Neural Circuits for Spatial Attention and Unilateral Neglect

Neurophysiological and Neuropsychological Aspects of Spatial Neglect, M. Jeannerod (editor) 0 Elsevier Science Publishers B.V. (North-Holland), 1987

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NEURAL CIRCUITS FOR SPATIAL A m N T I O N AND UNILATERAL NEGLECT Giacomo R i z z o l a t t i and R o s o l i n o Camarda

What i s t h e r e l a t i o n s h i p between a t t e n t i o n and u n i l a t e r a l n e g l e c t ? I n t h i s a r t i c l e we review t h r e e t h e o r i e s t h a t have been advanced t o e x p l a i n t h i s n e u r o l o g i c a l syndrome, d i s c u s s t h e i r l i m i t a t i o n s , and advance an a l t e r n a t i v e h y p o t h e s i s . The t h e o r i e s a r e : t h e h e m i s p h e r i c h y p o a r o u s a l h y p o t h e s i s (Heilman & Watson, 1 9 7 7 ) , t h e h y p o t h e s i s of an a t t e n t i o n a l m a s t e r c e n t e r ( s e e De R e n z i , 1982) and t h e h y p o t h e s i s of a c o r t i c a l c i r c u i t f o r d i r e c t i n g a t t e n t i o n (Mesulam, 1981). The a n a l y s i s of t h e s e t h e o r i e s shows t h a t none of them i s a b l e t o accomodate t h r e e b a s i c f i n d i n g s : a ) t h e m u l t i p l i c i t y of b r a i n c e n t e r s whose l e s i o n produces n e g l e c t ; b) t h e congruence b e t w e e n a t t e n t i o n a l a n d m o t o r d e f i c i t s a f t e r l e s i o n of t h e s e c e n t e r s ; c ) t h e a n a t o m i c a l independence of c e n t e r s w h o s e damage c a u s e s n e g l e c t . A model of s p a t i a l a t t e n t i o n i s proposed based on a s e r i e s of c i r c u i t s l a r g e l y independent one from a n o t h e r and formed by c e n t e r s which program motor p l a n s i n a s p a t i a l framework. T h i s c o n c e p t i o n i s r a d i c a l l y d i f f e r e n t from t h a t of a s i n g l e a t t e n t i o n a l c e n t e r because i t c o n c e i v e s s p a t i a l a t t e n t i o n n o t a s a s u p r a o r d i n a t e f u n c t i o n c o n t r o l l i n g t h e a c t i v i t y of t h e b r a i n a s a whole, b u t a s a p r o p e r t y i n t r i n s i c a l l y l i n k e d t o t h e premotor a c t i v i t y and d i s t r i b u t e d among v a r i o u s c e r e b r a l c e n t e r s . I n o t h e r words, s p a t i a l a t t e n t i o n i s a v e r t i c a l modular f u n c t i o n p r e s e n t i n several independent c i r c u i t s . Introduction U n i l a t e r a l n e g l e c t i s a r a t h e r common n e u r o l o g i c a l syndrome o b s e r v e d i n many s p e c i e s of a n i m a l s and i n man ( s e e De R e n z i , 1982; F r i e d l a n d and W e i n s t e i n , 1977; Heilman and Watson, 1977; Heilman, Watson & V a l e n s t e i n , 1985). The d i s t i n c t i v e f e a t u r e s of t h i s syndrome a r e t h e f o l l o w i n g : 1 ) s t i m u l i p r e s e n t e d c o n t r a l a t e r a l t o t h e l e s i o n a r e n o t responded t o a n d , a p p a r e n t l y , n o t p e r c e i v e d ; 2 ) t h e r e is a marked d e c r e a s e of e x p l o r a t o r y movements towards t h e s p a c e c o n t r a l a t e r a l t o t h e l e s i o n ; 3 ) e l e m e n t a r y s e n s o r y d e f i c i t s o r d i s t u r b a n c e s i n e x e c u t i o n of movements a r e i n s u f f i c i e n t , when p r e s e n t , t o e x p l a i n t h e symptomatology; 4 ) when t h e a c u t e symptoms r e c e d e , a c o n t r a l a t e r a l d e f i c i t can be d e m o n s t r a t e d w i t h a s i m u l t a n e o u s p r e s e n t a t i o n of two s t i m u l i . P a t i e n t s t e s t e d i n t h i s way may r e p o r t of s e e i n g o n l y one s t i m u l u s , t h a t i p s i l a t e r a l t o t h e l e s i o n (extinction). I n t h e l a s t decade t h e r e h a s been a growing c o n s e n s u s t h a t h e m i n e g l e c t depends upon a n a t t e n t i o n a l d e f i c i t . The i d e a s however on t h e p r e c i s e a t t e n t i o n a l mechanisms impaired i n t h e syndrome d i v e r g e c o n s i d e r a b l y . B r o a d l y s p e a k i n g t h e r e a r e t h r e e p o s s i b l e ways of r e l a t i n g n e g l e c t t o

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a t t e n t i o n a n d , a c c o r d i n g l y , t h r e e p o s s i b l e v e r s i o n s of a n a t t e n t i o n t h e o r y of t h i s syndrome. The f i r s t one i s t h a t t h e d e f i c i t s c o n c e r n t h e i n t e n s i v e a s p e c t s of a t t e n t i o n . According t o t h i s t h e o r y e a c h s i d e of t h e b r a i n c o n t a i n s i t s own a c t i v a t i n g system. When t h i s system i s d e s t r o y e d h a l f of t h e b r a i n c a n n o t p r o c e s s p r o p e r l y t h e incoming s e n s o r y i n f o r m a t i o n and o r g a n i z e t h e a p p r o p r i a t e motor a c t i v i t y . Hence t h e n e g l e c t s y n d r o m e ( H e i l m a n a n d W a t s o n , 1977; Heilman, 1979). The second t h e o r y p r o p o s e s t h a t r e s p o n s i b l e f o r t h e n e g l e c t i s a l e s i o n of an a t t e n t i o n a l c e n t r a l mechanism which d i r e c t s a t t e n t i o n t o v a r i o u s p o r t i o n s of t h e s p a c e a c c o r d i n g t o t h e i n t e r n a l needs of t h e i n d i v i d u a l s o r i n r e s p o n s e t o r e l e v a n t s t i m u l i . The c e n t r a l a t t e n t i o n a l m e c h a n i s m s can be thought of e i t h e r a s l o c a l i z e d i n a p a r t i c u l a r b r a i n a r e a o r a s a network formed by a c h a i n of c o r t i c a l a r e a s and s u b c o r t i c a l c e n t e r s ( s e e De R e n z i , 1982; Mesulam, 1981). I n b o t h c a s e s t h e l e s i o n of a s e l e c t i v e a t t e n t i o n mechanism i s c o n s i d e r e d r e s p o n s i b l e f o r t h e n e g l e c t . The t h i r d t h e o r y , a s t h e p r e v i o u s o n e , m a i n t a i n s t h a t n e g l e c t i s due t o a d e f i c i t of selectiveattentionalmechanisms. However i t d e n i e s t h a t t h e r e i s a s i n g l e a t t e n t i o n a l c i r c u i t c o n t r o l l i n g s p a t i a l a t t e n t i o n . It proposes t h a t a t t e n t i o n t o v a r i o u s p a r t s of s p a c e r e s u l t s from t h e a c t i v i t y of d i f f e r e n t c i r c u i t s e a c h of them having a s i t s p r i m a r y f u n c t i o n t h a t of o r g a n i z i n g m o v e m e n t s t o w a r d a c e r t a i n p a r t of s p a c e ( R i z z o l a t t i , 1983). One f i n d i n g w h i c h a n y t h e o r y o f n e g l e c t m u s t a c c o m o d a t e i s t h a t n e g l e c t r e s u l t s f o l l o w i n g l e s i o n s of a l a r g e v a r i e t y of c o r t i c a l a r e a s and s u b c o r t i c a l c e n t e r s . I n p r i m a t e s , c o r t i c a l a r e a s whose l e s i o n produce n e g l e c t a r e t h e f r o n t a l eye f i e l d ( s e e r e f . i n Crowne, 19831, t h e i n f e r i o r area 6 ( R i z z o l a t t i , Matelli & Pavesi, 1983), the i n f e r i o r p a r i e t a l lobe (Denny-Brown and Chambers, 1958; Heilman, Pandya & Geschwind, 1970; R i z z o l a t t i , G e n t i l u c c i & M a t e l l i , 1985; S t e i n , 1978; V a l e n s t e i n , H e i l m a n & Watson, 1 9 8 2 ) , t h e p o l y s e n s o r i a l a r e a of t h e s u p e r i o r temporal s u l c u s (Luh, B u t t e r & B u c h t e l , 1979; P e t r i d e s & I v e r s e n , 1979) and t h e c i n g u l a t e g y r u s (Watson, Heilman, Cauthen & King, 1973). F u r t h e r m o r e n e g l e c t can be o b t a i n e d a f t e r l e s i o n of t h e s u p e r i o r c o l l i c u l u s (Albano, Mishkin, W e s t b r o o k & W u r t z , 1982; D e a n & R e d g r a v e , 1984; Denny-Brown, 1962; G o o d a l e & Murison, 1975; G o o d a l e , F o r e m a n & M i l n e r , 1978; S p r a g u e & M e i k l e , 1 9 6 5 ) , t h e l a t e r a l hypothalamus ( M a r s h a l l , T u r n e r & T e i t e l b a u m , 1971; M a r s h a l l & T e i t e l b a u m , 1 9 7 4 ) , t h e s u b s t a n t i a n i g r a , and t h e s t r i a t u m (Dunnet & I v e r s e n , 1982; Ljungberg & U n g e r s t e d t , 1976; M a r s h a l l , B e r r i o s & Sawyer, 1980). Evidence e x i s t s a l s o t h a t l e s i o n s of i n t r a l a m i n a r t h a l a m i c n u c l e i (Orem, Schlag-Rey & S c h l a g , 1973) and of some p a r t s of t h e b r a i n stem may produce n e g l e c t (Sprague, Chambers & S t e l l a r , 1961; W a t s o n , H e i l m a n , M i l l e r & K i n g , 1974). I n t h i s c h a p t e r w e w i l l d i s c u s s t h e t h e o r e t i c a l b a s i s of t h e s e t h e o r i e s and t h e n e u r a l c i r c u i t s t h a t a c c o r d i n g t o t h e v a r i o u s t h e o r i e s s u b s e r v e t h e a t t e n t i o n a l functions.

IntensiveAttentionandNeglect F i g u r e 1 s c h e m a t i c a l l y r e p r e s e n t s t h e c i r c u i t s which m e d i a t e t h e a t t e n t i o n a l p r o c e s s e s a c c o r d i n g t o t h e i n t e n s i v e a t t e n t i o n t h e o r y of n e g l e c t . The diagram i s based e s s e n t i a l l y on t h e i d e a s of Heilman and h i s coworkers (Heilman & Watson, 1977; Heilman e t a l . , 1985). I n t h e upper p a r t of t h e f i g u r e two boxes r e p r e s e n t t h e two c e r e b r a l hemispheres. Each of them c o n t a i n s s e v e r a l a r e a s . S q u a r e s i n d i c a t e s e n s o r y a r e a s , t r i a n g l e s motor a r e a s and c i r c l e s a s s o c i a t i o n s a r e a s . According t o Heilman and h i s coworkers (Heilman & Watson, 1977; Heilman e t a l . , 1985) some of t h e a s s o c i a t i o n a r e a s l i k e t h e f r o n t a l eye f i e l d , t h e i n f e r i o r p a r i e t a l l o b u l e

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and t h e c i n g u l a t e g y r u s e v a l u a t e t h e s i g n i f i c a n c e and t h e n o v e l t y of t h e s t i m u l i . When t h e s t i m u l u s a n a l y s i s performed i n t h e s e a r e a s meets c e r t a i n r e q u i s i t e s , t h e r e t i c u l a r f o r m a t i o n i p s i l a t e r a l t o them i s a c t i v a t e d . T h i s a c t i v a t i o n f a c i l i t a t e s t h e i p s i l a t e r a l hemisphere. A l e s i o n of any of t h e a s s o c i a t i o n a r e a s i n v o l v e d i n t h e c i r c u i t o r of t h e r e t i c u l a r f o r m a t i o n produces n e g l e c t because t h e hemisphere i p s i l a t e r a l t o t h e l e s i o n becomes h y p o a c t i v e and u n a b l e t o p r o c e s s p r o p e r l y s e n s o r y i n f o r m a t i o n . The g r e a t a s s e t of t h i s t h e o r y i s t h a t i t can e a s i l y e x p l a i n t h e f a c t t h a t l e s i o n s i n many d i f f e r e n t a r e a s produce a p p a r e n t l y s i m i l a r disturbances.The reticular formationacts a s alinkbetween cortical areas i n v o l v e d i n a t t e n t i o n and t h e r e s t of t h e c o r t e x and t h e r e f o r e l e s i o n s of t h e s e a r e a s as w e l l a s t h a t of t h e r e t i c u l a r f o r m a t i o n w i l l produce t h e same d e f i c i t s . T h e r e a r e however some d i f f i c u l t i e s w i t h t h i s t h e o r y .

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Figure 1 Schematic r e p r e s e n t a t i o n of t h e c i r c u i t which m e d i a t e s s p a t i a l a t t e n t i o n a c c o r d i n g t o t h e i n t e n s i v e a t t e n t i o n t h e o r y of n e g l e c t . S q u a r e s i n d i c a t e s e n s o r y a r e a s , t r i a n g l e s motor a r e a s and c i r c l e s a s s o c i a t i o n a r e a s . F i l l e d c i r c l e s represent the a r e a s involved i n a t t e n t i o n a l p r o c e s s e s . T h e i r a c t i v a t i o n , due t o novel o r i n t e r e s t i n g s t i m u l i c o n t r a l a t e r a l l y p r e s e n t e d , t r i g g e r s t h e r e t i c u l a r f o r m a t i o n which i n t u r n f a c i l i t a t e s the ipsilateralhemisphere. F o r o t h e r explanations see t e x t .

