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t " ~'7 .

, ; i lE L S E V I E R Neuroscience Letters 198 (1995) 169-172 T

Non -dom inant dorsal-prefrontal activation du ring chess problem solutionevidenced by s ingle pho ton em ission compu terized tomography (SPEC T)

M . O n o f r j ~ ,* , L . C u r a t o l a b , G . V a l e n t i n i c, M . A n t o n e l l i b, A . T h o m a s a , T . F u l g e n t e aaDepartment of Neurology, State University of C hieti, 66100 Chieti, ItalybDivisions of Neurology and Otolaringology, Hospital of S. B enedetto, S. Benedetto, USL 22, ItalyCDepartment of Nuclear M edicine, Hospital of Macerata, Macerata, U SL 15, Italy

Received 9 June 1995; revised version received 30 August 1995; accepted 30 August 1995

Ab s t r a c t

Exp ert chess players can recall meaningful chess posit ions with extraordinary precision in com parison with inexperienced players.We hypothesized, therefore, that their mental perfo rm anc e during chess deliberation could be an appropriate target for single photonem ission computeriz ed tomogr aphy (SPECT) studies. We studied cerebral activation with 1110 MB q 99mTc-Bicisate S PEC T in fiveexpert male chess players during mental solution of a complex chess problem. Region of interest (ROI) analysis, in comparison withavera ge weighted cerebellar counts, showed activation by 10% or more, of the non dominant prefrontal area (fight in four dominantright handed p layers, left in one dominant left handed player) and by 2-6% in the non-dominant middle tem poral areas. Ma xim umvariability of RO I analysis versus cerebellar c ounts in test/retest evaluation is in our laboratory, as in others, 1.5% . Ou r results are inagreem ent with neuropsychological studies suggesting that the non-dominant he misphere is specialized for chess skill, and show thatnon-dominant prefrontal and te mp oral lobe activation during chess deliberation can be detected by SPECT.K e y w o r d s : SPECT; Cerebral cortex; He misp here dominance; Frontal lobe; Chess

E x p e r i e n c e d c h e s s p l a y e r s a r e a b l e t o r e c a l l m e a n i n g -f u l c h e s s p o s i t i o n s a n d t o f i n d m e n t a l l y t h e s o l u t i o n o fc h e s s p r o b l e m s [ 2 , 4 , 1 4 ] a s t h e y d e v e l o p t h e a b i l i t y t os c h e m a t i z e c h e s s p o s i t i o n b y ' c h u n k i n g t h e b a s i c e l e -m e n t s ' i n t o r e l e v a n t s p a t i a l r e l a t i o n s [ 1 ] . W e h y p o t h e -s i z e d , t h e r e f o re , t h a t b r a i n a c t i v a t i o n s o f c h e s s e x p e r t st r y i n g t o s o l v e m e n t a l l y a c o m p l e x c h e s s p r o b l e m [ 1 0 ]c o u l d b e a n a p p r o p r i a t e t a r g e t f o r s i n g l e p h o t o n e m i s s i o nc o m p u t e r i z e d t o m o g r a p h y ( S P E C T ) s t u d i e s , a s t h e e f f e c to f d i r e c t v i s u a l s t i m u l i a n d m o t o r a c t i v i t y w i ll n o t i n t e r -f e r e . C h e s s p r o b l e m - s o l v i n g w a s n e v e r s t u d ie d p r e v i o u s l yw i t h S P E C T , a n d o n l y a p o s i t r o n e m i s s i o n t o m o g r a p h ys t u d y [ 1 5 ] w a s r e c e n t l y d e s c r i b e d , i n a v e r a g e c h e s s p l a y -e r s , d u r i n g a p a r a d i g m i n c l u d i n g d i r e c t c h e c k e r b o a r d o b -s e r v a t i o n a n d a c t i v e d i s p l a c e m e n t o f p ie c e s .

W e s t u d i e d , t h e r e f o r e , f i v e e x p e r t c h e s s p l a y e r s , i n -c l u d i n g t h r e e a u t h o r s o f t h e p r e s e n t p a p e r , a l l w i t h a n

* Corresponding author, Clinica Neurologica, Ospe dale ex Pediatrico,Via M artiri Lancianes i 6, 6 6100 C hieti, Italy. Tel.: +39 871 358814;fax: +39 871 355267 /355395.

