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Oculomotor influences on lateral geniculate body neurons
125
SHORT COMMUNICATIONS
Oculomotor influences on lateral geniculate body neurons Von Helmholtz was one of the first to point out that the subjective stability of the visual world during self-produced eye movements requires some specific mechanism whereby the 'feelings of innervation' can be taken into account in assigning shifts of the image across the retina to movements of the eyes rather than to displacements of external objects 5. In more recent versions of this idea 10, discharges originating in motor regions are assumed to reach the visual system, and there to enter into the evaluation of those shifts of the retinal image that are caused by voluntary movements of the eyes. Although there are subjective data favoring this hypothesis, the only conclusive evidence would be to show a modification of the activity of visual centers, (a) specifically related to an active displacement of the gaze, and (b) independent of the changes in retinal input resulting from this displacement. Recent experiments in the monkey, performed at the cortical level, failed to detect modifications fulfilling these criteria; according to Wurtz 12, striate cortex neurons are influenced when the eyes move across a patterned visual field, or when an object moves across the retina, but not when the eyes move across an empty field, or in the dark. Valleala 11, however, also using monkeys, has reported, in the absence of light, rhythmic changes in activity of units of area 17 synchronous with post-caloric nystagmus. On the other hand, spontaneous eye movements in cats and monkeys in complete darkness are associated with sharp E E G potentials recorded in the visual cortex and lateral geniculate body (LGB) 4,7. These results both indicate possible oculomotor influences on the visual system, and reinstate the need for a further analysis of the relations between eye movements and vision. LGB, which is known as a site of convergence of extraretinal inputs on the visual system3, 6, was chosen as the target in the present study. LGB neurons were recorded in l0 'enc6phale isol6' cats. Both eyes of the cat were covered with a concave mask, made of black plastic foam, fitted on the face to exclude any possible visual input. The mask cavity could be lit from the inside by a lamp embedded in the foam. When the light was on, it formed a random textured pattern, with a maximal luminance of 6 • 10 4 candle per sq cm. The pupils were dilated with atropine, and both the accommodation paralysis and the short distance (3 cm) between the eyes and the lighted background no doubt resulted in a highly blurred image. Single unit activity was recorded from the left LGB through tungsten microelectrodes, monitored and filmed on an oscilloscope, and stored on an FM tape recorder. Units were identified as geniculate both by their on or off reactions to light, and by histological check of the electrode tracks. Although 'enc6phale isol6' preparations exhibit spontaneous eye movements, direct electrical stimulation of the vestibular nuclei was also used; this procedure, modified from Yules and Gault 13, produced a reliable and long lasting afternystagmus, more suitable for an automatic data analysis. Horizontal eye movements were recorded bipolarly with electrodes implanted in the frontal sinus, using an AC-coupled amplifier (0.02 sec time constant), and stored on another channel of the tape recorder. The data were processed with a multichannel analyzer: the rapid phase of each saccade triggered off cumulative storage of the corresponding unit discharge during the following 400 msec, a duration selected so as Brain Research, 24 (I 970) 125 129
126
SHORT COMMUNICATIONS
to avoid a possible overlap between consecutive saccades. Some 30-200 sweeps were superimposed for each individual unit. realizing a 'poststimulus time" (PST) histogram (2 msec binwidth) of the unit discharge related to the onset of the saccades. The eye movements used to trigger the analysis were then averaged. Finally, the 'PST" histogram and the idealized movement were displayed on an X - Y plotter. Sixty units, from approximately 100 recorded, were processed in this way; 25 of these were influenced by eye movements under conditions of complete darkness. The change in activity could be an increase in discharge rate, represented either by a short burst of spikes, or by a more gradual increase, as shown in Fig. IA. This type of relation was the most frequently encountered, the peak of the PST histogram being related to the late phase of the movement (150-200 msec after the beginning of the saccade). In other units, rather infrequently observed, the discharge rate was decreased, the minimal rate also occurring some 150-200 msec after the onset of the saccade (Figs. 1B and 3A). Often the changes in rate were apparent only statistically, and could not be predicted during the experiment itself. Further, the intensity of the modification could vary with time. as exemplified by the neuron in Fig. 2. When spontaneous eye movements occurred, the discharge rate was modified as well, although this effect could not be studied statistically. When tested with the light on, neurons either showed essentially similar behavior as in the dark. e.g., increase (Fig. IA) or decrease (Fig.
