Fiziologicheskli Zhurnal SSSR irneni L M. Sechenova, vol, 53, no. I, pp. 82-90) 1967
PARTICIPATION OF FAST AND TONIC O C U L O M O T O R SYSTEMS IN STRETCH REFLEXES AND L A B Y R I N T H I N E REFLEXES OF E X T R A O C U L A R MUSCLES P. I. BAICHENKO, D. P. MATYUSHKIN AND V. V. SUVOROV D e p a r t m e n t of N o r m a l Physiology, P e d i a t r i c M e d i c a l Institute, L e n i n g r a d I n v e s t i g a t i o n s u s i n g v a r i o u s m e t h o d s have shown that two m o t o r s y s t e m s a r e p r e s e n t in the o c u l o m o t o r a p p a r a t u s of m a m m a l s (5-11): 1) a f a s t (phasic) s y s t e m r e p r e s e n t e d b y s t r o n g m u s c l e f i b e r s , conducting e x c i t a t i o n r a p i d l y and i n n e r v a t e d b y G - m o t o n e u r o n s and 2) a tonic s y s t e m , r e p r e s e n t e d b y slow and r e l a t i v e l y weak m u s c l e f i b e r s , m o s t l y not conducting e x c i t a t i o n , and i n n e r v a t e d p r i n c i p a l l y by 7 - m o t o n e u r o n s . In t h e i r p r o p e r t i e s t h e s e s y s t e m s r e s e m b l e the homologous s y s t e m s of the l o c o m o t o r a p p a r a t u s of a m p h i b i a n s (2). Two t y p e s of units have b e e n d i s t i n g u i s h e d in the tonic s y s t e m (9, 10),, one s l o w e r than the o t h e r , and it has been shown that s o m e of the tonic units a s s o c i a t e d with the s p i n d l e - s h a p e d p r o p r i o c e p t o r s of the o c u l a r m u s c l e s p e r f o r m the function of adjusting them (llL In connection with t h e s e findings the question a r o s e of the p a r t i c i p a t i o n of t h e s e m o t o r s y s t e m s in the v a r i o u s r e f l e x e s of the e x t r a o e u l a r m u s c l e s . P a r t i c i p a t i o n of t h e s e two o c u l o m o t o r s y s t e m s in s t r e t c h r e f l e x e s and c e r t a i n l a b y r i n t h i n e r e f l e x e s was thus examined. It will b e noted that w h e r e a s the l a b y r i n t h i n e r e f l e x e s of the o c u l a r m u s c l e s a r e g e n e r a l l y r e c o g n i z e d , the s t r e t c h r e f l e x e s of t h e s e m u s c l e s , d e s c r i b e d b y Kvasov et al. (3, 4) in the f o r m of potentiation of the e l e c t r o m y o g r a m (EMG), have hitherto b e e n d i s c l a i m e d by m o s t W e s t e r n p h y s i o l o g i s t s (12, 14). The r e a s o n h a s been that in i n v e s t i g a t i o n s of the b e h a v i o r of individual (fast) units during s t r e t c h i n g of the o c u l a r m u s c l e s , no s i g n s of a s t r e t c h r e f l e x have b e e n f o u n d (14). We have thus put f o r w a r d the h y p o t h e s i s t h a t the s t r e t c h r e f l e x i s effected b y the tonic s y s t e m . In the p r e s e n t i n v e s t i g a t i o n an a n a l y s i s was m a d e of the c o m b i n e d EMG of the o c u l a r m u s c l e s during s t r e t c h r e f l e x e s and l a b y r i n t h i n e r e f l e x e s ; the f a c t that the d e g r e e of e x c i t a t i o n of the f a s t and tonic s y s t e m s d i f f e r s was kept in mind. A s mentioned p r e v i o u s l y (5), the f a s t f i b e r s g e n e r a t e f a s t and u s u a l l y b i p h a s i c e l e c t r i c a l p o t e n t i a l s in the c o m b i n e d EMG [action p o t e n t i a l s (APs)], while the tonic f i b e r s g e n e r a t e r e l a t i v e l y slow and u s u a l l y m o n o p h a s i c p o t e n t i a l s [motor e n d - p l a t e p o t e n t i a l s (EPP)] v a r y i n g in d i r e c t i o n depending on the position of t h e i r s o u r c e s r e l a t i v e to the r e c o r d i n g e l e c t r o d e s . METHOD E x p e r i m e n t s w e r e c a r r i e d out on nine t h a l a m i c r a b b i t s and five r a b b i t s with an i n t a c t b r a i n , and ontwo intact c a t s . The head was r i g i d l y fixed to the e x p e r i m e n t a l f r a m e with the sinciput u p p e