E L O s c o r e [ 5 ] a b o v e 1 8 0 0 , w h o v o l u n t e e r e d f o r t h e s t u d y( w i th t h e i n t e r n a ti o n a l E L O r a t i n g s y s t e m , o n t h e a v e r a g ea g o o d a m a t e u r p l a y e r w h o r e a d s c h e s s m a n u a l s a n d p l a y si n t h e l o c a l c h e s s c l u b h a s a n E L O a b o v e 1 2 0 0 ; p l a y e r sc l a s s i f i e d a b o v e 2 0 0 5 E L O a r e r e g u l a r l y l i s t e d a s c h e s sm a s t e r s ) . A l l s u b j e c t s w e r e a b l e t o p l a y m o r e g a m e s s i -m u l t a n e o u s l y w i t h a v e r a g e a m a t e u r s , a n d c o u l d p l a y t h ec h e s s g a m e t u r n i n g t h e i r b a c k t o t h e c h e c k e r b o a r d ; t h ef i v e c h e s s p l a y e r s w h o w e r e s e l e c t e d f o r th e s t u d y w e r ea l l m a l e s , t w o n e u r o l o g i s ts ( 4 2 ( M . O . ) a n d 4 4 ( L . C . ) y e a r so l d , E L O 1 8 5 0 a n d 1 8 0 0 , r e s p e c t i v e l y ) , o n e p e d i a t r i c i a n( 3 7 y e a r s o l d , E L O 2 0 0 0 ) , o n e l a w y e r ( 5 3 y e a r s o l d , E L O2 2 0 0 ) , a n d o n e o t o l a r y n g o l o g y s u r g e o n ( 4 3 y e a r s o l d( M . A . ) , E L O 1 9 5 0 -- 2 1 00 ) . A l l su b j e c t s u n d e r w e n t M i n n e -s o t a m u l t i p h a s i c p e r s o n a l i ty i n v e n t o r y ( M M P I ) , W e c h s l e ra d u l t i n t e l l i g e n c e s c a l e ( W A I S ) I Q t e s t s a n d L Q E d i n -b u r g h q u e s t i o n n a i r e [ 1 6 ] . M M P I r e s u l t s w e r e i n s i d e n o r -m a l l i m i t s i n a ll ; a v e r a g e W A I S I Q w a s 1 33 6 . F o u rs u b j e c t s a r e d o m i n a n t r i g h t h a n d e d ( 9 5 - 1 0 0 % ) a n d o n e i s1 0 0 % l e f t h a n d e d : h e i s a s u r g e o n w h o o p e r a t e s , w r i t e san d u ses i n s t ru m en t s wi th t h e l e f t h an d .

0304-3940/95/$09.50 1995 Elsevier Science Ireland Ltd. All fights reservedS S D 1 0 3 0 4 - 3 9 4 0 ( 9 5 ) 1 1 9 8 5 - 3

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a b c d e f g hFig. 1. The administered chess problem. This game w as played betweenLasker and B auer in 1889 (Amsterdam). The w hite player attacks thecastled black king and sacrifices both his bishops (15, B:h7 + !K:h7;16, Q:h5 + K:g8; 17, B:g7 K:g7; 18, Q:g4 + K:h 7; 19. R: f3 e5; 20,R:h3 + Q:h6; 21, R:h6 + K:h6; 22, Q:d7 +-). Durin g the game , theblack player will, anyhow, lose one o f the bishops and be in definitedisadvantage.

