F o r this r e a s o n , in spite of the fact that f r o g s ' reactions to visual stimuli n o r m a l l y a r e d e t e r m i n e d not only by the a n g u l a r d i m e n s i o n s of the objects viewed but a r e c a r r i e d out with due r e g a r d for the distance to them [9], s p e c i a l i z e d "channelling" of the visual information entering the f r o g ' s brain f r o m RGC of p a r t i c u l a r c l a s s e s is n e c e s s a r y f o r organizing c e r t a i n biologically d i v e r s e f o r m s of behavior. F r o m this point of view, one could s p e a k of not one -- o r even two [10] -- visual s y s t e m s , evidently, but of s e v e r a l visual s y s t e m s in anuran amphibians and, p r o b a b l y , in o t h e r l o w e r v e r t e b r a t e s . In the r e t i n o - t e c t a l division, one m a y suppose that there is special significance in the level of distribution of the synaptic contacts f o r m e d by the axons of RGC of a p a r t i c u l a r c l a s s . The s t r a t i f i e d distribution of the t e c t a l t e r m i n a l s of RGC of different c l a s s e s o c c u r s not only in the n o r m a l animal [1,3], but gradually is r e s t o r e d also a f t e r the r e g e n e r a t i o n of retinot e c t a l f i b e r s (according to [11], as well as o u r own observations}. LITERATURE 1. 2, 3.
4. 5. 6. 7. 8. 9. !0. 11.
CITED
H . R . Maturana, J . Y. Lettvin, W. S. MacCulloch, and W. H. P i t t s , J. Gen. P h y s i o l . , 4__33,N o . 6 , P a r t 2, 129 (1960). W.R.A. Muntz, J . N e u r o p h y s i o l . , 2__55, 712 (1962). O . J . G r f / s s e r and U. G r f / s s e r - C o r n e h l s , in: H. Autrum et a l . , Handbook of Sensory Physiology, Vol. VH/3a, Central P r o c e s s i n g of Visual Information, P a r t A. (R. J u n g , e d . ) , S p r i n g e r - - V e r l a g , Berlin (1973), p. 333. D. Schneider, Biol. Z b l . , 7_33, 225 (1954). I . N . P i g a r e v and G. M. Zenkin, Zh. Vyssh. Nervn. D e y a t . , 2_.0.0, 170 (1970). R . W . S p e r r y , J . N e u r o p h y s i o l . , 7 , 57 (1944). R . M . G a z e , The F o r m a t i o n of N e r v e Connections, Acad. P r e s s , New Y o r k (1970). V . M . Vinogradova, V. A. Bastakov, L. N. D ' y a c h k o v a , and Yu. B. Mantefel', Neirofiziologiya, 5, 611 (1973). E . I . Kiseleva and Yu. B. Manteifel'., Zool. Z h . , 5__33,1817 (1974). D. Ingle, Science, !81, 1053 (1973). M . J . Keating and R. M. G a z e , Brain R e s . , 2_~1, 197 (1970).
SOMATOSENSORY L.
S. A l e e v
EVOKED and
Yu.
POTENTIALS P.
IN HEALTHY
PEOPLE UDC 612.825
Varezhkin
The: r e s u l t s of a study of s o m a t o s e n s o r y evoked potentials r e c o r d e d in 37 healthy stlbjects of both s e x e s a r e d e s c r i b e d . C o m p a r i s o n of the r e s u l t s of t e s t s on t h r e e age subgroups showed selectivity in the change in l a t e n e i e s and a m p l i t u d e s of w a v e s of the s o m a t o s e n s o r y r e s p o n s e s depending on the s u b j e c t ' s age. I p s i l a t e r a l r e s p o n s e s show g r e a t e r v a r i a b i l i t y but a l o w e r amplitude and frequency of a p p e a r a n c e of the individual components than c o n t r a l a t e r a l r e s p o n s e s . T h e i r latent p e r i o d s a l s o w e r e longer than those of the c o n t r a l a t e r a l r e s p o n s e s . INTRODUCTION N u m e r o u s investigations of cortical evoked potentials (EPs) in a n i m a l s have shown that the EP method is highly effective as a m e a n s of studying the conducting pathways and connections in the CNS. F o r v a r i o u s r e a s o n s of a technical nature human E P s have r e c e i v e d f a r l e s s study. When deciding to investigate s o m a t o s e n s o r y E P s of the human b r a i n it was r e a l i z e d that information on the c h a r a c t e r and p r o p e r t i e s of t h e s e r e s p o n s e s is scanty and s o m e t i m e s c o n t r a d i c t o r y . T h i s is the c a s e , for e x a m p l e , with the concept of " n o r m a l " as applied to c o n t r a l a t e r a l r e s p o n s e s and the g e n e s i s of i p s i l a t e r a l r e s p o n s e s . Another i n t e r e s t i n g p r o b l e m for study was the possibility of using data on E Ps in clinical neurology f o r diagnostic p u r p o s e s and also for investigating cortical c o m p e n s a t o r y m e c h a n i s m s in the c o u r s e of r e c o v e r y
Institute of C y b e r n e t i c s , A c a d e m y of Sciences of the Ukrainian SSR, Kiev. T r a n s l a t e d f r o m N e i r o f i z i o logiya, Vol. 8, No. 5, pp. 447-454, S e p t e m b e r - O c t o b e r , 1976. Original a r t i c l e submitted N o v e m b e r 6, 1975.
198
0097-0549/78/0902-0198507.50
9 1979 Plenum Publishing Corporation
of lost m o t o r and s e n s o r y functions. F o r this purpose it was decided to study certain p r o p e r t i e s of s o m a t o s e n s o r y EPs of healthy subjects, namely the effect of the method of r e c o r d i n g and of the subject's age on the c h a r a c t e r of the r e s p o n s e , and the p a r a m e t e r s of c o n t r a l a t e r a l and ipsilateral r e s p o n s e s were compared. EXPERIMENTAL
METHOD
To obtain s o m a t o s e n s o r y EPs the m e d i a n n e r v e was stimulated in the distal part of the f o r e a r m by single square pulses 0.5 m s e c in duration and separated by intervals of 2 sec. Electrical stimulation was applied f r o m a standard g e n e r a t o r with radiofrequency attachment. The level of stimulation evoking slight twitching of the thumb of the stimulated hand was taken as the m o t o r threshold and used throughout the investigation. The location of the r e c o r d i n g e l e c t r o d e s , approximating to the cortical projection a r e a s of both hands, was d e t e r m i n e d by K o r n i n g ' s method [6]. Another pair of e l e c t r o d e s used as "indifferent" for biopolar r e cording was placed 5 cm a n t e r i o r l y to the f i r s t e l e c t r o d e s along the parasagittal line. The indifferent electrode for monopolar r e c o r d i n g was fixed t o the bridge of the nose. The i n t e r e l e c t r o d e r e s i s t a n c e did not exceed 3-4 k~2. The technique of r e c o r d i n g and analysis of the s o m a t o s e n s o r y E P s was described m o r e fully previously [3]. Only a v e r a g e d (on the b a s i s of summation and averaging of 35 single EPs) r e s p o n s e s were analyzed. F r o m each subject four such a v e r a g e d r e s p o n s e s were obtained. Statistical analysis of the r e s u l t s was c a r r i e d out with the aid of S t r e l k o v ' s tables [8]. EXPERIMENTAL
RESULTS
Despite definite variability between individuals the a v e r a g e EP of all healthy subjects tested (by the m o n o p o l a r r e c o r d i n g method) p o s s e s s e d s i m i l a r features (Fig. lb). According to the r e s u l t s of these investigations the e o n t r a l a t e r a l s o m a t o s e n s o r y E P consisted of 7-9 s u c c e s s i v e waves of different p o l a r i t i e s extending over a period of 200 m s e c a f t e r stimulation. The latent period (LP) and amplitude of the r e s p o n s e s a r e given in Table 1. Since there is no single classification of the components of EP in the l i t e r a t u r e it was decided to use a n o m e n c l a t u r e illustrated in Fig. l a (P, N - polarity; a - i - s u c c e s s i v e EP components r e c o r d e d ; A, B, C . . . . . I - amplitudes of s u c c e s s i v e waves Pa, Nb, Pc . . . . . P i ' respectively).
a
b
A j-~ C -~] I !
,~ . . . . -i l i
#v
/ %
28
I
iI
I
I 16
.!
/sH .
,,
/
,,
M~A" ,eAr
",
91- ,
o
',
\
,
,,, \'
,
T . ~ i.~. . .~.
