- Email: [email protected]
Electrophysiological evidence for the existence of connections between the brain stem oculomotor areas and the visual system in the cat
225
SHORT COMMUNICATIONS
Electrophysiological
evidence for the existence of connections between the
brain stem oculomotor
areas and the visual system in the cat
Potential changes associated with eye movements have been found in the visual system of alert animals and during REM sleep. According to Jeannerod and Sakai5 the potential changes during sleep are less closely related to eye movements and should be considered as a separate type. A distinction can also be made between the potential changes associated with rapid conjugate eye movements in the alert animal. The first type of potential change is independent of retinal input or actual eye movement (eye movement potentials, EMP). These potential changes persist in darkness or after retina ablation or curarization. The second type of potential change is associated with saccades but is dependent on the retinal input. These potential changes only occur if the eyes move in an illuminated environment (saccade reafference potentials, SRP). The two types of potentials are differently represented in the visual systems of different mammalian species (Table I). Cohen and Feldman1 observed that in the monkey the first type of potential change was induced in LGB by direct stimulation of the anterior pontine oculomotor area. They did not find these potential changes at
TABLE I DISTRIBUTION
Tabulation Species
Cat Monkey
OF
EMPs
AND
SRPs
IN HlGHER
MAMMALS
of the results of Cohen and Feldman 2, Feldman
and Cohen4, Jeannerod and Sakais.
Level LGB
VC
EMP EMP
EMP SRP
the cortical level of the monkey 3. The present experiments demonstrate that in the cat the first type of eye movement potential change can be induced at both cortical and geniculate levels by stimulation of the mesencephalic or pontine oculomotor areas. Experiments were performed on encephale isole cats. Surgery was done under ether anesthesia and wound edges and pressure points were infiltrated with 1% xylocaine. Bipolar concentric electrodes were introduced into LGB and visual cortex (VC) for recording and into the brain stem for stimulation. Eye movements were observed and monitored in darkness by electrooculography (EOG). The EOG was recorded through screws in the frontal sinuses. The brain stem was stimulated with 20 msec volleys of 0.5 msec pulses of 5 V at 400 c/set. The threshold for inducing LGB and VC potentials as well as eye movements was also determined. Brain
Research,
41 (1972) 225-22
226
SHORT COMMUNICATIONS DARK
DARK
LIGHT
Fig. 1. Eye movements and VC and LGB responses evoked by anterior pontine oculomotor area (APOA) stimulation. Stimulation used was a standard volley of 20 msec duration with 0.5 msec pulses of 5 V at 400 c/sec. Sites of stimulation (numbered 1-7) shown in drawing on the left; unresponsive sites: open dots; responsive sites: full dots. On the right the oculomotor and visual system responses evoked by stimulation at the indicated sites: in the left column EOG (above) and VC response (below) in darkness; in the right columns GL (above) and VC (below) responses in dark and light. Time base is horizontal bar showing 200 msec. Vertical bar is 150/~V for VC recording and 400 t~V for GL recording. CS, colliculus superior; CG, central gray; Nip, nucleus interpeduncularis; PCM, pedunculus cerebellaris medius. Stimulation o f b o t h the mesencephalic and p o n t i n e o c u l o m o t o r areas elicited potential changes in L G B and VC which were similar to those which occur d u r i n g eye m o v e m e n t . This is illustrated in Fig. 1. N o potential changes were induced by stimulation at the two u p p e r m o s t points (open dots). A c t i v a t i o n at sites 3 a n d 4 e v o k e d c o n t r a l a t e r a l eye m o v e m e n t s and at 5 a n d 6 ipsilateral eye movements. Only facial c o n t r a c t i o n s were induced at site 7. Potential changes in L G B and VC (Fig. 1) were similar to the p o t e n t i a l changes which occur d u r i n g s p o n t a n e o u s eye m o v e m e n t s b o t h in light a n d d a r k (Fig. 2). The wave f o r m o f the L G B and VC potentials was similar as was their latency (between 20 and 35 msec). These potentials persisted after c u r a r i z a t i o n a l t h o u g h their a m p l i t u d e was s o m e w h a t reduced. The stimulus t h r e s h o l d at which potential changes in L G B and VC were evoked was the same at all brain stem sites which were investigated. The lowest t h r e s h o l d s for evoked potentials were f o u n d in the medial p a r t o f the mesencephalic and p o n t i n e t e g m e n t u m . T h r e s h o l d values for evoked potentials were generally lower t h a n for induced conjugate eye movements. In the medial p a r t o f the a n t e r i o r pontine tegm e n t u m , however, stimulus thresholds for eye m o v e m e n t s and evoked potentials were similar (Fig. 3). Brain Research, 41 (1972) 225-229
227
SHORT COMMUNICATIONS
A 3.0
./
A 6.5
I Fig. 2. VC and GL recordings during spontaneous eye movements. Sites of recording (VC above, GL below) shown in sections on the left. Upper row, VC recordings; lower row, GL recordings. On the left responses to light flash, in the center EMP in darkness, on the right EMP in light (in VC recordings flash artifact or EOG above and VC below; in GL recordings flash artifact or EOG below and GL above). Time base is horizontal bar showing 200 msec. Vertical bar is 150/~V for VC recording and 400/zV for GL recording. Note the similarity between EMPs and responses evoked by A P O A stimulation in Fig. 1 (all records were made in the same animal).
