ratedit from 0 to 100 according to whether they weresure that the sequence had not appeared duringtraining (0) or sure that the sequence had ap-peared (100). The score was the rating given thecorrect sequence minus the average rating giventhe four incorrect sequences. The order of the fivesequences was presented to half of the subjects ineach group in one fLxed order and to half the sub-jects in the reverse of that order, with the correctsequence always appearing in either the second orfourth positions. The results did not change whenthe ratings given the first and last sequences(which were always incorrect) were discarded.

The CON-2 group was given a recognition

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memory test different than the one describedhere. The recognition test that was used was basedon one described by Perruchet and Amorim(1992). Subjects were presented with four-itemsubsequences drawn from the original training se-quence. Subjects saw 10 such target subsequencesand 10 foils (randomly intermixed) and made ayes/no recognition judgment after the presenta-tion of each sequence. Overall control subjectswer e c orr ect only 52.5% (S.E. 3.0) of the time, no tsignificantly different from chance (t0.10]. In the first session, boththe control and amnesic groups exhibited knowl-edge of the sequence as indicated by a gradualdecrease in reaction times comp ared wi th the Ran-dom group (Fig. 1A). Separate analyses of variance(ANOVAs) yielded significant within-subject ef-fects of block [F (3,93 ) = 6.06, P


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of block [F(3,57) = 13.0, P


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LEARNING WITH AND WlTHOUT AWARENESS

The random subjects were also rescored, based onthe first seven locations of their verbal reportsyielding a score of 2.62---0.18, and this value wasused as a replacement score for the amnesic pa-tients who did not guess. Using these revised mea-sures, the control subjects continued to scoremarginally higher than the amnesic patients[t(31)= 1.85, P


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than in the random sequence. In the two trainingsequences that we used (DBCACBDCBA and BAD-CABDAC), three locations appeared twice every10 trials and two locations appeared once. In therandom sequence, all four locations appearedequally often.

A direct test of the frequency-learning inter-pretation can be conduc ted by presenting trainingtrims such that each location in the repeating se-quence occurs equally often. In this way, the fre-quency distribution of the four locations duringtraining is the same as in the random sequence.Any speed advantage of the repeating sequenceover the random sequence would indicate thatsubjects are learning more than just frequency in-formation, that is, sequential probabilities aboutthe structu re of the sequence itself.

M a t e ri al s a n d M e t h o d sSUBJECTS

Eight of the nine amnesic patients who partic-ipated in Experime nt 1 also participated in Exper-iment 2. Patient J.W. was not included in Experi-ment 2 because of his extremel y slow reactiontimes on the first block of the task (805 msec,>3.0 S.D. slower than the other subjects) eventhough he otherwise exhibited normal learning ofthe SRT task. Subsequently, we de termi ned that hehad been ill.

The 12 control subjects who received a ran-dom sequence of trials in the first session of Ex-periment 1 served as control subjects for Experi-ment 2.

MATERIALSThe SRT task was presented using the same

computer equipment as in Experiment 1. A 12-item repeating sequence (BCDBADACABDC)wasconstructed such that the frequency of locationsand the transition frequency between locationswas balanced. Specifically, each location occu rredthree times in the repeating sequence, and eachtransition (e.g., AB, AC, AD, BA, BC, BD, etc.) oc-curred once. Accordingly, reaction time improve-ment on this task could not result simply by learn-ing about frequency or transition frequency. Each96-trial block of training consisted of eight repeti-

tions of the sequence for 96 trials. Four blockswere administered for a total of 384 training trials.

PROCEDUREAll subjects completed four blocks of training

trims with the 12-item sequence, followed by twotests of explicit knowledge: verbal report and rec-ognition memory. The verbal report task was iden-tical to the one given in Experiment 1. The recog-nition memory task was identical except that thefour incorrect sequences (foils)were all 12-itemsequences balanced for frequency. These two testswere followed immediately by an additional blockof 96 training trials with the same repeating se-quence and then by a final block of 96 trials witha random sequence in which all four locations ap-peared equally.

