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Eye movement related activity in the visual cortex of dark-reared kittens
Electroencephalography and Clinical Neurophysiology, 1975, 38:295-301 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
295
EYE M O V E M E N T R E L A T E D ACTIVITY IN THE VISUAL CORTEX OF D A R K - R E A R E D KITTENS 1 F. VITAL-DURAND AND M . JEANNEROD Laboratoire de Neurophysiologie exp~rimentale, I N S E R M U 94, 16 avenue Doyen L~pine, 69500 Bron (France) (Accepted for publication: October 14, 1974)
Animals reared in the dark during their early life appear to be blind when tested in a lighted environment (see e.g., Riesen 1965). Correlative anatomical deficits have been extensively described in these animals. Although total visual deprivation during maturation only produces mild changes in the retina (Weiskrantz 1958), upper visual centers can be more deeply altered by this procedure. Changes in the number of cells or in the fine structure of neurons and synapses are found in the lateral geniculate body (Wiesel and Hubel 1963a) and in the superior colliculus (Lund and Lund 1972). In the striate cortex, apical dendrites show a loss of spines, or an alteration in the pattern of spininess (Globus and Scheibel 1967). On the other hand, after a 2-3 month post-natal monocular deprivation in kittens, cortical neurons fail to respond to visual stimuli presented to the deprived eye (Wiesel and Hubel 1963b). Contrastingly, very few studies have been devoted to possible changes in EEG patterns after visual deprivation. Baxter (1966), dealing with spontaneous EEG activity of deprived kittens, reports mostly negative findings. In the present study, however, we focused our attention on EEG transients related to saccadic eye movements. In normal animals scanning visual objects, sharp potentials can be recorded from the visual cortex, concomitant with each ocular saccade (eye movement potentials, EMPs) (Brooks 1968; Jeannerod and Sakai 1970). EMPs which, in the cat, persist when saccades are performed in the dark, have been interpreted as resulting from motor discharges signalling i Supported by INSERM and FRMF (Paris).
shifts of the gaze axis to the visual system (Jeannerod and Sakai 1970; Orban et al. 1972; Sakal 1973) (see Discussion). Similar cortical potentials are also associated with the rapid eye movements of paradoxical sleep (ponto-geniculo-occipital, PGO activity). Visual deprivation in animals was thus considered as a possible paradigm by which to evaluate the contribution of visual experience to these activities. METHODS
Seven kittens from two litters were used. Three kittens were reared in normal laboratory conditions and served as controls. The four others were reared in a dark room from the day of their birth. Darkness was controlled by a photographic film (400 ASA) permanently exposed in the room. Feeding, cleaning and weighing manipulations were done in the dark. At the ages of 15, 16, 18 and 20 weeks respectively, electrodes were implanted in dark-reared kittens under Nembutal anesthesia (35 mg/kg). The eyes were protected from illumination during surgery by wet cotton wool. Steel bipolar transcortical electrodes were inserted in both visual cortices, at the level of the posterolateral gyrus. Electrodes were also inserted in the sensori-motor cortex on one side, in the frontal sinus for recording eye movements, and in the neck muscles for recording EMG activity. A head fixation device was sealed to the skull together with the electrodes. Recording sessions started after 2 days in the dark. Animals were placed in a dark cage, which could be illuminated by continuous or stroboscopic light. EEG, EOG and EMG were recorded on a Grass Polygraph
296
r'. V1TAL-I)URAND AND M. JFANNEROD
(P7), with the usual bandpass. However, EOG was recorded with DC amplifiers in two animals. At the end of the recording period, animals were placed in a lighted environment to study the visual behavior. Standard testing was used to study visual reflexes and visuo-motor responses. In addition, opto-kinetic nystagmus (OKN) was recorded by placing the animal with the head fixed in front of a screen on which black stripes were displaced at various speeds, and with various orientations. The control kittens underwent exactly the same procedures, except darkrearing. RESULTS
Visual behavior Dark-reared kittens were in good general condition, and their growth weight curves were LIGHT