r m o s t . The o c u l a r m u s c l e s w e r e s e p a r a t e d f r o m the s u r r o u n d i n g t i s s u e s a f t e r r e m o v a l of the e y e b a l l and kept u n d e r a l a y e r of m i n e r a l o i l o r a m i x t u r e of m i n e r a l oil with p a r a f f i n at a t e m p e r a t u r e of 39 ~ The i n v e s t i g a t i o n s b e g a n 60-90 m i n a f t e r r e c o v e r y f r o m the e t h e r a n e s t h e s i a u s e d f o r the o p e r a t i o n . The s t r e t c h r e f l e x w a s studied on d i f f e r e n t m u s c l e s of the r a b b i t and cat, m o s t l y on the i n f e r i o r r e c t u s m u s c l e of the r a b b i t . The EMG was r e c o r d e d b y needle e l e c t r o d e s f r o m the b e l l y and tendon of the m u s c l e during s t r e t c h i n g b y d i f f e r e n t weights. The EMG was r e c o r d e d
350
PHASIC AND TONIC OCULOMOTOR SYSTEMS r e p e a t e d l y with single fast sweeps of the b e a m of the c a t h o d e - r a y oscilloscope. The r e c o r d s were made in the i n i t i a l position (with a load of 0.5 g) at the m o m e n t of pulling the m u s c l e by an additional load, and again 15, 30, and 45 see a f t e r the beginning of the i n c r e a s e d load (during the constant action of the load). R e c o r d i n g s were made at the s a m e time of the i n c r e a s e i n t h e lengthof the m u s c l e (by m e a n s of an optical myograph). In control e x p e r i m e n t s analogous r e c o r d i n g s were made f r o m denervated m u s c l e s (Fig. 1, I). The l a b y r i n t h i n e r e f l e x was i n v e s t i g a t e d in r a b b i t s on the left s u p e r i o r r e c t u s m u s c l e , working in i s o m e t r i c conditions. The reflex was e l i c i t e d by rotating the a n i m a l (fixed to a special o s c i l l a t i n g frame) around the long axis of the body f r o m l i~ %1 the position of sinciput u p p e r m o s t (0 ~ to the left to an angle of 85 ~ The EMG of the r e f l e x was studied d u r i n g r o t a tion of the a n i m a l (the single sweeps of the b e a m were a u t o m a t i c a l l y switched EMG on at angles of 5, 45 and 85 ~ and in the s t a t i o n a r y a n i m a l t u r n e d through angie s of 20, 40, 45, 60 and 80-85 ~ (Fig. 1, II). The EMG (on fluorographic film) was analyzed after c o n s i d e r a b l e e n II l a r g e m e n t . The shapes of the p o t e n t i a l s EMG were i n v e s t i g a t e d and t h e i r p e r i o d s , m a x i m a l amplitudes in each single p~ sweep, and o v e r a l l f r e q u e n c i e s were m e a s u r e d . The m e a n v a l u e s of the m e a s u r e m e n t were calculated, together with the i n d i c e s of a c c u r a c y of the m e a n s (mean e r r o r / - C n u m b e r of m e a surements). c
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Stretch reflex (12 experiments). In Fig. 1. D i a g r a m s of methods used in the i n vestigation. I - - Method of r e c o r d i n g EMG d u r i n g s t r e t c h i n g of o c u l a r m u s c l e . R e l e a s e of the weight (W) a u t o m a t i c a l l y switches on a single sweep of the b e a m of CRO r e c o r d i n g E MG. As the weight f a l l s , s t r e t c h i n g the m u s cle it t u r n s the pulley (P), and the axle (A) to which the m i r r o r (M) i s fixed i s i l l u m i n a t e d b y a b e a m of light. Movement of the reflected b e a m i s r e c o r d e d by a photokymograph on f i l m . Degree of s t r e t c h i n g is d e t e r m i n e d f r o m the scale (S). II - - Method of r e c o r d i n g EMG l a b y r i n t h i n e reflex. O s c i l l a t i n g f r a m e is t u r n e d by the fall of the weight (W'), t u r n i n g the pulley (P'). The size of the weight (W') d e t e r m i n e s speed of rotation. Counterpoise (C) b a l a n c e s the f r a m e withthe a n i m a l . During r o t a t i o n the single sweeps of the CRo r e c o r d i n g the EMG a r e switched on by a Contact m e c h a n i s m (CM).
