ELECTROPHYSIOLOGICAL EVIDENCE FOR AN L-SHAPED
INTERHEMISPHERIC CONNECTION IN THE CAT
A. CUKIERT — C. TIMO-IARIA
S U M M A R Y — T r a n s c a l l o s a l p o t e n t i a l s e v o k e d b y e l e c t r i c a l s t i m u l a t i o n w i t h r e c t a n g u l a r p u l s e s o f 1 m s , 5 c / s a n d v a r i a b l e i n t e n s i t y w e r e r e c o r d e d f r o m t h e c o r t i c a l s u r f a c e i n c a t s a n e s t h e t i z e d w i t h k e t a m i n e h y d r o c h l o r i d e . S i t e s o f s t i m u l a t i o n a n d r e c o r d i n g w e r e s e l e c t e d b y m e a n s o f a c a r t e s i a n m a p o f m o s t o f t h e n e o c o r t e x . I n a d d i t i o n t o t h e w e l l k n o w n t r a n s c a l l o s a l p r o j e c t i o n p a t t e r n i t w a s f o u n d t h a t s t i m u l a t i o n o f a r e s t r i c t e d p o s t e r i o r a r e a e v o k e s l o w v o l t a g e p o t e n t i a l s o v e r t h e c o n t r a l a t e r a l s y m m e t r i c a r e a w h i l e h i g h v o l t a g e p o t e n t i a l s a r e r e c o r d e d f r o m a f e w s i t e s l o c a t e d at t h e i p s i l a t e r a l a n t e r i o r c o r t e x a n d f r o m t h e a r e a s y m m e t r i c as t o t h e latter. T h i s L - s h a p e d t r a n s c a l l o s a l c o n n e c t i o n m a y b e i n v o l v e d in c o m p l e x c o r t i c a l p r o c e s s e s a n d i s c o m p a t i b l e w i t h e f f e c t i v e r e s u l t s o f p a r t i a l a n t e r i o r c a l l o s o t o m i e s i n p a t i e n t s w i t h m u l t i f o c a l e p i l e p s y a n d f r o n t a l b i s y n c h r o n i s m .
Evidência eletrofisiológica da presença de uma conexão inter-hemisférica em forma de ' L ' no gato.
R E S U M O — F o r a m o b t i d o s p o t e n c i a i s e v o c a d o s t r a n s c a l o s o s p o r a p l i c a ç ã o d e p u l s o s q u a d r a d o s d e 1 m s , 5 c / s e i n t e n s i d a d e v a r i á v e l e r e g i s t r o s o b r e a c o r t i c a l i d a d e d e g a t o s a n e s t e s i a d o s c o m q u e t a m i n a . O s l o c a i s d e e s t i m u l a ç ã o e r e g i s t r o e r a m s e l e c i o n a d o s a t r a v é s d e m a p a c a r t e s i a n o d e g r a n d e p a r t e d o n e o c ó r t e x . A l é m d a s b e m c o n h e c i d a s p r o j e ç õ e s c a l o s a s , f o r a m d i s c r i m i n a d a s á r e a s p o s t e r i o r e s c u j a e s t i m u l a ç ã o e v o c a v a p o t e n c i a i s d e b a i x a a m p l i t u d e e m s u a á r e a h o m ó l o g a e p o t e n c i a i s d e g r a n d e a m p l i t u d e e m r e g i õ e s m a i s a n t e r i o -r e s , i p s i - e c o n t -r a l a t e -r a l m e n t e . E s t a c o n e x ã o t -r a n s c a l o s a e m f o -r m a d e ' L ' p o d e e s t a -r e n v o l v i d a e m p r o c e s s o s c o r t i c a i s c o m p l e x o s e é c o m p a t í v e l a o s b o n s r e s u l t a d o s o b t i d o s p o r c a l o s o t o m i a s p a r c i a i s a n t e r i o r e s e m p a c i e n t e s c o m e p i l e p s i a m u l t i f o c a l e b i s s i n c r o n i a f r o n t a l .
Interhemispheric i n t e g r a t i o n is p a r t of higher c o r t i c a l functional p r o c e s s e s and intrahemispheric c o r t i c a l p a t h w a y s a r e i n v o l v e d in t r a n s f e r r i n g i n f o r m a t i o n b e t w e e n different a r e a s o f the s a m e s i d e . T h e c o r p u s c a l l o s u m , the thickest brain c o m m i s s u r e , has b e e n e x t e n s i v e l y studied f r o m the clinical and e x p e r i m e n t a l p o i n t s o f v i e w 1,8,9,11,13.