normal, as compared to the control group. The pupillary reaction to light was present, but slow and inComplete. Blinking to light and to a rapidly approaching object was absent. Placing reactions could not be elicited. When placed in a lighted open field, all four kittens behaved like blind animals: they explored mainly with their vibrissae, bumped into obstacles, and were unable to descend from a small platform placed only 10 cm above the floor. This behavioral impairment following dark-rearing has already been mentioned by several authors (e.,q., Wiesel and Hubel 1963b: Riesen 1965). Perception of motion, however, was less altered. OKN could be readily elicited in all four kittens by stripes moving in any direction except downw~trd (see Vital-Durand et a/. 1974). Eve mot~ement potentials ( E M P s ) Frequent saceadic eye movements, either DARK
CONTROL
DARKREARED
Fig. 1. Occipital potentials related to saccadic eye movements (eye movement potentials, EMPs) in one normally reared (control) and one dark-reared kitten. Note decrease in EMP amplitude and change in background activity in the dark-reared kitten, in the light condition. In this and the following figures: E.M. = EOG recording with a DC bandpass; V.C. = visual cortex activity. Vertical calibration marks represent 100 pV.
297
EEG IN VISUALLY DEPRIVED KITTENS
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Fig. 2. Effect of retinal illumination on eye movement potentials (EMPs) in one dark-reared kitten, aged 18 weeks. A: The animal is in the dark. Note an E M P in relation to each saccadic eye movement. B: In the light (between arrows), EMPs are strongly depressed. They reappear immediately when the light is turned off. VCr, VCL right, left visual cortex activity.
spontaneous, or triggered by acoustic stimuli, were recorded when the animals were in the dark. They were apparently normal as to their amplitude and dynamics. Three of the four kittens occasionally presented short episodes of spontaneous nystagmus. However, no sustained nystagmus resembling the so-called ~'amblyopic nystagmus" described in subjects born blind was ever recorded. In the dark, EMPs were clearly recorded in all four dark-reared kittens, associated with each saccade (Figs. 1 and 2). Peak latencies of these potentials were measured with respect to the onset of the corresponding saccade. Comparison of these values with those obtained in one control kitten (Table I) shows that EMP latencies in dark-reared animals are shorter than in the normal kitten, and than in normal adult cats (about 170 msec. Sakai 1973) recorded in the same conditions. We have no explanation of this difference.
In the dark-reared kittens, shifting from dark to light induced a change in background EEG activity of the visual cortex. Background amplitude and frequency tended to increase, and the activity was more "synchronized". Although eye movements were still present, and even at a greater rate than in the dark, EMPs were hardly detectable; they were present, however, but with a considerably reduced amplitude (Fig. 2). For this reason, latencies were not measured under this condition. On returning to darkness, EMPs reappeared immediately (Fig. 2, B). In control kittens, as in normal adult cats, changes in background illumination have the reverse effect: EMPs are generally of greater amplitude in the light than in the dark. Visual cortex responses to flashes of light were obtained in all four dark-reared kittens, with flicker fusion at frequencies around 15 flashes/sec. The mean latency of responses (to the peak of the initial positivity) was about 35 msec.
TABLE 1 Peak latencies in milliseconds for EMPs in one control and four dark-reared kittens. Each value is an average of 50 individual latencies. All animals in the dark.
Control
Peak latency S.D.
188.4 51
Dark-reared 1
2
3
4
104.6 24.5
157.4 63.2
143.9 42.8
131,8 50.5
S.D. : standard deviation.
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Fig, 3. Sleep-waking cycle in one dark-reared kitten, aged 18 weeks. Upper row: waking stage, animal in the dark. S e c o n d row: slow wave sleep. Note slow rolling of the eyes and unusually high voltage activity of the visual cortex. Two lower rows: continuous tracing. Note onset of paradoxical sleep episode. Within a few seconds, rapid eye movements, ponto-geniculooccipital activity in the visual cortex and muscular twitches (EMG from the neck muscles) are clearly observed.