u n a n e s t h e t i z e d a n i m a l s the e x t r a o c u l a r m u s c l e s , even without s t r e t c h i n g , show a s m a l l , constant e l e c t r i c a l activity, r e p o r t e d p r e v i o u s l y by Kvasov et al. (3, 4). With the high sweep s p e e d s u s e d in the p r e s e n t e x p e r i m e n t s this e l e c t r i cal activity took the f o r m of r e l a t i v e l y slow (with a period of about 10 msee) potentials with amplitudes between 40 and 300 ~ v (Fig. 2, I, II; Fig. 3, II), at 8 0 - 2 0 0 / s e e . The shape and duration of these waves c o r r e s p o n d e d approxim a t e l y to the E P P s of the tonic f i b e r s (9). Consequently, they were g e n e r a t e d by tonic units. Against the background of these slow waves, fast A P s of s m a l l amplitude were s o m e t i m e s o b s e r v e d , i.e., b u r s t s of activity of the f a s t u n i t s . J e r k i n g and constant s t r e t c h i n g of the m u s c l e s with loads of 0.5--1.0 g as a rule did not affect its e l e c t r i c a l activity. Denervafion of the m u s c l e abolished its i n i t i a l e l e c t r i c a l activity and led to a slight i n c r e a s e in length (when loaded with 0.5-1.0 g), and this lengthening was g r e a t e r
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F i g . 2. S t r e t c h r e f l e x e s of e x t r a o c u l a r m u s c l e s . I - F r o m top to bottom: EMG of i n f e r i o r r e c t u s m u s c l e of a r a b b i t with s t a t i o n a r y l o a d s o f 0 . 5 , 5.7, 10.5, and 20.5 g (the a m p l i t u d e of the slow waves i n c r e a s e s ) . I I - f r o m top to bottom: EMG of r a b b i t i n f e r i o r r e c t u s m u s c l e with s t a t i o n a r y l o a d s of 0.5, 5.7, 10.5, and 20.5 g. Beneath t i m e m a r k e r b u r s t s of f a s t a c t i v i t y of m u s c l e (for c o m p a r i n g s h a p e s of A P s ) . I I I - - g r a p h s showing r e l a t i o n s h i p between the load (P) and the length of the m u s c l e (L) in t h e s e e x p e r i m e n t s . L a r g e c i r c l e s r e p r e s e n t v a l u e s in p r e s e n c e of a s t r e t c h r e f l e x ; b l a c k dots, a f t e r d e n e r v a t i o n of the m u s c l e s (explanation in text). the m o r e m a r k e d the p r e c e d i n g e l e c t r i c a l a c t i v i t y (Fig. 4B). Consequently, the e l e c t r i c a l a c t i v i t y of the u n s t r e t c h e d o r v e r y s l i g h t l y s t r e t c h e d m u s c l e was a s s o c i a t e d with i t s slight tonic c o n t r a c t i o n . T h i s i s the s o - c a l l e d " c e n t r a l t o n u s " of the o c u l a r m u s c l e s (3), c a u s a l l y u n r e l a t e d to p r o p r i o c e p t i o n (11). Stretching of the m u s c l e s with weights of 2 and 5 g o r m o r e c a u s e d i n t e n s i f i c a t i o n of t h e i r e l e c t r i c a l activity, an index of the s t r e t e h r e f l e x ( r e c o r d e d in a l l the e x p e r i m e n t s ) . Upon Jerking the m u s c l e even with a heavy (10-20 g) weight the EMG was u s u a l l y unchanged, i . e . , u s u a l l y no f a s t s t r e t c h r e f l e x was found, but in one e x p e r i m e n t in these conditions a s h o r t b u r s t of low, f a s t A P s was o b s e r v e d (Fig. 4), and t h i s m a y be r e g a r d e d a s a weak, f a s t r e f l e x to the Jerk. Soon a f t e r the Jerk of the m u s c l e b y the load, the