stiPrl, s i t e
st im sde I
2
6
>
25V
1525V
15
30reset 20msec
20Y
10
~
3
~
4
~
5
--
0
I0 m s e ¢ t hreshotd P05
Fig. 3. Thresholds of eye movements and visual system responses for two penetrations at the P 0.5 level. Left and right diagrams: on ordinate stimulation sites, on abscissa thresholds; full line, VC and LGB responses thresholds; dotted line, ocular response thresholds; > indicates thresholds were higher than maximal stimulation tested. In the central diagram: corresponding stimulation sites; arrows indicate direction of the conjugate eye movements. Abbreviations as in Fig. 1.
Brain Research, 41 (1972) 225-229
228
SHORT
Stirn p a r a m e l e r s
COMMUNICATIONS
lOrnsec.
20 rnsec
20 msec
z.OOc/sec.
400 c / s e c
Z.OOc/sec.
~V
5V 0,5 m s e ¢
0.5 m s e c
0,5 m s e c .
5V
Dark
ero
4
18
J
J
m
.....
G.L
Light
18
~J
150 jJr. L~...O~s ec
150pV
aoo ~Jv
L2OOmsec
L2OOmsec
A 2 200m_sec
200reset
200msec.
Fig. 4. Effect of nucleus III stimulation on visual cortex. Upper row recordings in dark, lower row in light. Responses on the left obtained by IIIrd nucleus stimulation: one with a very weak stimulus, the other with the standard stimulation. For comparison the responses of a APOA point to the standard volley are given on the right (the weak one used for nucleus stimulation was uneffective in the APOA). Note that in dark the nucleus stimulation produces no visual system response. CS, colliculus superior; GM, corpus geniculatum mediale; GC, central gray; IP, nucleus interpeduncularis; PCM, pedunculus cerebellaris medius. TABLE 11 D I S T R I B U T I O N 1N H I G H E R M A M M A L S O F V I S U A L S Y S T E M R E S P O N S E S E V O K E D I N D A R K N E S S BY S T I M U L A T I O N OF THE MESENCEPHALIC OR PONTINE OCULOMOTOR
AREAS
Tabulation of the results of Cohen and Feldman 1, Cohen et al. 3 and our results.
Species
Cat Monkey
Level LGB
VC
+ ÷
+ --
In the region o f the o c u l o m o t o r nucleus the stimulation intensity for inducing an eye m o v e m e n t was m u c h less (Fig. 4). Even at suprathreshold levels, stimulation o f the II[ nucleus did not evoke eye m o v e m e n t potentials in visual structures in darkness. In light, however, potential changes appeared which were due to retinal reafference. Table II shows a tabulation o f our results in the cat along with results described previously in the m o n k e y . In the cat mesencephalic or pontine o c u l o m o t o r area stimulation elicited evoked responses in both lateral geniculate body and visual cortex where E M P s are found. This result supports the hypothesis that a corollary discharge which originates in the brain stem m a y project rostrally to the visual system. The hypothesis is further supported by findings o f Sparks and Travis 6 which s h o w that reticular neurons discharge in relation to rapid eye m o v e m e n t s . It is not k n o w n why there is a different time relation between evoked responses in the visual system and induced eye m o v e m e n t s on stimulation, or between eye m o v e m e n t s and potential Brain Research, 41 (1972) 225-229
SHORT COMMUNICATIONS
229
changes d u r i n g s p o n t a n e o u s eye m o v e m e n t s . The n a t u r e o f the a n a t o m i c a l c o n n e c t i o n s between the b r a i n stem a n d the visual system remains to be elucidated.