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Fig. 4. Paradoxical sleep episode in one normally reared (A) and one dark-reared kitten (B). In both cases the episode begins about 40 sec after the beginning of the tracing. In A and B, the two rows are continuous. Note similar patterns of rapid eye movements,isolated or in bursts. Also note ponto-geniculo-occipitalactivity in the visual cortex in both kittens. Paradoxical sleep Transition from waking to slow wave sleep was marked, in dark-reared kittens, by the occurrence of sporadic high voltage positivenegative spikes, recorded synchronously from both visual cortices, but absent from the sensorimotor cortex. They were not related to eye movements or to muscular twitches. These "spikes" might correspond to the so-called pseudooccipital foci described in the EEG of children born blind (Kellaway et al. 1955; Jeannerod and Courjon 1964; Harrison et al. 1970). During slow wave sleep, the EEG of darkreared kittens was not different from that of normals. Slow rolling of the eyes was clearly present in the records when the EOG could he recorded with DC amplifiers (Fig. 3). At the onset of paradoxical sleep, the activity
of the visual cortex tended to become progressively desynchronized. However, bursts of slow activity persisted throughout the entire episode. PGO spiking was present but, because of this incomplete desynchronization, was less conspicuous than in control kittens (Fig. 4). On the other hand, rapid eye movements, isolated or in bursts, were present in the dark-reared kittens during each paradoxical sleep episode. Fig. 4 shows the lack of significant difference between paradoxical sleep episodes in a normal (Fig. 4, A), and in a dark-reared kitten (Fig. 4, B). DISCUSSION
One important point made by this study is that EMPs are present in animals totally devoid of visual experience. The appearance of EMPs
300 during ontogeny is thus independent of visual stimulation, and particularly of changes in visual afferentation produced by saccades. This finding fits the hypothesis, already put forward by several authors, that EMPs are related to central mechanisms controlling the execution of saccades (Brooks 1968; Cohen and Feldman 1968; Jeannerod and Sakai 1970). The fact that these signals propagate exclusively to the visual system (lateral geniculate body and visual cortex) leads to the further interpretation that they are part of a visuo-motor process, integrating some characteristics of the saccades (e.g., speed, amplitude) and the resulting visual input. This process would result in adequate localization and stabilization of visual objects. However, the finding that the presence of EMPs is not influenced by visual experience suggests that they should be involved in more elementary mechanisms, such as signalling the occurrence ofa saccade to the visual system (Jung's "timing", 1972) and clearing the visual pathways at the time when new visual information is arriving (Jung's "cancellation", 1972). Decrease in amplitude, or almost complete disappearance, of EMPs in dark-reared animals when they are in the light, is more intriguing. Although we have no direct explanation for this phenomenon, we can suggest that sudden illumination in these animals may produce considerable changes in retinal activity which, in turn, may alter the excitability of cortical neurons and their responsiveness to non-visual inputs. Persistence of PGO waves after visual deprivation from birth is in accordance with the present understanding of this activity, which is known to originate in the brain-stem and to reach the visual system through the lateral geniculate body (Jouvet 1972). In normal kittens, PGO activity appears (in the geniculate) around the third week of age (Bowe-Anders et aL 1974). Deprivation of visual input in adult cats (by enucleation of both eyes)does not prevent cortical PGO waves to occur during paradoxical sleep episodes (Jeannerod et al. 1965). It is thus not surprising that rapid movements, .which are behavioral correlates of PGO activity, are still present in our kittens. This is in accordance with previous studies in monkeys deprived