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Fig. 3. C h a r a c t e r i s t i c s of s t r e t c h r e f l e x o f e x t r a o c u l a r m u s c l e s . I - - Relationship between m e a n amplitude of EMG (A) and f r e q u e n c y of potentials (n) of EMG of r a b b i t i n f e r i o r r e c t u s m u s c l e and the load applied (P). V e r t i c a l b a r s show probable e r r o r of the m e a n s . II - EMG of l a t e r a l r e c t u s m u s c l e of a cat (cerveau isol~) with a load of 2 (toptrace) and22 g (bottom t r a c e ) ; b e neath EMG, graph of s t r e n g t h of s t r e t c h reflex of the i n f e r i o r r e c t u s m u s c l e s of r a b b i t v e r s u s amplitude of EMG. H I - - A m p l i t u d e of the EMG (A) v e r s u s s t r e n g t h (F) of s t r e t c h reflex of i n t e r i o r r e c t u s m u s c l e s of r a b b i t s to the load applied, P (mean of three e x p e r i m e n t s ) ; c u r v e s A for s e p a r a t e e x p e r i m e n t s a r e indicated by thin lines. I V - - The same r e l a t i o n s h i p with P plotted on a l o g a r i t h m i c scale. In all graphs v a l u e s of A given in percentage of control values (without load). slow-wave a c t i v i t y b e g a n to i n c r e a s e . The l a t e n c y of this r e a c t i o n could not be d e t e r m i n e d a c c u r a t e l y , but it was c e r t a i n l y longer than 30 m s e c . With subsequent s t a t i o n a r y loading by the weights mentioned above the r e f l e x took the f o r m of a steadily i n c r e a s e d amplitude of the slow waves (Fig. 2 and 3), s o m e t i m e s r e a c h i n g 125% of t h e i r i n i t i a l amplitude. The frequency of the waves in the EMG was i n c r e a s e d by not m o r e than 30% (Fig. 2 and 3; Table 1). This is the tonic s t r e t c h reflex, effected by a m a s s of tonic u n i t s , and evidently o c c u r r i n g with p a r t i a l s y n c h r o n i z a t i o n of t h e i r activity. The i n c r e a s e in the amplitude of the EMG was p r o p o r t i o n a l to the load (Fig. 2 and 3). Removing the load f r o m the m u s c l e abolished this reflex.
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F i g . 4. " C e n t r a l t o n u s " and s t r e t c h r e f l e x e s in the e x t r a o e u l a r m u s c l e s. A - - EMG of u n s t r e t c h e d m e d i a l r e c t u s m u s c l e of a cat. B - - R e l a t i o n s h i p between s h o r t e n i n g of i n f e r i o r r e c t u s m u s c l e of r a b b i t (load 0.5 g) and amplitude of i t s E M G . C - - Development of s t r e t c h r e f l e x of i n f e r i o r r e c t u s m u s c l e of a r a b b i t during loading with 20.5 g (1 - - at m o m e n t of falling of the weight; 2 - - 15 s e c , and 3 - - 30 s e c a f t e r loading). D - - Case of i n t e n s i f i e d a c t i v i t y of f a s t s y s t e m of i n f e r i o r r e c t u s m u s c l e of a r a b b i t in s t r e t c h r e f l e x d u r i n g loading with 10 g (4 - - b a c k ground; 5 - s t r e t c h r e f l e x ) .