I
I
I
Ioo
200 m s e c 0
Fig. 1
I
,
e,;
F
,.", ,'.iN
v l
,'oo
I
200 r n s e c
Fig. 2
Fig. i. Explanatory scheme of waves ofaveraged evolved potential (EP) of somatosensory cortex (a) and individual differences in averaged EP of three healthy subjects (1-3) (b). P. N) polarity; a, b, c ..... J) successive components of EP recorded; A, B, C, .... I) amplitudes of successive waves Pa, Nb, Pe .... Pi respectively. Inall eases left median nerve was stimulated. Each response averaged on the basis of 35 single EP. Fig. 2. Changes in amplitudes of waves of contralateral somatosensory EP with age. I, If, Ill) Age subgroups: 18-30, 31-40, and 41-53 years respectively. Remainder of legend as in Fig. i.
199
In m o s t c a s e s the averagd response began with a negative deflection Nb. L P of this wave (P=0.01) had confidendce limits of 20.58 9 0.52 m s e c . In r a r e c a s e s it was preceded by a small positive deflection Pa with L P 15.67=~ 0.73 m s e c (P=0.01). As a rule the Nb wave was followed immediately by a p o s i t i v e - n e g a t i v e positive complex of waves Pc, Nd, Pe, with LP limits of 2.5.55~ 0.68, 34.25~= 1.39, and 48.47=~ 1.87 m s e c r e s p e c t i v e l y (P=0.01). The confidence limits of L P s of the l a t e r waves (P=0.01) were r e s p e c t i v e l y : Nf 66.63• 2.33, Pg 96.11e 2.36, Nh 127.19~= 2.86, and Pi 178.37~ 3.72 m s e c . The amplitude of the r e c o r d e d waves of s o m a t o s e n s o r y E P s varied. The waves Pa, Nb, and Nd had the lowest amplitudes, 2.34~: 0.52, 3.97~= 0.41, and 4.54~ 0.68 pV, r e s p e c t i v e l y (P=0.01). Waves in the late part of the r e s p o n s e had the highest amplitude. 17or instance, the amplitude of wave Nh (H) was 10.77 9 1.01, and that of wave Pi (I) was 15.25~: 1.16/iV (P=0.01). T h e duration of the investigation did not significantly affect the c h a r a c t e r of the EPs if the subject r e m a i n e d in a state of relaxed wakefulness all the time. R e c o r d s obtained after longer time intervals (6-12 months) showed a s i m i l a r i t y in the c h a r a c t e r of E P s r e c o r d e d in the same subject ( P = 0.05). To c o m p a r e r e s p o n s e s obtained the same age subgroup (18-30 y e a r s ) . the waves appeared less frequently in f e r e n c e s in the r e c o r d e d values of L P
by monopolar and bipolar recording, averaged EPs were chosen f r o m Bipolar r e s p o n s e s were s i m i l a r with monopolar, but in some cases the e a r l y part of EP (0-60 msec) and were l e s s well e x p r e s s e d . Difwere not statistically significant (P=0.05) and in p r a c t i c e could t h e r e -
T A B L E 1. Mean Values of L P and Amplitudes of S o m a t o s e n s o r y E P s of Control Group of (37) Subjects with Monopolar Recording Expressiveness of comp0nent,
Components l LP. msec of EPs Mi m
Pa Pc Nd
15,67_+ 0,28 20,58• 25,55 _+0,26 34,25-4-0,54
Pe
48,47+--0,72
Nf Pz Nh Pl
66,63___0,90 96,11 -+0,91 127,19~-_, 1,I1 178,37• 1,44
Nb
39,3 " 85,7 85,7 78 6 97,6 89,3 85,7 88, I 90,5
Range, msec 13 18 19--23 24 - 28 2"}- 38 40 --57 58--81 82 103 107--140 165--204
Amplitude.
P=0.01 m~ec M ~ m
0,7.3 0,52
0,68 1,39 1,87
2,33 2,36 2,86 3.72
2,34~0,12 3,97_+0,16 7,44• 4,54_+0,26 6,71~0.26 9,95:~_ 0,33 9,19• 10,77_+0,39 15,24:t:0,45
P = 0.01
0,52 0,41 0,64 0,68 0.67 0.85 0,90 1,01 1,16
T A B L E 2. Changes in S o m a t o s e n s o r y E P with Age in Healthy Subjects (P = 0.01} Waves
of EP
I= II= III ~-
Pa Nb
Pr Na Pe /dr
+ + + +
Pl
Tamp~'=" i tuae LP
I compared with II
I compared with II
amvlitud~
+
t t
Pg Nr
withI comparediI
t t t t t
+
Legend: c r o s s e s denote no change in p a r a m e t e r s in all subgroups; a r r o w s pointing downward show d e c r e a s e in numerical value of these p a r a m e t e r s (msec, pV) compared with older of subgroups compared; a r r o w s pointing upward indicate i n c r e a s e in n u m e r i c a l value of these p a r a m e t e r s (msec, #V) c o m p a r e d with older of subgroups compared. I, II, III) Age subgroups: 18-30, 31-40, and 41-53 y e a r s , respectively.
200
fore be d i s r e g a r d e d . The amplitude of the P a - Pe complex of waves on bipolar r e c o r d i n g w e r e s m a l l e r than those of the analogous" E P waves on m o n o p o l a r r e c o r d i n g , w h e r e a s the amplitudes of the l a t e r waves ( N f - Pi) w e r e s i m i l a r to those r e c o r d e d by the m onopolar method (P = 0.05). Changes in S o m a t o s e n s o r y C o r t i c a l E P s with Age. To determine the variability of EPs with age the subjects w e r e divided into t h r e e subgroups. The f i r s t subgroup consisted of 14 p e r s o n s aged from 18 to 30 y e a r s (mean age 24.3 y e a r s ) ; the second of 15 subjects aged from 31 to 40 y e a r s (mean age 35.5 y e a r s ) , and the third of eight subjects aged f r o m 41 to 53 y e a r s (mean age 48.7 y e a r s ) . Average r e s p o n s e s obtained b y the m o n o p o l a r method w e r e compared. Changes detected in the r e s p o n s e s of subjects of different ages a r e shown in Table 2. F o r instance L P s of waves Pa, Nb, Pc, Nd, and Pi w e r e unchanged in subjects of all three age c a t e g o r i e s (P=0.01). LPS of w a v e s Pc and Nf w e r e i n c r e a s e d in the r e s p o n s e s of the subjects of the second subgroup compared with the f i r s t , L P of waves Pe was reduced in the subjects of the third subgroup. L P s of waves Pg and Nh were inc r e a s e d in the subjects of the third age subgroup only. As r e g a r d s changes in amplitudes the folIowing patt e r n could be noted. The amplitude of the f i r s t positive wave Pa (A) was unchanged in all three age subgroups. The amplitudes of waves Nb and Pc, which w e r e unchanged in the f i r s t and second subgroups, were i n c r e a s e d in the r e s p o n s e s of the subjects of the third age subgroup (P = 0.01). Compared with the evoked r e s p o n s e s in the subjects of the f i r s t subgroup, the amplitudes of waves Nd, Nh, and Pi were reduced in the r e s p o n s e s of the subjects of the second subgroup (P=0.01). L a t e r , with an i n c r e a s e in age the amplitude of the complex of w a v e s i n c r e a s e d . The c h a r a c t e r of the changes in amplitude of E P waves observed in the various age subgroups of healthy subjects is shown in Fig. 2. I p s i l a t e r a l r e s p o n s e s . During r e c o r d i n g of E P s of the ipsilateral c e r e b r a l h e m i s p h e r e the r e s p o n s e s w e r e s i m i l a r in configuration to the c o n t r a l a t e r a l r e s p o n s e s . By analogy with the latter, the ipsilateral E P s w e r e designated as P a P Nbi, and so on. The i p s i l a t e r a l waves differed from the c o n t r a l a t e r a l in t h e i r lower amplitude and g r e a t e r variability; they w e r e m o r e often absent and they were difficult to distinguish from the background EEG. The r e s u l t s of m e a s u r e m e n t s of LPs and amplitudes of the ipsilateral r e s p o n s e s a r e given in Table 3. C o m p a r e d with the mean values of L P s and amplitudes of the c o n t r a l a t e r a l r e s p o n s e s the following changes w e r e observed. In the i p s i l a t e r a l r e s p o n s e s the e x p r e s s i v e n e s s of the e a r l y complex of waves was reduced. It was m o r e difficult to find waves Nbi (41.1%) and Ndi (39.9%). The other waves also appeared in a lower p e r c e n t a g e of c a s e s than the c o r r e s p o n d i n g waves of the c o n t r a l a t e r a l r e s p o n s e s . Values of LPS of the waves of the i p s i l a t e r a l E P s were significantly g r e a t e r ( P = 0.01) than the values of L P s of the c o r r e s p o n d i n g waves of the c o n t r a l a t e r a l r e s p o n s e s . On a v e r a g e this difference between the L P s of the ipsilateral and c o n t r a l a t e r a l E P s i n c r e a s d with an i n c r e a s e in L P of the waves r e c o r d e d and it varied between 3 and 7 m s e c . The amplitudes of these w a v e s of the i p s i l a t e r a l E P s also w e r e changed c o m p a r e d with those of the c o n t r a l a t e r a l r e s p o n s e s . The g r e a t e s t difference was observed in the amplitudes of the e a r l y part of the r e s p o n s e (0-60 m s e c ) . The values of the amplitudes of the l a t e r components of the response approximated to the amplitude of the analogous waves of the c o n t r a l a t e r a l E P s .