B e s i d e s the multitude o f s h o r t such c o n n e c t i o n s l o n g p a t h w a y s are w e l l k n o w n to i n t e r c o n n e c t a r e a s m e d i a t i n g p r o c e s s e s such as s p e e c h and v i s u o m o t o r i n t e g r a t i o n . In e x p e r i m e n t s aiming at a detailed s t u d y o f t r a n s c a l l o s a l c o n n e c t i o n s in the c a t4 w e f o u n d e l e c t r o p h y s i o l o g i c a l e v i d e n c e o f transfer of i n f o r m a t i o n f r o m o n e a r e a from o n e h e m i s p h e r e to sites far from the c o n t r a l a t e r a l s y m m e t r i c area. T h e present p a p e r r e p o r t s the e x p e r i m e n t s that led t o f i n d i n g this L - s h a p e d c o n n e c t i o n .
M A T E R I A L . A N D M E T H O D S
Ten adult cats of either s ex were anesthetized with ketamine hydrochloride and the
neocortex was exposed and electrocorticographic recordings obtained according to procedures described elsewhere 4.
L a b o r a t o r i e s o f F u n c t i o n a l N e u r o s u r g e r y a n d C l i n i c a l P h y s i o l o g y , S c h o o l o f M e d i c i n e , U n i v e r s i t y o f S ã o P a u l o , B r a z i l .
T h i s r e s e a r c h w a s s u p p o r t e d b y F A P E S P (84/1078-9 a n d 85/3531-5), F 1 N E P (43.86.0222.00) a n d L I M I n s t i t u t e ( L I M 74-45).
382 Arq Neuro-Psiquiat (Sao Paulo) 47(4) 1989
Stimulation with rectangular pulses of variable frequency (0.5 to 10 H z ) , duration (0.1 to 3 ms) and current (0.5 to 5 m A ) w a s performed through bipolar silver electrodes 0.8 mm in diameter, one milimiter apart. F o r mapping purposes only 1 H z , 0.5 m s and 4 m A pulses were used. T h e other parameters were used for testing. T h e recording electrode was also
a silver ball 0.8 mm in diameter.
Evoked potentials were recorded from sites along the anteroposterior parallels and then from the dorsoventral meridians, having the homologous locus at its center. F o r each site twenty potentials were electronically averaged. W h e n signs of the L-shaped connection were well established experiments were performed in which some of the links involved were sectioned.
R E S U L T S
The potentials evoked contralateral^ b y stimulation of most areas in one hemisphere
were, in which morphology, latency and amplitude are concerned, quite similar to those pre-viously described 2,3,5,6. W e found, however, that stimulation of a few sites located posteriorly at the marginal and suprasylvian gyri evoked small or moderate responses from the homologous contralateral areas, while larger potentials were elicited over contralateral more anterior areas,
mainly in the medio-anterior region of the marginal or suprasylvian gyri (Fig. 1 ) . These responses were evoked from areas poorly interconnected by the corpus callosum 7.
T o check the presence of an intrahemispheric connection that might account for these potentials three types of experiments were performed. 1. W h i l e stimulating one of the areas poorly interconnected by callosal neurons (S in Fig. 2 — Left) potentials were recorded from the symmetric area ( R l ) and from the anterior site where a higher amplitude potential had been recorded ( R 2 ) . T w o percortical sections (which included the subjacent white matter) were made with a sharp knife, the first medial and the second anterior to S. After the first section (1 in Fig. 2 — Left) was performed the evoked potential in R l completely disappeared whereas that evoked in the anterior region (R2) was only slightly reduced. After sectioning at site 2, the more anterior evoked potential (R2) was abolished.
2. In the second type of experiment serial sections (numbered 1,2 and 3 in Fig. 2 — Middle) were made in the hemisphere being stimulated. Sections 1 and 2 were anterior to the R 2 meridian while section 3 was done between the R l and R 2 meridians. Sections 1 and 2 did not modify R 2 potentials and section 3, as expected from experiment 1, abolished the response.