T h e a d m i n i s t e re d c h e s s p r o b l e m r e q u i r e d t h e d e v e l-o p m e n t o f a c o m p l e x s t r a t e g y , w i th t h e s a c r i fi c e o f t w ob i s h o p s , d e s c r i b e d i n c h e s s m a n u a l s [ 1 8 ] a s t h e L a s k e r -B a u e r g a m e ( 1 8 8 9 ) . F i g . 1 s h o w s t h e c h es s p r o b l e m . A l lp l a y e r s o b s e r v e d t h e c h e s s p r o b l e m a n d m e n t a l l y s t u d i e di t f o r 1 5 m i n b e f o r e a n d 1 5 m i n a f t e r t h e t r a c e r i n je c t i o n .T h e c o r r e c t s o l u t i o n w a s p l a y e d b y a l l a t th e e n d o f t h e1 5 m in .S P E C T b r a i n a c t i v a t i o n w a s s t u d i e d w i t h 9 9 m T c -B i c i s a t e ( T c - B i , e t h y l c y s t e i n a t e d i m e r - N e u r o l i t e ) a n e wr a d i o p h a r m a c o l o g i c a l a g e n t , w i t h a h i g h l y f a v o r a b l e d o -s i m e t r y [ 1 3 ] . T c - B i S P E C T h a d a l r e a d y b e e n u s e d i ns i m p l e v i s u a l a c t i v a t i o n s t u d i e s [ 1 2 ] a n d h a s s h o w n p e r -c e n t a c t i v a t i o n s s i m i l a r t o t h o s e o b s e r v e d w i t h 9 9 m T c -H M P A O [ 1 9 ] . B r a i n u p t a k e i s e x t r e m e l y r a p i d a n dr e a c h e s it s m a x i m u m ( a p p r o x i m a t e l y 6 % o f th e i n je c t io nd o s e ) w i t h i n 5 m i n o f i n t r a v e n o u s i n j e c t i o n .

A l l s u b j e c t s u n d e r w e n t T c - B i S P E C T s c a n i n r e s t i n gc o n d i t i o n s ( b a s a l ) , a n d 4 8 - 7 2 h l a te r , d u r i n g s t i m u l a t i o n .A l l p l a y e r s g a v e t h e i r i n f o r m e d c o n s e n t t o t h e s t u d y , a c -c o r d i n g t o f o r m s a n d p r o c e d u r e s a p p r o v e d b y t h e R a d i a -t i o n S a f e t y C o m m i t t e e a n d t h e N a t i o n a l I n s t i t u t e f o rN e r v o u s D i s e a s e a n d S t r o k e ( N I N D S ) o n H u m a n R e -s e a r c h S u b j e c t s o f t h e N a t i o n a l I n s t i t u t es o f H e a l t h( p r o t o c o l n o . 9 3 0 0 7 7 ) . S u b j e c t s f a s t e d f o r a t l e a s t 5 hp r i o r t o i n t r a v e n o u s T c - B i i n j e c t i o n , a n d d i d n o t c o n s u m ea l c o h o l, t o b a c c o , c o f f e e o r t e a o n t h e d a y o f S P E C T . T c -B i ( l l l 0 M B q ) w e r e i n j ec t e d i n b o t h s c an s . S P E C T a c -q u i s i t io n w a s p e r f o r m e d 9 0 m i n a f t e r i n j e c ti o n w i t h ar o t a t i n g s i n g l e h e a d c a m e r a ( G E ) w i t h h i g h r e s o l u t i o nc o l l i m a t o r . D a t a w e r e a c q u i r e d f r o m 6 4 p r o j e c t i o n s ( 3 6 0d e g re e ro t a t io n ) , i n 3 0 s s t e p s , o n a 6 4 x 6 4 m a t r ix .E i g h t a x i a l i m a g e s w e r e r e c o n s t r u c t e d w i t h a t h i c k n e s s o ft w o p i x e l s b y B u t t e r w o r t h b a c k f i l t e r i n g ( 0 . 5 f r e -q u e n c y / 1 0 p o w e r f a c t o r ) ; t h e a t t e n u a t i o n c o r r e c t i o n w a sb a s e d o n C h a n g s a l g o r i t h m ( c o e f f i c i e n t 0 . 0 9 c m - l ) . A x i a li m a g e s w e r e r e s l i c e d o n c o r o n a l a n d s a g i t t a l p l a n e sb y u s i n g t h e c a n t o m e a t h a l ( C M ) c o o r d i n a t e . T h e C Mp l a n e h a d b e e n d e t e r m i n e d p r i o r t o 9 9 m T c - B i c i s a t ei n j e c t i o n o n a l a t e r a l p l a n a r p r o j e c t i o n u s i n g m a r k e r st a p e d t o t h e p a t i e n t ' s h e a d . T h e n u m b e r o f c o u n t s i n e a c hs t u d y w a s m o r e t h a n 6 x 1 0 6. B e c a u s e o f r e s u lt s o b -t a i n e d w i t h t h e f ir s t p r o c e d u r e ( T a b l e 1 ), R O I s w e r e a n a -l y z e d i n l e f t a n d r i g h t h e m i s p h e r e a n d , f i n a l l y , b y p o o l i n gR O I s o f d o m i n a n t v e r s us n o n - d o m i n a n t h e m i s p h e re .T o o b t a i n a n a t o m i c a l r e p r e s e n t a t i o n , t h e s c a n s w e r es c a l e d t o s t a n d a r d s t e r e o t a x i c c o o r d i n a t e s , b a s e d o n t h eT a l a i r a c h A t l a s a s r e v i s e d b y t h e D a m a s i o a n d D a m a s i oA t l a s [ 3 ] . P r e - a n d p o s t - a c t i v a t i o n s c a n s w e r e c o m p a r e dw i t h c u r r e n t R O I a n a l y s i s [ 1 8 ] . R O I s w e r e d e l i n e a t e do v e r t h e p e r i p h e r a l r i m o f c o r t e x i n e a c h s l i c e a n d o nc a u d a t e - l e n t i c u l a r n u c l e i . R O I s w e r e p r e f r o n t a l c o r t e x( F 0 4 , F 0 7 i n D a m a s i o a n d D a m a s i o A t l a s [ 3 ] ) , i n f e r i o rf r o n ta l ( F 1 1 - 1 2 ) , f r o n ta l o p e r c u l u m ( F 0 6 ) , s u p p l e m e n t a r ym o t o r a r e a ( F 0 3 ) , p r e m o t o r a n d r o l a n d i c r e g i o n ( F 0 8 ) ,in fe r io r p a r i e t a l l o b u le (P 0 1 , P 0 2 ) , s u p e r io r p a r i e t a l l o b u le( P 0 3 , P 0 4 ) , m i d d l e t e m p o r a l r e g i o n ( T 0 3 , T 0 4 ) , i n f e r i o rt e m p o r a l g y r u s ( T 0 5 , T 0 6 ) , m e s i a l t e m p o r a l l o b e ( T 1 0 ,T l l , T 1 2 ) , o c c i p i t a l l o b e ( O 0 1 - O 0 7 ) a n d a s u p p l e m e n -

