CENTRIFUGAL OF
THE V.
AND CAT
VISUAL
M.
Shaban
CONNECTIONS
CENTRIPETAL CORTEX
UDC 612.825.5:612.843.7
In experiments on curarized Cats unit responses in the dorsal lateral geniculate body to stimulation of various zones in area 17 of the visual cortex were analyzed. Of all cells tested 69% were found to respond antidromically and 8% orthodromicalty; in 7.6% of cells IPSPs occurred either after an initial antidromic spike or without it: The velocities of conduction of excitation along the corticopetaI fibers of the optic radiation varied from 28 to 4.3 m / s e c , but the three commonest groups of fibers had conduction velocities of 28-19, 14-12, and 10-9.5 m / s e c . A difference between latent periods of antidromic responses of the same neurons was found to stimulation of different zones of the visual cortex; this indicates that axons of genieulo-cortical fibers split into several branches which form contacts with several neurons in area 17 of the visual cortex. The degree and possible mechanisms of cortical influences on neurons of the lateral geniculate body are discussed. INTI~ O D U C T I O N Although it is now known that besides corticopetal fibers the optic radiation also contains a certain number of corticofugal fibers [5, 7, 11,12,16], the relative proportion of each of the two groups of fibers, the velocity of conduction of excitation along them, and also the degree and character of cortical influences on the thalamic formations of the visual system have been inadquately studied. The present investigation, in which unit responses of the dorsal lateral geniculate body (DLGB) to stimulation of various zones of area 17 of the visual cortex (VC} were analyzed, was undertaken in order to elucidate the problems mentioned above. EXPERIMENTAL
METHOD
Experiments were carried out on unanesthetised sexually mature cats weighing 2.0-2.8 kg. After preliminary tracheotomy under local anesthesia with procaine, the animals were immobilized with Dtubocurarine (i mg/kg body weight, intravenously), artificially ventilated, and secured into a stereotaxie apparatus. A burr-hole 1 mm in diameter was drilled in the skull above DLGB at a point corresponding to coordinates A-7, L-10 (in Reinoso-Suarez' Atlas). A thick conical glass tube, into which a glass microelectrode was inserted so that its tip did not penetrate beyond its end, was lowered into the burrhole. The tube was inserted into the brain strictly vertically to a depth of 13 ram, i,e., as far as the dorsal boundary of DI/SB, and fixed. By means of a special design the microelectrode, the tip of which pro~ected beyond the end of the tube, could be inserted into the nucleus. Glass microelectrodes with a resistance of 2-15 M~, filled with 2.5 M potassium chloride solution, were used. To determine whether the microeleetrode had entered the nucleus responses of DLGB neurons to flashes and to stimulation of the optic chiasma (OC) were recorded. For this purpose, a stimulating bipolar electrode, through which square pulses of current with an amplitude of 5-10 V and a duration of 0.2 msec were passed, was inserted into OC. In response to stimulation of OC a focal potential of the nucleus could also be recorded (Fig. ic). Since this potential was recorded only when the recording electrode was in the nucleus, the boundaries of the nucleus could be determined by moving the microelectrode vertically. A histological control was carried out to verify the site of recording of the electrical activity. Electrolyric tags were left in the nucleus and located in brain sections cut with the aid of a freezing microtome. A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 8, No. 3, pp. 243-249, May-June, 1976. Original article submitted April 4, 1975.
216
0097-0549/77/0803-0216507.50
9 1978 Plenum Publishing Corporation
Db
b~
a
ab
Fig. 1. Antidromic and o r t h o d r o m i c r e s p o n ses of neurons of d o r s a l lateral geniculate body (DLGB) to stimulation of a r e a 17 of visual c o r t e x : A) intracellular and B , D , 1-3) e x t r a cellular r e c o r d s of antidromic r e s p o n s e s . C,D) e x t r a c e l l u l a r r e c o r d s of o r t h o d r o m i c r e s p o n s e s . D, 4) o r t h o d r o m i c r e s p o n s e s of a neuron to s t i m ulation of OC. a,b) NS and SD-components of spike r e s p e c t i v e l y , c) focal potential of DLGB in r e s p o n s e to stimulation of OC. Calibration: 20 mV (4A); 5 mV, I msec (4 B - E ) .