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F i r s t , i t is hard t o b e l i e v e t h a t a l e s i o n i n one of many a r e a s projecting t o t h e r e t i c u l a r formation is s u f f i c i e n t t o determine t h e i n a c t i v a t i o n of t h i s s t r u c t u r e a n d , a s a consequence, t h e g l o b a l h y p o a c t i v i t y of one hemisphere. The r e t i c u l a r f o r m a t i o n r e c e i v e s s o many a f f e r e n t s from s u b c o r t i c a l pathways and c e n t e r s t h a t t o a s s i g n t o t h r e e c o r t i c a l a r e a s a c r u c i a l r o l e i n c o n t r o l l i n g i t s a c t i v i t y a p p e a r s t o be a post-hoc c o n c e p t u a l c o n s t r u c t i o n r a t h e r t h a n a n a n a t o m i c a l f a c t . Second, t h e i n t e n s i v e a t t e n t i o n t h e o r y p r e d i c t s ( s e e F i g . 1 ) t h a t n e g l e c t s h o u l d be g l o b a l , polymodal and t h a t i t s h o u l d i n v o l v e p e r s o n a l and e x t r a p e r s o n a l space. We w i l l show l a t e r t h a t t h i s c l a i m is n o t s u p p o r t e d by t h e e x p e r i m e n t a l f i n d i n g s . T h i r d , and most i m p o r t a n t , t h e i n t e n s i v e t h e o r y p r e d i c t s t h a t t h e most s e v e r e forms of n e g l e c t s h o u l d b e t h o s e consequent t o a l e s i o n of t h e r e t i c u l a r f o r m a t i o n s i n c e t h e a c t i v i t y of t h i s s t r u c t u r e i s r e s p o n s i b l e f o r t h e i n t e n s i v e a s p e c t s of a t t e n t i o n . A l t h o u g h W a t s o n a n d h i s coworkers (Watson, Heilman, Miller & K i n g , 1974) have r e p o r t e d some d a t a i n t h i s d i r e c t i o n , a v e r y d e t a i l e d s t u d y performed by Sprague e t a l . (1961) on t h e e f f e c t of m i d b r a i n l e s i o n s on c a t s ' b e h a v i o r a l l o w s one t o d i s p r o v e t h i s prediction. Sprague a n d h i s a s s o c i a t e s p l a c e d w e l l c o n t r o l l e d l e s i o n i n t h e l a t e r a l p a r t of t h e m i d b r a i n i n c o r r e s p o n d e n c e t o t h e l e m n i s c a l r e g i o n , and i n t h e c e n t r a l p a r t of i t i n c o r r e s p o n d e n c e w i t h m i d b r a i n r e t i c u l a r f o r m a t i o n . Animals w i t h l a t e r a l l e s i o n s s p a r i n g t h e r e t i c u l a r f o r m a t i o n p r e s e n t e d marked t a c t i l e , a u d i t o r y , p r o p r i o c e p t i v e , g u s t a t o r y a s w e l l a s v i s u a l and o l f a c t o r y d e f i c i t s . They showed a g e n e r a l i z e d , b u t l a r g e l y u n a d a p t i v e and u n l o c a l i z e d a r o u s a l even t o s t r o n g s t i m u l a t i o n . They were mute, l a c k e d f a c i a l e x p r e s s i o n and d i d not show any s i g n of a f f e c t . Much of t h e i r motor a c t i v i t y c o n s i s t e d of an a i m l e s s s t e r e o t y p e d wandering. I n c o n t r a s t , a n i m a l s w i t h l a r g e r e t i c u l a r l e s i o n showed no s p a t i a l a t t e n t i o n d e f i c i t s . They were drowsy, p r e s e n t e d a s y n c h r o n i z e d EEG and remained s l u g g i s h f o r o v e r a month. The a u t h o r s ' c o n c l u s i o n was t h a t "a l a r g e r e t i c u l a r l e s i o n s p a r i n g t h e l e m n i s c i r e s u l t s i n an animal whose g e n e r a l b e h a v i o r i s much l i k e t h a t of a normal c a t e x c e p t f o r c h r o n i c h y p o k i n e s i a o r drowsiness".In o t h e r words a r e t i c u l a r f o r m a t i o n l e s i o n produces a n a r o u s a l d e f i c i t , but n o t a d e f i c i t i n t h e capacityof orientingattention. The p o s s i b i l i t y of d i s s o c i a t e n e g l e c t from h y p o a c t i v i t y of one hemisphere h a s been r e c e n t l y d e m o n s t r a t e d by Deuel, C o l l i n s & C a s t o n ( 1 9 8 0 ) u s i n g t h e deoxyglucose method. They found t h a t monkeys showing h e m i n e g l e c t f o l l o w i n g a f r o n t a l l e s i o n had a s t r i k i n g d e c r e a s e i n t h e deoxyglucose uptake i n s e v e r a l s u b c o r t i c a l s t r u c t u r e s but not i n t h e c o r t i c a l a r e a s i p s i l a t e r a l t o t h e l e s i o n . F u r t h e r m o r e , among t h e s u b c o r t i c a l s t r u c t u r e s , some, as f o r example t h e s e n s o r y t h a l a m u s , were normal. I t i s o b v i o u s t h a t t h e s e d a t a a r e not c o m p a t i b l e w i t h any i n t e n s i v e a t t e n t i o n t h e o r y of n e g l e c t . I f indeed t h e b r a i n stem f a c i l i t a t o r y s y s t e m s were c r u c i a l l y i n v o l v e d i n t h e n e g l e c t syndrome one s h o u l d e x p e c t a g l o b a l d e c r e a s e i n t h e a c t i v i t y of t h e c e r e b r a l hemisphere i p s i l a t e r a l t o t h e l e s i o n . T h i s d e c r e a s e w a s n o t found. I n c o n c l u s i o n , t h e i n t e n s i v e a t t e n t i o n h y p o t h e s i s has a t p r e s e n t e s s e n t i a l l y a h i s t o r i c a l i n t e r e s t . I t h a s had t h e enormous m e r i t of s t r e s s i n g t h e importance of a t t e n t i o n i n t h e n e g l e c t syndromes when o t h e r h y p o t h e s e s were more popular ( s e e Heilman & Watson, 1977). The mechanisms however i t proposes d o e s n o t e x p l a i n t h e d e f i c i t s o b s e r v ed i n h e m i n e g l e c t .

SelectiveAttentionandNeglect: ThenasterCenterHypothesis Once e s t a b l i s h e d t h a t h e m i n e g l e c t cannot be e x p l a i n e d by a reduced a c t i v i t y o f one hemisphere t h e m o s t l i k e l y h y p o t h e s i s on i t s g e n e s i s i s t h a t i t i s r e l a t e d t o a d e f i c i t of s e l e c t i v e a t t e n t i o n . S e l e c t i v e a t t e n t i o n i s

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u s u a l l y thought of a s a f u n c t i o n above and beyond t h o s e r e l a t e d t o t h e a n a l y s i s of s e n s o r y i n f o r m a t i o n and t h e programming of motor a c t s . Thus i t i s n o t s u r p r i s i n g t h a t i t i s a l s o u s u a l l y p o s t u l a t e d t h a t t h e mechanisms responsible f o r spatial attention are located outside the c i r c u i t s r e s p o n s i b l e f o r s e n s o r y and motor f u n c t i o n s . I n i t s s i m p l e s t v e r s i o n t h e t h e o r y goes a s f o l l o w s : a ) t h e r e is a c e r e b r a l c e n t e r whose f u n c t i o n i s t o r e n d e r v i v i d c e r t a i n p a r t s of t h e e x t r a p e r s o n a l o r p e r s o n a l s p a c e ; b) i n man, t h i s c e n t e r is l o c a t e d i n t h e r i g h t p a r i e t a l l o b e . Although r a t h e r na'ive and r e m i n i s c e n t of f r e n o l o g i c a l l o c a l i z a t i o n s of f u n c t i o n s , t h i s i n t e r p r e t a t i o n i s p r o b a b l y t h e most p o p u l a r among c l i n i c a l n e u r o l o g i s t s ( c f . De R e n z i , 1982; V a l l a r & P e r a n i , 1986). There i s one i n i t i a l d i f f i c u l t y w i t h t h i s t h e o r y . L e s i o n s of t h e r i g h t hemisphere, t h e p u t a t i v e a t t e n t i o n m a s t e r c e n t e r , produce a n e g l e c t of t h e l e f t hemispace, but l e a v e t h e c a p a c i t y t o move a t t e n t i o n i n t h e r i g h t hemispace, w i t h i n c e r t a i n l i m i t s , normal. T h i s o b v i o u s l y i m p l i e s t h a t movements of a t t e n t i o n i n t h e r i g h t hemispace can be c o n t r o l l e d by a c e n t e r d i f f e r e n t from t h a t of t h e r i g h t p a r i e t a l 1 o b e . T h i s d i f f i c u l t y h o w e v e r can be o v e r c o m e . B i l a t e r a 1 p a r i e t a l l e s i o n s produce v e r y s e v e r e b i l a t e r a l a t t e n t i o n a l d e f i c i t s a s i n t h e c a s e of t h e B a l i n t syndrome ( s e e De R e n z i , 1982). I t i s t h e r e f o r e c o n c e i v a b l e t h a t t h e a t t e n t i o n a l c e n t e r i s formed by two m o i e t i e s l o c a t e d r e s p e c t i v e l y i n t h e two p a r i e t a l l o b e s . The r i g h t moiety i s dominant and c o n t r o l s t h e a t t e n t i o n movements b i l a t e r a l l y , t h e l e f t one, p o s s i b l y because of t h e e x p a n s i o n of language c e n t e r s i n t h i s hemisphere, p l a y s a minor r o l e and can c o n t r o l t h e a t t e n t i o n m o v e m e n t s o n l y i n t h e c o n t r a l a t e r a l space. The l a r g e p o p u l a r i t y of t h e m a s t e r c e n t e r i d e a stems from t h e f a c t t h a t i t seems t o e x p l a i n two v e r y common n e u r o l o g i c a l o b s e r v a t i o n s i n a parsimonious way: a ) t h e a s s o c i a t i o n i n t h e v a s t m a j o r i t y of t h e c a s e s of a severe c l i n i c a l neglect with a r i g h t p a r i e t a l l e s i o n ; b) the g l o b a l , p o l y s e n s o r y c h a r a c t e r of many c a s e s of n e g l e c t . Taken t o g e t h e r t h e s e two o b s e r v a t i o n s seem t o i n d i c a t e t h a t an a n a t o m i c a l c e n t e r f o r s h i f t i n g a t t e n t i o n d o e s e x i s t and t h a t i t i s l o c a l i z e d i n t h e r i g h t p a r i e t a l l o b e . The c o r r e c t n e s s of t h e s e o b s e r v a t i o n s i s beyond any d o u b t s , b u t t h e i r r e l e v a n c e f o r t h e u n d e r s t a n d i n g of n e g l e c t i s not so obvious. I n a l l a n i m a l s i n which e x p e r i m e n t a l l e s i o n s have beenmade, n e g l e c t has b e e n o b t a i n e d a l s o f o l l o w i n g damage t o a r e a s o t h e r t h a n t h e i n f e r i o r p a r i e t a l l o b u 1 e . T h e c l a i m t h a t , a s f a r a s s p a t i a l a t t e n t i o n i s concerned, man i s r a d i c a l l y d i f f e r e n t from a l l o t h e r a n i m a l s i n c l u d i n g p r i m a t e s , i s a v e r y d a r i n g c o n c l u s i o n . E s p e c i a l l y s o i f one c o n s i d e r s t h a t t h e r e a r e s e v e r a l c a s e r e p o r t s of n e g l e c t a l s o i n man f o l l o w i n g l e s i o n s of f r o n t a l l o b e o r s u b c o r t i c a l s t r u c t u r e s ( s e e r e f e r e n c e s i n Heilman e t a l . , 1985). Any t h e o r y t h e r e f o r e t h a t m a i n t a i n s t h a t p a r i e t a l l o b e i s t h e s i t e of t h e c e n t r a l a t t e n t i o n a l mechanism s h o u l d f a c e t h e dilemma of e i t h e r t o d i s c a r d a l l t h e r e p o r t s of n o n - p a r i e t a l n e g l e c t a s a r t e f a c t s O K t o admit t h a t a c e r t a i n p o r t i o n of human p o p u l a t i o n h a s a b r a i n o r g a n i z a t i o n more s i m i l a r t o t h a t of i n f e r i o r p r i m a t e s t h a n t o t h e o t h e r human beings. Both s o l u t i o n s seem t o be unacceptable. While t h e f r e q u e n t a s s o c i a t i o n of n e g l e c t w i t h a p a r i e t a l l e s i o n i s by no means a c o n c l u s i v e e v i d e n c e i n f a v o r of a m a s t e r c e n t e r of a t t e n t i o n , n e v e r t h e l e s s t h i s a s s o c i a t i o n d e s e r v e s some comments. I n g e n e r a l , t h e f r e q u e n c y w i t h which a g i v e n c e r e b r a l a r e a i s h i t by a p a t h o l o g i c a l l e s i o n has no r e l a t i o n w i t h i t s f u n c t i o n a l p r o p e r t i e s b u t depends on f a c t o r s i n t r i n s i c t o t h e p a t h o l o g y i t s e l f . In t h e c a s e of v a s c u l a r i n j u r i e s , f o r example, t h e f r e q u e n c y of l e s i o n s i n c e r t a i n c e r e b r a l d i s t r i c t s w i l l depend o n t h e t y p e of v a s c u l a r i z a t i o n p r o p e r t o t h e r e g i o n , t h e r i c h n e s s of anastomoses p r e s e n t i n i t , and s o on. Thus, i f , l e t u s s a y , t h e p a r i e t a l l o b e