Laboratory for Neuro- and Psychophysiology, University o f Louvain, B-3000 Louvain (Belgium)
GUY ORBAN* ERIK VANDENBUSSCHE MARK CALLENS
1 COHEN, B., AND FELDMAN, M., Relationship of electrical activity in pontine reticular formation
and lateral geniculate body to rapid eye movements, J. Neurophysiol., 31 (1968) 806-817. 2 COHEN,B., AND FELDMAN, M., Potential changes associated with rapid eye movements in the calcarine cortex, Exp. Neurol., 31 (1971) 100-113. 3 COHEN,B., FELDMAN,M., AND DIAMOND, S. P., Effects of eye movement, brainstem stimulation, and alertness on transmission through lateral geniculate body of monkey, J. Neurophysiol., 32 (1969) 583-594. 4 FELDMAN,M., AND COHEN,B., Electrical activity in the lateral geniculate body of the alert monkey associated with eye movements, J. Neurophysiol., 31 (1968) 455--466. 5 JEANNEROD,M., AND SAKAI,K., Occipital and geniculate potentials related to eye movements in the unanesthetized cat, Brain Research, 19 (1970) 361-377. 6 SPARKS, D . L . , AND TRAVIS, JR., R. P., Firing patterns of reticular formation neurons during horizontal eye movements, Brain Research, 33 (1971) 477-481. (Accepted March 1st, 1972)
* Aspirant NFWO
Brain Research, 41 (1972) 225-229
SHORT COMMUNICATIONS
Electrophysiological
evidence for the existence of connections between the
brain stem oculomotor
areas and the visual system in the cat
Potential changes associated with eye movements have been found in the visual system of alert animals and during REM sleep. According to Jeannerod and Sakai5 the potential changes during sleep are less closely related to eye movements and should be considered as a separate type. A distinction can also be made between the potential changes associated with rapid conjugate eye movements in the alert animal. The first type of potential change is independent of retinal input or actual eye movement (eye movement potentials, EMP). These potential changes persist in darkness or after retina ablation or curarization. The second type of potential change is associated with saccades but is dependent on the retinal input. These potential changes only occur if the eyes move in an illuminated environment (saccade reafference potentials, SRP). The two types of potentials are differently represented in the visual systems of different mammalian species (Table I). Cohen and Feldman1 observed that in the monkey the first type of potential change was induced in LGB by direct stimulation of the anterior pontine oculomotor area. They did not find these potential changes at
TABLE I DISTRIBUTION
Tabulation Species
Cat Monkey
OF
EMPs
AND
SRPs
IN HlGHER
MAMMALS
of the results of Cohen and Feldman 2, Feldman
and Cohen4, Jeannerod and Sakais.