In o r d e r to stimulate OC t h r e e bipolar electrodes were inserted into different parts of the cortex of a r e a 17 to a depth of i ram. Square pulses (2-10 V, 0.2 msec) were applied. EXPERIMENTAL
RESULTS
Antidromic Responses of DLGB Neurons to Stimulation of A r e a 17 of VC. Antidromic r e s p o n s e s of DLGB neurons were r e c o r d e d e x t r a c e l l u t a r l y and partly i n t r a c e l l u l a r l y f r o m 90 of 130 cells tested. The following c r i t e r i a were used to d e t e r m i n e an antidromic r e s p o n s e : the p r e s e n c e of a s h o r t e r latent period of the r e s p o n s e s than for orthodromieally excited neurons; stability of the latent period during repetitive stimulation; ability to r e p r o d u c e a higher frequency of stimulation than with o r t h o d r o m i cally excited neurons. An important additional c r i t e r i o n of antidromic excitation of the cell was the phenomenon of detachment of the IS component of the spike f r o m its SD component, observed during repetitive
I0" 16
'!IIH
:
Fig. 2. Histograms of latencies of antid r o m i c r e s p o n s e s of DI/3B neurons to s t i m ulation of visual c o r t e x . A b s c i s s a , time, m s e c ; ordinate, number of neurons, n.
217
TABLE 1. Latencies of DIA;B Unit Orthodromic and Antidrornic Responses to Stimulation of Points in Area 17 of VC Orthodromie excitation
Antidromic excitation
points I
2
points 3
I
2
1
1,0 1,6 2,6
3,6 3,3 3,2 3,0 2,3 2,5 2,5 2,6 1,9
3
2,1 2,4 2,5
2,3 1,2
2,0 2,7
2
3
0.7 1,6 2,4 2,1 1,7 2,1 2.1 2,3 2.3 2.0
1,2
2,0
2,7 2,0 1,7
2,0
3,5
3,0
1,1 2.0
2.0
stimulation at a c e r t a i n frequency. Although the NS component can also be found during orthodromic excitation of a neuron [9,10], its s e p a r a t i o n under c e r t a i n conditions is observed as a rule in the case of antidromic activation. The probabIe explanation of this phenomenon is a d e c r e a s e in the rate of s p r e a d of excitation as it p a s s e s a c r o s s the ]unction between the initial segment of the axon and the body of the nerve cell; if excitation is orthodromic, the action potential s p r e a d s into the cell body which has already been partially depolarized by the E P S P [8], so faciltating its p r o g r e s s . It is important to note than an NS-component could be found not only in intracellular, but also in e x t r a c e l l u l a r r e c o r d i n g s of unit activity in LGB (Fig. 1). tn the case of extracellular r e c o r d i n g s , m o r e over, the NS component had positive polarity instead of the expected negative; other w o r k e r s have obs e r v e d the same phenomenon [8]. During repetitive stimulation at 500 Hz only the NS component could be r e c o r d e d without the r e s t of the spike (Fig. 1 D, graph 3). An e x t r a c e l l u l a r response of the same neuron as in Fig. 1 D graphs 1-3 is shown in Fig. 1 D graph 4but in this c a s e during o r t h o d r o m i e excitation in r e s p o n s e to stimulation of OC. Under these conditions splitting of the spike into NS and SD components did not take place. This phenomenon of splitting of the spike essentially s e r v e d as important evidence that e l e c t r i c a l activity was in fact being r e c o r d e d f r o m the body of the neuron and not its axon. A h i s t o g r a m of latencies of antidromic r e s p o n s e s of 90 DLGB neurons to stimulation of VC is shown in Fig. 2. Clearly the latent periods varied between 0.65 and 4.6 msec (in Fig. 1B an example of an orthod r o m i c r e s p o n s e of a neuron with such a long latent period is given). In most cases latent periods varied between 0.7 and 1.1 (14.4%), f r o m 1.4 to 1.6 (13.3%), and f r o m 1.7 to 2.1 (32.2%) m s e e . The optic radiation thus contained corticopetal fibers with a conduction velocity of between 28 and 4.3 m / s e c . T h r e e groups of fibers with conduction velocities of 28-19, 14-12, and 10-9.5 m / s e c , a c c e p ting that the distance f r o m DIX;B to the c o r t e x is 20 mm) were most frequently found. Orthodromic Responses of DLGB Neurons to Stimulation of A r e a 17 of VC. Eleven of the 130 DLGB neurons tested responded o r t h o d r o m i c a l l y to stimulation of VC (8%). Orthodromic r e s p o n s e s were obtained in seven neurons to stimulation of two points in a r e a 17 of VC, but in four neurons the stimulation of only one point (Table 1). Examples of orthodromic r e s p o n s e s are given in Fig. 1C, E and Fig. 3B. The cells did not r e p r o d u c e a high frequency of stimulation (Fig. 1C); they were c h a r a c t e r i z e d by instability of latent periods during repetitive stimulation, as is p a r t i c u l a r l y well shown in Fig. 1E and Fig, 3B. Responses of the Same DLGB Neurons to Stimulation of Different Points of Area 17 of VC. The sites of the stimulating electrodes in the r e g i o n of the right gyrus lateralis a r e shown in Fig. 313. Sixty cells were found to respond (56 antidromically) to stimulation of only one point of VC, 30 cells (23 antidromically) responded to stimulation of two points, and six cells (all antidromically) to stimulation of three points. The difference between minimal latent periods of the orthodromic DLGB unit r e s p o n s e s to stimulation of different c o r t i c a l points was 0.1-0.2 msec for four neurons, whereas for three neurons the latencies were the s a m e .