I n d i r e c t i n f o r m a t i o n m a y be obtained about the m e c h a n i c a l s t r e n g t h of t h i s r e f l e x b y c o n s i d e r i n g the length (L) of a p a r t i c u l a r m u s c l e d u r i n g the action of a s e r i e s of s t a n d a r d l o a d s b e f o r e and a f t e r i t s denervation. Since in s t a t i o n a r y conditions the t e n s i o n of the m u s c l e (F) i s equal to the weight of the load (P), the r e l a t i o n s h i p between L and P m a y be t r a n s f o r m e d into a r e l a t i o n s h i p between F and L (Fig. 2). If the o r d i n a t e s of t h i s c u r v e f o r the d e n e r v a t e d m u s c l e (the i n d i c e s of p a s s i v e tension of an e x t e n s i b l e s t r u c t u r e ) a r e s u b t r a c t e d f r o m the o r d i n a t e s of the analogous c u r v e of the i n n e r v a t e d m u s c l e (giving a s t r e t c h r e f l e x ) , the a p p r o x i m a t e v a l u e s of the a c t i v e t e n s i o n of the m u s c l e in the tonic r e f l e x e s to the c o r r e s p o n d i n g l o a d s m a y be obtained (Fig. 2). By p e r f o r m i n g t h i s i n v e s t i g a t i o n p a r a l l e l with r e c o r d i n g the EMG, a c o r r e l a t i o n w a s found b e t w e e n the amplitude of the slow w a v e s of the EMG and the magnitude of the active t e n s i o n of the m u s c l e (Fig. 3). In the i n f e r i o r r e c t u s m u s c l e of the r a b b i t t h i s t e n s i o n m a y r e a c h 8 g, a value e v i d e n t l y c l o s e to the m a x i m u m s t r e n g t h of the tonic s y s t e m f o r this p a r t i c u l a r m u s c l e . In the oblique m u s c l e s t h i s value was much s m a l l e r (up to 2 g).
354
PHASIC AND TONIC OCULOMOTOR SYSTEMS Table 1. E x a m p l e s of c h a r a c t e r i s t i c s of the EMGfor s t r e t c h r e f l e x e s of the i n f e r i o r r e c t u s m u s c l e of the rabbit
Object
Load on muscle (in g)
2 R a b b i t with intact brain t
T h a l a m i c rabbit
Parameters of slow.wave a c t i v i t y Mean amplitude (in }1v)
Mean frequency (per sec)
58i2 6 5 ~ 1 ~.
140i 5 153~ 9 147~ 9
05 I0
66:~3 941 2
20
123:~ 3
153~ 15
180~: 4
160~ 6 168~I0
190~ 4 200•
10.5
193~ 8 267f27
20.5
290~ 20
0.5 2.7 5.7
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9
201~ 5 190~ 3
The r e c t i l i n e a r r e l a t i o n s h i p between the magnitude of the tonic s t r e t c h r e f l e x and the load s o m e t i m e s p e r s i s t e d throughout the range used (0-20 g), but m o r e often it was d i s t u r b e d in the r e g i o n of the higher loads. With a load of 20.5 g the reflex was s o m e what s m a l l e r than with a load of 10.5 g (Fig. 3), probably b e c a u s e of inhibition (4). During the development of the tonic s t r e t c h r e f l e x fast A P s u s u a l l y disappeared f r o m the EMG. This effect was described by Whitteridge (14), who made o b s e r v a t i o n s on the behavior of the fast units of the extraocular m u s c l e s of goats. However, f r o m t i m e to t i m e , in the p r e s e n c e of considerable activity of the fast units in the background, i n v o l v e m e n t of the fast s y s t e m in the tonic s t r e t c h r e f l e x was o b s e r v e d (Fig. 4). The labyrinthine reflex (4 experiments). In this s e r i e s of e x p e r i m e n t s the s u p e r i o r r e c t u s m u s c l e was investigated and showed r e l a t i v e l y low e l e c t r i c a l activity when the a n i m a l ' s head was fixed with the sinciput u p p e r m o s t (Fig. 5). When the a n i m a l was t u r n e d to the side of the r e c o r d e d m u s c