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and t h e f r o n t a l eye f i e l d a r e e q u a l l y i m p o r t a n t i n s h i f t i n g a t t e n t i o n , b u t f o r v a s c u l a r r e a s o n s , t h e p a r i e t a l l o b e i s h i t more f r e q u e n t l y t h a n t h e f r o n t a l l o b e , t h e r e i s no doubt t h a t t h e p a r i e t a l n e g l e c t w i l l be much more f r e q u e n t t h a n f r o n t a l n e g l e c t . Any c o n c l u s i o n however about t h e i m p o r t a n c e of t h e s e t w o a r e a s i n a t t e n t i o n w i l l be c o m p l e t e l y a r b i t r a r y . T h e r e i s a n o t h e r a s p e c t of t h e a s s o c i a t i o n b e t w e e n n e g l e c t and p a r i e t a l l e s i o n s which r e q u i r e s comment. Although e a c h c o r t i c a l a r e a , p r o b a b l y w i t h no e x c e p t i o n i n t h e c a s e of n e o c o r t e x , r e c e i v e s a t h a l a m i c i n p u t , t h e r e i s l i t t l e doubt t h a t t h e main s t r e a m of s e n s o r y i n f o r m a t i o n f l o w s from t h e r e t r o r o l a n d i c a r e a s t o t h e p r e r o l a n d i c a r e a s . Given t h i s , i t s h o u l d f o l l o w t h a t l a r g e l e s i o n s of t h e p a r i e t a l l o b e , a s t h o s e o b s e r v e d i n n e g l e c t p a t i e n t s , have two e € f e c t s . F i r s t , by d e s t r o y i n g t h e n e u r a l c i r c u i t s of t h e p a r i e t a l l o b e , t h e y produce d e f i c i t s due t o t h e l a c k of t h e i n t r i n s i c a c t i v i t y of t h i s l o b e , second, by d i s c o n n e c t i n g t h e f r o n t a l l o b e from t h e i n f o r m a t i o n coming from t h e p o s t e r i o r a r e a s , t h e y i m p a i r t h e f u n c t i o n of t h i s l o b e . F r o n t a l l e s i o n s of a comparable e x t e n t must have much l e s s s e v e r e e f f e c t s . They d e s t r o y t h e i n t r i n s i c f r o n t a l l o b e c i r c u i t s , b u t l e a v e r e a s o n a b l y i n t a c t t h o s e of t h e p a r i e t a l lobe. Thus i t i s n o t s u r p r i s i n g t h a t p a r i e t a l l e s i o n s produce n e g l e c t more f r e q u e n t l y and of g r e a t e r s e v e r i t y than f r o n t a l lesions.

SelectiveAttentionandNeglect: Thesingle Circuit Hypothesis A s shown above a t h e o r y of n e g l e c t which p o s t u l a t e s a n a n a t o m i c a l c e n t e r c o n t r o l l i n g s p a t i a l a t t e n t i o n i s n o t s u p p o r t e d by e m p i r i c a l f a c t s . The t e n e t however t h a t s p a t i a l a t t e n t i o n is a n i n d e p e n d e n t , supramodal f u n c t i o n can be r e f o r m u l a t e d by assuming t h a t a t t e n t i o n i s c o n t r o l l e d by a c i r c u i t i n c l u d i n g s e v e r a l b r a i n a r e a s . T h i s i d e a h a s been r e c e n t l y d e v e l o p e d w i t h g r e a t i n g e n u i t y byMesulam (1981). Mesulam, i n c o n t r a s t w i t h t h e a n a t o m i c a l s i n g l e c e n t e r t h e o r y a d m i t s t h a t a l s o i n man hemineglect c a n o c c u r a f t e r l e s i o n s o u t s i d e p a r i e t a l lobe. He s u r m i s e s however t h a t i n p r i m a t e s c o r t i c a l a r e a s a r e p a r t i c u l a r l y i m p o r t a n t i n d i r e c t i n g a t t e n t i o n . A s a consequence he does n o t i n c l u d e s u b c o r t i c a l c e n t e r s i n t h e a t t e n t i o n a l c i r c u i t which i s e x c l u s i v e l y c o r t i c a l . T h i s c i r c u i t i s formed by t h e f r o n t a l eye f i e l d , t h e p o s t e r i o r p a r i e t a l l o b e and t h e c i n g u l a t e c o r t e x . The r e t i c u l a r f o r m a t i o n i s t h o u g h t of a s a n a s p e c i f i c f a c i l i t a t o r y s y s t e m i n l i n e w i t h t h e c l a s s i c a l n o t i o n o f Moruzzi and Magoun (1949). F i g u r e 2 , upper p a r t , shows t h e c i r c u i t diagram of s p a t i a l a t t e n t i o n a c c o r d i n g t o t h i s t h e o r y . The lower p a r t of t h e f i g u r e i l l u s t r a t e s w h a t M e s u l a m c a l l s t h e n e t w o r k approach t o t h e c o r t i c a l l o c a l i z a t i o n of complex f u n c t i o n s . According t o t h i s approach c e r t a i n complex f u n c t i o n s , l i k e s p a t i a l a t t e n t i o n , r e s u l t from t h e i n t e r a c t i o n of s e v e r a l d i s t i n c t r e g i o n s , none of which i s e x c l u s i v e l y devoted t o t h a t f u n c t i o n . A s f a r a s t h e s p a t i a l a t t e n t i o n i s concerned, t h e f r o n t a l eye f i e l d (Box 1) , t h e p a r i e t a l c o r t e x (Box 2 ) and t h e c i n g u l a t e c o r t e x (Box 3 ) a l l c o n t a i n c o r t i c a l columns ( i n d i c a t e d w i t h a ) i n v o l v e d i n t h i s f u n c t i o n . Each of t h e s e a r e a s h a s a l s o o t h e r columns r e s p o n s i b l e f o r o t h e r complex f u n c t i o n s ( b , c , d ) . The p r e s e n c e of t h e s e a d d i t i o n a l columns e x p l a i n why, b e s i d e s h e m i n e g l e c t , o t h e r d e f i c i t s may emerge a f t e r l e s i o n of one of t h e s e a r e a s . F o r example, a n o s o g n o s i a , d r e s s i n g a p r a x i a and c o n s t r u c t i o n a l a p r a x i a f r e q u e n t l y o c c u r a f t e r a r i g h t p a r i e t a l l e s i o n . These d i s t u r b a n c e s should be due t o damage of columns of the p a r i e t a l lobe physically adjacent t o those mediating s p a t i a l a t t e n t i o n b u t f u n c t i o n a l l y independent of them. The s e l e c t i v e a t t e n t i o n h y p o t h e s i s as f o r m u l a t e d by Mesulam seems t o g i v e a r e a s o n a b l e a n a t o m i c a l b a s i s t o t h e n e g l e c t phenomena. However i t h a s two weak p o i n t s : f i r s t , i t i s n o t c l e a r how t h e a t t e n t i o n a l c i r c u i t

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i n t e r a c t s w i t h t h e c i r c u i t s which p r o c e s s s e n s o r y i n f o r m a t i o n and o r g a n i z e t h e movements. The i n t e n s i v e a t t e n t i o n h y p o t h e s i s overcame t h i s d i f f i c u l t y by i n d i c a t i n g i n t h e r e t i c u l a r f o r m a t i o n t h e c e n t e r t h a t c o n t r o l s t h e a t t e n t i o n a l s t a t e of t h e b r a i n . Second, t h e M e s u l a m v e r s i o n o f t h e s e l e c t i v e a t t e n t i o n h y p o t h e s i s a d m i t s t h e e x i s t e n c e of a s i n g l e a t t e n t i o n a l c i r c u i t . I n t h e n e x t s e c t i o n w e w i l l show t h a t t h e r e i s s t r o n g e v i d e n c e a g a i n s t t h i s assumption.

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network approach

Figure 2 A : Schematic r e p r e s e n t a t i o n of t h e c i r c u i t which m e d i a t e s s p a t i a l a t t e n t i o n a c c o r d i n g t o t h e a t t e n t i o n a l c i r c u i t t h e o r y of n e g l e c t ( s i n g l e c i r c u i t v e r s i o n ) . A l l c o n v e n t i o n s a s i n F i g u r e 1. F i l l e d c i r c l e s r e p r e s e n t f r o n t a l , p a r i e t a l and l i m b i c a r e a s i n v o l v e d i n s e l e c t i v e a t t e n t i o n . For other explanations see t e x t . B : Network a p p r o a c h t o l o c a l i z a t i o n of s e l e c t i v e a t t e n t i o n . Circles r e p r e s e n t t h e a s s o c i a t i o n a r e a s i n v o l v e d i n s p a t i a l a t t e n t i o n . Each a r e a c o n t a i n s independent columns ( i n d i c a t e d by l e t t e r s ) r e s p o n s i b l e f o r complex p s y c h o l o g i c a l f u n c t i o n s . S p a t i a l a t t e n t i o n (column a ) i s r e p r e s e n t e d i n a l l a r e a s . Other complex f u n c t i o n s a r e r e p r e s e n t e d i n o n e o r two a r e a s ( c o l u m n s b t o g ) .

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Selective Attentionand AtypicalCasesof Neglect a) Vertical neglects T h e r e a r e c a s e s of n e g l e c t i n which a t t e n t i o n a l d e f i c i t s a r e p r e s e n t and y e t t h e i r d i s t r i b u t i o n i n s p a c e i s d i f f e r e n t from t h a t o b s e r v e d i n t h e c l a s s i c a l n e g l e c t syndrome f o l l o w i n g r i g h t p a r i e t a l l o b e i n j u r y i n t h e man o r f r o n t a l eye f i e l d l e s i o n i n t h e monkey. we w i l l r e f e r t o t h e s e c a s e s a s a t y p i c a l n e g l e c t . A s u r v e y of some of them w i l l show how t h e i d e a of a s i n g l e a t t e n t i o n a l c i r c u i t i s u n s a t i s f a c t o r y and how s p a t i a l a t t e n t i o n i s c l o s e l y l i n k e d w i t h t h e o r g a n i z a t i o n o f m o v e m e n t i n space. A t y p i c a l n e g l e c t i s observed i n c a t s a f t e r s a g i t t a l s e c t i o n of t e c t a l commissures. Some y e a r s ago i n a s t u d y of i n t e r o c u l a r t r a n s f e r of v i s u a l i n f o r m a t i o n , B e r l u c c h i , B u c h t e l 6 Lepor6 (1978) r e p o r t e d t h a t a n i m a l s w i t h a l e s i o n of t h e m i d b r a i n commissures have d i f f i c u l t y i n d e t e c t i n g s t i m u l i moved above t h e i r head. More r e c e n t l y t h e v i s u a l b e h a v i o r of a n i m a l s w i t h such a l e s i o n were reexamined by M a t e l l i , O l i v i e r i , S a c c a n i & R i z z o l a t t i ( 1 9 8 3 ) . The a n i m a l s were n e u r o l o g i c a l l y t e s t e d and t h e i r v i s u a l f i e l d was mapped u s i n g a s p e c i a l p e r i m e t e r which a l l o w e d t h e e x p e r i m e n t e r s t o t e s t p o i n t s l o c a t e d a b o v e a n d below t h e h o r i z o n t a l m e r i d i a n .

Figure 3 Responses of normal and commissurotomized a n i m a l s t o s t i m u l i p r e s e n t e d i n t h e upper and lower v i s u a l space. Note t h e head p o s t u r e of t h e o p e r a t e d a n i m a l s and t h e i r l a c k of r e s p o n s e t o food i n t h e upper s p a c e ( f r o m M a t e l l i e t a l . , 1983).