218
A
C
Fig. 3. Antidromie and orthodromic r e s p o n s e s of DIX3B neurons to stimulation of different points of VC. A,C) Antidromie, B) orthodromic unit r e s p o n s e s . D) r N h t h e m i s p h e r e ; 1-3) sites of stimulating e l e c t r o d e s in a r e a 17 of VC. C a l i b r a t i o n : 5 mV, 1 m s e c . Explanation i n t e x t ,
Among 23 neurons responding antidrmically to stimulation of two cortical points, no difference in latent periods was found for 12 cells and for the other 11 the difference varied from 0.1 to 0.5 msec. Latencies of neurons responding to stimulation of three cortical points also differed only very little (Table i). Examples of antidromic responses of two neurons with equal (C) and unequal (A) latent periods to stimulation of three cortical points are given in Fig. 3. Special interest is attached to neuron (A) which responded to stimulation of three cortical points. The latent period of its response was greatest during stimulation of point 2. The neuron did not reproduce a high frequency of stimulation applied to this point (500 Hz). It did reproduce this frequency during stimulation of points i and 3 and the latencies of its responses to stimulation of these last points were smaller. It can be concluded from these facts that axons of DLGB cells in some cases divide into branches of different diameters, which form synaptic contacts with neurons in different zones of area 17 of VC. Inhibition in DLGB Neurons during Stimulation of VC. During the experiments activity was recorded from ten neurons in which IPSPs were found on intracellular recording in response to stimulation of VC. In seven neurons the inhibitory potentials were preceded by antidromic excitation consisting of a single spike, but in three neurons IPSPs were found without preceding excitation. The latencies of the IPSPs varied from 3.5 to 5 msec, their amplitude was 3.5 mV, and their duration 10-40 reset. Examples of IPSPs of three DLGB neurons in response to stimulation of VC are given in Fig. 4.
I
A
,,
B |
]
I~ll'lll
I1,,
Fig. 4. Antidromic spike responses and IPSPs of DLGB neurons to stimulation of VC. A,B) Ar~idromic spike responses of neurons and IPSPs; c) IPSP without preceding excitation. Calibration: 20mV (4A,B); 5mY, l m s e c (4C). InA: 1,2) recordings from same neuron but with different sweep.
219
DISCUSSION As these investigations showed, the optic radiation contains mainly cortieopetal fibers wi~hconduction velocities of between 28 and 4.3 m/see. Very similar results were obtained by other workers previously [8, 17,18, 20]. For instance, Bishop et al~ [8] found that latencies of antidromic responses of DLGB neurons to stimulation of VC vary from 0.54 to 3.8 msec; these workers accept the possibility of the existence of even thinner fibers. Different values for latent periods were obtained by Vastola [18], namely from 0.2 to 2.4 msec; however, besides antidromic responses of DLGB neurons, this worker also r e corded axon activity in the optic radiation. Although Vastola was able to record a response of only one cell with a latency of 0.2 reset, he discovered a large percentage of neurons with a latent period of 0.3 msec. Studies of corticopetal connections of the optic radiation have led to the distinguishing of one [8, 20] or s e v e r a l [18] groups of fibers that occur most commonly. According to r e s u l t s of the present i n v e s t i gation, the optic radiation contains t h r e e predominant groups of corticopetal fibers. T h e s e r e s u l t s conf i r m our e a r l i e r hypothesis according to which t h r e e principal volleys of excitation r e a c h VC f r o m DLGB, and a r r i v e t h e r e at the s a m e time as the t h r e e initial components of the p r i m a r y r e s p o n s e , which a r e thus presynaptic in nature [5]. An interesting feature of the organization of the corticopetal fibers is the