R e s u l t sSEQUENCE LEARNING III

Scores for each 96-trial block wer e calculatedas the mean of the median reaction times, exclud-ing errors, for each 12-trial repetition of the se-quence. The amnesic patients made errors on anaverage of 3.1% of trials, wher eas cont rol subje ctsmade errors on an average of 2.6% of trials[F(1 ,18) < 1.0 ]. A 2 4 ANOVA co mpa rin g perfor-mance of the two groups with repeated measuresacross the first four training blocks indicated im-prove ment across blocks [F(3,54) = 4.08, P


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, ~ 5 5 0

45 0

Sequence Learning III

AMN ( 8)CON-3 (12)

I I I I l I1 2 3 4 5 6B l o c k ( 9 6 T r i a ls ) R a n d o m

Figure 3: Performance of amnesic pat ients (AMN) andcontrol subjects (CON-3) on a 12- i tem repeat ing se-quence ba lanced for the f requency w i th which the fourlocations appeared. Both groups exh ib i ted know ledge ofthe sequence by decreasing their react ion t imes ( /ef t) .The increase in react ion t imes on the f inal block of ran-dom tr ials indicates that knowledge of the repeat ing se-quence was present dur ing b lock 5 (right). The numberof subjects in each grou p is sho wn in parentheses. Thestandard er ror o f the mean ranged f rom 15 to 31 msec.

s e q u e n c e t h a t w a s r e p o r t e d ( F ig . 4 A ). C o n t r o l s u b -j e c ts r e p o r t e d 3 . 8 3 e l e m e n t s o f t h e r e p e a t i n g s e -q u e n c e , s i g n if i ca n t ly m o r e t h a n t h e 2 . 6 9 e l e m e n t sr e p o r t e d b y t h e a m n e s i c p a ti e n t s [ t ( 1 8 ) = 2 . 3 2 ,P < O . 0 5 ] . T h r e e o f t h e a m n e s i c p a t i e n t s w e r e u n -w i l l i n g t o g u e s s , m a i n t a i n i n g t h a t t h e r e w a s n os e q u e n c e . T o e s t i m a t e a s c o r e f o r t h e s e t h r e e p a -t ie n t s , t h e r e s p o n s e s t h a t h a d b e e n m a d e b y t h ec o n t r o l s u b j e c t s a f t e r s e e i n g a r a n d o m s e q u e n c e( i n E x p e r i m e n t 1 , S e q u e n c e L e a r n i n g I) w e r es c o r e d t o d e t e r m i n e h o w m u c h o f t h e r e p e a ti n gs e q u e n c e i n E x p e r i m e n t 2 t h e y h a d g e n e r a t e d ( b yc h a n c e ) . T h e s e r e p o r t s c o n t a i n e d a n a v e r a g e o f2 . 8 3 e l e m e n t s o f th e 1 2 - i te m s e q u e n c e . A c c o r d -i n gl y , t h e t h r e e a m n e s i c p a t i e n t s w h o d i d n o tg u e s s w e r e a s s i g n e d t h i s v a l u e a s t h e i r s c o r e f o rt h e v e r b a l r e p o r t t e s t ( t h e m e a n n u m b e r o f e le -m e n t s r e p o r t e d c o r r e c t l y b y th e p a t ie n t s w h o d i da t t e m p t t o r e p o r t a s e q u e n c e w a s 2 . 6 0 ) . T h e r e s u ltw a s t h e s a m e w h e n t h e t h r e e p a t ie n t s w h o d i d n o tg u e s s w e r e a s s i g n e d s c o r e s e q u a l t o t h e a v e r a g e o ft h e o t h e r p a t ie n t s [ t ( 1 8 ) = 2 . 2 1 , P < 0 . 0 5 ] . T h u s ,t h e a m n e s i c p a t i e n t s c o u l d r e p o r t t h e r e p e a t i n gs e q u e n c e n o b e t t e r t h a n c o n t r o l s u b j e ct s w h o s a wa r a n d o m s e q u e n c e .