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A l l a n i m a l s w i t h m i d b r a i n commissure l e s i o n s showed motor and a t t e n t i o n a l d e f i c i t s . Motor d e f i c i t s c o n s i s t e d i n a marked r e d u c t i o n o r even absence of v e r t i c a l eyemovement s a n d i n a n a b n o r m a l p o s t u r e o f t h e head t h a t was k e p t s l i g h t l y v e n t r o f l e x e d ( F i g u r e 3 , upper p a r t , Cat L a n d C a t N ) . A t v a r i a n c e w i t h normal c a t s , commissurotomized a n i m a l s never looked u p a n d e x p l o r e d t h e s p a c e above t h e i r head. V i s u a l s t i m u l i p r e s e n t e d i n t h e upper v i s u a l space were n e g l e c t e d , w h e r e a s t h o s e i n t h e l o w e r s p a c e w e r e responded t o rapidly. This d i f f e r e n t r e a c t i v i t y t o stimulus location is i l l u s t r a t e d i n F i g u r e 3 , where i s a l s o shown, f o r comparison, t h e b e h a v i o r of a normal c a t t e s t e d i n t h e same way. The c a p a c i t y t o f o l l o w o b j e c t s a l o n g t h e v e r t i c a l p l a n e was a l s o impaired. When a p i e c e of f o o d w a s m o v e d i n a n u p w a r d d i r e c t i o n s t a r t i n g f r o m t h e lower f i e l d , t h e animal f o l l o w e d i t u n t i l a p p r o x i m a t e l y t h e head midplane. Then t h e head movement s t o p p e d and t h e c a t appeared t o i g n o r e where t h e food was. When t h e foodwasmoveddownwards s t a r t i n g f r o m t h e u p p e r v i s u a l f i e l d t h e a n i m a l had a s t a r t l i n g r e a c t i o n a s soon a s t h e food c r o s s e d t h e head midplane; u n t i l t h a t moment t h e a n i m a l appeared t o be c o m p l e t e l y unawareof t h e s t i m u l u s . The r e s u l t s of a formal t e s t i n g of upper and lower v i s u a l s p a c e i n one c a t w i t h a complete s e c t i o n of t e c t a l commissure i s shown i n F i g u r e 4 . The t e s t i n g was done by c o n d i t i o n i n g t h e a n i m a l t o f i x a t e t h e c e n t e r of a p e r i m e t e r and by p r e s e n t i n g a s m a l l p i e c e of food e i t h e r a t t h i s p o i n t ( c o n t r o l t r i a l s ) o r a t t h e p e r i p h e r y ( t e s t t r i a l s ) . The animal was rewarded when he walked s t r a i g h t t o t h e c e n t e r of t h e p e r i m e t e r i n c a s e of c o n t r o l t r i a l s o r towards t h e p e r i p h e r a l s t i m u l u s i n c a s e of t e s t t r i a l s . The t e s t showed a marked upper v i s u a l space d e f i c i t . The d e f i c i t was p r e s e n t b o t h when t h e s c o r e was b a s e d o n a c t u a l r e a c h i n g o f t h e food ( A ) o r on t h e p r e s e n c e of an o r i e n t i n g r e s p o n s e even i f not followed by t h e a p p r o a c h t o t h e s t i m u l u s (B). S i m i l a r r e s u l t s were o b t a i n e d i n a l l a n i m a l s w i t h a complete t e c t a l l e s i o n . The d e f i c i t was l o n g l a s t i n g a l t h o u g h some r e c o v e r y was o b s e r v e d w i t h time. The a n i m a l s i n which t h e l e s i o n of t h e t e c t a l c o m m i s s u r e w a s i n c o m p l e t e showed t h e same symptoms a s t h o s e w i t h a complete s e c t i o n b u t r e c o v e r e d r a t h e r r a p i d l y , i n a b o u t twoweeks. I n two animal s t he l e s i o n w a s p l a c e d m o r e r o s t r a l l y and i n v o l v e d t h e p o s t e r i o r commissure and t h e r o s t r a l p a r t of t h e i n t e r t e c t a l commissure. These a n i m a l s showed a b e h a v i o r d i f f e r e n t from t h o s e w i t h i n t e r t e c t a l l e s i o n . There was no v e n t r a l f l e x i o n of t h e head and no tendency t o e x p l o r e t h e lower space. I n c o n t r a s t t h e head was k e p t d o r s i f l e x e d and t h e r e was a p r e f e r e n c e f o r t h e s t i m u l i p r e s e n t e d i n t h e upper space. Downwards t r a c k i n g head movementswere s l o w and l e s s a c c u r a t e t h a n t h o s e upwards. When two s t i m u l i were s i m u l t a n e o u s l y moved i n o p p o s i t e d i r e c t i o n s t h e a n i m a l s c o n s t a n t l y f o l l o w e d t h a t d i r e c t e d upwards. Formal t e s t i n g of v i s u a l f i e l d performed i n one a n i m a l showed a normal performance i n t h e upper v i s u a l f i e l d and a l o n g t h e h o r i z o n t a l m e r i d i a n . C o r r e c t r e s p o n s e s i n t h e lower f i e l d were l e s s t h a n 60%. Both a n i m a l s r e c o v e r e d rather rapidly. M o d i f i c a t i o n s of t h e head p o s t u r e a f t e r c o m m i s s u r a l l e s i o n s a r e i n g o o d agreement w i t h t h e d a t a of Hess and h i s coworkers (Hess, 1954; Hess, B u r g i & Bucher, 1946). According t o Hess ( s e e a l s o H a s s l e r , 1972) t h e r e a r e two r e g i o n s i n t h e m i d b r a i n p a r t i c u l a r l y i n v o l v e d i n t h e c o n t r o l of head movements. The f i r s t , r e l a t e d t o head e l e v a t i o n , h a s i t s c e n t e r i n c o r r e s p o n d e n c e t o t h e n u c l e u s p r a e s t i t i a l i s ( r o s t r a l p a r t of t h e n u c l e u s i n t e r s t i t i a l i s of C a j a l ) and comprises t h e s y s t e m o f f i b e r s d e s c e n d i n g f r o m i t and t h e r e t i c u l a r neurons l o c a t e d a l o n g t h e i r c o u r s e . E l e c t r i c a l s t i m u l a t i o n of t h i s system e l i c i t s r a i s i n g of t h e head, whereas i t s destruction causes aheaddorsiflexion.The secondmidbrain region

298

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CAT- N

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0 0 0 0 0 30' 60'

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Figure 4 V i s u a l f i e l d c h a r t b e f o r e and a f t e r t h e m i d b r a i n commissure s e c t i o n . Right upper s i d e of t h e f i g u r e : r e c o n s t r u c t i o n o f t h e m i d b r a i n l e s i o n . The d a r k a r e a i n d i c a t e s t h e e x t e n t of t h e l e s i o n . L e f t upper s i d e and remainder of t h e f i g u r e : p r e o p e r a t i v e and p o s t o p e r a t i v e v i s u a l f i e l d s . I n each v i s u a l f i e l d c h a r t a square i n d i c a t e s a v i s u a l f i e l d point t h a t has beentested; the s q u a r e w i t h t h e cross inside represents t h e f i x a t i o n p o i n t . Empty s q u a r e s , p e r c e n t a g e of c o r r e c t r e s p o n s e s g r e a t e r t h a n 75%; f i l l e d s q u a r e s , c o r r e c t r e s p o n s e s less t h a n 25%; half-filled s q u a r e s , c o r r e c t r e s p o n s e s between 25% and 50%; q u a r t e r - f i l l e d s q u a r e s , c o r r e c t r e s p o n s e s between 50% and 75%. A , o r i e n t i n g r e s p o n s e s ; B , r e a c h i n g responses.

Neural circuits for spatial attention

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c o n t r o l l i n g head movements i n c l u d e s t h e n u c l e u s of p o s t e r i o r commissure and i t s a s c e n d i n g and d e s c e n d i n g p r o j e c t i o n s , most of which p a s s t h r o u g h t h e p o s t e r i o r commissure. S t i m u l a t i o n of t h e n u c l e i o f t h e p o s t e r i o r c o m m i s s u r e e l i c i t s l o w e r i n g of head and f o r e t r u n k , whereas i t s d e s t r u c t i o n c a u s e s d o r s i f l e x i o n of head, and a p e c u l i a r g o o s e - l i k e w a l k i n g . I f one accepts t h e n o t i o n t h a t v e r t i c a l head movements r e q u i r e b i l a t e r a l a c t i v a t i o n of t h e m i d b r a i n c e n t e r s a n a l o g o u s t o t h a t n e c e s s a r y f o r v e r t i c a l eye movements (Bender, 1960; P a s i k , P a s i k & Bender, 1 9 6 9 ) , t h e d a t a of M a t e l l i e t a l . can be e a s i l y accounted f o r by a d m i t t i n g t h a t t h e two s y s t e m s of f i b e r s which c o n t r o l v e r t i c a l head movements c r o s s m i d l i n e i n two d i f f e r e n t p o i n t s . P r e c i s e l y t h e system r e s p o n s i b l e f o r head l o w e r i n g c r o s s e s m i d l i n e r o s t r a l l y i n c o r r e s p o n d e n c e of t h e p o s t e r i o r commissure and p o s s i b l y of t h e r o s t r a l p a r t of t h e i n t e r t e c t a l commissure, whereas t h e s y s t e m r e s p o n s i b l e f o r head e l e v a t i o n c r o s s e s i t more c a u d a l l y i n t h e t e c t a l commissure. The two s y s t e m s a p p e a r t o be a n t a g o n i s t and a l e s i o n of one of them d e t e r m i n e s t h e p r e v a l e n c e of t h e o t h e r . The i n t e r e s t of t h e s e f i n d i n g s f o r n e g l e c t i s twofold. F i r s t , i t i n d i c a t e s t h a t an a t t e n t i o n a l d e f i c i t can be o b t a i n e d w i t h a l e s i o n of c e n t e r s whose primary r o l e i s t h a t of c o n t r o l l i n g head and eye movements; second, i t shows t h a t d i f f e r e n t t y p e s of motor d e f i c i t s a r e a s s o c i a t e d w i t h d i f f e r e n t t y p e s of a t t e n t i o n a l d e f i c i t s and t h e l a t t e r a r e c o n g r u e n t w i t h t h e former. Evidence o b t a i n e d i n p a t i e n t s a f f e c t e d by p r o g r e s s i v e s u p r a n u c l e a r p a l s y p o i n t s o u t t h a t t h i s a s s o c i a t i o n i s not p r o p e r o n l y of animals b y t m a y o c c u r a l s o i n m a n . P a t i e n t s w i t h p r o g r e s s i v e s u p r a n u c l e a r p a l s y show many n e u r o l o g i c a l d e f i c i t s among which a p a r t i a l o r t o t a l i n c a p a c i t y t o move t h e e y e s v e r t i c a l l y , e s p e c i a l l y downwards, and a s l i g h t d o r s i f l e x i o n of t h e head ( s e e S t e e l e , R i c h a r d s o n & O l s z e w s k i , 1964). These symptoms a r e accompanied by b e h a v i o r a b n o r m a l i t i e s v e r y l i k e l y caused by a d i f f i c u l t y of s h i f t i n g a t t e n t i o n toward lower space. R a f a l and G r i m m ( 1 9 8 1 ) , f o r example, r e p o r t e d t h a t p a t i e n t s t h a t a r e a b l e t o l o o k down o n command fumble w i t h t h e i r meal l o o k i n g s t r a i g h t a g a i n . They have problems w i t h p u t t i n g o n t h e i r s h o e s o r w i t h t y i n g s h o e l a c e s . F r e q u e n t l y t h e y stumble o v e r o b j e c t s i n t h e i r p a t h . R e c e n t l y Camarda ( u n p u b l i s h e d o b s e r v a t i o n s ) s t u d i e d a p a t i e n t w i t h p r o g r e s s i v e s u p r a n u c l e a r p a l s y whose main d e f i c i t s were a s l i g h t g l o b a l a k i n e s i a , a g a i t d i s t u r b a n c e , an abnormal p o s t u r e of t h e head and a p a r a l y s i s of downwards d i r e c t e d v e r t i c a l eye movements. T h i s p a t i e n t , when t e s t e d w i t h one s t i m u l u s a t a time, d i d n o t show any o b v i o u s a t t e n t i o n a l d e f e c t . However when two s t i m u l i were s i m u l t a n e o u s l y p r e s e n t e d one i n h i s upper f i e l d , t h e o t h e r i n h i s lower f i e l d , he r e p o r t e d of s e e i n g o n l y t h e upper one. CT s c a n showed, b e s i d e a z o n e o f h y p o d e n s i t y i n t h e p e s p e d u n c u l i , a marked h y p o d e n s i t y i n correspondence of t h e r o s t r a l p o l e of t h e s u p e r i o r c o l l i c u l i a t t h e l e v e l of t h e i r m i d l i n e . The a n a l o g y between t h e s e d a t a and the syndromeobtainedinthe cat followingmidbrain l e s i o n , seemsevident. A formal proof t h a t p a t i e n t s w i t h p r o g r e s s i v e s u p r a n u c l e a r p a l s y have a t t e n t i o n a l d e f i c i t s h a s been provided by P o s n e r a n d h i s coworkers ( P o s n e r , Cohen & R a f a l , 1982). They used t h e f o l l o w i n g e x p e r i m e n t a l procedure. The p a t i e n t s were i n s t r u c t e d t o respond as f a s t as p o s s i b l e (manual r e a c t i o n t i m e ) t o s t i m u l i p r e s e n t e d e i t h e r on one s i d e o r on t h e o t h e r of a f i x a t i o n p o i n t , w i t h o u t moving t h e i r eyes. A p e r i p h e r a l cue preceded t h e t a r g e t s t i m u l u s and i n d i c a t e d a h i g h p r o b a b i l i t y (80%)of t a r g e t o c c u r e n c e on t h a t s i d e . The t r i a l s i n which t h e cue and t h e t a r g e t were congruent were r e f e r r e d t o a s v a l i d t r i a l s , t h o s e i n which t h e y were n o t congruent were r e f e r r e d t o a s i n v a l i d t r i a l s . The cue was p r e s e n t e d For 300 msec f o l l o w e d by t a r g e t o c c u r r i n g a t d i f f e r e n t time i n t e r v a l s a f t e r t h e cue o n s e t . S t i m u l i were p r e s e n t e d i n t h e v e r t i c a l and h o r i z o n t a l dimension.

3 00

G. Rizzolatti and R. Camarda

The r e s u l t s showed t h a t p a t i e n t s w i t h p r o g r e s s i v e s u p r a n u c l e a r p a l s y can o r i e n t r a p i d l y i n t h e h o r i z o n t a l d i r e c t i o n . An a d v a n t a g e of t h e cued s i d e was p r e s e n t a l r e a d y a t 50 msec and remained p r e s e n t o v e r t h e e n t i r e i n t e r v a l range. I n c o n t r a s t , i n t h e v e r t i c a l d i r e c t i o n t h e r e was no d i f f e r e n c e between t h e v a l i d and i n v a l i d t r i a l s u n t i l 1000 s e c a f t e r t h e cue. So i t was c l e a r t h a t t h e t e s t e d p a t i e n t s can o r i e n t i n all d i r e c t i o n s . However t h e y needed a l o n g e r t i m e when t h e y had t o s h i f t a t t e n t i o n " i n t h e d i r e c t i o n i n w h i c h s a c c a d e s w e r e m o s t a f f e c t e d " ( P o s n e r e t a l . , 1982). b)Personalandperipersonalneglect Another t y p e of n e g l e c t i n which t h e a t t e n t i o n a l d e f i c i t h a s a d i f f e r e n t p a t t e r n from t h e one commonly observed f o l l o w i n g p a r i e t a l l o b e l e s i o n i n man i s t h a t observed i n t h e monkey a f t e r a l e s i o n of i n f e r i o r a r e a 6 ( R i z z o l a t t i e t a l . , 1983).Figure5 (upper r i g h t corner) s h o w s a l a t e r a l

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Figure 5 R e c o n s t r u c t i o n of t h e c o r t i c a l l e s i o n and of t h e t h a l a m i c d e g e n e r a t i o n i n one monkey w i t h p e r s o n a l and p e r i p e r s o n a l n e g l e c t . T h e h i s t o l o g i c a l s e c t i o n s a r e c o r o n a l . They were p r o g r e s s i v e l y numbered and t h e r e s p e c t i v e number i s s h o w n n e a r e a c h s e c t i o n . D o t t e d a r e a s = d e n e r v a t e d c o r t e x , w h i t e m a t t e r and t h a l a m i c d e g e n e r a t i o n . AS = a r c u a t e s u p e r i o r . A 1 = arcuate inferior. C = central.MD=nucleusmedialis dorsalis.SP= i n t r a p a r i e t a l . P = p r i n c i p a l i s . X = n u c l e u s X of Olszewski (From R i z z o l a t t i e t a l . , 1983).