fact that some axons divide into s e v e r a l b r a n c h e s which f o r m contacts evidently with s e v e r a l c o r t i c a l neurons of a r e a 17. A s i m i l a r phenomenon was d i s c o v e r e d previously by Stone et al. [17], but only as r e g a r d s axons running into d i f f e r ent a r e a s of VC, namely a r e a s 17 and 18. This division of axons evidently takes place within the c o r t e x itself, as is confirmed by morphological observations [6]. The question of the existence of corticofugal connections of VC with nervous formations of DLGB and the c h a r a c t e r of c o r t i c a l influences on these formations has so far r e c e i v e d little study and it r e m a i n s a m a t t e r for active d i s c u s s i o n . Although the p r e s e n c e of corticofugal connections in this p a r t i c u l a r s y s t e m has been established both by morphologists [7, 11,12, 16] and by physiologists [8, 18, 20], the actual a r e a s of VC whose neurons p o s s e s s such connections a r e not yet known. For instance, in a morphological investigation by Hollander [13] descending pr0iections a r i s i n g in a r e a 18, and not in a r e a 17, were found. The d i s a g r e e m e n t between r e s u l t s obtained by different morphologists may perhaps be explained by differences i n t h e depth of the injury to a r e a 17 of VC produced in their e x p e r i m e n t s : With deep lesions the white m a t t e r containing corticofugal axons of neighboring a r e a 18 also may be involved, so that the results of investigation of degeneration in DLGB a r e d i s t o r t e d . Exactly the s a m e e r r o r may also a r i s e in an electrophysiological experiment if the depth of insertion of the stimulating e l e c t r o d e s in a r e a 17 or the strength of stimulation used a r e so g r e a t that they involve the cortifugal axons of neighboring a r e a s in excitation. In the p r e s e n t experiments o r t h o d r o m i c r e s p o n s e s of DLGB neurons were obtained to stimulation of various zones of a r e a 17; most cells, m o r e o v e r , responded to stimulation of two cortical points, one of which was c l o s e r to a r e a 18, the other some distance away f r o m the f i r s t point. The electrodes were ins e r t e d into the c o r t e x i n t h i s case not below its third or fourth l a y e r s . The fact that DLGB neurons r e sponded to both these stimuli makes the hypothesis that axons of a r e a 18 a r e involved in excitation unlikely. F u r t h e r m o r e , the w r i t e r previously [5] obtained a n t i d r o m i c unit r e s p o n s e s in a r e a 17 to s t i m u l a tion of DLGB, and this also confirms the p r e s e n c e of eorticofugal fibers in the optic radiation. In a v e r y few c a s e s IPSPs of DLGB neurons are found in r e s p o n s e to stimulation of the visual c o r t e x : They may be evidence of a possible inhibitory influence of the c o r t e x on its thalamic formation. Neverthel e s s , it must be r e m e m b e r e d that some IPSPs could a r i s e as a r e s u l t of involvement of intrinsic mechani s m s of r e c i p r o c a l inhibition in DLGB itself in r e s p o n s e to antidromic activation of cortieopetal fibers of the optic radiation. However, data obtained in experiments with t e m p o r a r y blocking of VC [1-4, 14, 15, 19] a r e to be found in the literature and support the view that VC has both an excitatory and an inhibitory action on D LGB neurons. LITERATURE
Io 2.
220
CITED
A.M. Mass and G. D. Smirnov, "Cortical control of the conduction of excitation in the rabbit lateral geniculate body," Dokl. Akad. Nauk SSSR, 196, 729 (1971). S . P . Narikashvili, "Someresults of an electrophysiological study of cortical regulation of the activity of subcortical formations," Zh. Vyssh. Nerv. Deyat., 17, 925 (1967).
3. 4. 5.
6. 7.
8. 9o 10. 11.
12. 13.
14. 15. 16. 17. :3. 19. 20.