B
A
LIGHT .
I
I
.
DARK
i
i
i! ¸ L rnsec
Fig. 1. Poststimulus time histograms of the discharge of two lateral geniculate body neurons (A, B), in the light and in the dark, as triggered by the beginning of nystagmic saccades. The number Of spikes (n) is given in arbitrary units, per 2 msec bins. EM is an average of the corresponding eye movements. Brain Research, 24 (1970) 125-129
SHORT COMMUNICATIONS
127
A" EM [_G
B
Fig. 2. Pattern of firing of a lateral geniculate body neuron (LG) in relation with the afternystagmus following vestibular stimulation. EM := eye movement recording with a 0.02 sec time constant, with the light on (A) and the light off (B, C). Record B starts immediately after the end of vestibular stimulation. Record C is taken several minutes later, during the late phase of the afternystagmus. 1B) in discharge rate; or a strikingly different pattern, which was the reverse o f the change in rate observed in the dark. This latter type is exemplified in Figs. 2 and 3A, which show the corresponding PST histograms. In addition, one neuron in this series showed a peak in activity in the dark, and no change in the light. The reverse effect (positive relation with the movement in the light only) was more c o m m o n l y observed, which is less surprising (Fig. 3B). Our results clearly show that during eye movements o f vestibular origin, definite changes in activity occur in a significant population o f geniculate neurons, independently o f direct visual input. Although nystagmus is a special case o f eye movements, there are indications that our findings may be generalized to eye movements in other situations. In our experiments, the fact that spontaneous eye movements also influence L G B excludes a direct effect o f the stimulation on the L G B neurons, as well as a possible spread o f the stimulus to surrounding structures, such as the reticular formation. On the other hand, as shown by Bizzi 1 the activity o f L G B neurons is modified in a somewhat similar fashion during the rapid eye movements o f sleep. Whether the 'voluntary' eye m o v e m e n t s p e r se also influence these neurons remains to be demonstrated. So far, only cells from the frontal eye fields o f the m o n k e y have been shown to be activated during voluntary eye movements, as well as driven by caloric nystagmus '~. Experimental data from other authors indicate that the excitability o f optic terminals entering the L G B can be modified at the time o f eye movements 8, or by vestibular volleys 9. The 'statistical' character o f the effects in the dark that we have described, as well as their changes in intensity with time, could be explained by Brain Research, 24 (1970) 125-129
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SHORT COMMUNICATIONS
A
B
LIGHT
EM/~-~'~.__.._.~
DARK
I
msec Fig. 3. Poststimulus time histograms of the discharge of two other neurons, as in Fig. 1. The firing pattern of neuron A is shown in Fig. 2.