Neural circuits f o r spatial attention

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view of a monkey b r a i n . I n f e r i o r a r e a 6 i s t h e r o s t r a 1 p a r t of a g r a n u l a r f r o n t a l c o r t e x l y i n g l a t e r a l t o t h e s p u r of t h e a r c u a t e s u l c u s . T h i s p a r t of a r e a 6 c a n be d i s t i n g u i s h e d from t h e upper p a r t ( m e d i a l t o t h e s p u r ) f o r i t s c y t o a r c h i t e c t o n i c , c o n n e c t i o n a l and e n z y m a t i c p r o p e r t i e s ( s e e M a t e l l i , Camarda, G l i c k s t e i n & R i z z o l a t t i , 1986). I n a g r o u p of monkeys R i z z o l a t t i e t a l . (1983) p l a c e d small l e s i o n s , l i k e t h a t i l l u s t r e d i n F i g u r e 5 , t o i n f e r i o r a r e a 6. The l e s i o n d i d n o t invade t h e r o s t r a l l y l o c a t e d f r o n t a l eye f i e l d a s d e m o n s t r a t e d by t h e r e c o n s t r u c t i o n of t h e c o r t i c a l damage and t h a l a m i c d e g e n e r a t i o n . The a n i m a l b e f o r e and a f t e r l e s i o n underwent a g e n e r a l n e u r o l o g i c a l e x a m i n a t i o n . I n addition, the animal's responses t o v i s u a l s t i m u l i located outside i t s r e a c h ( f a r s p a c e ) , w i t h i n t h e r e a c h of i t s arm ( d i s t a n t p e r i p e r s o n a l s p a c e ) and around i t s mouth ( p e r i c u t a n e o u s b u c c a l s p a c e ) were s t u d i e d w i t h p a r t i c u l a r c a r e . The t e s t i n g was done: a ) by moving a p i e c e of food h e l d by a p a i r of f o r c e p s a t d i f f e r e n t d i s t a n c e s from t h e a n i m a l ; b ) by moving s i m u l t a n e o u s l y two p i e c e s of €ood. The two p i e c e s were k e p t i n i t i a l l y c l o s e one t o a n o t h e r , t h e n , when t h e a n i m a l f i x a € e d them, t h e y were moved l a t e r a l l y i n o p p o s i t e d i r e c t i o n s ; c ) by p r e s e n t i n g a b r u p t l y a p i e c e of food p e r i p h e r a l l y w h e n t h e animal was f i x a t i n g a n o t h e r one c e n t r a l l y l o c a t e d ; d ) by p r e s e n t i n g f r i g h t e n i n g s t i m u l i . The f i r s t p o s t - s u r g e r y t e s t i n g w a s performed t h e f i r s t day a f t e r t h e o p e r a t i o n . The monkey's b e h a v i o r i n i t s home cage was i n d i s t i n g u i s h a b l e from i t s b e h a v i o r b e f o r e t h e o p e r a t i o n e x c e p t f o r a l e s s f r e q u e n t u s e of t h e r i g h t hand. When t e s t e d i n a p r i m a t e c h a i r t h e a n i m a l d i d n o t show any o b v i o u s v i s u a l d e f i c i t € o r s t i m u l i p r e s e n t e d i n t h e f a r s p a c e and i n t h e d i s t a n t p e r i p e r s o n a l space. S t i m u l i o n r i g h t o r l e f t s i d e s were immediately d e t e c t e d and t h e p r e s e n t a t i o n of two s i m u l t a n e o u s s t i m u l i , one i p s i l a t e r a l , t h e o t h e r c o n t r a l a t e r a l t o t h e l e s i o n d i d not produce any s i d e p r e f e r e n c e . When food s t i m u l i were i n t r o d u c e d i n d i s t a n t p e r i p e r s o n a l s p a c e t h e monkey c o n s i s t e n t l y reached € o r them u s i n g t h e hand i p s i l a t e r a l t o t h e l e s i o n . Only when t h i s hand was b l o c k e d , t h e a n i m a l , a l t h o u g h r e l u c t a n t l y , employed t h e c o n t r a l a t e r a l arm. T h e r e was no m i s r e a c h i n g , b u t movements of t h i s arm were somewhat s l o w e r t h a n t h o s e o f t h e n o r m a l arm. The most s t r i k i n g d e f i c i t was o b s e r v e d i n t h e p e r i c u t a n e o u s s p a c e around t h e mouth. When t h e a n i m a l was f i x a t i n g a c e n t r a l s t i m u l u s , t h e i n t r o d u c t i o n of a p i e c e of food i p s i l a t e r a l t o t h e l e s i o n produced, a s i n normal a n i m a l s , an immediate mouth g r a s p i n g r e s p o n s e ; t h e same s t i m u l u s shown c o n t r a l a t e r a l l y was i g n o r e d . S i m i l a r l y , a r a p i d movement of a s t i m u l u s from t h e c e n t e r of t h e mouth t o t h e c o n t r a l a t e r a l s i d e d i d n o t e l i c i t any r e a c t i o n . When a s t i m u l u s was moved s l o w l y from a c e n t r a l p o s i t i o n n e a r t h e mouth t o t h e n e g l e c t e d s i d e , t h e a n i m a l a p p e a r e d t o be aware of t h e s t i m u l u s and tended t o f o l l o w i t . However i t had g r e a t d i f f i c u l t y i n o r g a n i z i n g t h e a p p r o p r i a t e h e a d andmouthmovements n e c e s s a r y € o r g r a p s i n g i t . Most commonly t h e a n i m a l s l o w l y opened i t s mouth and f o l l o w e d t h e s t i m u l u s w i t h t h e mouth open b u t w i t h o u t t r y i n g t o t a k e t h e o b j e c t . When l a t e r a l g r a s p i n g o c c u r r e d , i t w a s e x e c u t e d i n a s t e r e o t y p e d w a y w i t h o u t t h e r i c h n e s s of b u c c a l and f a c i a l movements o b s e r v e d on t h e o t h e r side. D e f i c i t s s i m i l a r t o t h o s e d e m o n s t r a t e d w i t h v i s u a l s t i m u l i were p r e s e n t when t h e hemif a c e and e s p e c i a l l y t h e p e r i o r a l r e g i o n c o n t r a l a t e r a l t o t h e l e s i o n was s t i m u l a t e d w i t h t a c t i l e s t i m u l i . S t i m u l a t i o n of t h e l i p s w i t h food o r o t h e r s t i m u l i produced e i t h e r no r e s p o n s e o r t h e o p e n i n g of t h e mouth n o t accompanied by any a t t e m p t t o b i t e . S i m i l a r l y t h e r a i s i n g of t h e c o r n e r of t h e l i p s a s w e l l a s t h e o t h e r f a c i a l movements which n o r m a l l y accompany food g r a s p i n g w i t h t h e mouthwere a b s e n t . L i c k i n g m o v e m e n t s c o u l d n o t be e l i c i t e d by w e t t i n g t h e c o n t r a l a t e r a l l i p w i t h w a t e r o r j u i c e ; a

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s i m i l a r s t i m u l a t i o n promptly evoked t h e r e s p o n s e on t h e i p s i l a t e r a l s i d e . B l i n k i n g t o t h r e a t e n i n g s t i m u l i moved towards t h e c o n t r a l a t e r a l hemiface was a b s e n t . S i m i l a r l y t h e r e w a s no s i g n o f f e a r o r rage. In c o n t r a s t , f a c i a l movements and a r i c h emotional r e s p o n s e w e r e e a s i l y e l i c i t e d by t h r e a t e n i n g s t i m u l i p r e s e n t e d f a r from t h e animal. The eye movements which were hard t o e l i c i t w i t h t a c t i l e o r p e r i b u c c a l s t i m u l i , were e a s i l y t r i g g e r e d w i t h s t i m u l i p r e s e n t e d f a r fromthemonkey. T h e r e was a marked and r a t h e r f a s t r e c o v e r y w i t h time. S i x t y d a y s a f t e r t h e o p e r a t i o n t h e o n l y r e s i d u a l d e f i c i t s were t h e p r e f e r e n c e i n u s i n g t h e hand i p s i l a t e r a l t o t h e l e s i o n and a c o n s t a n t t u r n i n g , i n t h e t e s t w i t h two peribuccalstimuli, towardsthe oneipsilateral t o t h e lesion. T h e r e a r e t h r e e a s p e c t s of t h e s e f i n d i n g s t h a t a r e of p a r t i c u l a r i n t e r e s t . F i r s t , t h e p r e s e n c e of a d i s s o c i a t i o n between t h e c a p a c i t y t o s h i f t a t t e n t i o n i n t h e f a r s p a c e and t h e c a p a c i t y t o do i t i n t h e p e r s o n a l and p e r i p e r s o n a l space. The same monkey which r e a c t e d p r o p e r l y t o a g l o v e p r e s e n t e d c o n t r a l a t e r a l t o t h e l e s i o n a t a d i s t a n c e of one m e t e r , n e g l e c t e d amenacingstimulus near i t s face. Second, a s i n t h e v e r t i c a l n e g l e c t , t h e r e was a congruence between a t t e n t i o n a l ad motor d e f i c i t s . In monkeys w i t h a r e a 6 l e s i o n s t h e a t t e n t i o n a l d e f i c i t s d i d n o t i n c l u d e t h e f a r s p a c e a n d , on t h e motor s i d e , t h e r e was no eye movement d e f i c i t s . The a t t e n t i o n d e f i c i t concerned t h e s p a c e w i t h i n which s t i m u l i can be reached, g r a s p e d and m a n i p u l a t e d w i t h hands and mouth. In a c c o r d a n c e w i t h t h e d i s t r i b u t i o n of t h e a t t e n t i o n a l d e f i c i t t h e motor d e f i c i t comprised head-mouth movements and t o a lower d e g r e e arm-hand movements. I t i s hard t o s a y why t h e arm-hand movements were l e s s impaired t h a t one could e x p e c t from t h e e l e c t r o p h y s i o l o g i c a l d a t a on t h i s a r e a ( s e e Godschalk, Lemon, N i j s & Kuypers, 1981; R i z z o l a t t i , S c a n d o l a r a , G e n t i l u c c i & Camarda, 1981a; R i z z o l a t t i , S c a n d o l a r a , M a t e l l i & G e n t i l u c c i , 1981b, c ) . S e v e r a l i n t e r p r e t a t i o n can be o f f e r e d o n t h i s p o i n t ( s e e R i z z o l a t t i e t a l . , 1983). What i s i m p o r t a n t h e r e , however, i s t h a t i n accordance w i t h t h e g r e a t e r s e v e r i t y of d e f i c i t s of f a c i a l and mouth movements, t h e r e was a l s o a g r e a t e r d e f i c i t i n a t t e n t i o n t o p e r i b u c c a l s p a c e than t o d i s t a n t peripersonalspace. T h i r d , t h e a n a t o m i c a l s i t e of t h e l e s i o n was o u t s i d e t h e c e n t e r s normally c o n s i d e r e d c r u c i a l f o r d i r e c t i n g a t t e n t i o n . The l e s i o n w a s w i t h i n a premotor a r e a , t h a t i s i n an a r e a which o r g a n i z e s body movements and i s s t r i c t l y connected w i t h a r e a 4 . We do n o t b e l i e v e t h a t t h i s a s s o c i a t i o n between n e g l e c t and t h e l e s i o n of a premotor a r e a i s a n odd f i n d i n g . On t h e c o n t r a r y , t h i s a s s o c i a t i o n may be a c l u e f o r a b e t t e r u n d e r s t a n d i n g of t h e n e g l e c t syndrome. c) Extrapersonal neglect The o b s e r v a t i o n t h a t i n t h e monkey a u n i l a t e r a l l o b e e x c i s i o n r o s t r a 1 t o t h e granular frontal cortexproduces acontralateralneglect i s v e r y o l d . A t t h e end of t h e l a s t c e n t u r y B i a n c h i (1895) r e p o r t e d t h a t f o l l o w i n g s u c h a l e s i o n monkeys p r e s e n t e d r o t a t o r y movements t o t h e s i d e of t h e l e s i o n and a v i s u a l d i s t u r b a n c e t h a t appeared a s a c o n t r a l a t e r a l hemianopia. Those f i n d i n g s were confirmed by Kennard (Kennard & E c t o r s , 1938; Kennard, 1939) who d e s c r i b e d i n a d d i t i o n t o v i s u a l d i s t u r b a n c e s a d e f i c i t i n r e s p o n d i n g t o cutaneous s t i m u l a t i o n of t h e c o n t r a l a t e r a l body. A s i m i l a r o b s e r v a t i o n w a s made by Welchand S t u t e v i l l e (1958) a f t e r a l e s i o n p l a c e d i n t h e d e p t h o f t h e a r c u a t e s u l c u s . More r e c e n t l y , L a t t o and Cowey (1971a. b) i n a v e r y c a r e f u l s t u d y of monkey's d e f i c i t s f o l l o w i n g l e s i o n s l o c a l i z e d t o t h e f r o n t a l e y e f i e l d f a i l e d t o confirm t h e somatosensory n e g l e c t , whereas t h e y showed, i n addition t o the v i s u a l a t t e n t i o n d e f i c i t , oculomotordisturbances. R i z z o l a t t i e t a l . (1983) t e s t e d two m o n k e y s w i t h a u n i l a t e r a l l e s i o n o f