V . L . Silakov, "Descending regulatory cortical influences in the system of the optic analyzer," Zh. Vyssh. Nerv. Deyat., 19, 1044 (1969). V . L . Silakov, "Cortieofugal control of spike responses of lateral geniculate body neurons," Neirofiziologiya, 4, 367 (1973). V . M . Shaban, "On the conduction of excitation in the cat visual system," Neirofiziologiya, 7, 589 (1975). E.G. Shkol'nik-Yarros, Neurons and Interneuronal Connections~ The Visual Analyzer [in Russian], Meditsina, Leningrad (1965)~ W~ A. Beresford, "Fibre degeneration following lesions of the visual cortex of the eat," in: Neurophysiologie und Psychophysikdes visueIlen Systems (edo by R. Jung and H~ Kornhuber), Springer, Berlin-- Gottingen-- Heidelberg (1961), pp. 241-255. P. O~ Bishop, W. Burke, and K~ Davis, "Singleunit recording from antidromically activated optic radiation neurones," J. Physiol. (London), 162, 432 (1962). J . S . Coombs, D. R. Curtis, and J. C. Eccles, "The interpretation of spike potentials of motoneurones," J~ Physiol. (London), 139, 198 (1957). J~ S. Coombs, D. Ro Curtis, and J. C. Eccles, "The generation of impulses in motoneurones," J. Physiol. (London), 139, 232 (1957). L. J~ Garey, E. G~ Jones, and T. P. S. Powell, "Interrelationships of striate and extrastriate cortex with primary relay sites of the visual pathway," J. Neurol~ Neurosurg. Psychiat~ 31, 135 (1968)~ R ~ W~ Guillery, "Patterns of fibre degeneration in the dorsal lateral geniculate nucleus of the cat following lesions in the visual cortex," J. Comp. Neurol., 130, 197 (1967). H. Hollander, "Projections of the visual cortex to the lateral geniculate nucleus in the cat," in: Corticothalamic Projections and Sensorimotor Activities (ed~ by T. Frigyesi et al.), Raven, New York (1972), pp. 475-489. E. Hull, "Cortifugal influence in the macaque lateral geniculate nucleus," Vision Res., _.8, 1285 (1968)~ R. E~ Kalil and R~ Chase, "Corticofugal influence on activity of lateral geniculate neurons in the cat," J. Neurophysiol., 33, 459 (1970). R. Niimi, S. Kawamura, and S~ Ishimaru, "Anatomical organisation of cort i eogeni cul at epr o je c tions in the cat," Proc~ Jap. Acad., 46, 878 (1970). J. Stone and B. Dreger, "Projection of x- and y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex," J. Neurophysiol., 36, 551 (1973). E . F . Vastola, "Conduction velocities in single fibers of the visual radiation," Exptl. Neurol., 7, 1 (1963). E . F . Vastola, "Steady-state effects of visual cortex on geniculate cells," Vision Res.~ -7, 299 (1966). L. Widen and C. Ajmone-Marsan, "Effects of corticipetal and corticofugal impulses upon single elements of the dorsolateral geniculate nucleus," Exptl. Neurol., 2, 468 (1960).
221
THE V.
AND CAT
VISUAL
M.
Shaban
CONNECTIONS
CENTRIPETAL CORTEX
UDC 612.825.5:612.843.7
In experiments on curarized Cats unit responses in the dorsal lateral geniculate body to stimulation of various zones in area 17 of the visual cortex were analyzed. Of all cells tested 69% were found to respond antidromically and 8% orthodromicalty; in 7.6% of cells IPSPs occurred either after an initial antidromic spike or without it: The velocities of conduction of excitation along the corticopetaI fibers of the optic radiation varied from 28 to 4.3 m / s e c , but the three commonest groups of fibers had conduction velocities of 28-19, 14-12, and 10-9.5 m / s e c . A difference between latent periods of antidromic responses of the same neurons was found to stimulation of different zones of the visual cortex; this indicates that axons of genieulo-cortical fibers split into several branches which form contacts with several neurons in area 17 of the visual cortex. The degree and possible mechanisms of cortical influences on neurons of the lateral geniculate body are discussed. INTI~ O D U C T I O N Although it is now known that besides corticopetal fibers the optic radiation also contains a certain number of corticofugal fibers [5, 7, 11,12,16], the relative proportion of each of the two groups of fibers, the velocity of conduction of excitation along them, and also the degree and character of cortical influences on the thalamic formations of the visual system have been inadquately studied. The present investigation, in which unit responses of the dorsal lateral geniculate body (DLGB) to stimulation of various zones of area 17 of the visual cortex (VC} were analyzed, was undertaken in order to elucidate the problems mentioned above. EXPERIMENTAL
METHOD
Experiments were carried out on unanesthetised sexually mature cats weighing 2.0-2.8 kg. After preliminary tracheotomy under local anesthesia with procaine, the animals were immobilized with Dtubocurarine (i mg/kg body weight, intravenously), artificially ventilated, and secured into a stereotaxie apparatus. A burr-hole 1 mm in diameter was drilled in the skull above DLGB at a point corresponding to coordinates A-7, L-10 (in Reinoso-Suarez' Atlas). A thick conical glass tube, into which a glass microelectrode was inserted so that its tip did not penetrate beyond its end, was lowered into the burrhole. The tube was inserted into the brain strictly vertically to a depth of 13 ram, i,e., as far as the dorsal boundary of DI/SB, and fixed. By means of a special design the microelectrode, the tip of which pro~ected beyond the end of the tube, could be inserted into the nucleus. Glass microelectrodes with a resistance of 2-15 M~, filled with 2.5 M potassium chloride solution, were used. To determine whether the microeleetrode had entered the nucleus responses of DLGB neurons to flashes and to stimulation of the optic chiasma (OC) were recorded. For this purpose, a stimulating bipolar electrode, through which square pulses of current with an amplitude of 5-10 V and a duration of 0.2 msec were passed, was inserted into OC. In response to stimulation of OC a focal potential of the nucleus could also be recorded (Fig. ic). Since this potential was recorded only when the recording electrode was in the nucleus, the boundaries of the nucleus could be determined by moving the microelectrode vertically. A histological control was carried out to verify the site of recording of the electrical activity. Electrolyric tags were left in the nucleus and located in brain sections cut with the aid of a freezing microtome. A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 8, No. 3, pp. 243-249, May-June, 1976. Original article submitted April 4, 1975.