1:. V H , M . - D U R A N D AND M, JEANNEROI)
of pattern vision: at the age of 18 months these animals have almost normal rapid eye movements (Berger and Meier 1969). A similar result (though more controversial) has also been reported in human subjects born blind (Amadeo and Gomez 1966). SUMMARY
Kittens reared in total darkness from birth were found to be behaviorally blind, when tested at the age of 15 20 weeks. Visual cortex EEGs were recorded with transcortical electrodes. During waking, potentials related to saccadic eye movements (EMPs) were present in the dark. though they were depressed in amplitude in the light. During paradoxical sleep, rapid eye movements, isolated or in bursts, were present at a normal rate, as were occipital waves related to ponto~geniculo-oecipital activity. It is concluded that EMPs during waking and phasic bursts during paradoxical sleep represent central "built in" events uninfluenced by visual experience, RESUME
ACTIVITES
EN RAPPORT
AVEC DES MOUVEMENTS
OCULAIRES. RECUEILLIES DANS LE CORTEX VISUEL DE CHATONS ELEVEg A L'OBSCURITE
Des chatons 61eves dans l'obscurite totale depuis [a naissance paraissent totalement aveugles lorsqu'ils sont test6s vers l"~ge de 15 20 semaines. Chez ces animaux, l'activit6 61ectrique du cortex visuel a 6t~ enregistr6e fi l'aide d'61ectrodes transcorticales. Pendant l'6veil, les potentiels lies aux saccades oculaires [EMPs} 6taient enregistr6s lorsque l'animal ~tait dans l'obscurit6: lorsque l'animal 6tait ~ la lumiere, par contre. leur amplitude 6tait diminu~e. Pendant le sommeil paradoxal, les mo uvements oculaires rapides, isol6s ou en bouff~es. 6taient pr6sents avec une fr6quence normale: de m~me, les pointes occipitales correspondant fi l'activit6 ponto-g6niculooccipitale 6taient pr6sentes. On conclut que les EMPs pendant l'6veil, comme les manifestations phasiques du sommeil paradoxal repr6sentent des ph6nom6nescentraux"pr~programm~s", non influenc6s par l'exp6rience visueUe
EEG IN VISUALLY DEPRIVED KITTENS Thanks are due to Dr. K. Sakai who kindly participated in some of these experiments.
REFERENCES AMADEO, M. and GOMEZ, E. Eye movements, attention and dreaming in subjects with life-long blindness. Canad. psychiat. Ass. J., 1966, II : 501-507. BAXTER, B. Effect of visual deprivation during postnatal maturation on the electroencephalogram of the cat. Exp. Neurol., 1966, 14: 224-237. BEGGER. R. J. and MEIER, G. W. Eye movements during sleep and waking in infant monkeys (Maeaca mulatta) deprived of patterned vision. Develop. Psyehobiol., 1969, 1 : 266-275. BOWE-ANDERS. C., ADRIEN, J. and ROFFWARG, H. Ontogenesis of PGO waves in the lateral geniculate nucleus of the developing kitten, Exp. Neurol., 1974, 43: 242-260. BROOKS, D. C. Waves associated with eye movements in the awake and sleeping cat. Eleetroenceph. elin. Neurophysiol., 1968, 24: 532-541. COHEN. B. and FELDMAN, M. Relationship of electrical activity in pontine reticular formation and lateral geniculate body to rapid eye movements. J. Neurophysiol., 1968, 31: 806-817. GLoaus, A. and SCHEIBEL,A. B. The effect of visual deprivation on cortical neurons. A Golgi study. Exp. Neurol., 1967, 19: 331-345. HARRISON~A., LAIRY,G. C. et LEGER,E. M. EEG et privation visuelle. Electroenceph. clin. NeurophysioL, 1970, 29: 20-37. JEANNEROD, M. et COURJON, J. Les pointes occipitales survenant pendant le sommeil chez l'enfant amblyope. Rev. neurol., 1964, 111: 346-350. JEANNEROD, M. and SAKAL K. Occipital and geniculate potentials related to eye movements in the unanesthetized cat. Brain Res., 1970, 19: 361-377. JEANNEROD,M., MOURET,J. et JOUVET.M. Effets secondaires de la d6-aff6rentation visuelle sur l'activit6 61ectrique