Table 1Significant activation foci, measured as % increment in com parison with cerebellar activity

Subject 1 Subject 2 Subject 3 Subject 4 Subject 5Left Right Left Right Left Right Left Right Left Right

Dorsa l pre-fron tal cortex - 10 - 11 - 10 - 12 12 -Middle temporal cortex - 4.5 - 4 - 5 - 4 6 -2Superior parietal l o b u l e . . . . 3 . . . . 2Percent activations of different RO Is obtained with the com parison versus cerebellar mean counts pre- and po st-activation. Only R OI where percentchanges exceeded the reported 1.5% coefficient of v ariation for test/retest reliability limits [7,11] are reported. Notice that subject 5 (M.A.) is left handdominant, while subjects 1 to 4 are right hand dominant. Notice the right frontal and tem poral activation in the dominant right handed subjects, and themirror activation in subject 5 (dominant left handed).

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17 2 M . O no f r j e t a l . / Ne urosc i e nc e L e t t e r s 198 ( 1995 ) 169- 1 72d o m i n a n t t e m p o r o -m e d i a l re g io n ( t - ( 1 . 5 ) = - 5 . 1 5 , P =0 . 0 0 1 ; t - ( 1 . 5 ) = - 3 . 9 8 , P = 0 .0 1 ) .