216
0097-0549/77/0803-0216507.50
9 1978 Plenum Publishing Corporation
Db
b~
a
ab
Fig. 1. Antidromic and o r t h o d r o m i c r e s p o n ses of neurons of d o r s a l lateral geniculate body (DLGB) to stimulation of a r e a 17 of visual c o r t e x : A) intracellular and B , D , 1-3) e x t r a cellular r e c o r d s of antidromic r e s p o n s e s . C,D) e x t r a c e l l u l a r r e c o r d s of o r t h o d r o m i c r e s p o n s e s . D, 4) o r t h o d r o m i c r e s p o n s e s of a neuron to s t i m ulation of OC. a,b) NS and SD-components of spike r e s p e c t i v e l y , c) focal potential of DLGB in r e s p o n s e to stimulation of OC. Calibration: 20 mV (4A); 5 mV, I msec (4 B - E ) .
In o r d e r to stimulate OC t h r e e bipolar electrodes were inserted into different parts of the cortex of a r e a 17 to a depth of i ram. Square pulses (2-10 V, 0.2 msec) were applied. EXPERIMENTAL
RESULTS
Antidromic Responses of DLGB Neurons to Stimulation of A r e a 17 of VC. Antidromic r e s p o n s e s of DLGB neurons were r e c o r d e d e x t r a c e l l u t a r l y and partly i n t r a c e l l u l a r l y f r o m 90 of 130 cells tested. The following c r i t e r i a were used to d e t e r m i n e an antidromic r e s p o n s e : the p r e s e n c e of a s h o r t e r latent period of the r e s p o n s e s than for orthodromieally excited neurons; stability of the latent period during repetitive stimulation; ability to r e p r o d u c e a higher frequency of stimulation than with o r t h o d r o m i cally excited neurons. An important additional c r i t e r i o n of antidromic excitation of the cell was the phenomenon of detachment of the IS component of the spike f r o m its SD component, observed during repetitive
I0" 16
'!IIH
:
Fig. 2. Histograms of latencies of antid r o m i c r e s p o n s e s of DI/3B neurons to s t i m ulation of visual c o r t e x . A b s c i s s a , time, m s e c ; ordinate, number of neurons, n.
217
TABLE 1. Latencies of DIA;B Unit Orthodromic and Antidrornic Responses to Stimulation of Points in Area 17 of VC Orthodromie excitation
Antidromic excitation
points I
2
points 3
I
2
1
1,0 1,6 2,6
3,6 3,3 3,2 3,0 2,3 2,5 2,5 2,6 1,9
3
2,1 2,4 2,5
2,3 1,2
2,0 2,7
2
3
0.7 1,6 2,4 2,1 1,7 2,1 2.1 2,3 2.3 2.0
1,2
2,0
2,7 2,0 1,7
2,0
3,5
3,0
1,1 2.0
2.0
stimulation at a c e r t a i n frequency. Although the NS component can also be found during orthodromic excitation of a neuron [9,10], its s e p a r a t i o n under c e r t a i n conditions is observed as a rule in the case of antidromic activation. The probabIe explanation of this phenomenon is a d e c r e a s e in the rate of s p r e a d of excitation as it p a s s e s a c r o s s the ]unction between the initial segment of the axon and the body of the nerve cell; if excitation is orthodromic, the action potential s p r e a d s into the cell body which has already been partially depolarized by the E P S P [8], so faciltating its p r o g r e s s . It is important to note than an NS-component could be found not only in intracellular, but also in e x t r a c e l l u l a r r e c o r d i n g s of unit activity in LGB (Fig. 1). tn the case of extracellular r e c o r d i n g s , m o r e over, the NS component had positive polarity instead of the expected negative; other w o r k e r s have obs e r v e d the same phenomenon [8]. During repetitive stimulation at 500 Hz only the NS component could be r e c o r d e d without the r e s t of the spike (Fig. 1 D, graph 3). An e x t r a c e l l u l a r response of the same neuron as in Fig. 1 D graphs 1-3 is shown in Fig. 1 D graph 4but in this c a s e during o r t h o d r o m i e excitation in r e s p o n s e to stimulation of OC. Under these conditions splitting of the spike into NS and SD components did not take place. This phenomenon of splitting of the spike essentially s e r v e d as important evidence that e l e c t r i c a l activity was in fact being r e c o r d e d f r o m the body of the neuron and not its axon. A h i s t o g r a m of latencies of antidromic r e s p o n s e s of 90 DLGB neurons to stimulation of VC is shown in Fig. 2. Clearly the latent periods varied between 0.65 and 4.6 msec (in Fig. 1B an example of an orthod