brief and incomplete presynaptic changes in the tonic retinal input to L G B neurons. Thus, if, as seems likely, L G B changes time-locked with eye movements result f r o m o c u l o m o t o r projections, or at least f r o m projections corresponding to the activation o f o c u l o m o t o r centers, then our results would c o n f o r m with the concept o f ' c o r o l l a r y discharge', understood as the integration o f m o t o r information with the corresponding sensory input 10. Furthermore, the differences observed in some neurons between the responses to o c u l o m o t o r influences in the dark and in the light stress the c o m plexity o f this sensorimotor integration. This work was supported by grants from D.R,M.E. (contract 143-68) and from I.N.S.E.R.M. (Unit6 U.52, Prof. Jouvet). Laboratoire de Mddecine Expdrimentale, Facultd de Mddecine. Lyon (France)
M. JEANNEROD P. T. S. PUTKONEN*
1 Bizzl, E., Discharge patterns of single geniculate neurons during the rapid eye movements of sleep, J. Neurophysiol., 29 (1966) 1087"1095. 2 BIzzl, E., Discharge of frontal eye field neurons during eye movements in unanaesthetized monkeys, Science, 157 (1967) 1588,1590. * Present address: Institute of Physiology, University of Helsinki, Finland. Brain Research, 24 (1970) 125-129
SHORT COMMUNICATIONS
129
3 BusEa, P., ET SEGUNDO, J. P., Influences r6ticulaires, somesth6siques et corticales au niveau du corps genouill6 lat6ral du thalamus chez le chat, C.R. Acad. Sci. (Paris), 249 (1959)571-573. 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 HELMHOLTZ, H. VON, Handbuch der Physiologischen Optik, Vos, Leipzig, 1867. 6 HOTTA, T., AND KAMEDA,K., Interaction between somatic and visual or auditory responses in the thalamus of the cat, Exp. NeuroL, 8 (1963) 1-14. 7 JEANNEROD, M., AND SAKAI, K., Occipital and geniculate potentials related to eye movements in the unanaesthetized cat, Brain Research, 19 (1970) 361-377. 8 KAWAMURA,H., AND MARCHIAFAVA,P. L., Excitability changes along visual pathways during eye tracking movements, Arch. ital. Biol., 106 (1968) 141-156. 9 MARCHIAFAVA,P. L., AND POMPEIANO,O., Excitability changes of the intra-geniculate optic tract fibres produced by electrical stimulation of the vestibular system, Pfliigers Arch. ges. Physiol., 290 (1966) 275-278. l0 TEUBER, H. L., Alterations of perception after brain injury. In J. C. ECCLES (Ed.), Brain and Conscious Experience, Springer, New York, 1966, pp. 182-216. I I VALLEALA,P., Nystagmus and the activity of visual cortex cells, Experientia (Basel), 24 (1968) 358-359. 12 WURTZ, R. H., Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey, J. Neurophysiol., 32 (1969) 987-994. 13 YULES, R. B., ANn GAULT, F. P., The relationship of nystagmus to lateral vestibular nucleus stimulation, Exp. Neurol., 15 (1966)475-483. (Accepted September 4th, 1970)
Brain Research, 24 (1970) 125-129
SHORT COMMUNICATIONS
Oculomotor influences on lateral geniculate body neurons Von Helmholtz was one of the first to point out that the subjective stability of the visual world during self-produced eye movements requires some specific mechanism whereby the 'feelings of innervation' can be taken into account in assigning shifts of the image across the retina to movements of the eyes rather than to displacements of external objects 5. In more recent versions of this idea 10, discharges originating in motor regions are assumed to reach the visual system, and there to enter into the evaluation of those shifts of the retinal image that are caused by voluntary movements of the eyes. Although there are subjective data favoring this hypothesis, the only conclusive evidence would be to show a modification of the activity of visual centers, (a) specifically related to an active displacement of the gaze, and (b) independent of the changes in retinal input resulting from this displacement. Recent experiments in the monkey, performed at the cortical level, failed to detect modifications fulfilling these criteria; according to Wurtz 12, striate cortex neurons are influenced when the eyes move across a patterned visual field, or when an object moves across the retina, but not when the eyes move across an empty field, or in the dark. Valleala 11, however, also using monkeys, has reported, in the absence of light, rhythmic changes in activity of units of area 17 synchronous with post-caloric nystagmus. On the other hand, spontaneous eye movements in cats and monkeys in complete darkness are associated with sharp E E G potentials recorded in the visual cortex and lateral geniculate body (LGB) 4,7. These results both indicate possible oculomotor influences on the visual system, and reinstate the need for a further analysis of the relations between eye movements and vision. LGB, which is known as a site of convergence of extraretinal inputs on the visual system3, 6, was chosen as the target in the present study. LGB neurons were recorded in l0 'enc6phale isol6' cats. Both eyes of the cat were covered with a concave mask, made of black plastic foam, fitted on the face to exclude any possible visual input. The mask cavity could be lit from the inside by a lamp embedded in the foam. When the light was on, it formed a random textured pattern, with a maximal luminance of 6 • 10 4 candle per sq cm. The pupils were dilated with atropine, and both the accommodation paralysis and the short distance (3 cm) between the eyes and the lighted background no doubt resulted in a highly blurred image. Single unit activity was recorded