T A B L E 3. Latent P e r i o d s and Amplitudes of Ipsilateral Somatos e n s o r y E P s in Healthy Subjects Waves of ipsilateral EPs
LP, m s e c M~m
P=O,05
P=O,OI
0,62 0,74 3,21
0,84 0,~ 4,38 2,60 2,14 3,50 3,~ 5,~
Amplitude, JuV, M +m
P-O,05
P=O.O1
0,24 0,46 0.89 0,43 0,48 0,81 0,84
0,32 0,61
Pal Nbl
24,364-0,30
Pcl
29,64-+0,37 42,53• 1,59 54,82-+l,O0 74,064-0,83 102,78-+1,35 137,90-+-[,31 186,85-+2,20 *
Ndt Pe!
Nfl
Pgl ~Vm PiJ
1,97
1,63 2,09 2,58 4.32
1,354-0,1 l 3,37---9,23 2,89d:0,43" 3,71-+0,21 5,884-0,24 5,77---0,41 7,914-0,43 10,84 +-0,53
1,04
1.22
0,56 0.63 1,06 I.II 1 37
201
DISCUSSION The number and polarity of Waves r e c o r d e d in the E P s agreed basically with the corresponding data published previously and r e c o r d e d during investigation of healthy human subjects [4, 5, 10, 13, 15]. It can evidently be concluded from the r e s u l t s of C r a c c o ' s experiments [10] that the Pa wave is not an artifact but is i n t r a c r a n i a l in origin and is the e l e c r o g r a p h i c reflection of activation in p r e s y n a p t i c t h a l a m o c o r t i c a l fibers of the p r i m a r y s o m a t o s e n s o r y projection. Since this wave is the most variable of all components of the s o m a t o s e n s o r y cortical E P s , it is not atways r e c o r d e d and its amplitude is low, m o s t w o r k e r s usually do not take it into account. The designation of the components of the s o m a t o s e n s o r y E P s as a rule begins with the e a r l y negative wave with L P s of 19-24 m s e c (Nb}. Some w o r k e r s who have investigated the nature of the human s o m a t o s e n s o r y cortical E P s have attempted to c o m p a r e p a r t i c u l a r wave complexes of the r e s o n s e with certain f o r m s of evoked e l e c t r i c a l activity recorded in e x p e r i m e n t s on animals. F o r instance, the Nb-N d wave complex i n c o r p o r a t e s the " c l a s s i c a l ~ p r i m a r y r e s p o n s e [13, 15]. According to the observations of L u d e r s [15], the Pe and Nf waves a r e closely s i m i l a r in t h e i r L P values to the " a s s o c i a t i v e " response. The l a t e r wave complex (Pg, Nh, Pi} d e m o n s t r a t e d in the p r e s e n t experiments probably c o r r e l a t e s with the "K complex" [13, 15]. According to this subdivision, the first, e a r l y complex of the EP is thus generally r e g a r d e d as the " p r i m a r y " or "specific" r e s p o n s e (the l e m n i s c a l conduction system}. The second p a r t of the response, or the "nonspecific" response, is due to activation of the nonspecific, or e x t r a l e m n i s c a l , conduction s y s t e m . However, this a l m o s t u n r e s e r v e d extrapolation to man of data obtained by the study of EP in animals has r e cently been challenged by facts which cast doubts on the hypothesis that a s t r i c t l y dual s y s t e m of conduction of excitation p a r t i c i p a t e s in the generation of the s o m a t o s e n s o r y E P [11, 19, 20]. A m o r e complex view of the c h a r a c t e r of genesis of the s o m a t e s e n s o r y EP has a r i s e n as a r e s u l t of e x p e r i m e n t s on animals [1, 2, 7]. In the w r i t e r ' s opinion further light will be shed on this problem by investigations of patients with d i s e a s e s of the CNS. Evidence of the s i m i l a r i t y in c h a r a c t e r of s o m a t o s e n s o r y cortical E P s r e c o r d e d in healthy subjects a f t e r long periods of time points to the stationary nature of the e l e c t r i c a l p r o c e s s e s revealed. A dynamic approach is accordingly possible to the a s s e s s m e n t of the functional state of the nervous s y s t e m by the use of EP (as well as by other methods} in the c o u r s e of treatment. In the w r i t e r ' s investigations E P s r e c o r d e d in the s o m t o s e n s o r y cortex were well d e m o n s t r a t e d by both methods of r e c o r d i n g although the e a r l y complex of waves was b e t t e r e x p r e s s e d by monopolar recording, as is confirmed by the weaker manifestation of these waves or, s o m e t i m e s , even their total disappearance and by the g r e a t e r i n t r a - and interindividual variability of the r e s p o n s e s with bipolar r e c o r d i n g . No significant differences were observed in the changes in L P s of the homonymous waves r e c o r d e d by the two methods. N e v e r t h e l e s s , we consider that monopolar r e c o r d i n g is the p r e f e r a b l e method for investigating s o m a t o s e n s o r y E P s in man. As was pointed out above, each wave of the s o m a t o s e n s o r y EP v a r i e s depending on the s u b j e c t ' s age. In the investigations of Mural [16] no significant d e c r e a s e was found in the velocity of conduction of nervous excitation in healthy subjects of different age groups {from 15 to 67 y e a r s ) . It t h e r e f o r e s e e m s probable that age changes a r e f i r s t reflected in neuronal function, i.e., basically in synaptic t r a n s m i s s i o n and the slow m e m b r a n e potentials of cortical and subcortical levels. The p r e s e n t r e s u l t s indicating changes in L P of certain waves of the s o m a t o s e n s o r y EP with an i n c r e a s e in the subject's age a g r e e with results of previous investigations of E P s of the s o m a t o s e n s o r y [15, 17] and visual [12] a r e a s of the cortex. Results obtained by r e c o r d i n g ipsilateral EPs showed definite s i m i l a r i t y in the e x p r e s s i v e n e s s of the c o n t r a l a t e r a l and ipsilateral r e s p o n s e s . In m o s t cases the ipsilateral r e s p o n s e s began with a positive wave Pci. Spike latencies of waves of the ipsilateral r e s p o n s e s w e r e found to be delayed by 3-7 m s e c compared with the c o n t r a l a t e r a l EPs. It was also shown that the amplitudes of the ipsilateral r e s p o n s e s were lower than those of the homonymous c o n t r a l a t e r a l r e s p o n s e s , especially in the e a r l y part of the response. T h e s e r e s u l t s confirm the views of those w o r k e r s [14, 18, 20] who consider that the opposite (contralateral) c e r e b r a l h e m i s p h e r e participates in the genesis of human ipsilateral EPs. If this is so, the question a r i s e s of how the ipsilateral h e m i s p h e r e is activated. T h e r e are two possible ways of this activation: through "volume dissipation" and with the aid of specific i n t e r h e m i s p h e r i c somatic pathways for the conduction of excitation. In the w r i t e r s ' opinion the second method of activation of the ipsilateral h e m i s p h e r e is m o s t likely. This suggestion was confirmed by investigations of s o m a t o s e n s o r y EPs in patients with certain d i s e a s e s of the
202
n e r v o u s s y s t e m [3, 18, 20]. The s t r u c t u r e responsible for this connection between the h e m i s p h e r e s could be the c o r p u s callosum. The r e s u l t s of e x p e r i m e n t s by Innocenti et al. [14] provide evidence of the somatotopical distribution of EP o v e r the s u r f a c e of the corpus callosum. The work of A l b e - F e s s a r d [9] has shown that division of the corpus callosum d e p r e s s e s i p s i l a t e r a l E P s without changing the c o n t r a l a t e r a l EPs. It can a c c o r d i n g l y be postulated on the b a s i s of the r e s u l t s described above that the difference between L P s r e c o r d e d for h o m o n y m o u s waves of i p s i l a t e r a l and c o n t r a l a t e r a l E P s can evidently be attributed to the p r e d o m i n a n t l y s u c c e s s i v e activation of the ipsilateral h e m i s p h e r e through i n t e r h e m i s p h e r i c t r a n s m i s s i o n via the corpus callosum. In the case of activation of the ipsilateral h e m i s p h e r e mainly by ipsilateral axon pathways running d i r e c t l y f r o m the p e r i p h e r y without decussation, no such difference between spike latencies of the i p s i l a t e r a l and c o n t r a l a t e r a l E P s and no significant d e c r e a s e in amplitude of the waves of the ips!lateral r e s p o n s e s would be observed. F u r t h e r m o r e , in patients with unilateral brain lesions well m a r k e d ipsilateral r e s p o n s e s would be observed even in the absence or considerable reduction of the c o n t r a l a t e r a l r e s p o n s e s . However, this was not found in investigations conducted on neurological patients [3, 18, 20]. On the b a s i s of our own experimental data and those obtained by other w o r k e r s it can be postulated that the genesis of the human s o m a t o s e n s o r y c o r t i c a l EP as a whole, as well of its individual components, is complex in nature. Investigations of patients with pathological lesions at different h i e r a r c h i c a l levels of the n e r vous s y s t e m would help to shed light on their nature. LITERATURE 1.