Level LGB
VC
EMP EMP
EMP SRP
the cortical level of the monkey 3. The present experiments demonstrate that in the cat the first type of eye movement potential change can be induced at both cortical and geniculate levels by stimulation of the mesencephalic or pontine oculomotor areas. Experiments were performed on encephale isole cats. Surgery was done under ether anesthesia and wound edges and pressure points were infiltrated with 1% xylocaine. Bipolar concentric electrodes were introduced into LGB and visual cortex (VC) for recording and into the brain stem for stimulation. Eye movements were observed and monitored in darkness by electrooculography (EOG). The EOG was recorded through screws in the frontal sinuses. The brain stem was stimulated with 20 msec volleys of 0.5 msec pulses of 5 V at 400 c/set. The threshold for inducing LGB and VC potentials as well as eye movements was also determined. Brain
Research,
41 (1972) 225-22
226
SHORT COMMUNICATIONS DARK
DARK
LIGHT
Fig. 1. Eye movements and VC and LGB responses evoked by anterior pontine oculomotor area (APOA) stimulation. Stimulation used was a standard volley of 20 msec duration with 0.5 msec pulses of 5 V at 400 c/sec. Sites of stimulation (numbered 1-7) shown in drawing on the left; unresponsive sites: open dots; responsive sites: full dots. On the right the oculomotor and visual system responses evoked by stimulation at the indicated sites: in the left column EOG (above) and VC response (below) in darkness; in the right columns GL (above) and VC (below) responses in dark and light. Time base is horizontal bar showing 200 msec. Vertical bar is 150/~V for VC recording and 400 t~V for GL recording. CS, colliculus superior; CG, central gray; Nip, nucleus interpeduncularis; PCM, pedunculus cerebellaris medius. Stimulation o f b o t h the mesencephalic and p o n t i n e o c u l o m o t o r areas elicited potential changes in L G B and VC which were similar to those which occur d u r i n g eye m o v e m e n t . This is illustrated in Fig. 1. N o potential changes were induced by stimulation at the two u p p e r m o s t points (open dots). A c t i v a t i o n at sites 3 a n d 4 e v o k e d c o n t r a l a t e r a l eye m o v e m e n t s and at 5 a n d 6 ipsilateral eye movements. Only facial c o n t r a c t i o n s were induced at site 7. Potential changes in L G B and VC (Fig. 1) were similar to the p o t e n t i a l changes which occur d u r i n g s p o n t a n e o u s eye m o v e m e n t s b o t h in light a n d d a r k (Fig. 2). The wave f o r m o f the L G B and VC potentials was similar as was their latency (between 20 and 35 msec). These potentials persisted after c u r a r i z a t i o n a l t h o u g h their a m p l i t u d e was s o m e w h a t reduced. The stimulus t h r e s h o l d at which potential changes in L G B and VC were evoked was the same at all brain stem sites which were investigated. The lowest t h r e s h o l d s for evoked potentials were f o u n d in the medial p a r t o f the mesencephalic and p o n t i n e t e g m e n t u m . T h r e s h o l d values for evoked potentials were generally lower t h a n for induced conjugate eye movements. In the medial p a r t o f the a n t e r i o r pontine tegm e n t u m , however, stimulus thresholds for eye m o v e m e n t s and evoked potentials were similar (Fig. 3). Brain Research, 41 (1972) 225-229
227
SHORT COMMUNICATIONS
A 3.0
./
A 6.5
I Fig. 2. VC and GL recordings during spontaneous eye movements. Sites of recording (VC above, GL below) shown in sections on the left. Upper row, VC recordings; lower row, GL recordings. On the left responses to light flash, in the center EMP in darkness, on the right EMP in light (in VC recordings flash artifact or EOG above and VC below; in GL recordings flash artifact or EOG below and GL above). Time base is horizontal bar showing 200 msec. Vertical bar is 150/~V for VC recording and 400/zV for GL recording. Note the similarity between EMPs and responses evoked by A P O A stimulation in Fig. 1 (all records were made in the same animal).
stiPrl, s i t e
st im sde I
2
6
>
25V
1525V
15
30reset 20msec
20Y
10
~
3
~
4
~
5
--
0
I0 m s e ¢ t hreshotd P05
Fig. 3. Thresholds of eye movements and visual system responses for two penetrations at the P 0.5 level. Left and right diagrams: on ordinate stimulation sites, on abscissa thresholds; full line, VC and LGB responses thresholds; dotted line, ocular response thresholds; > indicates thresholds were higher than maximal stimulation tested. In the central diagram: corresponding stimulation sites; arrows indicate direction of the conjugate eye movements. Abbreviations as in Fig. 1.
Brain Research, 41 (1972) 225-229
228
SHORT
Stirn p a r a m e l e r s
COMMUNICATIONS
lOrnsec.
20 rnsec
20 msec
z.OOc/sec.
400 c / s e c
Z.OOc/sec.