F u n d a m e n t a l l y , o u r s t u d y s h o w s t h e u n p r e c e d e n t e de v i d e n c e t h a t t h e n o n - d o m i n a n t f r o n t a l l o b e i s a c t i v e i nt h e b r a i n o f c h e s s e x p e r t s w h e n t h e y e l a b o r a t e a s o l u t i o no f a c o m p l e x c h e s s p r o b l e m . A c t i v a t i o n w a s a l s o d e t e c te di n n o n - d o m i n a n t t e m p o r a l l o b e s . T h e a m o u n t o f ac t i v a -t i o n i n p r e f r o n t a l l o b e s w a s a b o v e 1 0 % , c o m p a r a b l e w i t ha c t i v a t i o n d e t e c t e d i n v i s u a l o r m o t o r a r e a s d u r i n g v i s u a lo r m o t o r p e r f o r m a n c e s [ 1 1 ] . S u r p ri s i n g l y , l i tt le o r n o a c t i -v a t i o n w a s o b s e r v e d i n t h e p a r i e t o - o c c i p i t a l j u n c t i o n( T a b l e 1 ) , a n a r e a p r o b a b l y i n v o l v e d i n t h e p r o d u c t i o n o fm e n t a l i m a g e r y [ 6 ] .

P r e v i o u s S P E C T s t ud i e s s h o w e d a c t iv a t io n o f d o m i -n a n t fr o n t a l l o b e s d u r i n g t h e T o w e r o f L o n d o n t a s k [ 1 4 ] ,a n d d u r i n g t h e S t r o o p p a r a d i g m [ 1 2 ] . T h e a c t i v a t i o n o ft h e n o n - d o m i n a n t f r o n t a l l o b e o b s e r v e d i n o u r s t u d y c o r -r o b o r a t e s t h e h y p o t h e s i s t h a t t h e n o n - d o m i n a n t h e m i -s p h e r e i s c r i t i c a l f o r c h e s s s k i l l : o n e p r e v i o u s s t u d y [ 1 ] ,p e r f o r m e d w i t h t a c h i s t o s c o p i c s p l i t s c r e e n p r e s e n t a t i o n ,s h o w e d t h a t c h e s s p r o b l e m s w e r e s o l v e d m o r e e f f i c i e n tl yi f t h e p r e s e n t a t i o n w a s o n t h e l e f t h e m i f ie l d . T h e a u t h o r sh y p o t h e s i z e d t h a t th e c h u n k i n g o f b a s i c e le m e n t s i n t om e a n i n g f u l g r o u p i n g a n d t h e p a r s i n g o f v i s u a l s ti m u l iw e r e p r o m i n e n t f u n c t i o n s o f t h e n o n - d o m i n a n t h e m i -s p h e r e , s u g g e s t i n g t h a t t h e r i g h t n o n - d o m i n a n t h e m i -s p h e r e m a y b e r e l a t i v e l y s p e c i a l i z e d f o r p a r s i n g s i m p l ev i s u a l s t i m u l i a c c o r d i n g t o d e f a u l t r u l e s , s u c h a s t h e G e -s t al t l aw s o f p e r c e p t u a l o r g a n i z a t i o n , w h e r e a s t h e l e f th e m i s p h e r e m a y b e r e l a t i v e l y s p e c i a l i z e d f o r o v e r r i d i n gs u c h r u l es . O u r f i n d i n g s s h o w t h a t t h e a c t iv i t y o f th e n o n -d o m i n a n t h e m i s p h e r e i s p r o m i n e n t l y l o c a l i z e d i n t h e d o r -s a l p r e f r o n t a l c o r t e x .C l a s s i c d e s c r i p t io n s o f h e m i s p h e r i c f u n c t i o n a t t r ib u t ep r o m i n e n t s k i l l s i n n o n - v e r b a l p e r c e p t i o n a n d p a r a l i n -g u i s t i c c o m p e t e n c e t o t h e n o n - d o m i n a n t h e m i s p h e r e .W i t h o u r s t u d y w e s h o w , i n t h e n o n - d o m i n a n t h e m i -s p h e r e , a l o c a l i z e d f u n c t i o n , t h a t i s d e f i n i t e l y n o n -l i n g u i s t i c , b u t t h a t c o n s i s t s , h o w e v e r , i n c o m p l e x c a t e g o -r i z a ti o n p r o p e r t i e s a n d s t r a t e g i c p l a n n i n g .[!] Chab ris, C.F. and Ham ilton, S.E., Hem ispheric specialization for

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