2. 3.
4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18.
CITED
F . A . Ata-Muradova, "The nature of the cortical evoked potential. An evolutionary analysis," Usp.
Fiziol. Nauk, 5, No. 3, 29 (1974). A.B. Batuev, "On the origin of components of the cortical primary response," Fiziol. Zh. SSSR, 5_.44, 659 (1968). Yu. P. Varezhkin and G. P. Guba, "Informativeness of somatosensory evoked potentials in some diseases of the nervous system," in: Neurobionics and Problems in Bioelectrical Control [in Russian], Institute of Cybernetics, Academy of Sciences of the Ukrainian SSR, Kiev (1975), p. 69. M.S. Zalkind, A. V. Naidel', and E. I. Koz'myan, "Effect of stimulus strength on amplitude of components of the human somatosensory cortical evoked response," Neirofiziologiya, _7, 93 (1975). A.M. Ivanitskii and V. B. Strelets, "Somatosensory evoked potentials in man during self-stimulation," Zh. Vyssh. Nerv. Deyat., 2__4,1048 (1974). G.K. Korning, Topographical Anatomy [in Russian], Moscow-Leningrad (1931), pp. 36-37. F.N. Serkov, "On the genesis and functional significance of cortical evoked potentials," Neirofiziologiya, 2, 349 (1970). R.B. Strelkov, A Method of Calculating the Standard Error and Confidence Limits of Arithmetic Mean Values with the Aid of a Table [in Russian], Alashara, Sukhumi (1966). D. Albe-Fessard, in: The Thalamus (ed. by D. P. Purpura and M. D. Yahr), Columbia University Pr., New York (1966), p. 206. R. Cracco, "The initial positive potential of the human scalp recorded SERs," Electroenceph. Clin. Neurophysiol., 3__22,623 (1972). E . F . Domino, S. Matsuoka, J. Waltz, and I. Cooper, "Effects of cryogenic thalamic lesions on the somesthetic evoked responses in man," Electroenceph. Clin. Neurophysiol., 1__99,127 (1965). R.E. Dustman and E. Beck, "The effect of maturation and aging on the wave form of visually evoked responses," Eleetroenceph. Clin. Neurophysiol., 2__66,2 (1969). W.R. Golf, B. S~Rosner, and T. Allison, "Distribution of cerebral somatosensory evoked responses in normal man," Electroenceph. Clin. Neurophysiol., 1_44,697 (1962). G.M. Innocenti, T. Manzoni, and G. Spidalieri, "Patterns of the somesthetic messages transferred through the corpus callosum," Exp. Brain Res., 1__99,447 (1974). H. Luders, "The effects ofaging on the wave form of the somatosensory cortical evoked potentials," Electroenceph. Clin. Neurophysiol., 2__99,450 (1970). Y. Mural, M. Ohta, J. Kuroiwa, and K. Yamaguchi, "Sensory conduction velocity and biopsy findings of sural nerves in normal and neuropathic subjects," Brain Nerve (Jpn.), 2__1,233 (1969). C. Shagass and M. Sehawatz, "Age, personality, and sornatosensory cerebral evoked responses," Science, 148, 1359 (1965). K. Tamura, "Ipsilateral somatosensory evoked responses in man," Folia Psychiat. Neurol. Jpn., 2__6, 83 (1972)o
203
19. 20.
H . G . Vaughan, "The relationship of b r a i n activity to the scalp r e c o r d i n g of e v e n t - r e l a t e d potentials," in: The Averaged Evoked Potentials, edited by Donchin and Lindsley, New York (1969). P . D . Williamson, W. R. Goff, and T. Allison, "Somatosensory evoked r e s p o n s e s 'in patients with unilateral c e r e b r a l lesions," Electroenceph. Clin. Neurophysiol., 2_._88,566 (1970).
DEPRESSION THALAMIC
OF
VENTRO-BASAL
SOMATOSENSORY M.
EVOKED
V. K i r z o n
CORTEX and
POTENTIALS COMPLEX AFTER
A. Ya.
IN R A T AND
RETICULAR
Kaplan
STIMULATION UDC 612.826.1-612.825.5:612.829.1
Experiments on unanesthetized r a t s immobilized with D-tubocurarine showed that e l e c t r i c a l stimulation (100/sec) of the central gray m a t t e r and the m e s e n c e p h a l i c and m e d u l l a r y r e t i c u l a r formation considerably d e p r e s s e d potentials in the somatic thalamic r e l a y nucleus and s o m a t o s e n s o r y cortex evoked by stimulation of the forelimb or medial lemniscus. The mean threshold values of the c u r r e n t used for electrical stimulation of these s t r u c t u r e s did not differ significantly and were 70 (20-100}, 100 (20-120}, and 120 (50-200} # A , r e s p e c 9tively. On comparison of the a m p l i t u d e - t e m p o r a l c h a r a c t e r i s t i c s of inhibition of evoked potentials during e l e c t r i c a l stimulation of the above-mentioned s t r u c t u r e s by a c u r r e n t of twice the threshold strength, no significant differences were found. Immediately a f t e r the end of e l e c t r i c a l stimulation the amplitude of the cortical evolved potential and the postsynaptic components of the thalamic evoked potential was 50-60% (P < 0.01) below the control values. The duration of this d e p r e s s i o n varied from 0.5 to 1 sec. An i n c r e a s e in the intensity of e l e c t r i c a l stimulation of b r a i n - s t e m s t r u c t u r e s tobetween t h r e e and five t i m e s the threshold led to d e p r e s s i o n of the presynaptie component of the thalamic evoked potential also. D e p r e s s i o n of the evoked potential as d e s c r i b e d above was found with various ratios between the intensities of conditioning and testing stimuli. INTRODUCTION T r a n s m i s s i o n of the afferent signal in the thalamic somatic r e l a y nucleus (TSR), just as in certain s t r u c t u r e s in other a n a l y z e r s , is e x t r e m e l y variable if the p r o c e s s is studied in the s l e e p - w a k i n g cycle [25], in the course of the orienting reflex [5, 24], or during an attention r e s p o n s e [12]. At the same time it is well known that s t r u c t u r e s of the b r a i n stem play a very important role in the m e c h a n i s m of these r e s p o n s e s [1, 7] On the other hand, in acute experiments on animals e l e c t r i c a l stimulation o r b l o c k i n g of many brain formations, including specific c o r t i c a l projection zones, cerebellum, caudate nucleus, s t r u c t u r e s of the limbic system, and hypothalamus, leads to changes in p r i m a r y r e s p o n s e s in the s t r u c t u r e s of the s o m a t o s e n s o r y a n a l y z e r [2, 6, 9, 11, 23, 26, 29], but the s t r o n g e s t influence in this r e s p e c t was that a r i s i n g from certain p a r t s of the b r a i n stem [2, 23, 26, 27]. Despite the existence of d i r e c t corticofugal influences on TSR [3, 10, 17], modulation of its relay function is probably l a r g e l y effected through s t r u c t u r e s of the brain stem. Several regions of the b r a i n stem have been identified - the ventromedial region of the medulla [23], the central g r a y m a t t e r [11], and the m e s e n c e phalic r e t i c u l a r formation at the level of the red nucleus [23, 29], - e l e c t r i c a l stimulation of which causes considerable d e p r e s s i o n of evoked potentials (EPs} in s t r u c t u r e s of the s o m a t o s e n s o r y analyzer. However, in the a c c e s s i b l e l i t e r a t u r e no details could be found of a m p l i t u d e - t e m p o r a l c h a r a c t e r i s t i c s of this p r o c e s s , taking into account the intensity of the conditioning and testing stimuli, and it is still not clear to what degree the effects of stimulation of b r a i n stem s t r u c t u r e s differ, on the one hand, or how p r o c e s s e s of d e p r e s s i o n developing at different levels of the s o m a t o s e n s o r y a n a l y z e r differ, on the other hand. The elucidation of
M. V. Lomonosov Moscow State University. T r a n s l a t e d from Neirofiziologiya, Vol. 8, No. 5, pp. 467475, September-October, 1976. Original article submitted August 4, 1975.