301 phasique ponto-geniculo-occipitale. J. Physiol. (Paris), 1965, 57: 255-256. JOUVET, M. The role of monoamines and acetylcholine containing neurones in the regulation of the sleep-waking cycle. Ergbn. Physiol., 1972, 64: 166-307. JUNG, R. Neurophysiological and psychophysical correlates in vision research. In A. G. KARCZMARand J. C. ECCLES (Eds.), Brain and human behavior. Spinger-Verlag, Berlin, 1972: 209-258. KELLAWAY,P., BLOXSOM,A. and MACGREGOR,M. Occipital spike foci associated with retro-lental fibroplasia and other forms of retinal loss in children. Electroenceph. clin. NeurophysioL, 1955, 7: 469-470. LUND, J. S. and LUND, R. D. The effects of varying periods of visual deprivation on synaptogenesis in the superior colliculus of the rat. Brain Res., 1972, 42: 21-32. ORBAN, G., VANDENBUSSCHE, E. and CALLENS, M. Electrophysiological evidence for the existence of connections between the brainstem oculomotor areas and the visual system in the cat. Brain Res., 1972, 41: 225-229. RtESEN, A. H. Effects of visual deprivation on perceptual functions and the neural substrate. In J. DE AJURIAGUERRA(Ed.), Desaff&entation exp&imentale et clinique. Masson, Paris, 1965: 47~56. SAKAI, K. Phasic electrical activity in the brain associated with eye movement in waking cats. Brain Res., 1973, 56: 135-150. VITAL-DURAND, F., PUTKONEN,P. T. S. and JEANNEROD, M. Motion detection and optokinetic responses in darkreared kittens. Vision Res., 1974, 14: 141-142. WEISKRAr~TZ, L. Sensory deprivation and the cat's optic nervous system. Nature (Lond.), 1958, 181: 1047-1050. W1ESEL,T. N. and HUBEL,D. H. Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. J. Neurophysiol., 1963a, 26: 978-993. WIESEL, T. N. and HUBEL, D. H. Single cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol., 1963b, 26: 1003-1017.
295
EYE M O V E M E N T R E L A T E D ACTIVITY IN THE VISUAL CORTEX OF D A R K - R E A R E D KITTENS 1 F. VITAL-DURAND AND M . JEANNEROD Laboratoire de Neurophysiologie exp~rimentale, I N S E R M U 94, 16 avenue Doyen L~pine, 69500 Bron (France) (Accepted for publication: October 14, 1974)
Animals reared in the dark during their early life appear to be blind when tested in a lighted environment (see e.g., Riesen 1965). Correlative anatomical deficits have been extensively described in these animals. Although total visual deprivation during maturation only produces mild changes in the retina (Weiskrantz 1958), upper visual centers can be more deeply altered by this procedure. Changes in the number of cells or in the fine structure of neurons and synapses are found in the lateral geniculate body (Wiesel and Hubel 1963a) and in the superior colliculus (Lund and Lund 1972). In the striate cortex, apical dendrites show a loss of spines, or an alteration in the pattern of spininess (Globus and Scheibel 1967). On the other hand, after a 2-3 month post-natal monocular deprivation in kittens, cortical neurons fail to respond to visual stimuli presented to the deprived eye (Wiesel and Hubel 1963b). Contrastingly, very few studies have been devoted to possible changes in EEG patterns after visual deprivation. Baxter (1966), dealing with spontaneous EEG activity of deprived kittens, reports mostly negative findings. In the present study, however, we focused our attention on EEG transients related to saccadic eye movements. In normal animals scanning visual objects, sharp potentials can be recorded from the visual cortex, concomitant with each ocular saccade (eye movement potentials, EMPs) (Brooks 1968; Jeannerod and Sakai 1970). EMPs which, in the cat, persist when saccades are performed in the dark, have been interpreted as resulting from motor discharges signalling i Supported by INSERM and FRMF (Paris).