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t h e f r o n t a l eye f i e l d employing t h e same t e s t i n g p r o c e d u r e used i n t h e i r a r e a 6 s t u d y . I n t h e s e monkeys s p o n t a n e o u s o c u l a r s a c c a d e s and head movements towards t h e s i d e c o n t r a l a t e r a l t o t h e l e s i o n were r a r e . F u r t h e r m o r e when a v i s u a l s t i m u l u s , p r e s e n t e d i n t h e n e g l e c t e d s p a c e , evoked a s a c c a d e , t h e f i x a t i o n was s h o r t - l a s t i n g and t h e e y e s r e t u r n e d immediately t o t h e r e s t i n g p o s i t i o n . S t i m u l i p r e s e n t e d i n t h e f a r s p a c e c o n t r a l a t e r a l t o t h e l e s i o n were n e g l e c t e d . T h i s w a s p a r t i c u l a r l y c l e a r when t h e a n i m a l ' s a t t e n t i o n w a s a l r e a d y e n g a g e d o n a n o t h e r s t i m u l u s ; i n t h i s c a s e a s t i m u l u s i n t h e i p s i l a t e r a l f i e l d was responded t o , w h i l e a c o n t r a l a t e r a l one was n e g l e c t e d . When two s t i m u l i w e r e s i m u l t a n e o u s l y m o v e d from a c e n t r a l p o s i t i o n towards r i g h t o r l e f t , t h e c o n t r a l a t e r a l one was always p r e f e r r e d . I n s h a r p c o n t r a s t w i t h t h e b e h a v i o r of monkeys w i t h a r e a 6 l e s i o n , t h e t a c t i l e s t i m u l a t i o n of t h e mouth w i t h a p i e c e of food produced a b r i s k g r a s p i n g r e s p o n s e . S i m i l a r l y , t h e p r e s e n t a t i o n of a s t i m u l u s i n t h e p e r i b u c c a l s p a c e evoked a p r e c i s e mouth g r a s p movement a l s o on t h e s i d e c o n t r a l a t e r a l t o t h e l e s i o n . The movement was accompanied by t h e normal p a t t e r n of f a c i a l muscle c o n t r a c t i o n s . When two s t i m u l i were moved i n t h e s p a c e around t h e mouth, i n one animal t h e i p s i l a t e r a l s t i m u l u s was u s u a l l y p r e f e r r e d , i n t h e o t h e r no s i d e p r e f e r e n c e was observed. Thus t h e r e i s l i t t l e doubt t h a t a f t e r a f r o n t a l eye f i e l d l e s i o n t h e animal can a t t e n d t o t h e personal space. Furthermore i t appears t h a t the peripersonal space i s onlymoderatly affected. Prompted by t h e s e f i n d i n g s G e n t i l u c c i , G e n t i l i n i , P o r r o , M a t e l l i & R i z z o l a t t i ( u n p u b l i s h e d o b s e r v a t i o n s ) t e s t e d two a d d i t i o n a l monkeys w i t h f r o n t a l eye f i e l d l e s i o n s i n a more formal s i t u a t i o n . The a n i m a l s were c o n d i t i o n e d t o perform two t a s k s o r i g i n a l l y d e v i s e d by Wurtz (1969). In t h e f i r s t one - f i x a t i o n t a s k - t h e a n i m a l has t o d e t e c t t h e dimming of a LED l o c a t e d i n f r o n t of i t and, in o r d e r t o g e t a reward, t o r e l e a s e a l e v e r d u r i n g t h e dimming. I n t h e second one - s a c c a d e t a s k - t h e c e n t r a l LED was t u r n e d o f f a f t e r a f i x e d time i n t e r v a l a n d , s i m u l t a n e o u s l y , a n o t h e r l i g h t was t u r n e d on. The second l i g h t dimmed a f t e r a v a r i a b l e i n t e r v a l and, a s i n t h e f i x a t i o n t a s k , t h e a n i m a l had t o r e l e a s e t h e b a r d u r i n g t h e dimming i n o r d e r t o be rewarded. F i x a t i o n t r i a l s and s a c c a d e t r i a l s were i n t e r m i x e d . Eyemovementswere r e c o r d e d u s i n g t h e m a g n e t i c s e a r c h c o i l t e c h n i q u e . The t e s t i n g w a s done u s i n g t h r e e p e r i m e t e r s , l o c a t e d a t t h e d i s t a n c e o f 1 0 , 30 and 150 cm from t h e monkey. Each p e r i m e t e r c a r r i e d rows of LEDs t h a t p e r m i t t e d t h e t e s t i n g of t h e u p p e r , lower, r i g h t and l e f t s e c t o r s of t h e v i s u a l f i e l d . I n e a c h p e r i m e t e r t h e s e t of LEDs was l o c a t e d a t t h e same a n g u l a r d i s t a n c e from t h e c e n t e r . I n b o t h a n i m a l s t h e f r o n t a l eye f i e l d l e s i o n was u n i l a t e r a l and r e s t r i c t e d t o t h e lower ( l a t e r a l ) p a r t of i t . T h e p u r p o s e o f a l i m i t e d l e s i o n was t h a t of d e s t r o y i n g t h e s e c t o r of f r o n t a l eye f i e l d t h a t r e c e i v e s v i s u a l i n p u t , while sparing t h a t r e l a t e d t o t h e a c o u s t i c a l modality (Barbas & Mesulam, 1981). T h i s was done i n o r d e r t o i n t e r f e r e a s l i t t l e a s p o s s i b l e w i t h t h e c a p a c i t y of t h e a n i m a l t o make s a c c a d e s . One of t h e a n i m a l s used i n t h e e x p e r i m e n t underwent, s e v e r a l months b e f o r e t h e f r o n t a l eye f i e l d e x c i s i o n , a n a b l a t i o n of t h e r o s t r a 1 p a r t of i n f e r i o r p a r i e t a l l o b u l e ( a r e a 7b) and a v e r y r e s t r i c t e d l e s i o n of p o s t a r c u a t e c o r t e x . Both a n i m a l s preoperativelyperformed q u i t e w e l l o n a l l t h r e e perimeters. The c a p a c i t y t o e x e c u t e b o t h t h e f i x a t i o n and t h e s a c c a d e t a s k w a s n o t i m p a i r e d by t h e l e s i o n . However, t h e l a t e n c y of e y e movements towards s t i m u l i i n t h e c o n t r a l a t e r a l f i e l d i n c r e a s e d i n b o t h a n i m a l s . In t h e a n i m a l w i t h a p r e v i o u s f r o n t o - p a r i e t a l l e s i o n t h i s i n c r e a s e concerned n e a r and f a r s t i m u l i , but t h e impairment was s i g n i f i c a n t l y g r e a t e r f o r f a r s t i m u l i . I n t h e second animal o n l y t h e l a t e n c y t o f a r s t i m u l i i n c r e a s e d .

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Taken t o g e t h e r t h e s e d a t a i n d i c a t e t h a t even i n t h e c a s e of c l a s s i c a l , " t y p i c a l " n e g l e c t t h e a t t e n t i o n a l d e f i c i t i s n o t g l o b a l . The d i s t u r b a n c e a f t e r f r o n t a l eye f i e l d l e s i o n a p p e a r s t o c o n c e r n e s s e n t i a l l y t h e f a r s p a c e . R e s u l t s congruent w i t h t h i s p o i n t of view can be a l s o found i n c a s e s of h u m a n n e g l e c t . I n a r e c e n t s t u d y B i s i a c h a n d h i s coworkers ( B i s i a c h , P e r a n i , V a l l a r & B e r t i , 1986) a s s e s s e d t h e p r e s e n c e of p e r s o n a l and e x t r a p e r s o n a l n e g l e c t i n a l a r g e number of r i g h t brain-damaged p a t i e n t s . The e x t r a p e r s o n a l n e g l e c t was t e s t e d by r e q u i r i n g t h e p a t i e n t s t o c r o s s c i r c l e s on a s h e e t of paper. The p e r s o n a l n e g l e c t was a s s e s s e d by p o i n t i n g t o t h e p a t i e n t ' s r i g h t hand ( t h a t on t h e normal s i d e ) and by o r d e r i n g him t o t o u c h w i t h t h i s hand t h e o t h e r one ( t h a t on t h e n e g l e c t e d s i d e ) . As one can e x p e c t i n most p a t i e n t s b o t h e x t r a p e r s o n a l and p e r s o n a l n e g l e c t was p r e s e n t . However o u t of 27 c a s e s showingaverysevereextrapersonalneglect, 9 h a d n o d e f i c i t a t a l l i n t h e p e r s o n a l space. S i m i l a r l y o u t of 6 c a s e s w i t h marked p e r s o n a l n e g l e c t one was f r e e of any d i s t u r b a n c e i n t h e e x t r a p e r s o n a l space. The d i s s o c i a t i o n between e x t r a p e r s o n a l and p e r s o n a l s p a c e was confirmed by t h e f a c t t h a t i n a l a r g e number of p a t i e n t s t h e s e v e r i t y of t h e two d e f i c i t s d i d n o t c o r r e l a t e . Thus, i n good agreement w i t h animal s t u d i e s , a l s o i n man, t h e n e u r a l s u b s t r a t e s c o n t r o l l i n g a t t e n t i o n i n t h e p e r s o n a l and e x t r a p e r s o n a l s p a c e a r e n o t t h e same. I t i s i n t e r e s t i n g t o n o t e h e r e t h e f r e q u e n t p r e s e n c e of oculomotor d i s t u r b a n c e s i n human n e g l e c t ( s e e S c h o t t , J e a n n e r o d & Zahin, 1966). T h e s e d e f i c i t s cannot be a consequence of t h e a t t e n t i o n a l d e f i c i t s i n c e t h e c o n j u g a t e gaze p a r a l y s i s i n s t r o k e p a t i e n t s i s much more f r e q u e n t a f t e r r i g h t hemisphere i n j u r y ( t h e s i d e t h a t produces more f r e q u e n t l y n e g l e c t i n humans) t h a n a f t e r t h e l e f t h e m i s p h e r e i n j u r y ( D e R e n z i , C o l o m b o , F a g l i o n i & G i b e r t o n i , 1982). These f i n d i n g s i n d i c a t e t h e c l o s e r e l a t i o n s between t h e eye movement mechanisms and e x t r a p e r s o n a l a t t e n t i o n i n t h e c l a s s i c a l parietallobeneglect.

SelectiveAttention: ADistributedSystem I n primary v i s u a l a r e a s t h e l o c a t i o n of s t i m u l i i n s p a c e i s coded a c c o r d i n g t o a r e t i n o t o p i c s y s t e m of c o o r d i n a t e s . T h e r e i s l i t t l e doubt however t h a t t h e o r g a n i z a t i o n of movements i n s p a c e r e q u i r e s a system of c o o r d i n a t e s independent of t h e r e t i n a . Evidence f o r t h i s comes from t h e common e x p e r i e n c e t h a t movements of t h e e y e s , head o r arms towards a t a r g e t can be e x e c u t e d w i t h o u t v i s u a l s t i m u l i , f o r example i n d a r k n e s s t o a remembered p o s i t i o n o r t o a u d i t o r y s t i m u l i . E x p e r i m e n t a l l y , t h e importance of spatial coordinates can be demonstrated by presenting t a c h i s t o s c o p i c a l l y two l i g h t s i n sequence and by i n s t r u c t i n g t h e s u b j e c t s t o make s e q u e n t i a l s a c c a d e s towards them ( H a l l e t 6 L i g h t s t o n e , 1976; Mays & S p a r k s , 1980). Suppose t h a t t h e two l i g h t s a r e r e s p e c t i v e l y 5 " and 10" o n t h e r i g h t of a f i x a t i o n p o i n t and t h e i n s t r u c t i o n i s tomake t h e f i r s t s a c c a d e t o t h e more p e r i p h e r a l l i g h t , t h e second s a c c a d e t o t h e less p e r i p h e r a l l i g h t . I f t h e d u r a t i o n of t h e l i g h t s i s s h o r t t h e y w i l l s t i m u l a t e t h e r e t i n a a t t h e two e c c e n t r i c i t i e s c o r r e s p o n d i n g t o t h e d i s t a n c e between t h e i r l o c a t i o n s and t h e f i x a t i o n p o i n t . I f themotorcommands w e r e c o d e d i n r e t i n a l t e r m s t h e s u b j e c t a f t e r t h e Eirst s a c c a d e t o t h e 10" s t i m u l u s s h o u l d e x e c u t e a n o t h e r one 5 " f u r t h e r t o t h e r i g h t , s i n c e t h e r e t i n a l informationindicatesapoint 5 " on t h e r i g h t of t h e f i x a t i o n p o i n t . Yet t h e experiment s h o w s t h a t s u b j e c t s a r e a b l e t o e x e c u t e t h e t a s k . T h i s i n s p i t e of t h e f a c t t h a t t h e "go t o l e f t " o r d e r s h o u l d be i s s u e d , a c c o r d i n g t o t h e r e t i n o t o p i c a l r u l e s , by t h e b r a i n h a l f t h a t h a s n e v e r s e e n t h e l i g h t . I t i s o b v i o u s t h a t even f o r s u c h a s i m p l e t a s k t h e v i s u a l i n f o r m a t i o n must be t r a n s l a t e d from r e t i n a l t o s p a t i a l coordinates. A s t a g e t h e r e f o r e e x i s t s where v i s u a l s t i m u l i a r e coded i n s p a t i a l

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t e r m s and i t i s c l e a r t h a t t h o s e c o r t i c a l a r e a s and s u b c o r t i c a l c e n t e r s t h a t o r g a n i z e movements must use t h i s code of r e f e r e n c e . One might a r g u e t h a t a l l systemsinvolvedintheorganizationofmovementsareundercontrolof a

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Figure 6 S t u d y of a soma-related v i s u a l l y r e s p o n s i v e neuron. Upper row (left s i d e ) : s c h e m a t i c drawing of t h e d e v i c e used f o r s t i m u l u s p r e s e n t a t i o n ; ( r i g h t side): stimulus t r a j e c t o r y i n respect t o the animal's face. Middle row: Neuron's r e s p o n s e s i n r e l a t i o n t o t h e s t i m u l u s p o s i t i o n . t h e s t i m u l u s was moved c i r c u l a r l y around t h e a n i m a l ' s f a c e i n a f r o n t a l p l a n e . The s t i m u l u s t r a j e c t o r y was r e c o r d e d on a X-Y s t o r a g e o s c i l l o s c o p e and t h e b r i g h t n e s s of t h e o s c i l l o s c o p e beam was i n t e n s i f i e d i n c o r r e s p o n d e n c e w i t h t h e o c c u r r e n c e of a c t i o n p o t e n t i a l s . Each d o t r e p r e s e n t s one a c t i o n p o t e n t i a l . Note t h e c o n c e n t r a t i o n of t h e d o t s i n t h e lower p a r t of t h e t r a j e c t o r y . D o t s i n t h e upper p a r t of i t a r e due t o t h e n e u r o n ' s s p o n t a n e o u s a c t i v i t y . Lower row: I n A l , B1 and C 1 a r e shown t h e X-Y r e c o r d s of t h e movements of t h e r i g h t eye d u r i n g t h e s t i m u l u s p r e s e n t a t i o n A , B and C , r e s p e c t i v e l y . Given t h e n o n - l i n e a r i t y of t h e EOG when t h e e y e s a r e i n s t r o n g l y e c c e n t r i c p o s i t i o n s , t h e r e c o r d i n d i c a t e s t h e eye e x c u r s i o n o n l y a p p r o x i m a t e l y . Note t h e l a c k of c o r r e l a t i o n between eye p o s i t i o n and t h e n e u r o n ' s d i s c h a r g e ( F r o m G e n t i l u c c i e t a l . , 1983).