204
0097-0549/78/0902-0204507.50
9 1979 Plenum Publishing Corporation
4. 5. 6. 7. 8. 9. !0. 11.
CITED
H . R . Maturana, J . Y. Lettvin, W. S. MacCulloch, and W. H. P i t t s , J. Gen. P h y s i o l . , 4__33,N o . 6 , P a r t 2, 129 (1960). W.R.A. Muntz, J . N e u r o p h y s i o l . , 2__55, 712 (1962). O . J . G r f / s s e r and U. G r f / s s e r - C o r n e h l s , in: H. Autrum et a l . , Handbook of Sensory Physiology, Vol. VH/3a, Central P r o c e s s i n g of Visual Information, P a r t A. (R. J u n g , e d . ) , S p r i n g e r - - V e r l a g , Berlin (1973), p. 333. D. Schneider, Biol. Z b l . , 7_33, 225 (1954). I . N . P i g a r e v and G. M. Zenkin, Zh. Vyssh. Nervn. D e y a t . , 2_.0.0, 170 (1970). R . W . S p e r r y , J . N e u r o p h y s i o l . , 7 , 57 (1944). R . M . G a z e , The F o r m a t i o n of N e r v e Connections, Acad. P r e s s , New Y o r k (1970). V . M . Vinogradova, V. A. Bastakov, L. N. D ' y a c h k o v a , and Yu. B. Mantefel', Neirofiziologiya, 5, 611 (1973). E . I . Kiseleva and Yu. B. Manteifel'., Zool. Z h . , 5__33,1817 (1974). D. Ingle, Science, !81, 1053 (1973). M . J . Keating and R. M. G a z e , Brain R e s . , 2_~1, 197 (1970).
SOMATOSENSORY L.
S. A l e e v
EVOKED and
Yu.
POTENTIALS P.
IN HEALTHY
PEOPLE UDC 612.825
Varezhkin
The: r e s u l t s of a study of s o m a t o s e n s o r y evoked potentials r e c o r d e d in 37 healthy stlbjects of both s e x e s a r e d e s c r i b e d . C o m p a r i s o n of the r e s u l t s of t e s t s on t h r e e age subgroups showed selectivity in the change in l a t e n e i e s and a m p l i t u d e s of w a v e s of the s o m a t o s e n s o r y r e s p o n s e s depending on the s u b j e c t ' s age. I p s i l a t e r a l r e s p o n s e s show g r e a t e r v a r i a b i l i t y but a l o w e r amplitude and frequency of a p p e a r a n c e of the individual components than c o n t r a l a t e r a l r e s p o n s e s . T h e i r latent p e r i o d s a l s o w e r e longer than those of the c o n t r a l a t e r a l r e s p o n s e s . INTRODUCTION N u m e r o u s investigations of cortical evoked potentials (EPs) in a n i m a l s have shown that the EP method is highly effective as a m e a n s of studying the conducting pathways and connections in the CNS. F o r v a r i o u s r e a s o n s of a technical nature human E P s have r e c e i v e d f a r l e s s study. When deciding to investigate s o m a t o s e n s o r y E P s of the human b r a i n it was r e a l i z e d that information on the c h a r a c t e r and p r o p e r t i e s of t h e s e r e s p o n s e s is scanty and s o m e t i m e s c o n t r a d i c t o r y . T h i s is the c a s e , for e x a m p l e , with the concept of " n o r m a l " as applied to c o n t r a l a t e r a l r e s p o n s e s and the g e n e s i s of i p s i l a t e r a l r e s p o n s e s . Another i n t e r e s t i n g p r o b l e m for study was the possibility of using data on E Ps in clinical neurology f o r diagnostic p u r p o s e s and also for investigating cortical c o m p e n s a t o r y m e c h a n i s m s in the c o u r s e of r e c o v e r y
Institute of C y b e r n e t i c s , A c a d e m y of Sciences of the Ukrainian SSR, Kiev. T r a n s l a t e d f r o m N e i r o f i z i o logiya, Vol. 8, No. 5, pp. 447-454, S e p t e m b e r - O c t o b e r , 1976. Original a r t i c l e submitted N o v e m b e r 6, 1975.
198
0097-0549/78/0902-0198507.50
9 1979 Plenum Publishing Corporation
of lost m o t o r and s e n s o r y functions. F o r this purpose it was decided to study certain p r o p e r t i e s of s o m a t o s e n s o r y EPs of healthy subjects, namely the effect of the method of r e c o r d i n g and of the subject's age on the c h a r a c t e r of the r e s p o n s e , and the p a r a m e t e r s of c o n t r a l a t e r a l and ipsilateral r e s p o n s e s were compared. EXPERIMENTAL
METHOD
To obtain s o m a t o s e n s o r y EPs the m e d i a n n e r v e was stimulated in the distal part of the f o r e a r m by single square pulses 0.5 m s e c in duration and separated by intervals of 2 sec. Electrical stimulation was applied f r o m a standard g e n e r a t o r with radiofrequency attachment. The level of stimulation evoking slight twitching of the thumb of the stimulated hand was taken as the m o t o r threshold and used throughout the investigation. The location of the r e c o r d i n g e l e c t r o d e s , approximating to the cortical projection a r e a s of both hands, was d e t e r m i n e d by K o r n i n g ' s method [6]. Another pair of e l e c t r o d e s used as "indifferent" for biopolar r e cording was placed 5 cm a n t e r i o r l y to the f i r s t e l e c t r o d e s along the parasagittal line. The indifferent electrode for monopolar r e c o r d i n g was fixed t o the bridge of the nose. The i n t e r e l e c t r o d e r e s i s t a n c e did not exceed 3-4 k~2. The technique of r e c o r d i n g and analysis of the s o m a t o s e n s o r y E P s was described m o r e fully previously [3]. Only a v e r a g e d (on the b a s i s of summation and averaging of 35 single EPs) r e s p o n s e s were analyzed. F r o m each subject four such a v e r a g e d r e s p o n s e s were obtained. Statistical analysis of the r e s u l t s was c a r r i e d out with the aid of S t r e l k o v ' s tables [8]. EXPERIMENTAL
RESULTS
Despite definite variability between individuals the a v e r a g e EP of all healthy subjects tested (by the m o n o p o l a r r e c o r d i n g method) p o s s e s s e d s i m i l a r features (Fig. lb). According to the r e s u l t s of these investigations the e o n t r a l a t e r a l s o m a t o s e n s o r y E P consisted of 7-9 s u c c e s s i v e waves of different p o l a r i t i e s extending over a period of 200 m s e c a f t e r stimulation. The latent period (LP) and amplitude of the r e s p o n s e s a r e given in Table 1. Since there is no single classification of the components of EP in the l i t e r a t u r e it was decided to use a n o m e n c l a t u r e illustrated in Fig. l a (P, N - polarity; a - i - s u c c e s s i v e EP components r e c o r d e d ; A, B, C . . . . . I - amplitudes of s u c c e s s i v e waves Pa, Nb, Pc . . . . . P i ' respectively).
a
b
A j-~ C -~] I !
,~ . . . . -i l i
#v
/ %
28
I
iI
I
I 16
.!
/sH .
,,
/
,,
M~A" ,eAr
",
91- ,
o
',
\
,
,,, \'
,
T . ~ i.~. . .~.
I
I
I
Ioo
200 m s e c 0
Fig. 1
I
,
e,;
F
,.", ,'.iN
v l
,'oo
I
200 r n s e c
Fig. 2
Fig. i. Explanatory scheme of waves ofaveraged evolved potential (EP) of somatosensory cortex (a) and individual differences in averaged EP of three healthy subjects (1-3) (b). P. N) polarity; a, b, c ..... J) successive components of EP recorded; A, B, C, .... I) amplitudes of successive waves Pa, Nb, Pe .... Pi respectively. Inall eases left median nerve was stimulated. Each response averaged on the basis of 35 single EP. Fig. 2. Changes in amplitudes of waves of contralateral somatosensory EP with age. I, If, Ill) Age subgroups: 18-30, 31-40, and 41-53 years respectively. Remainder of legend as in Fig. i.