r o m i c r e s p o n s e of a neuron with such a long latent period is given). In most cases latent periods varied between 0.7 and 1.1 (14.4%), f r o m 1.4 to 1.6 (13.3%), and f r o m 1.7 to 2.1 (32.2%) m s e e . The optic radiation thus contained corticopetal fibers with a conduction velocity of between 28 and 4.3 m / s e c . T h r e e groups of fibers with conduction velocities of 28-19, 14-12, and 10-9.5 m / s e c , a c c e p ting that the distance f r o m DIX;B to the c o r t e x is 20 mm) were most frequently found. Orthodromic Responses of DLGB Neurons to Stimulation of A r e a 17 of VC. Eleven of the 130 DLGB neurons tested responded o r t h o d r o m i c a l l y to stimulation of VC (8%). Orthodromic r e s p o n s e s were obtained in seven neurons to stimulation of two points in a r e a 17 of VC, but in four neurons the stimulation of only one point (Table 1). Examples of orthodromic r e s p o n s e s are given in Fig. 1C, E and Fig. 3B. The cells did not r e p r o d u c e a high frequency of stimulation (Fig. 1C); they were c h a r a c t e r i z e d by instability of latent periods during repetitive stimulation, as is p a r t i c u l a r l y well shown in Fig. 1E and Fig, 3B. Responses of the Same DLGB Neurons to Stimulation of Different Points of Area 17 of VC. The sites of the stimulating electrodes in the r e g i o n of the right gyrus lateralis a r e shown in Fig. 313. Sixty cells were found to respond (56 antidromically) to stimulation of only one point of VC, 30 cells (23 antidromically) responded to stimulation of two points, and six cells (all antidromically) to stimulation of three points. The difference between minimal latent periods of the orthodromic DLGB unit r e s p o n s e s to stimulation of different c o r t i c a l points was 0.1-0.2 msec for four neurons, whereas for three neurons the latencies were the s a m e .
218
A
C
Fig. 3. Antidromie and orthodromic r e s p o n s e s of DIX3B neurons to stimulation of different points of VC. A,C) Antidromie, B) orthodromic unit r e s p o n s e s . D) r N h t h e m i s p h e r e ; 1-3) sites of stimulating e l e c t r o d e s in a r e a 17 of VC. C a l i b r a t i o n : 5 mV, 1 m s e c . Explanation i n t e x t ,
Among 23 neurons responding antidrmically to stimulation of two cortical points, no difference in latent periods was found for 12 cells and for the other 11 the difference varied from 0.1 to 0.5 msec. Latencies of neurons responding to stimulation of three cortical points also differed only very little (Table i). Examples of antidromic responses of two neurons with equal (C) and unequal (A) latent periods to stimulation of three cortical points are given in Fig. 3. Special interest is attached to neuron (A) which responded to stimulation of three cortical points. The latent period of its response was greatest during stimulation of point 2. The neuron did not reproduce a high frequency of stimulation applied to this point (500 Hz). It did reproduce this frequency during stimulation of points i and 3 and the latencies of its responses to stimulation of these last points were smaller. It can be concluded from these facts that axons of DLGB cells in some cases divide into branches of different diameters, which form synaptic contacts with neurons in different zones of area 17 of VC. Inhibition in DLGB Neurons during Stimulation of VC. During the experiments activity was recorded from ten neurons in which IPSPs were found on intracellular recording in response to stimulation of VC. In seven neurons the inhibitory potentials were preceded by antidromic excitation consisting of a single spike, but in three neurons IPSPs were found without preceding excitation. The latencies of the IPSPs varied from 3.5 to 5 msec, their amplitude was 3.5 mV, and their duration 10-40 reset. Examples of IPSPs of three DLGB neurons in response to stimulation of VC are given in Fig. 4.
I
A
,,
B |
]
I~ll'lll
I1,,
Fig. 4. Antidromic spike responses and IPSPs of DLGB neurons to stimulation of VC. A,B) Ar~idromic spike responses of neurons and IPSPs; c) IPSP without preceding excitation. Calibration: 20mV (4A,B); 5mY, l m s e c (4C). InA: 1,2) recordings from same neuron but with different sweep.