l e , the e l e c t r i c a l activity of the m u s c l e was i n c r e a s e d . At the m o m e n t of t u r n i n g , ff done r a p i d l y (at the rate of 80-90 d e g / s e c ) , the r e f l e x (statokinetic) r e a c t i o n took the f o r m of a m a r k e d i n c r e a s e in slow-wave activity with the appearance of fast A P s (Fig. 5), i.e., it was effected by both tonic and fast u n i t s . During rotation at slow speeds (3-25 deg/sec) and after rotation into a fixed p o s i tion, the r e a c t i o n at each angle took the f o r m of an i n t e n s i f i e d slow-wave activity, i n c r e a s e d both i n amplitude and f r e q u e n c y , i.e., it was effected by the tonic s y s t e m only (Table 2). The s t r e n g t h of the r e a c t i o n s d e s c r i b e d , indicated by the i n c r e a s e in amplitude of the EMG, b o r e a d i r e c t r e l a t i o n s h i p to the angle of r o t a t i o n (Fig. 5), and within the r a n g e investigated this r e l a t i o n s h i p was a l m o s t l i n e a r . Table 2. E x a m p l e s of c h a r a c t e r i s t i c s of the EMG for labyrinthine r e f l e x e s of the superior r e c t u s m u s c l e of rabbits rotated into a fixed position
Object
Angle of rotation (in degrees)
Parameters of slow-wave a c t i v i t y Mean amplitude (in p v)
frequency
Mean (per sec)
R a b b i t No, 1 with intact brain
0 20 60
91~ 9 135~11 192~21
126 i 18 180~ 8 1 9 4 i 18
Rabbit No. 2 with i n t a c t brain
0 45 85
50~ 3 187~ 8 248 i 10
174i 8 246,11 2 8 0 i 13
355
PHASIC AND TONIC OCULOMOTOR SYSTEMS
-1
I 300 -A
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o
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7 tOOo
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n
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iO00
/
o
k
0o05 6o
85"
F i g . 5. V e s t i b u l a r r e f l e x e s in s u p e r i o r r e c t u s m u s c l e in r a b b i t s . I Top to bottom: EMG of left m u s cle at different a n g l e s of r o t a t i o n of the body to a fixed p o s i t i o n around the long axis to the left [1 - - at an angle of 0 ~ (sinciput u p p e r m o s t ) ; 2 - - at 45 ~ , 3 - at 85 ~ , 4, 5 - - at 0~ 6, 7 - - at 45~ 8, 9 - - at 85~ II - - R e a c t i o n s of the s a m e m u s c l e i n t h e c o u r s e of f a s t r o t a t i o n to the left (V= 8 0 d e g / s e c ) at a n g l e s of 5, 45, and 85 ~ (from top to bottom). The tonic a c t i v i t y i s s u p p l e m e n t e d by f a s t activity. I I I - - R e l a t i o n s h i p of m e a n a m p l i t u d e of EMG (A) and m e a n f r e q u e n c y (n) to the angle of r o t a t i o n to a f i x e d p o s i tion. - -
Turning the a n i m a l to the side opposite the t e s t m u s c l e d e p r e s s e d the i n i t i a l tonus of this m u s c l e ( s o m e t i m e s to z e r o ) . This d e m o n s t r a t e s the r e c i p r o c a l i n h i b i tion of the c e n t e r s of i n n e r v a t i o n of t h i s m u s c l e during activation of i t s antagonist. DISCUSSION The r e s u l t s obtained show, f i r s t that the phasic (fast) and tonic (slow) s y s t e m s of the o c u l o m o t o r a p p a r a t u s p l a y d i f f e r e n t r o l e s . As a r u l e the f a s t s y s t e m was involved only in r e s p o n s e to s t r o n g and a b r u p t s t i m u l a t i o n of the l a b y r i n t h i n e r e c e p t o r s (maculae, a m p u l l a e , s e m i c i r c u l a r canals). Only in the p r e s e n c e of a c c e s s o r y f a c i l i t a t i n g influences did the f a s t s y s t e m b e c o m e r e s p o n s i v e to p r o p r i o c e p t i v e i m p u l s e s .