199
In m o s t c a s e s the averagd response began with a negative deflection Nb. L P of this wave (P=0.01) had confidendce limits of 20.58 9 0.52 m s e c . In r a r e c a s e s it was preceded by a small positive deflection Pa with L P 15.67=~ 0.73 m s e c (P=0.01). As a rule the Nb wave was followed immediately by a p o s i t i v e - n e g a t i v e positive complex of waves Pc, Nd, Pe, with LP limits of 2.5.55~ 0.68, 34.25~= 1.39, and 48.47=~ 1.87 m s e c r e s p e c t i v e l y (P=0.01). The confidence limits of L P s of the l a t e r waves (P=0.01) were r e s p e c t i v e l y : Nf 66.63• 2.33, Pg 96.11e 2.36, Nh 127.19~= 2.86, and Pi 178.37~ 3.72 m s e c . The amplitude of the r e c o r d e d waves of s o m a t o s e n s o r y E P s varied. The waves Pa, Nb, and Nd had the lowest amplitudes, 2.34~: 0.52, 3.97~= 0.41, and 4.54~ 0.68 pV, r e s p e c t i v e l y (P=0.01). Waves in the late part of the r e s p o n s e had the highest amplitude. 17or instance, the amplitude of wave Nh (H) was 10.77 9 1.01, and that of wave Pi (I) was 15.25~: 1.16/iV (P=0.01). T h e duration of the investigation did not significantly affect the c h a r a c t e r of the EPs if the subject r e m a i n e d in a state of relaxed wakefulness all the time. R e c o r d s obtained after longer time intervals (6-12 months) showed a s i m i l a r i t y in the c h a r a c t e r of E P s r e c o r d e d in the same subject ( P = 0.05). To c o m p a r e r e s p o n s e s obtained the same age subgroup (18-30 y e a r s ) . the waves appeared less frequently in f e r e n c e s in the r e c o r d e d values of L P
by monopolar and bipolar recording, averaged EPs were chosen f r o m Bipolar r e s p o n s e s were s i m i l a r with monopolar, but in some cases the e a r l y part of EP (0-60 msec) and were l e s s well e x p r e s s e d . Difwere not statistically significant (P=0.05) and in p r a c t i c e could t h e r e -
T A B L E 1. Mean Values of L P and Amplitudes of S o m a t o s e n s o r y E P s of Control Group of (37) Subjects with Monopolar Recording Expressiveness of comp0nent,
Components l LP. msec of EPs Mi m
Pa Pc Nd
15,67_+ 0,28 20,58• 25,55 _+0,26 34,25-4-0,54
Pe
48,47+--0,72
Nf Pz Nh Pl
66,63___0,90 96,11 -+0,91 127,19~-_, 1,I1 178,37• 1,44
Nb
39,3 " 85,7 85,7 78 6 97,6 89,3 85,7 88, I 90,5
Range, msec 13 18 19--23 24 - 28 2"}- 38 40 --57 58--81 82 103 107--140 165--204
Amplitude.
P=0.01 m~ec M ~ m
0,7.3 0,52
0,68 1,39 1,87
2,33 2,36 2,86 3.72
2,34~0,12 3,97_+0,16 7,44• 4,54_+0,26 6,71~0.26 9,95:~_ 0,33 9,19• 10,77_+0,39 15,24:t:0,45
P = 0.01
0,52 0,41 0,64 0,68 0.67 0.85 0,90 1,01 1,16
T A B L E 2. Changes in S o m a t o s e n s o r y E P with Age in Healthy Subjects (P = 0.01} Waves
of EP
I= II= III ~-
Pa Nb
Pr Na Pe /dr
+ + + +
Pl
Tamp~'=" i tuae LP
I compared with II
I compared with II
amvlitud~
+
t t
Pg Nr
withI comparediI
t t t t t
+
Legend: c r o s s e s denote no change in p a r a m e t e r s in all subgroups; a r r o w s pointing downward show d e c r e a s e in numerical value of these p a r a m e t e r s (msec, pV) compared with older of subgroups compared; a r r o w s pointing upward indicate i n c r e a s e in n u m e r i c a l value of these p a r a m e t e r s (msec, #V) c o m p a r e d with older of subgroups compared. I, II, III) Age subgroups: 18-30, 31-40, and 41-53 y e a r s , respectively.
200
fore be d i s r e g a r d e d . The amplitude of the P a - Pe complex of waves on bipolar r e c o r d i n g w e r e s m a l l e r than those of the analogous" E P waves on m o n o p o l a r r e c o r d i n g , w h e r e a s the amplitudes of the l a t e r waves ( N f - Pi) w e r e s i m i l a r to those r e c o r d e d by the m onopolar method (P = 0.05). Changes in S o m a t o s e n s o r y C o r t i c a l E P s with Age. To determine the variability of EPs with age the subjects w e r e divided into t h r e e subgroups. The f i r s t subgroup consisted of 14 p e r s o n s aged from 18 to 30 y e a r s (mean age 24.3 y e a r s ) ; the second of 15 subjects aged from 31 to 40 y e a r s (mean age 35.5 y e a r s ) , and the third of eight subjects aged f r o m 41 to 53 y e a r s (mean age 48.7 y e a r s ) . Average r e s p o n s e s obtained b y the m o n o p o l a r method w e r e compared. Changes detected in the r e s p o n s e s of subjects of different ages a r e shown in Table 2. F o r instance L P s of waves Pa, Nb, Pc, Nd, and Pi w e r e unchanged in subjects of all three age c a t e g o r i e s (P=0.01). LPS of w a v e s Pc and Nf w e r e i n c r e a s e d in the r e s p o n s e s of the subjects of the second subgroup compared with the f i r s t , L P of waves Pe was reduced in the subjects of the third subgroup. L P s of waves Pg and Nh were inc r e a s e d in the subjects of the third age subgroup only. As r e g a r d s changes in amplitudes the folIowing patt e r n could be noted. The amplitude of the f i r s t positive wave Pa (A) was unchanged in all three age subgroups. The amplitudes of waves Nb and Pc, which w e r e unchanged in the f i r s t and second subgroups, were i n c r e a s e d in the r e s p o n s e s of the subjects of the third age subgroup (P = 0.01). Compared with the evoked r e s p o n s e s in the subjects of the f i r s t subgroup, the amplitudes of waves Nd, Nh, and Pi were reduced in the r e s p o n s e s of the subjects of the second subgroup (P=0.01). L a t e r , with an i n c r e a s e in age the amplitude of the complex of w a v e s i n c r e a s e d . The c h a r a c t e r of the changes in amplitude of E P waves observed in the various age subgroups of healthy subjects is shown in Fig. 2. I p s i l a t e r a l r e s p o n s e s . During r e c o r d i n g of E P s of the ipsilateral c e r e b r a l h e m i s p h e r e the r e s p o n s e s w e r e s i m i l a r in configuration to the c o n t r a l a t e r a l r e s p o n s e s . By analogy with the latter, the ipsilateral E P s w e r e designated as P a P Nbi, and so on. The i p s i l a t e r a l waves differed from the c o n t r a l a t e r a l in t h e i r lower amplitude and g r e a t e r variability; they w e r e m o r e often absent and they were difficult to distinguish from the background EEG. The r e s u l t s of m e a s u r e m e n t s of LPs and amplitudes of the ipsilateral r e s p o n s e s a r e given in Table 3. C o m p a r e d with the mean values of L P s and amplitudes of the c o n t r a l a t e r a l r e s p o n s e s the following changes w e r e observed. In the i p s i l a t e r a l r e s p o n s e s the e x p r e s s i v e n e s s of the e a r l y complex of waves was reduced. It was m o r e difficult to find waves Nbi (41.1%) and Ndi (39.9%). The other waves also appeared in a lower p e r c e n t a g e of c a s e s than the c o r r e s p o n d i n g waves of the c o n t r a l a t e r a l r e s p o n s e s . Values of LPS of the waves of the i p s i l a t e r a l E P s were significantly g r e a t e r ( P = 0.01) than the values of L P s of the c o r r e s p o n d i n g waves of the c o n t r a l a t e r a l r e s p o n s e s . On a v e r a g e this difference between the L P s of the ipsilateral and c o n t r a l a t e r a l E P s i n c r e a s d with an i n c r e a s e in L P of the waves r e c o r d e d and it varied between 3 and 7 m s e c . The amplitudes of these w a v e s of the i p s i l a t e r a l E P s also w e r e changed c o m p a r e d with those of the c o n t r a l a t e r a l r e s p o n s e s . The g r e a t e s t difference was observed in the amplitudes of the e a r l y part of the r e s p o n s e (0-60 m s e c ) . The values of the amplitudes of the l a t e r components of the response approximated to the amplitude of the analogous waves of the c o n t r a l a t e r a l E P s .