I t i s u n l i k e l y t h a t t h e r e s u l t s c o u l d h a v e b e e ni n f l u e n c e d b y a l e s s e r w i ll i n g n e s s o f t h e a m n e s i cp a t i e n t s t o s e l e c t l o c a t i o n s . T h e c o n t r o l s u b j e c t ss e l e c t e d a n a v e r a g e o f 8 .5 l o c a t i o n s , a n d t h e a m -n e s i c p a t i e n t s w h o g u e s s e d s e l e c t e d a n a v e r a g e o f9 . 4 l o c a t i o n s .

RECOGNITION MEMORY TESTN e i t h e r g r o u p d e m o n s t r a t e d m e a s u r a b l e

( a b o v e z e r o ) r e c o g n i t i o n o f t h e r e p e a t i n g s e -q u e n c e ( F i g. 4 B ). T h e m e a n s c o r e f o r t h e a m n e s i cp a t i e n t s w a s - 2 . 5 - - - 1 2 ) ; t h e m e a n s c o r e f o r t h ec o n t r o l s u b j e c t s w a s 4 . 1 _ 1 2 ) . T h e t w o g r o u p sp e r f o r m e d s i m i l a r l y [t ( 1 8 ) < 1 . 0] .

D i s c u s s i o nA l t h o u g h t h e a m n e s i c p a t i e n t s l e a r n e d 1 O- a n d

1 2 - it e m s e q u e n c e s a s w e l l a s c o n t r o l s u b j e c t s( F ig s . 1 a n d 3 ) , o n l y t h e c o n t r o l s u b j e c t s d e v e l -o p e d d e c la r a ti v e k n o w l e d g e a b o u t w h a t t h e y h a dl e a r n e d ( F i g s . 2 a n d 4 ) . T h e c o n t r o l s u b j e c t s p e r -f o r m e d b e t t e r t h a n b o t h t h e R a n d o m g r o u p a n dt h e a m n e s i c p a t i e n t s o n t h e v e r a l r e p o r t , r e c o g n i -t i o n m e m o r y , a n d p r e d i c t i o n t a sk s ( a ll P s < O . 0 5 ) .O v e r a ll , w i t h t h e e x c e p t i o n o f t h e p r e d i c t i o n t a s k( F i g . 2 C ) , t h e a m n e s i c p a t i e n t s p e r f o r m e d n o b e t -t e r t h a n t h e R a n d o m g r o u p o n a n y o f t h e t as k s. I ti s i m p o r t a n t t o n o t e t h a t t h e a m n e s i c p a t i e n t s d i dn o t f a il t h e a w a r e n e s s t a sk s s i m p l y b e c a u s e t h e yq u i c k l y f o r g o t w h a t t h e y h a d j u s t l e a rn e d . I m m e -d i a t e l y a f t e r f a i l i n g t o d e m o n s t r a t e a w a r e n e s s o ft h e s e q u e n c e , t h e a m n e s i c p a t i e n t s w e r e a b l e tor e s u m e n o r m a l p e r f o r m a n c e o n t h e s e q u e n c e t a sk( F i gs . 1 and 3 ) .

M o s t o f t h e t e s t s d e s i g n e d t o a s s e s s d e c l a r a t i v ek n o w l e d g e s u c ce s sf u ll y d e t e c t e d k n o w l e d g e o f

5 1 0 0

o 4

8~ 3oo "o0~ 2O

U.I

60r/3O: ~ 4 0o~ 2o

0 - 20

-B

A M N C O N - 3 A M N C O N - 3(8 ) (12) (8 ) (12)Figure 4: (A) Verbal report . Am nes ic patients (AM N) re-ported less of the repeat ing sequence than the con trolsubjects (CO N-3). (B) Recognit ion m em ory. Ne ithergroup was able to recognize the repeat ing sequence insp i te o f the fact that each group ach ieved s ign i f icantknowledge of the sequence as measured by decreasedreact ion t imes. Bra cke ts sho w standard errors of themean.