L-shaped interhemispheric connection 383
Fig. 2 — Left: Summary of experiment 1. S (J28), stimulated posterior region. Rl (J28), contralateral area homologous to S. R2 (J 16), anterior site from which high amplitude potencials were recorded. Sections 1 and 2 are shown in the upper part of the figure. From bottom upwards: the first pair of traces shows recordings from Rl and R2 before sections 1 and 2 were performed; the intermediate traces show a slight R2 decrease and cessation of response in Rl; top traces show a complete disappearance of the response at R2 after section 2. Middle: Summary of experiment 2. S (J28), stimulated posterior region. Rl (J28), contralateral area homologous to S. R2, anterior site from which high amplitude potentials were evoked. Sections 1,2 and 3 are shown in the upper part of the figure. From bottom upwards: the first pair of traces shows recordings from Rl and R2 before sections 1,2 and 3 were performed; after section 1 (second pair of traces) and 2 (third pair) the response remained unchanged; section 3 (fourth pair) abolished R2.
Right: Summary of experiment 3. Intrahemispheric recording. S, posterior site
corres-ponding to J29. R, contralateral area homologous to S. R2, anterior site correscorres-ponding to J18, which exhibited high voltage response to stimulation at S. R2', anterior area corresponding to R2. The lower trace shows the potential evoked on S by stimulating R2'. The upper trace shows the potential evoked from R2* by stimulating S.
C O M M E N T S
T h e e x p e r i m e n t s a b o v e d e s c r i b e d d i s c l o s e d the existence o f an intrahemispheric c o n n e c t i o n that links s o m e p o s t e r i o r sites o f the c a t ' s n e o c o r t e x to s o m e anterior sites o f the contralateral c o r t e x by m e a n s o f an L - s h a p e d p a t h w a y . T h e potentials r e c o r d e d from n o n - s y m m e t r i c lateral a r e a s indicate that information from a specific site m a y be transferred to n o n - s y m m e t r i c , distant areas t h r o u g h rather simple p a t h w a y s . T h a t might be explained b y a s s u m i n g that the thalamus, receiving information from b o t h the ipsilateral and the contralateral c o r t e x , activates the cortical area far from the s y m m e t r i c l o c u s . T h e r e c o u l d b e a massive o b l i q u e callosal interhemispheric p a t h w a y b e t w e e n p o s t e r i o r areas of one side and anterior areas o f the other or a l o n g intrahemispheric c o n n e c t i o n linking the p o s t e r i o r to anterior a r e a s in series with a callosal c o n n e c t i o n to the s y m m e t r i c a l site at the anterior r e g i o n , thus m a k i n g up an L - s h a p e d l o n g p a t h w a y .
A thalamic m e c h a n i s m , if involved, w o u l d be difficult to r e c o g n i z e in our e x p e -riments but it c o u l d not be the main m e c h a n i s m , as s h o w n b y the drastic effect of local, s h a l l o w longitudinal d i s c o n n e c t i o n b e t w e e n the s y m m e t r i c ( a s to the stimu-lating site) p o s t e r i o r area and the s y m m e t r i c , anterior area o f the contralateral c o r t e x . A n o b l i q u e , direct c o n n e c t i o n of the c o r p u s callosum c a n n o t b e either invoked to explain the n o n - s y m m e t r i c callosal r e s p o n s e since a n a t o m i c a l data have s h o w n it t o b e a c o m i s s u r e with no massive o b l i q u e d e c u s s a t i o n s1 0
T h e assumption o f an intrahemispheric c o n n e c t i o n linking the ipsilateral p o s t e r i o r and anterior areas w a s fully demonstrated b y the d i s c o n n e c t i o n p r o c e d u r e s and the ipsilateral r e s p o n s e s e v o k e d b y stimulation o f b o t h anterior and p o s t e r i o r parts o f the cortex. T h e fact that the potentials e v o k e d in the anterior b y p o s t e r i o r stimulation are consistently larger in v o l t a g e than those r e c o r d e d f r o m r e c i p r o c a l experiments is indicative that there are p r o j e c t i o n p a t h w a y s c a r r y i n g information mainly o r o n l y
from the p o s t e r i o r to the anterior r e g i o n s . Potentials in the reverse direction m a y well be due to antidromic c o n d u c t i o n .