from the left LGB through tungsten microelectrodes, monitored and filmed on an oscilloscope, and stored on an FM tape recorder. Units were identified as geniculate both by their on or off reactions to light, and by histological check of the electrode tracks. Although 'enc6phale isol6' preparations exhibit spontaneous eye movements, direct electrical stimulation of the vestibular nuclei was also used; this procedure, modified from Yules and Gault 13, produced a reliable and long lasting afternystagmus, more suitable for an automatic data analysis. Horizontal eye movements were recorded bipolarly with electrodes implanted in the frontal sinus, using an AC-coupled amplifier (0.02 sec time constant), and stored on another channel of the tape recorder. The data were processed with a multichannel analyzer: the rapid phase of each saccade triggered off cumulative storage of the corresponding unit discharge during the following 400 msec, a duration selected so as Brain Research, 24 (I 970) 125 129
126
SHORT COMMUNICATIONS
to avoid a possible overlap between consecutive saccades. Some 30-200 sweeps were superimposed for each individual unit. realizing a 'poststimulus time" (PST) histogram (2 msec binwidth) of the unit discharge related to the onset of the saccades. The eye movements used to trigger the analysis were then averaged. Finally, the 'PST" histogram and the idealized movement were displayed on an X - Y plotter. Sixty units, from approximately 100 recorded, were processed in this way; 25 of these were influenced by eye movements under conditions of complete darkness. The change in activity could be an increase in discharge rate, represented either by a short burst of spikes, or by a more gradual increase, as shown in Fig. IA. This type of relation was the most frequently encountered, the peak of the PST histogram being related to the late phase of the movement (150-200 msec after the beginning of the saccade). In other units, rather infrequently observed, the discharge rate was decreased, the minimal rate also occurring some 150-200 msec after the onset of the saccade (Figs. 1B and 3A). Often the changes in rate were apparent only statistically, and could not be predicted during the experiment itself. Further, the intensity of the modification could vary with time. as exemplified by the neuron in Fig. 2. When spontaneous eye movements occurred, the discharge rate was modified as well, although this effect could not be studied statistically. When tested with the light on, neurons either showed essentially similar behavior as in the dark. e.g., increase (Fig. IA) or decrease (Fig.
B
A
LIGHT .
I
I
.
DARK
i
i
i! ¸ L rnsec
Fig. 1. Poststimulus time histograms of the discharge of two lateral geniculate body neurons (A, B), in the light and in the dark, as triggered by the beginning of nystagmic saccades. The number Of spikes (n) is given in arbitrary units, per 2 msec bins. EM is an average of the corresponding eye movements. Brain Research, 24 (1970) 125-129
SHORT COMMUNICATIONS
127
A" EM [_G
B
Fig. 2. Pattern of firing of a lateral geniculate body neuron (LG) in relation with the afternystagmus following vestibular stimulation. EM := eye movement recording with a 0.02 sec time constant, with the light on (A) and the light off (B, C). Record B starts immediately after the end of vestibular stimulation. Record C is taken several minutes later, during the late phase of the afternystagmus. 1B) in discharge rate; or a strikingly different pattern, which was the reverse o f the change in rate observed in the dark. This latter type is exemplified in Figs. 2 and 3A, which show the corresponding PST histograms. In addition, one neuron in this series showed a peak in activity in the dark, and no change in the light. The reverse effect (positive relation with the movement in the light only) was more c o m m o n l y observed, which is less surprising (Fig. 3B). Our results clearly show that during eye movements o f vestibular origin, definite changes in activity occur in a significant population o f geniculate neurons, independently o f direct visual input. Although nystagmus is a special case o f eye movements, there are indications that our findings may be generalized to eye movements in other situations. In our experiments, the fact that spontaneous eye movements also influence L G B excludes a direct effect o f the stimulation on the L G B neurons, as well as a possible spread o f the stimulus to surrounding structures, such as the reticular formation. On the other hand, as shown by Bizzi 1 the activity o f L G B neurons is modified in a somewhat similar fashion during the rapid eye movements o f sleep. Whether the 'voluntary' eye m o v e m e n t s p e r se also influence these neurons remains to be demonstrated. So far, only cells from the frontal eye fields o f the m o n k e y have been shown to be activated during voluntary eye movements, as well as driven by caloric nystagmus '~. Experimental data from other authors indicate that the excitability o f optic terminals entering the L G B can be modified at the time o f eye movements 8, or by vestibular volleys 9. The 'statistical' character o f the effects in the dark that we have described, as well as their changes in intensity with time, could be explained by Brain Research, 24 (1970) 125-129
128
SHORT COMMUNICATIONS
A
B
LIGHT
EM/~-~'~.__.._.~
DARK
I
msec Fig. 3. Poststimulus time histograms of the discharge of two other neurons, as in Fig. 1. The firing pattern of neuron A is shown in Fig. 2.