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PHASIC AND TONIC OCULOMOTOR SYSTEMS The s t a t i c s t r e t c h reflex and the static l a b y r i n t h i n e reflex were m a i n l y effected by the tonic (slow) m o t o r s y s t e m . The p r o p r i o c e p t o r s of the e x t r a o c u l a r m u s c l e s and the p o s t u r a l r e c e p t o r s of the l a b y r i n t h p o s s e s s c l o s e r c e n t r a l connections with t h e T - m o t o n e u r o n s of the tonic s y s t e m than with the a - m o t o n e u r o n s of the fast s y s t e m . Both the tonic r e f l e x e s examined a r e evidently polysynaptic. This a s s u m p t i o n is b a s e d on m a n y d e s c r i p t i o n s of the l a b y r i n t h i n e reflex (12), and evidence of this r e l a t i v e to the s t r e t c h reflex i s given by its long latent period. Both r e f l e x e s have t h e i r c e n t e r in the b r a i n s t e m and t h e i r c o u r s e is p r a c t i c a l l y identical in a n i m a l s with an intact b r a i n and in t h a l a m i c a n i m a l s . The r e s u l t s d e m o n s t r a t e the p r e s e n c e of a m a i n l y d i r e c t , and a l m o s t r e c t i l i n e a r r e l a t i o n s h i p between the s t r e n g t h of these r e f l e x e s and the s t r e n g t h of the n a t u r a l s t i m ulation. This i s biologically advantageous b e c a u s e each of the investigated r e f l e x e s c o m p e n s a t e s for a d i s t u r b a n c e in the position of the eye caused by e x t e r n a l action (the tonic s t r e t c h reflex c o m p e n s a t e s for d i s p l a c e m e n t of the eye r e l a t i v e to the axis of the o r b i t ; the l a b y r i n t h i n e reflex for d i s p l a c e m e n t of the eye r e l a t i v e to the g r a v i t a t i o n a l field). The r e c t i l i n e a r r e l a t i o n s h i p between the s t r e n g t h of the r e f l e x e s and the s t r e n g t h of the s t i m u l u s , combined with the l o g a r i t h m i c r e l a t i o n s h i p between the s t r e n g t h of the s t i m u l u s and the r e a c t i o n of the individual r e c e p t o r s , suggests the p r e s e n c e of " p o tentiating f a c t o r s . " One such f a c t o r could be the d i s t r i b u t i o n of the t h r e s h o l d s of the c o r r e s p o n d i n g r e c e p t o r s (11) and the c e n t r a l n e u r o n s . Both r e f l e x e s are effected m a i n l y in r e c r u i t m e n t of the s u b l i m i n a l f r i n g e of (inactive) tonic u n i t s , and this is r e f l e c t e d by the i n c r e a s e m a i n l y in the amplitude of the EMG, while its f r e q u e n c y shows only a slight change. The d i s t o r t i o n of the r e l a t i o n s h i p between the s t r e n g t h of the s t r e t c h reflex and l a r g e loads m a y be i n t e r p r e t e d as a sign of '~autogenous inhibition.' ' In connection with e a r l i e r data on the a s s o c i a t i o n between the p r o p r i o c e p t o r s of the o c u l a r m u s c l e s and p a r t of t h e i r tonic f i b e r s (11), it m a y be asked whether this " s p i n d l e " p a r t of the total m a s s of the tonic f i b e r s p a r t i c i p a t e s in the r e f l e x e s investigated. On the question of the p a r t i c i p a t i o n of the i n t r a f u s a l tonic u n i t s in the s t r e t c h r e f l e x it should be noted t h a t if this i n fact takes place, b e s i d e s the obvious negative feedback (removal of the load f r o m the r e c e p t o r s by c o n t r a c t i o n of the e x t r a f u s a l f i b e r s ) , a positive feedback (excitation of the r e c e p t o r s by fusal f i b e r s ) m u s t also act in this s t r e t c h reflex of the o c u l a r m u s c l