T A B L E 3. Latent P e r i o d s and Amplitudes of Ipsilateral Somatos e n s o r y E P s in Healthy Subjects Waves of ipsilateral EPs
LP, m s e c M~m
P=O,05
P=O,OI
0,62 0,74 3,21
0,84 0,~ 4,38 2,60 2,14 3,50 3,~ 5,~
Amplitude, JuV, M +m
P-O,05
P=O.O1
0,24 0,46 0.89 0,43 0,48 0,81 0,84
0,32 0,61
Pal Nbl
24,364-0,30
Pcl
29,64-+0,37 42,53• 1,59 54,82-+l,O0 74,064-0,83 102,78-+1,35 137,90-+-[,31 186,85-+2,20 *
Ndt Pe!
Nfl
Pgl ~Vm PiJ
1,97
1,63 2,09 2,58 4.32
1,354-0,1 l 3,37---9,23 2,89d:0,43" 3,71-+0,21 5,884-0,24 5,77---0,41 7,914-0,43 10,84 +-0,53
1,04
1.22
0,56 0.63 1,06 I.II 1 37
201
DISCUSSION The number and polarity of Waves r e c o r d e d in the E P s agreed basically with the corresponding data published previously and r e c o r d e d during investigation of healthy human subjects [4, 5, 10, 13, 15]. It can evidently be concluded from the r e s u l t s of C r a c c o ' s experiments [10] that the Pa wave is not an artifact but is i n t r a c r a n i a l in origin and is the e l e c r o g r a p h i c reflection of activation in p r e s y n a p t i c t h a l a m o c o r t i c a l fibers of the p r i m a r y s o m a t o s e n s o r y projection. Since this wave is the most variable of all components of the s o m a t o s e n s o r y cortical E P s , it is not atways r e c o r d e d and its amplitude is low, m o s t w o r k e r s usually do not take it into account. The designation of the components of the s o m a t o s e n s o r y E P s as a rule begins with the e a r l y negative wave with L P s of 19-24 m s e c (Nb}. Some w o r k e r s who have investigated the nature of the human s o m a t o s e n s o r y cortical E P s have attempted to c o m p a r e p a r t i c u l a r wave complexes of the r e s o n s e with certain f o r m s of evoked e l e c t r i c a l activity recorded in e x p e r i m e n t s on animals. F o r instance, the Nb-N d wave complex i n c o r p o r a t e s the " c l a s s i c a l ~ p r i m a r y r e s p o n s e [13, 15]. According to the observations of L u d e r s [15], the Pe and Nf waves a r e closely s i m i l a r in t h e i r L P values to the " a s s o c i a t i v e " response. The l a t e r wave complex (Pg, Nh, Pi} d e m o n s t r a t e d in the p r e s e n t experiments probably c o r r e l a t e s with the "K complex" [13, 15]. According to this subdivision, the first, e a r l y complex of the EP is thus generally r e g a r d e d as the " p r i m a r y " or "specific" r e s p o n s e (the l e m n i s c a l conduction system}. The second p a r t of the response, or the "nonspecific" response, is due to activation of the nonspecific, or e x t r a l e m n i s c a l , conduction s y s t e m . However, this a l m o s t u n r e s e r v e d extrapolation to man of data obtained by the study of EP in animals has r e cently been challenged by facts which cast doubts on the hypothesis that a s t r i c t l y dual s y s t e m of conduction of excitation p a r t i c i p a t e s in the generation of the s o m a t o s e n s o r y E P [11, 19, 20]. A m o r e complex view of the c h a r a c t e r of genesis of the s o m a t e s e n s o r y EP has a r i s e n as a r e s u l t of e x p e r i m e n t s on animals [1, 2, 7]. In the w r i t e r ' s opinion further light will be shed on this problem by investigations of patients with d i s e a s e s of the CNS. Evidence of the s i m i l a r i t y in c h a r a c t e r of s o m a t o s e n s o r y cortical E P s r e c o r d e d in healthy subjects a f t e r long periods of time points to the stationary nature of the e l e c t r i c a l p r o c e s s e s revealed. A dynamic approach is accordingly possible to the a s s e s s m e n t of the functional state of the nervous s y s t e m by the use of EP (as well as by other methods} in the c o u r s e of treatment. In the w r i t e r ' s investigations E P s r e c o r d e d in the s o m t o s e n s o r y cortex were well d e m o n s t r a t e d by both methods of r e c o r d i n g although the e a r l y complex of waves was b e t t e r e x p r e s s e d by monopolar recording, as is confirmed by the weaker manifestation of these waves or, s o m e t i m e s , even their total disappearance and by the g r e a t e r i n t r a - and interindividual variability of the r e s p o n s e s with bipolar r e c o r d i n g . No significant differences were observed in the changes in L P s of the homonymous waves r e c o r d e d by the two methods. N e v e r t h e l e s s , we consider that monopolar r e c o r d i n g is the p r e f e r a b l e method for investigating s o m a t o s e n s o r y E P s in man. As was pointed out above, each wave of the s o m a t o s e n s o r y EP v a r i e s depending on the s u b j e c t ' s age. In the investigations of Mural [16] no significant d e c r e a s e was found in the velocity of conduction of nervous excitation in healthy subjects of different age groups {from 15 to 67 y e a r s ) . It t h e r e f o r e s e e m s probable that age changes a r e f i r s t reflected in neuronal function, i.e., basically in synaptic t r a n s m i s s i o n and the slow m e m b r a n e potentials of cortical and subcortical levels. The p r e s e n t r e s u l t s indicating changes in L P of certain waves of the s o m a t o s e n s o r y EP with an i n c r e a s e in the subject's age a g r e e with results of previous investigations of E P s of the s o m a t o s e n s o r y [15, 17] and visual [12] a r e a s of the cortex. Results obtained by r e c o r d i n g ipsilateral EPs showed definite s i m i l a r i t y in the e x p r e s s i v e n e s s of the c o n t r a l a t e r a l and ipsilateral r e s p o n s e s . In m o s t cases the ipsilateral r e s p o n s e s began with a positive wave Pci. Spike latencies of waves of the ipsilateral r e s p o n s e s w e r e found to be delayed by 3-7 m s e c compared with the c o n t r a l a t e r a l EPs. It was also shown that the amplitudes of the ipsilateral r e s p o n s e s were lower than those of the homonymous c o n t r a l a t e r a l r e s p o n s e s , especially in the e a r l y part of the response. T h e s e r e s u l t s confirm the views of those w o r k e r s [14, 18, 20] who consider that the opposite (contralateral) c e r e b r a l h e m i s p h e r e participates in the genesis of human ipsilateral EPs. If this is so, the question a r i s e s of how the ipsilateral h e m i s p h e r e is activated. T h e r e are two possible ways of this activation: through "volume dissipation" and with the aid of specific i n t e r h e m i s p h e r i c somatic pathways for the conduction of excitation. In the w r i t e r s ' opinion the second method of activation of the ipsilateral h e m i s p h e r e is m o s t likely. This suggestion was confirmed by investigations of s o m a t o s e n s o r y EPs in patients with certain d i s e a s e s of the
202
n e r v o u s s y s t e m [3, 18, 20]. The s t r u c t u r e responsible for this connection between the h e m i s p h e r e s could be the c o r p u s callosum. The r e s u l t s of e x p e r i m e n t s by Innocenti et al. [14] provide evidence of the somatotopical distribution of EP o v e r the s u r f a c e of the corpus callosum. The work of A l b e - F e s s a r d [9] has shown that division of the corpus callosum d e p r e s s e s i p s i l a t e r a l E P s without changing the c o n t r a l a t e r a l EPs. It can a c c o r d i n g l y be postulated on the b a s i s of the r e s u l t s described above that the difference between L P s r e c o r d e d for h o m o n y m o u s waves of i p s i l a t e r a l and c o n t r a l a t e r a l E P s can evidently be attributed to the p r e d o m i n a n t l y s u c c e s s i v e activation of the ipsilateral h e m i s p h e r e through i n t e r h e m i s p h e r i c t r a n s m i s s i o n via the corpus callosum. In the case of activation of the ipsilateral h e m i s p h e r e mainly by ipsilateral axon pathways running d i r e c t l y f r o m the p e r i p h e r y without decussation, no such difference between spike latencies of the i p s i l a t e r a l and c o n t r a l a t e r a l E P s and no significant d e c r e a s e in amplitude of the waves of the ips!lateral r e s p o n s e s would be observed. F u r t h e r m o r e , in patients with unilateral brain lesions well m a r k e d ipsilateral r e s p o n s e s would be observed even in the absence or considerable reduction of the c o n t r a l a t e r a l r e s p o n s e s . However, this was not found in investigations conducted on neurological patients [3, 18, 20]. On the b a s i s of our own experimental data and those obtained by other w o r k e r s it can be postulated that the genesis of the human s o m a t o s e n s o r y c o r t i c a l EP as a whole, as well of its individual components, is complex in nature. Investigations of patients with pathological lesions at different h i e r a r c h i c a l levels of the n e r vous s y s t e m would help to shed light on their nature. LITERATURE 1.