brief and incomplete presynaptic changes in the tonic retinal input to L G B neurons. Thus, if, as seems likely, L G B changes time-locked with eye movements result f r o m o c u l o m o t o r projections, or at least f r o m projections corresponding to the activation o f o c u l o m o t o r centers, then our results would c o n f o r m with the concept o f ' c o r o l l a r y discharge', understood as the integration o f m o t o r information with the corresponding sensory input 10. Furthermore, the differences observed in some neurons between the responses to o c u l o m o t o r influences in the dark and in the light stress the c o m plexity o f this sensorimotor integration. This work was supported by grants from D.R,M.E. (contract 143-68) and from I.N.S.E.R.M. (Unit6 U.52, Prof. Jouvet). Laboratoire de Mddecine Expdrimentale, Facultd de Mddecine. Lyon (France)
M. JEANNEROD P. T. S. PUTKONEN*
1 Bizzl, E., Discharge patterns of single geniculate neurons during the rapid eye movements of sleep, J. Neurophysiol., 29 (1966) 1087"1095. 2 BIzzl, E., Discharge of frontal eye field neurons during eye movements in unanaesthetized monkeys, Science, 157 (1967) 1588,1590. * Present address: Institute of Physiology, University of Helsinki, Finland. Brain Research, 24 (1970) 125-129
SHORT COMMUNICATIONS
129
3 BusEa, P., ET SEGUNDO, J. P., Influences r6ticulaires, somesth6siques et corticales au niveau du corps genouill6 lat6ral du thalamus chez le chat, C.R. Acad. Sci. (Paris), 249 (1959)571-573. 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 HELMHOLTZ, H. VON, Handbuch der Physiologischen Optik, Vos, Leipzig, 1867. 6 HOTTA, T., AND KAMEDA,K., Interaction between somatic and visual or auditory responses in the thalamus of the cat, Exp. NeuroL, 8 (1963) 1-14. 7 JEANNEROD, M., AND SAKAI, K., Occipital and geniculate potentials related to eye movements in the unanaesthetized cat, Brain Research, 19 (1970) 361-377. 8 KAWAMURA,H., AND MARCHIAFAVA,P. L., Excitability changes along visual pathways during eye tracking movements, Arch. ital. Biol., 106 (1968) 141-156. 9 MARCHIAFAVA,P. L., AND POMPEIANO,O., Excitability changes of the intra-geniculate optic tract fibres produced by electrical stimulation of the vestibular system, Pfliigers Arch. ges. Physiol., 290 (1966) 275-278. l0 TEUBER, H. L., Alterations of perception after brain injury. In J. C. ECCLES (Ed.), Brain and Conscious Experience, Springer, New York, 1966, pp. 182-216. I I VALLEALA,P., Nystagmus and the activity of visual cortex cells, Experientia (Basel), 24 (1968) 358-359. 12 WURTZ, R. H., Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey, J. Neurophysiol., 32 (1969) 987-994. 13 YULES, R. B., ANn GAULT, F. P., The relationship of nystagmus to lateral vestibular nucleus stimulation, Exp. Neurol., 15 (1966)475-483. (Accepted September 4th, 1970)
Brain Research, 24 (1970) 125-129