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s i n g l e map which p r o v i d e s s p a t i a l i n f o r m a t i o n t o t h e premotor system. T h i s p o s s i b i l i t y i s not s u p p o r t e d by n e u r o p h y s i o l o g i c a l d a t a . Neurons c o d i n g v i s u a l i n f o r m a t i o n i n s p a t i a l terms have been d e s c r i b e d i n i n f e r i o r a r e a 6 ( G e n t i l u c c i , S c a n d o l a r a , P i g a r e v & R i z z o l a t t i , 1983). i n a r e a 7b (Leinonen & Nyman, 1979; Leinonen, Hyvarinen, Nyman & L i n n a n k o w s k i , 19791, i n a r e a 7a 1975; Lynch, ( M o u n t c a s t l e , Lynch, Georgopoulos, S a k a t a & Acuna, M o u n t c a s t l e , T a l b o t & Yin, 1977; S a k a t a , 1980) and i n t h e i n t r a l a m i n a r t h a l a m i c n u c l e i ( S c h l a g , Schlag-Rey, Peck and J o s e p h , 1980). I t i s v e r y l i k e l y t h a t t h e mechanisms bywhich t h e l o c a t i o n i n s p a c e i s c o m p u t e d v a r y i n d i f € e r e n t systems. In t h o s e p r i m a r i l y i n v o l v e d i n e x t r a p e r s o n a l s p a c e e x p l o r a t i o n and i n programming eye movements t h e computation i s based on i n f o r m a t i o n on p o s i t i o n of t h e e y e s i n o r b i t and t h e p a r t of t h e r e t i n a t h a t i s s t i m u l a t e d . Such a mechanism h a s been proposed f o r t h e f i x a t i o n neurons d e s c r i b e d i n t h e monkey's p a r i e t a l l o b e ( M o u n t c a s t l e e t a l . , 1975; Lynch e t a l . , 1977; S a k a t a , S h i b u t a n i & Kawano, 1980) and f o r some n e u r o n s of t h e c a t ' s i n t r a l a m i n a r t h a l a m i c n u c l e i ( S c h l a g e t a l . , 1980). A d i f f e r e n t mechanism i s v e r y l i k e l y t o be r e s p o n s i b l e f o r t h e s p a t i a l p r o p e r t i e s of neurons i n v o l v e d i n programming movements i n t h e p e r i p e r s o n a l space. I n b o t h a r e a 6 and 7b, bimodal neurons have been found which respond t o somatosensory and v i s u a l s t i m u l i . I n t h e s e n e u r o n s t h e somatosensory r e c e p t i v e f i e l d and t h e v i s u a l l y r e s p o n s i v e s p a t i a l r e g i o n a r e i n r e g i s t e r and t h e v i s u a l l y r e s p o n s i v e r e g i o n remains i n t h e same, b o d y - r e l a t e d , p o s i t i o n i r r e s p e c t i v e of t h e eye l o c a t i o n . F i g u r e 6 shows one of t h e s e soma-related n e u r o n s r e c o r d e d from i n f e r i o r a r e a 6 of t h e monkey. T h i s neuron had a b i l a t e r a l t a c t i l e r e c e p t i v e f i e l d e x t e n d i n g f r o m t h e lower l i p t o t h e c h i n . V i s u a l r e s p o n s e s were evoked by moving s t i m u l i i n t h e s p a c e around t h e t a c t i l e f i e l d . One can s e e t h a t , r e g a r d l e s s of eye p o s i t i o n , t h e r e s p o n s e ( d o t s i n t e n s i f y i n g t h e s t i m u l u s t r a j e c t o r y ) is always c o n c e n t r a t e d i n t h e lower p a r t of t h e v i s u a l space. Note that t h i s o c c u r r e d a l s o when t h e a n i m a l t r a c k e d t h e s t i m u l u s and t h e r e f o r e when t h e s t i m u l u s p o s i t i o n i n r e s p e c t t o t h e r e t i n a remained r e l a t i v e l y f i x e d . I t i s p o s s i b l e t h a t soma-related neurons l i k e t h a t i n F i g u r e 6 s i g n a l t h e s p a t i a l l o c a t i o n of t h e s t i m u l u s by comparing t h e p o s i t i o n of v i s u a l s t i m u l u s w i t h t h e v i s i o n of a body p a r t o r w i t h t h e knowledge of i t s p o s i t i o n based on p r o p r i o c e p t i o n . R e g a r d l e s s of t h e p h y s i o l o g i c a l mechanisms i n v o l v e d i n t h e g e n e s i s of s p a t i a l n e u r o n s , t h e d a t a reviewed i n t h i s s e c t i o n i n d i c a t e t h a t t h e o r g a n i z a t i o n of movement i m p l i e s s p a t i a l maps and t h a t neurons c o d i n g t h e p o s i t i o n of s t i m u l i i n s p a c e a r e d i s t r i b u t e d i n v a r i o u s i n d e p e n d e n t c e n t e r s . We propose t h a t t h e c a p a c i t y of s h i f t i n g a t t e n t i o n i s due t o t h e a c t i v i t y of t h o s e a r e a s which program motor p l a n s i n a s p a t i a l framework. T h i s c o n c e p t i o n i s r a d i c a l l y d i f f e r e n t from t h a t of a s i n g l e a t t e n t i o n a l c i r c u i t because i t c o n c e i v e s s p a t i a l a t t e n t i o n n o t a s a s u p r a o r d i n a t e f u n c t i o n c o n t r o l l i n g t h e a c t i v i t y of t h e b r a i n a s a whole, b u t as a p r o p e r t y i n t r i n s i c a l l y l i n k e d t o t h e premotoractivityanddistributedamongvarious c e r e b r a l c e n t e r s . I n o t h e r words, s p a t i a l a t t e n t i o n i s a modular v e r t i c a l f u n c t i o n p r e s e n t i n s e v e r a l independent c i r c u i t s .

APremotorTheoryof SpatialAttention I t i s g e n e r a l l y accepted t h a t a t t e n t i o n m a y b e a t t r a c t e d i n a passive, e f f o r t l e s s way by s t i m u l i endowed w i t h c e r t a i n c h a r a c t e r i s t i c s ( p a s s i v e a t t e n t i o n ) O K i t may be a c t i v e l y d i r e c t e d by t h e i n d i v i d u a l s ( a c t i v e a t t e n t i o n ) . During n e g l e c t t h e s e two a s p e c t s of a t t e n t i o n a r e impaired. A t h e o r y of s p a t i a l a t t e n t i o n s h o u l d t h e r e f o r e t a k e i n t o a c c o u n t b o t h t h e a c t i v e a n d passiveattentionphenomena. According t o t h e premotor t h e o r y o f s p a t i a l a t t e n t i o n ( s e e f o r a f o r m e r v e r s i o n R i z z o l a t t i , 1 9 8 3 ) , when a s t i m u l u s endowed w i t h a t t e n t i o n a l

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p r o p e r t i e s ( T i t c h n e r , 1966; B e r l y n e , 1960, 1970) i s p r e s e n t e d , i t t r i g g e r s neurons which p l a n a c t i o n i n space. T h e s e neurons a r e p r e s e n t i n v a r i o u s c i r c u i t s and, a c c o r d i n g t o s t i m u l u s l o c a t i o n , s e v e r a l c i r c u i t s c o n t r o l l i n g t h e same s p a c e s e c t o r a r e a c t i v a t e d . S t i m u l i , f o r example, p r e s e n t e d i n t h e e x t r a p e r s o n a l s p a c e may a c t i v a t e s i m u l t a n e o u s l y c o r t i c a l and m i d b r a i n c i r c u i t s , c o n t r o l l i n g s i m i l a r o r c o n g r u e n t movements. In c o n t r a s t , c i r c u i t s whose f u n c t i o n i s t o o r g a n i z e o t h e r t y p e s of movements, o r movements of t h e same e f f e c t o r s i n o t h e r d i r e c t i o n s w i l l b e n o t a c t i v a t e d o r e v e n i n h i b i t e d . T h e s e t t i n g of a m o t o r p l a n i n a g i v e n c i r c u i t i s a c c o m p a n i e d by " t a k i n g p o s s e s s i o n by t h e mind, i n a c l e a r and v i v i d form" (James, 1950) of t h e s p a c e s e c t o r where t h e motor p l a n w i l l be implemented, t h a t i s by a n a t t e n t i o n s h i f t towards t h i s s p a c e s e c t o r . A c r u c i a l q u e s t i o n , a t t h i s p o i n t , i s why t h e i n c r e a s e of a c t i v i t y of premotor neurons s h o u l d r e s u l t i n a t t e n t i o n towards t h e s p a c e s e c t o r c o n t r o l l e d by t h e s e neurons. One may a r g u e t h a t a new o r i n t e r e s t i n g s t i m u l u s s h o u l d s i m p l y e l i c i t a motor r e a c t i o n towards t h e s t i m u l u s . T h i s t y p e of c l o s e l i n k between s t i m u l u s and r e s p o n s e i s p r e s e n t i n lower v e r t e b r a t e s . The s t e r e o t y p e d r e s p o n s e of a t o a d t o a worm o r a worm-like s t i m u l u s ( s e e E w e r t , 1 9 7 9 ) , i s a n example of s u c h a r i g i d s t i m u l u s - r e s p o n s e r e l a t i o n s h i p . I n h i g h e r mammals, however, t h e i n c r e a s e of e n c e p h a l i z a t i o n h a s f r e e d , t o a l a r g e e x t e n t , t h e i n d i v i d u a l s from f i x e d r e a c t i o n s ( s e e J e r i s o n and h i s c o n c e p t of r e p r e s e n t a t i o n , 1973; 1985). The motor p l a n e l i c i t e d by t h e s t i m u l u s a c t i v a t e s t h e r e p r e s e n t a t i o n of t h e s p a c e s e c t o r where t h e p l a n w i l l be t r a n s f o r m e d i n t o a c t i o n . T h i s r e p r e s e n t a t i o n a l l o w s t h e i n d i v i d u a l s t o choose whether t o respond o r n o t and, i n c a s e of r e s p o n s e , t o s e l e c t t h e r e s p o n s e w h i c h is t h e m o s t a d e q u a t e . The n e x t q u e s t i o n c o n c e r n s t h e mechanisms by which a c t i v a t i o n of premotor neurons produces a n i n c r e a s e of a t t e n t i o n i n a c e r t a i n s p a c e r e g i o n . The answer t o t h i s q u e s t i o n c a n o b v i o u s l y be o n l y h y p o t h e t i c a l . Some s o l u t i o n s however can be advanced. A p o s s i b l e way t o s o l v e t h e problem i s t o p o s t u l a t e t h a t t h e world p e r c e p t i o n d o e s n o t depend on t h e a c t i v i t y of one o r few r e t r o l a n d i c a r e a s , b u t on t h e a c t i v i t y of a l l a r e a s where s p a c e i s coded. A s reviewed above, neurons w i t h s p a t i a l p r o p e r t i e s a r e p r e s e n t n o t o n l y i n t h e i n f e r i o r p a r i e t a l l o b e , b u t a l s o i n t h e f r o n t a l l o b e , i n t h e thalamus and p o s s i b l y i n o t h e r a r e a s . Thus t h e a c t i v a t i o n of a g i v e n premotor a r e a s h o u l d g i v e r e l e v a n c e t o t h e s p a c e c o n t r o l l e d by i t and r e s u l t t h e r e f o r e i n a g r e a t e r a t t e n t i o n t o t h a t p a r t of space. Another, c l o s e l y r e l a t e d s o l u t i o n of t h e problem, i s t h a t of p o s t u l a t i n g i n h i b i t o r y i n t e r a c t i o n s between premotor a r e a s c o n t r o l l i n g d i f f e r e n t motor p l a n s . P r o b a b l y t h e b e s t e v i d e n c e in f a v o r of t h e e x i s t e n c e of t h e s e i n t e r a c t i o n s i s t h e s o - c a l l e d "Sprague e f f e c t " ( S p r a g u e , 1966). T h i s e f f e c t c o n s i s t s i n t h e r e c o v e r y of v i s u a l r e s p o n s e s t o s t i m u l i c o n t r a l a t e r a l t o t h e a b l a t e d p o s t e r i o r n e o c o r t e x , when a second l e s i o n i s p l a c e d t o t h e i p s i l a t e r a l s u p e r i o r c o l l i c u l u s . The r e c o v e r y o c c u r s a l s o when t h e c o r t i c a l l e s i o n i s v e r y l a r g e and t h e c o n t r a l a t e r a l n e g l e c t permanent. Although t h e "Sprague e f f e c t " undoubtedly shows t h a t i n h i b i t o r y i n t e r a c t i o n s do e x i s t between a r e a s c o n t r o l l i n g a t t e n t i o n , i t i s d i f f i c u l t , a t t h e p r e s e n t , t o e v a l u a t e i f i n h i b i t o r y mechanisms c o n t r o l a t t e n t i o n o n l y i n opposite d i r e c t i o n s l i k e r i g h t - l e f t o r a l s o play a r o l e i n d i s t r i b u t i n g a t t e n t i o n among p e r s o n a l , p e r i p e r s o n a l and e x t r a p e r s o n a l s p a c e s e c t o r s . I n h i b i t i o n , however, c e r t a i n l y p l a y s a n i m p o r t a n t r o l e w i t h i n t h e c e n t e r s c o n t r o l l i n g a t t e n t i o n a l s h i f t s ( R i z z o l a t t i , Camarda, Grupp 6 P i s a , 1974; B u c h t e l , Camarda, R i z z o l a t t i 6 S c a n d o l a r a , 1979; Wurtz. Richmond & J u d g e , 1980). Anotherway t o explain the i n c r e a s e o f a t t e n t i o n t o a g i v e n s p a c e s e c t o r