219
DISCUSSION As these investigations showed, the optic radiation contains mainly cortieopetal fibers wi~hconduction velocities of between 28 and 4.3 m/see. Very similar results were obtained by other workers previously [8, 17,18, 20]. For instance, Bishop et al~ [8] found that latencies of antidromic responses of DLGB neurons to stimulation of VC vary from 0.54 to 3.8 msec; these workers accept the possibility of the existence of even thinner fibers. Different values for latent periods were obtained by Vastola [18], namely from 0.2 to 2.4 msec; however, besides antidromic responses of DLGB neurons, this worker also r e corded axon activity in the optic radiation. Although Vastola was able to record a response of only one cell with a latency of 0.2 reset, he discovered a large percentage of neurons with a latent period of 0.3 msec. Studies of corticopetal connections of the optic radiation have led to the distinguishing of one [8, 20] or s e v e r a l [18] groups of fibers that occur most commonly. According to r e s u l t s of the present i n v e s t i gation, the optic radiation contains t h r e e predominant groups of corticopetal fibers. T h e s e r e s u l t s conf i r m our e a r l i e r hypothesis according to which t h r e e principal volleys of excitation r e a c h VC f r o m DLGB, and a r r i v e t h e r e at the s a m e time as the t h r e e initial components of the p r i m a r y r e s p o n s e , which a r e thus presynaptic in nature [5]. An interesting feature of the organization of the corticopetal fibers is the fact that some axons divide into s e v e r a l b r a n c h e s which f o r m contacts evidently with s e v e r a l c o r t i c a l neurons of a r e a 17. A s i m i l a r phenomenon was d i s c o v e r e d previously by Stone et al. [17], but only as r e g a r d s axons running into d i f f e r ent a r e a s of VC, namely a r e a s 17 and 18. This division of axons evidently takes place within the c o r t e x itself, as is confirmed by morphological observations [6]. The question of the existence of corticofugal connections of VC with nervous formations of DLGB and the c h a r a c t e r of c o r t i c a l influences on these formations has so far r e c e i v e d little study and it r e m a i n s a m a t t e r for active d i s c u s s i o n . Although the p r e s e n c e of corticofugal connections in this p a r t i c u l a r s y s t e m has been established both by morphologists [7, 11,12, 16] and by physiologists [8, 18, 20], the actual a r e a s of VC whose neurons p o s s e s s such connections a r e not yet known. For instance, in a morphological investigation by Hollander [13] descending pr0iections a r i s i n g in a r e a 18, and not in a r e a 17, were found. The d i s a g r e e m e n t between r e s u l t s obtained by different morphologists may perhaps be explained by differences i n t h e depth of the injury to a r e a 17 of VC produced in their e x p e r i m e n t s : With deep lesions the white m a t t e r containing corticofugal axons of neighboring a r e a 18 also may be involved, so that the results of investigation of degeneration in DLGB a r e d i s t o r t e d . Exactly the s a m e e r r o r may also a r i s e in an electrophysiological experiment if the depth of insertion of the stimulating e l e c t r o d e s in a r e a 17 or the strength of stimulation used a r e so g r e a t that they involve the cortifugal axons of neighboring a r e a s in excitation. In the p r e s e n t experiments o r t h o d r o m i c r e s p o n s e s of DLGB neurons were obtained to stimulation of various zones of a r e a 17; most cells, m o r e o v e r , responded to stimulation of two cortical points, one of which was c l o s e r to a r e a 18, the other some distance away f r o m the f i r s t point. The electrodes were ins e r t e d into the c o r t e x i n t h i s case not below its third or fourth l a y e r s . The fact that DLGB neurons r e sponded to both these stimuli makes the hypothesis that axons of a r e a 18 a r e involved in excitation unlikely. F u r t h e r m o r e , the w r i t e r previously [5] obtained a n t i d r o m i c unit r e s p o n s e s in a r e a 17 to s t i m u l a tion of DLGB, and this also confirms the p r e s e n c e of eorticofugal fibers in the optic radiation. In a v e r y few c a s e s IPSPs of DLGB neurons are found in r e s p o n s e to stimulation of the visual c o r t e x : They may be evidence of a possible inhibitory influence of the c o r t e x on its thalamic formation. Neverthel e s s , it must be r e m e m b e r e d that some IPSPs could a r i s e as a r e s u l t of involvement of intrinsic mechani s m s of r e c i p r o c a l inhibition in DLGB itself in r e s p o n s e to antidromic activation of cortieopetal fibers of the optic radiation. However, data obtained in experiments with t e m p o r a r y blocking of VC [1-4, 14, 15, 19] a r e to be found in the literature and support the view that VC has both an excitatory and an inhibitory action on D LGB neurons. LITERATURE
Io 2.
220
CITED
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6. 7.
8. 9o 10. 11.
12. 13.
14. 15. 16. 17. :3. 19. 20.
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