2. 3.
4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18.
CITED
F . A . Ata-Muradova, "The nature of the cortical evoked potential. An evolutionary analysis," Usp.
Fiziol. Nauk, 5, No. 3, 29 (1974). A.B. Batuev, "On the origin of components of the cortical primary response," Fiziol. Zh. SSSR, 5_.44, 659 (1968). Yu. P. Varezhkin and G. P. Guba, "Informativeness of somatosensory evoked potentials in some diseases of the nervous system," in: Neurobionics and Problems in Bioelectrical Control [in Russian], Institute of Cybernetics, Academy of Sciences of the Ukrainian SSR, Kiev (1975), p. 69. M.S. Zalkind, A. V. Naidel', and E. I. Koz'myan, "Effect of stimulus strength on amplitude of components of the human somatosensory cortical evoked response," Neirofiziologiya, _7, 93 (1975). A.M. Ivanitskii and V. B. Strelets, "Somatosensory evoked potentials in man during self-stimulation," Zh. Vyssh. Nerv. Deyat., 2__4,1048 (1974). G.K. Korning, Topographical Anatomy [in Russian], Moscow-Leningrad (1931), pp. 36-37. F.N. Serkov, "On the genesis and functional significance of cortical evoked potentials," Neirofiziologiya, 2, 349 (1970). R.B. Strelkov, A Method of Calculating the Standard Error and Confidence Limits of Arithmetic Mean Values with the Aid of a Table [in Russian], Alashara, Sukhumi (1966). D. Albe-Fessard, in: The Thalamus (ed. by D. P. Purpura and M. D. Yahr), Columbia University Pr., New York (1966), p. 206. R. Cracco, "The initial positive potential of the human scalp recorded SERs," Electroenceph. Clin. Neurophysiol., 3__22,623 (1972). E . F . Domino, S. Matsuoka, J. Waltz, and I. Cooper, "Effects of cryogenic thalamic lesions on the somesthetic evoked responses in man," Electroenceph. Clin. Neurophysiol., 1__99,127 (1965). R.E. Dustman and E. Beck, "The effect of maturation and aging on the wave form of visually evoked responses," Eleetroenceph. Clin. Neurophysiol., 2__66,2 (1969). W.R. Golf, B. S~Rosner, and T. Allison, "Distribution of cerebral somatosensory evoked responses in normal man," Electroenceph. Clin. Neurophysiol., 1_44,697 (1962). G.M. Innocenti, T. Manzoni, and G. Spidalieri, "Patterns of the somesthetic messages transferred through the corpus callosum," Exp. Brain Res., 1__99,447 (1974). H. Luders, "The effects ofaging on the wave form of the somatosensory cortical evoked potentials," Electroenceph. Clin. Neurophysiol., 2__99,450 (1970). Y. Mural, M. Ohta, J. Kuroiwa, and K. Yamaguchi, "Sensory conduction velocity and biopsy findings of sural nerves in normal and neuropathic subjects," Brain Nerve (Jpn.), 2__1,233 (1969). C. Shagass and M. Sehawatz, "Age, personality, and sornatosensory cerebral evoked responses," Science, 148, 1359 (1965). K. Tamura, "Ipsilateral somatosensory evoked responses in man," Folia Psychiat. Neurol. Jpn., 2__6, 83 (1972)o
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19. 20.
H . G . Vaughan, "The relationship of b r a i n activity to the scalp r e c o r d i n g of e v e n t - r e l a t e d potentials," in: The Averaged Evoked Potentials, edited by Donchin and Lindsley, New York (1969). P . D . Williamson, W. R. Goff, and T. Allison, "Somatosensory evoked r e s p o n s e s 'in patients with unilateral c e r e b r a l lesions," Electroenceph. Clin. Neurophysiol., 2_._88,566 (1970).
DEPRESSION THALAMIC
OF
VENTRO-BASAL
SOMATOSENSORY M.
EVOKED
V. K i r z o n
CORTEX and
POTENTIALS COMPLEX AFTER
A. Ya.
IN R A T AND
RETICULAR
Kaplan
STIMULATION UDC 612.826.1-612.825.5:612.829.1
Experiments on unanesthetized r a t s immobilized with D-tubocurarine showed that e l e c t r i c a l stimulation (100/sec) of the central gray m a t t e r and the m e s e n c e p h a l i c and m e d u l l a r y r e t i c u l a r formation considerably d e p r e s s e d potentials in the somatic thalamic r e l a y nucleus and s o m a t o s e n s o r y cortex evoked by stimulation of the forelimb or medial lemniscus. The mean threshold values of the c u r r e n t used for electrical stimulation of these s t r u c t u r e s did not differ significantly and were 70 (20-100}, 100 (20-120}, and 120 (50-200} # A , r e s p e c 9tively. On comparison of the a m p l i t u d e - t e m p o r a l c h a r a c t e r i s t i c s of inhibition of evoked potentials during e l e c t r i c a l stimulation of the above-mentioned s t r u c t u r e s by a c u r r e n t of twice the threshold strength, no significant differences were found. Immediately a f t e r the end of e l e c t r i c a l stimulation the amplitude of the cortical evolved potential and the postsynaptic components of the thalamic evoked potential was 50-60% (P < 0.01) below the control values. The duration of this d e p r e s s i o n varied from 0.5 to 1 sec. An i n c r e a s e in the intensity of e l e c t r i c a l stimulation of b r a i n - s t e m s t r u c t u r e s tobetween t h r e e and five t i m e s the threshold led to d e p r e s s i o n of the presynaptie component of the thalamic evoked potential also. D e p r e s s i o n of the evoked potential as d e s c r i b e d above was found with various ratios between the intensities of conditioning and testing stimuli. INTRODUCTION T r a n s m i s s i o n of the afferent signal in the thalamic somatic r e l a y nucleus (TSR), just as in certain s t r u c t u r e s in other a n a l y z e r s , is e x t r e m e l y variable if the p r o c e s s is studied in the s l e e p - w a k i n g cycle [25], in the course of the orienting reflex [5, 24], or during an attention r e s p o n s e [12]. At the same time it is well known that s t r u c t u r e s of the b r a i n stem play a very important role in the m e c h a n i s m of these r e s p o n s e s [1, 7] On the other hand, in acute experiments on animals e l e c t r i c a l stimulation o r b l o c k i n g of many brain formations, including specific c o r t i c a l projection zones, cerebellum, caudate nucleus, s t r u c t u r e s of the limbic system, and hypothalamus, leads to changes in p r i m a r y r e s p o n s e s in the s t r u c t u r e s of the s o m a t o s e n s o r y a n a l y z e r [2, 6, 9, 11, 23, 26, 29], but the s t r o n g e s t influence in this r e s p e c t was that a r i s i n g from certain p a r t s of the b r a i n stem [2, 23, 26, 27]. Despite the existence of d i r e c t corticofugal influences on TSR [3, 10, 17], modulation of its relay function is probably l a r g e l y effected through s t r u c t u r e s of the brain stem. Several regions of the b r a i n stem have been identified - the ventromedial region of the medulla [23], the central g r a y m a t t e r [11], and the m e s e n c e phalic r e t i c u l a r formation at the level of the red nucleus [23, 29], - e l e c t r i c a l stimulation of which causes considerable d e p r e s s i o n of evoked potentials (EPs} in s t r u c t u r e s of the s o m a t o s e n s o r y analyzer. However, in the a c c e s s i b l e l i t e r a t u r e no details could be found of a m p l i t u d e - t e m p o r a l c h a r a c t e r i s t i c s of this p r o c e s s , taking into account the intensity of the conditioning and testing stimuli, and it is still not clear to what degree the effects of stimulation of b r a i n stem s t r u c t u r e s differ, on the one hand, or how p r o c e s s e s of d e p r e s s i o n developing at different levels of the s o m a t o s e n s o r y a n a l y z e r differ, on the other hand. The elucidation of
M. V. Lomonosov Moscow State University. T r a n s l a t e d from Neirofiziologiya, Vol. 8, No. 5, pp. 467475, September-October, 1976. Original article submitted August 4, 1975.
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0097-0549/78/0902-0204507.50
9 1979 Plenum Publishing Corporation