~V
5V 0,5 m s e ¢
0.5 m s e c
0,5 m s e c .
5V
Dark
ero
4
18
J
J
m
.....
G.L
Light
18
~J
150 jJr. L~...O~s ec
150pV
aoo ~Jv
L2OOmsec
L2OOmsec
A 2 200m_sec
200reset
200msec.
Fig. 4. Effect of nucleus III stimulation on visual cortex. Upper row recordings in dark, lower row in light. Responses on the left obtained by IIIrd nucleus stimulation: one with a very weak stimulus, the other with the standard stimulation. For comparison the responses of a APOA point to the standard volley are given on the right (the weak one used for nucleus stimulation was uneffective in the APOA). Note that in dark the nucleus stimulation produces no visual system response. CS, colliculus superior; GM, corpus geniculatum mediale; GC, central gray; IP, nucleus interpeduncularis; PCM, pedunculus cerebellaris medius. TABLE 11 D I S T R I B U T I O N 1N H I G H E R M A M M A L S O F V I S U A L S Y S T E M R E S P O N S E S E V O K E D I N D A R K N E S S BY S T I M U L A T I O N OF THE MESENCEPHALIC OR PONTINE OCULOMOTOR
AREAS
Tabulation of the results of Cohen and Feldman 1, Cohen et al. 3 and our results.
Species
Cat Monkey
Level LGB
VC
+ ÷
+ --
In the region o f the o c u l o m o t o r nucleus the stimulation intensity for inducing an eye m o v e m e n t was m u c h less (Fig. 4). Even at suprathreshold levels, stimulation o f the II[ nucleus did not evoke eye m o v e m e n t potentials in visual structures in darkness. In light, however, potential changes appeared which were due to retinal reafference. Table II shows a tabulation o f our results in the cat along with results described previously in the m o n k e y . In the cat mesencephalic or pontine o c u l o m o t o r area stimulation elicited evoked responses in both lateral geniculate body and visual cortex where E M P s are found. This result supports the hypothesis that a corollary discharge which originates in the brain stem m a y project rostrally to the visual system. The hypothesis is further supported by findings o f Sparks and Travis 6 which s h o w that reticular neurons discharge in relation to rapid eye m o v e m e n t s . It is not k n o w n why there is a different time relation between evoked responses in the visual system and induced eye m o v e m e n t s on stimulation, or between eye m o v e m e n t s and potential Brain Research, 41 (1972) 225-229
SHORT COMMUNICATIONS
229
changes d u r i n g s p o n t a n e o u s eye m o v e m e n t s . The n a t u r e o f the a n a t o m i c a l c o n n e c t i o n s between the b r a i n stem a n d the visual system remains to be elucidated.
Laboratory for Neuro- and Psychophysiology, University o f Louvain, B-3000 Louvain (Belgium)
GUY ORBAN* ERIK VANDENBUSSCHE MARK CALLENS
1 COHEN, B., AND FELDMAN, M., Relationship of electrical activity in pontine reticular formation
and lateral geniculate body to rapid eye movements, J. Neurophysiol., 31 (1968) 806-817. 2 COHEN,B., AND FELDMAN, M., Potential changes associated with rapid eye movements in the calcarine cortex, Exp. Neurol., 31 (1971) 100-113. 3 COHEN,B., FELDMAN,M., AND DIAMOND, S. P., Effects of eye movement, brainstem stimulation, and alertness on transmission through lateral geniculate body of monkey, J. Neurophysiol., 32 (1969) 583-594. 4 FELDMAN,M., AND COHEN,B., Electrical activity in the lateral geniculate body of the alert monkey associated with eye movements, J. Neurophysiol., 31 (1968) 455--466. 5 JEANNEROD,M., AND SAKAI,K., Occipital and geniculate potentials related to eye movements in the unanesthetized cat, Brain Research, 19 (1970) 361-377. 6 SPARKS, D . L . , AND TRAVIS, JR., R. P., Firing patterns of reticular formation neurons during horizontal eye movements, Brain Research, 33 (1971) 477-481. (Accepted March 1st, 1972)
* Aspirant NFWO
Brain Research, 41 (1972) 225-229