T h e areas thus interconnected c o i n c i d e with those p o o r l y interconnected b y the c o r p u s c a l l o s u m , r e v e a l i n g the possibility o f n o n - s y m m e t r i c callosal activation b y means o f transcallosal p a t h w a y s ( f r o m o n e side to the o t h e r ) in series with intra-hemispheric p a t h w a y s in the posterior to anterior direction. H o w e v e r , the e v o k e d potential in R 2 in the first percortical section w a s r e d u c e d but did not disappear. T h i s is s u g g e s t i v e that an L-shaped c o n n e c t i o n m a d e up b y the s e q u e n c e S - R 1 - R 2 c a r r y i n g c o n c u r r e n t but less information m a y also exist. Such a c o n n e c t i o n has already been s u g g e s t e di 2
. If this p a t h w a y d o e s also exist in man it is p r o b a b l y involved in speech and v i s u o m o t o r integration.
R E F E R E N C E S
1. A v i l a J O , R a d v a n y J, H u c k F R , C a m a r g o C H P , M a r i n o R Jr, R a g a z z o P C , R i v a D — A n t e r i o r c a l l o s o t o m y as a s u b s t i t u t e f o r h e m i s p h e r e c t o m y . A c t a N e u r o c h i r 30 ( S u p p l ) : 137, 1980.
2. C h a n g H T — C o r t i c a l r e s p o n s e t o a c t i v i t y o f c a l l o s a l n e u r o n s . J N e u r o p h y s i o l 16 : 117, 1953. 3. C h a n g H T — I n t e r a c t i o n o f e v o k e d c o r t i c a l p o t e n t i a l s . J N e u r o p h y s i o l 16 : 133, 1953. 4. C u k i e r t A , T i m o - I a r i a C — A n e v o k e d p o t e n t i a l m a p p i n g o f t r a n s c a l l o s a l p r o j e c t i o n s in
the c a t . A r q N e u r o - P s i q u i a t ( S ã o P a u l o ) 47 :1, 1989.
5. C u r t i s H J — I n t e r c o r t i c a l c o n n e c t i o n s o f c o r p u s c a l l o s u m as i n d i c a t e d b y e v o k e d p o t e n t i a l s . J N e u r o p h y s i o l 3 : 405, 1940.
6. C u r t i s H J — A n a n a l y s i s o f c o r t i c a l p o t e n t i a l s m e d i a t e d b y t h e c o r p u s c a l l o s u m . J N e u r o p h y s i o l 3 : 414, 1940.
7. E b n e r F F , M y e r s R W — D i s t r i b u t i o n o f c o r p u s c a l l o s u m a n d a n t e r i o r c o m m i s s u r e in c a t a n d r a c o o n . J C o m p N e u r o l 124 : 353, 1965.
8. H u b e l D H , W i e s e l T N — C o r t i c a l a n d c a l l o s a l c o n n e c t i o n s c o n c e r n e d w i t h t h e v e r t i c a l m e r i d i a n o f v i s u a l f i e l d s i n t h e c a t . J N e u r o p h y s i o l 30 : 1561, 1967.
9. L u e s s e n h o p A J — I n t e r h e m i s p h e r i c c o m m i s s u r o t o m y . A m S u r g 36 : 265, 1970.
10. M a r c u s E M , W a t s o n C W — B i l a t e r a l s y n c h r o n o u s s p i k e a n d w a v e e l e c t r o g r a p h i c p a t t e r n s in t h e c a t . A r c h N e u r o l 14 : 601, 1966.
11. P o l j a k S — A n e x p e r i m e n t a l s t u d y o f t h e a s s o c i a t i o n , c a l l o s a l a n d p r o j e c t i o n f i b e r s o f t h e c e r e b r a l c o r t e x o f t h e c a t . J C o m p N e u r o l 44 : 197, 1927.
12. P t i t o M , T a s s i n a r i G, A n t o n i n i A — E l e c t r o p h y s i o l o g i c a l e v i d e n c e f o r i n t e r h e m i s p h e r i c c o n n e c t i o n s in t h e a n t e r i o r e c t o s y l v i a n s u l c u s in t h e c a t . E x p B r a i n R e s 66 : 90, 1987. 13. T o m a s c h J — S i z e , d i s t r i b u t i o n a n d n u m b e r o f f i b e r s in t h e h u m a n c o r p u s c a l l o s u m .