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the sequence in the control subjects (all exceptthe Generation task in Experiment 1 and the Rec-ognition task in Experiment 2). Previous work(e.g., Willingham et al. 1989) has also shown thatcontrol subjects do not always acquire much de-clarative knowledge about a repeating sequence.In contrast to the generally good performance ofour control subjects, the amnesic patients consis-tently exhibited impaired or no awareness on ev-ery test of declarative knowledge involving threedifferent sequences.

Experiment 2 demonstrated that subjectslearned more about the repeating sequence thansimply that the four cue locations can appear withdifferent frequencies. Learning also occurredwhen the four cue locations appeared with equalfrequences. These results do not rule out the pos-sibility that frequency learning occu rs in this task.However, other information about the sequencemust also be acquired (e.g., sequential probabili-ties).

It is worth mentioning that the same conclu-sion can be drawn, albeit less directly, from thefindings of Experiment 1. Specifically, the slowerreaction times on the sixth (random) block (Fig.1B) demonstrate that subjects had learned moreabout the repeating sequence than simply that thefour cue locations appeared with different fre-quencies (specifically, locations A and D had oc-curred three times in each l O-item sequence, andlocations B and C had occurred twice). The fre-quency-learning hypothesis (Shanks et al. 1994)correctly predicts that overall slowing should oc-cur on the sixth block because block 6 contains adifferent mix of cue locations than block 5. That is,the two cue locations that were low frequency inblocks 1-5 (and were therefore slower to respondto) are presented relatively more frequency inblock 6 than in block 5 (i.e., locations A, B, C, andD now all appear equally often). The frequency-learning hypothesis, however, does not accountfor the finding that slowing in block 6 was evidenteven when reaction times were considered inde-pendently for each cue location. The average re-action time to each cue location on the fifth blockwas 481, 549 , 551, and 479 msec for locations A,B, C, and D, respectively. In block 6, the reactiontimes to each location increased by 57, 65, 57, 50msec for A, B, C, and D [each increase was signif-icant, ts(32)>2.86; Ps


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must be at least as sensitive to detecting groupdifferences as tests of declarative knowlege. Ourimplicit test (the SRT task) was sensitive enoughto obtain a difference between amnesic patientsand the Random group. We also found that theamnesic patients and control subjects demon-strated equivalent learning in the SRT task.Whereas test sensitivity cannot be estimated froma finding of no difference, it is worth noting thatwe found amnesic patients and control subjects tobe indistinguishable in five separate comparisonsinvolving the SRT task: initial learning of three se-quences and performance on two sequences aftercompletion of the tests of declarative knowledge.

In summary, the findings for amnesic patientsprovide compelling evidence that tacit knowledgecan be acquired in the absence of awareness ofwhat is learned. The brain's multiple memory sys-tems provide for separate and parallel learningabilities. Declarative memory affords conscious ac-cess to and awareness of what is learned. Non-declarative memory depends on other brain sys-tems and accumulates tacit knowledge that is ex-pressed through performance and is inaccessibleto awareness. The biological and psychologicaldata suggest that the various kinds of informationacquired by these memory systems are not storedin a common knowledge base but are acquired inparallel and distributed in multiple memory sys-tems (Squire 1992; Squire et al. 1994). In thissense, memory is analogous to perception, whichis also supported by parallel and multiple brainareas (Ungerleider and Mishkin 1982; Goodale1993).

A c k n o w l e d g m e n t sWe thank N . Champagne, B. Kronenberg, and J.

Zouzounis for research ass is tance. This work was suppor tedby the Medical Research Serv ice of the Depar tment ofVeterans Affairs, Nat ional Inst i tute of Mental Health grantM H 2460 0 , t he Of f ic e o f N av a l R es earc h , t he M c Kn igh tF ounda t i on , and t he M c D onne l l -Pew C en t e r f o r C ogn i t i v eNeurosc ience, San Diego, CA.

The pu bl icat ion cos ts of th is ar t ic le were def rayed inpar t by pa ymen t of pa ge charges . This ar t ic le must thereforebe hereby marked "adver t isement " in accordance wi th 18USC sect ion 1734 solely to indicate this fact .

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Received December 7 , 1994; accepted in revised formJanuary 27 , 1995.

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