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a f t e r a premotor a c t i v a t i o n i s t h a t of a d m i t t i n g a f a c i l i t a t o r y i n f l u e n c e o f t h e premotor a r e a s on s e n s o r y c e n t e r s connected w i t h them. An example of t h i s i s t h e f a c i l i t a t i o n t h a t i n a n expectancy paradigm premotor neurons l o c a t e d i n t h e i n t e r m e d i a t e l a y e r s of t h e s u p e r i o r c o ~ ~ i c u ~e xuesr t on s e n s o r y neurons of t h e s u p e r f i c i a l l a y e r s of t h e same s t r u c t u r e (Mohler & Wurtz, 1976).The d i f f e r e n c e between t h i s m o d e l and t h o s e p r e s e n t e d a b o v e i s t h a t h e r e t h e a t t e n t i o n i s a t t r i b u t e d t o a n i n c r e a s e of r e s p o n s i v e n e s s Of s e n s o r y neurons caused by t h e a c t i v i t y of premotor n e u r o n s , whereas i n t h e o t h e r models i t i s a t t r i b u t e d t o t h e f i r i n g of premotor neurons per se. Obviouslythesetwo p o s s i b i l i t i e s arenotmutuallyexclusive. B e s i d e s b e i n g p a s s i v e l y a t t r a c t e d by changes i n t h e environment, a t t e n t i o n can be a c t i v e l y c o n t r o l l e d by t h e s u b j e c t . A s h i f t of a t t e n t i o n can precede t h e appearance of a s t i m u l u s ( " s e t " o r " expectancy") and a c c o r d i n g l y i n f l u e n c e t h e p r o c e s s i n g of i n p u t (Hebb, 1949; c f . a l s o P o s n e r , 1978). A t a f i r s t g l a n c e a c t i v e l y d i r e c t e d a t t e n t i o n seems t o pose some problems t o t h e premotor t h e o r y of a t t e n t i o n . I f no c e n t r a l a t t e n t i o n a l c e n t e r of c i r c u i t e x i s t s , howcanattentionbeactivelyshiftedtodifferent space s e c t o r s ? The answer i s r a t h e r simple. S i n c e s p a t i a l a t t e n t i o n i s a consequence of t h e o r g a n i z a t i o n of motor p l a n s i n a s p a t i a l framework, t h e s e l e c t i o n of a m o t o r p l a n s h o u l d a u t o m a t i c a l l y produce a s h i f t of a t t e n t i o n toward t h e s p a t i a l s e c t o r where t h e a c t i o n w i l l be e x e c u t e d . I t i s beyond t h e scope of t h i s c h a p t e r t o d i s c u s s how c e r t a i n a c t i o n s a r e s e l e c t e d and t h e v a r i o u s m o t i v a t i o n a l , hormonal and m e t a b o l i c f a c t o r s t h a t may i n t e r v e n e i n t h i s choice. A l e s i o n however of a r e a s s e l e c t i n g f u t u r e a c t i o n s s h o u l d n o t produce d e f i c i t s of a t t e n t i o n of t h e type d i s c u s s e d i n t h i s c h a p t e r . The m o t i v a t i o n a l l y d e t e r m i n e d long-term g o a l a r e d e c i d e d a t a s t a g e p r e c e d i n g t h a t where motor p l a n s a r e o r g a n i z e d . L e s i o n s of t h e s e s t a g e s , s h o u l d produce i n a b i l i t y t o organize f u t u r e a c t i v i t y , distractability, v u l n e r a b i l i t y t o i n t e r f e r e n c e , d i m i n i s h e d e x p l o r a t o r y d r i v e s and o t h e r d i s t u r b a n c e s of t h i s k i n d , b u t s p a t i a l a t t e n t i o n s h o u l d remain normal d u r i n g t h i s p o o r l y o r g a n i z e d p u r p o s i v e behavior. To c o n c l u d e , a model of s p a t i a l a t t e n t i o n based on a s e r i e s of c i r c u i t s l a r g e l y i n d e p e n d e n t one from a n o t h e r is a b l e t o e x p l a i n how t h e a t t e n t i o n i s s h i f t e d a c t i v e l y o r i n responsetoexternalstimuli. I n c o n t r a s t , a n y s i n g l e a t t e n t i o n a l C i r c u i t t h e o r y h a s enormous e x p l a n a t o r y d i f f i c u l t i e s when examined in relation to real brain anatomy. Neither the f ronto-parietal-cingulate c i r c u i t (Mesulam, 1 9 8 1 ) , n o r o t h e r c o r t i c a l c i r c u i t s can e a s i l y account f o r t h e a t t e n t i o n a l d e f i c i t f o l l o w i n g l e s i o n s of midbrain s t r u c t u r e s o r t h e n i g r o - s t r i a t a l system. What is more i m p o r t a n t anatomical d a t a on c o r t i c o - c o r t i c a l c o n n e c t i o n s a l s o f a i l t o s u p p o r t a s i n g l e C i r c u i t theory. I n t h e monkey t h e r e a r e t h r e e main pathways which connect t h e f r o n t a l and p a r i e t a l l o b e s ( s e e P e t r i d e s & Pandya , 1984). The f i r s t l i n k s t h e s u p e r i o r p a r i e t a l l o b u l e ( a r e a 5) w i t h t h e d o r s a l p a r t of a r e a s 6 a n d w i t h t h e supp1ementarymotorarea.The s e c o n d l e a v e s t h e r o s t r a l p a r t of t h e i n f e r i o r p a r i e t a l l o b u l e ( a r e a 7b) and t e r m i n a t e s i n i n f e r i o r a r e a 6 , i n a r e a 46 below t h e s u l c u s p r i n c i p a l i s and i n t h e f r o n t a l and p e r i c e n t r a l o p e r c u l a r c o r t e x . The t h i r d pathway c o n n e c t s t h e c a u d a l p a r t of t h e i n f e r i o r p a r i e t a l l o b u l e ( a r e a 7a) w i t h a r e a 8 , a r e a 46, t h e most r o s t r a 1 p a r t of d o r s a l a r e a 6 a n d t h e c i n g u l a t e g y r u s . The f i K S t of t h e s e c i r c u i t s conveys e s s e n t i a l l y p r o p r i o c e p t i v e i n f o r m a t i o n (Mountcastle e t a l . , 1975). The second c i r c u i t i s m o s t l y , a l t h o u g h n o t e x c l u s i v e l y , i n v o l v e d i n v i s u a l l y g u i d e d oculo-motor b e h a v i o r (Hyvarinen, 1982; Lynch, 1980). The t h i r d c i r c u i t i s formed, a t l e a s t i n p a r t , by p o l y s e n s o r y neurons t h a t respond t o somatosensory and v i s u a l s t i m u l i l o c a t e d i n t h e animal' s p e r i p e r s o n a l s p a c e (Hyvarinen, 1982; R i z z o l a t t i e t a l . , 1981, a , b, c ) . A l e s i o n of t h e s e two l a s t c i r c u i t s

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produces n e g l e c t , b u t t h e t y p e s of n e g l e c t a r e d i f f e r e n t a c c o r d i n g t o which c i r c u i t i s d e s t r o y e d . The l e s i o n of a r e a 7b-area 6 c i r c u i t d e t e r m i n e s a " p e r i p e r s o n a l space-reaching'' n e g l e c t , t h e l e s i o n o f a r e a 7a-area 8 c i r c u i t produce a n " e x t r a p e r s o n a l s p a c e - oculomotor n e g l e c t " . T h i s l a s t t y p e of n e g l e c t is not due t o a l e s i o n of t h e a t t e n t i o n a l c i r c u i t , b u t t o a l e s i o n of o n e o f s e v e r a l premotor c i r c u i t s i n v o l v e d i n s p a t i a l a t t e n t i o n . I n conclusion, the premotortheoryof s e l e c t i v e a t t e n t i o n a p p e a r s t o b e t h e o n l y one a b l e t o accomodate t h e t h r e e b a s i c f i n d i n g s which a n y t h e o r y of n e g l e c t must e x p l a i n : a)Themultiplicityof braincenterswhoselesionproduces neglect. b) The congruence between a t t e n t i o n a l and motor d e f i c i t s a f t e r l e s i o n of these centers. c ) T h e a n a t o m i c a l independence of t h e c e n t e r s w h o s e d a m a g e c a u s e s n e g l e c t . References Mishkin. M . . Westbrook. L . E . & Wurtz. R.H. Visuomotor Albano. J.E.. d e f i c i t s f o l l o w i n g a b l a t i o n of monkey s u p e r i o r c o l l i c u l u s . J o u r n a l of Neurophysiology, 1 9 8 2 , 2 , 338-351. B a r b a s , H. &Mesulam, M . M . 0 r g a n i z a t i o n o f a f f e r e n t i n p u t t o s u b d i v i s i o n s o f a r e a 8 i n t h e r h e s u s monkey. J o u r n a l of Comparative Neurology, 1981, 200, 407-431. B e n d e r M . B . Comments on t h e p h y s i o l o g y and p a t h o l o g y of eye movements i n t h e v e r t i c a l p l a n e . J o u r n a l of nervous and mental D i s e a s e s , 1 9 6 0 , 1 3 0 , 4 5 6-460. B e r l u c c h i , G . , B u c h t e l , H.A. & L e p o r e , F . S u c c e s s f u l i n t e r o c u l a r t r a n s f e r of v i s u a l p a t t e r n d i s c r i m i n a t i o n i n s p l i t - c h i a s m c a t s w i t h s e c t i o n o f t h e i n t e r t e c t a l and p o s t e r i o r commissures. P h y s i o l o g y and B e h a v i o r , 1 9 7 8 , 2 , 331-338. B e r l y n e , D.E. C o n f l i c t , a r o u s a l and c u r i o s i t y . New York: Mc Graw-Hill, 1960. B e r l y n e , D.E. A t t e n t i o n a s a problem i n b e h a v i o r t h e o r y . I n D . I . Mostofsky (Ed.), A t t e n t i o n : Contemporary Theory and A n a l y s i s . Appleton Century C r o f t s . 1970., DD. .. 25-49. B i a n c h i , L. The f u n c t i o n o f t h e f r o n t a l l o b e s . B r a i n , 1 8 9 5 , s , 497-530. Bisiach, E., Perani, D.,Vallar,G. & B e r t i , A . U n i l a t e r a l n e g l e c t : personal and e x t r a p e r s o n a l . Forthcoming. B u c h t e l , H . A . , Camarda, R . , R i z z o l a t t i , G. & S c a n d o l a r a , C. The e f f e c t of h e m i d e c o r t i c a t i o n on t h e i n h i b i t o r y i n t e r a c t i o n s i n t h e s u p e r i o r c o l l i c u l u s of t h e c a t . J o u r n a l of Comparative Neurology, 1979, 184, 795-810. Crowne, D.P. The f r o n t a l eye f i e l d and a t t e n t i o n . P s y c h o l o g i c a l B u l l e t i n , 1 9 8 3 , s . 232-260. Dean, P . & R e d g r a v e , P.The s u p e r i o r c o l l i c u l u s a n d v i s u a l n e g l e c t i n r a t and hamster. I . B e h a v i o u r a l evidence. B r a i n R e s e a r c h Review, 1984, 5 , 129-141. Denny-Brown, D. The m i d b r a i n and motor i n t e g r a t i o n . P r o c e e d i n g s of t h e Royal S o c i e t y o f Medicine, 1 9 6 2 , s , 527-538. Denny-Brown, D. & Chambers, R.A. The p a r i e t a l l o b e and behavior. P r o c e e d i n g of t h e A s s o c i a t i o n f o r Research i n Nervous and Mental D i s e a s e s , 1958, 3 6 , 35-117. D e R e z i , E . D i s o r d e r s of s p a c e e x p l o r a t i o n and c o g n i t i o n . London: J. Wiley. 1982. D e R e n z i , E . , Colombo, A . , F a g l i o n i , P . 6 G i b e r t o n i , M. Conjugate gaze p a r e s i s i n s t r o k e p a t i e n t s w i t h u n i l a t e r a l damage. A r c h i v e s of Neurology, 1 9 8 2 , 2 , 482-486.

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Acknowledgements : T h i s workwas s u p p o r t e d i n p a r t by a N . I . H . R01 NS 19206-01A1 and i n p a r t by a CNR g r a n t .

grant 1