e s . Since a d i r e c t l i n e a r r e l a t i o n s h i p was found b e t w e e n the static s t r e t c h reflex and the load, it m u s t be concluded that this positive feedback, ff it e x i s t s , cannot be p r e d o m i n a n t in this p a r t i c u l a r s y s t e m . Other v a r i a n t s a r e t h e o r e t i c a l l y a d m i s s i b l e : the "absence of any influence of proprioceptive i m p u l s e s on f u s i m o t o n e u r o n s o r the i n h i b i t o r y c h a r a c t e r of such i n f l u e n c e s , b e c a u s e the f u s a l tonic u n i t s evidently p o s s e s s ~ ' c e n t r a l " (~'nonproprioceprive") tonus (1, 13). As f a r as the i n v o l v e m e n t of the f u s a l tonic u n i t s i n the l a b y r i n t h i n e r e f l e x e s i s c o n c e r n e d , this s e e m s possible although doubts have b e e n e x p r e s s e d about it in the l i t e r a t u r e (14). CONCLUSIONS 1. The e x t r a o c u l a r m u s c l e s of m a m m a l s in m o s t c a s e s do not give a ' f f a s t " r e f l e x to s t r e t c h i n g with a Jerk. During s t a t i o n a r y s t r e t c h i n g by loads exceeding 2 g, a tonic s t r e t c h reflex develops as a rule and i s effected by a m a s s of tonic u n i t s , m a i n l y by the b r i n g i n g into play of r e s e r v e units. 2. The s t r e n g t h of the s t r e t c h r e f l e x of the o c u l a r m u s c l e s is p r o p o r t i o n a l to the load within the range of m o d e r a t e loads; with overloading the r e f l e x i s d e p r e s s e d . 3. The o c u l a r m u s c l e s p o s s e s s weak tonus even without stretching. I n these c o n ditions the activity of the group of tonic u n i t s i s f r e q u e n t l y combined with the r a n d o m activity of some of the fast units. During the development of the tonic s t r e t c h r e f l e x the activity of the fast u n i t s i s m o s t c o m m o n l y d e p r e s s e d , but o c c a s s i o n a l l y it i s intensified.
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PHASIC AND TONIC OCULOMOTOR SYSTEMS 4. The statokinetic labyrinthine reflex of the superior rectus muscle to rapid rotation of the rabbit's body around the long axis is effected by fast and tonic systems working together. 5. The labyrinthine reflex to rotation to a fixed position is effected by the tonic system. The strength of this reflex (within the range 0-85 ~) is proportional to the angle of rotation. REFERENCES
1. GRANIT, R. Electrophysiological Investigation of Reception. Foreign Literature Press, Moscow, 1957. 2. ZHUKOV, E. K. Investigations of the Tonus of Skeletal Muscles. Medgtz, 1956. 3. KVASOV, D. G., G. I. BULYGINSKII and I. G. ANTONOVA. Byull. Eksp. Biol. Med. 32(7):16, 1951. 4. KOROVINA, M. V. Data on the Physiology of the Extrinsic Ocular Muscles and Their Central Nervous Regulation. Dissertation, Leningrad, 1956. 5. MATYUSHKIN, D. P. Fiziol. Zh. SSSR. 47(7):878, 1961. 6. MATYUSHKIN, D. P. Fiziol. Zh. SSSR. 48(2):188, 1962. 7. MATYUSHKIN, D. P. Fiziol. Zh. SSSR. 48(5):534, 1962. 8. MATYUSI-IKIN, D. P. Byull. Eksp. Biol. Med. 53(4):121, 1962. 9. MATYUSHKIN, D. P. Fiziol. Zh. SSSR. 49(5):603, 1963. Translation published in Federation Proceedings, Part II, Translation Supplement. 23(5):T1103-T1106, 1964. 10. MATYUSHKIN, D. P. Byull. Eksp. Biol. Med. 55(3):3, 1963. 11. MATYUSHKIN, D. P. The Fast (Phasic) and Slow (Tonic) Systems of the Oculomotor Apparatus. Dissertation, Leningrad, 1964. 12. DAVSON, H. (Editor) The Eye, 3. Muscular Mechanisms. New York-London, 1962. 13. MATTHEWS, P. B. C. Physiol. Rev. 44(2):219, 1964. 14. WHITTERIDGE, D. Handbook o f Physiology, Sect. 1. Neurophysiol. 2:1089, 1959.
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