shifts of the gaze axis to the visual system (Jeannerod and Sakai 1970; Orban et al. 1972; Sakal 1973) (see Discussion). Similar cortical potentials are also associated with the rapid eye movements of paradoxical sleep (ponto-geniculo-occipital, PGO activity). Visual deprivation in animals was thus considered as a possible paradigm by which to evaluate the contribution of visual experience to these activities. METHODS
Seven kittens from two litters were used. Three kittens were reared in normal laboratory conditions and served as controls. The four others were reared in a dark room from the day of their birth. Darkness was controlled by a photographic film (400 ASA) permanently exposed in the room. Feeding, cleaning and weighing manipulations were done in the dark. At the ages of 15, 16, 18 and 20 weeks respectively, electrodes were implanted in dark-reared kittens under Nembutal anesthesia (35 mg/kg). The eyes were protected from illumination during surgery by wet cotton wool. Steel bipolar transcortical electrodes were inserted in both visual cortices, at the level of the posterolateral gyrus. Electrodes were also inserted in the sensori-motor cortex on one side, in the frontal sinus for recording eye movements, and in the neck muscles for recording EMG activity. A head fixation device was sealed to the skull together with the electrodes. Recording sessions started after 2 days in the dark. Animals were placed in a dark cage, which could be illuminated by continuous or stroboscopic light. EEG, EOG and EMG were recorded on a Grass Polygraph
296
r'. V1TAL-I)URAND AND M. JFANNEROD
(P7), with the usual bandpass. However, EOG was recorded with DC amplifiers in two animals. At the end of the recording period, animals were placed in a lighted environment to study the visual behavior. Standard testing was used to study visual reflexes and visuo-motor responses. In addition, opto-kinetic nystagmus (OKN) was recorded by placing the animal with the head fixed in front of a screen on which black stripes were displaced at various speeds, and with various orientations. The control kittens underwent exactly the same procedures, except darkrearing. RESULTS
Visual behavior Dark-reared kittens were in good general condition, and their growth weight curves were LIGHT
normal, as compared to the control group. The pupillary reaction to light was present, but slow and inComplete. Blinking to light and to a rapidly approaching object was absent. Placing reactions could not be elicited. When placed in a lighted open field, all four kittens behaved like blind animals: they explored mainly with their vibrissae, bumped into obstacles, and were unable to descend from a small platform placed only 10 cm above the floor. This behavioral impairment following dark-rearing has already been mentioned by several authors (e.,q., Wiesel and Hubel 1963b: Riesen 1965). Perception of motion, however, was less altered. OKN could be readily elicited in all four kittens by stripes moving in any direction except downw~trd (see Vital-Durand et a/. 1974). Eve mot~ement potentials ( E M P s ) Frequent saceadic eye movements, either DARK
CONTROL
DARKREARED
Fig. 1. Occipital potentials related to saccadic eye movements (eye movement potentials, EMPs) in one normally reared (control) and one dark-reared kitten. Note decrease in EMP amplitude and change in background activity in the dark-reared kitten, in the light condition. In this and the following figures: E.M. = EOG recording with a DC bandpass; V.C. = visual cortex activity. Vertical calibration marks represent 100 pV.
297
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Fig. 2. Effect of retinal illumination on eye movement potentials (EMPs) in one dark-reared kitten, aged 18 weeks. A: The animal is in the dark. Note an E M P in relation to each saccadic eye movement. B: In the light (between arrows), EMPs are strongly depressed. They reappear immediately when the light is turned off. VCr, VCL right, left visual cortex activity.
spontaneous, or triggered by acoustic stimuli, were recorded when the animals were in the dark. They were apparently normal as to their amplitude and dynamics. Three of the four kittens occasionally presented short episodes of spontaneous nystagmus. However, no sustained nystagmus resembling the so-called ~'amblyopic nystagmus" described in subjects born blind was ever recorded. In the dark, EMPs were clearly recorded in all four dark-reared kittens, associated with each saccade (Figs. 1 and 2). Peak latencies of these potentials were measured with respect to the onset of the corresponding saccade. Comparison of these values with those obtained in one control kitten (Table I) shows that EMP latencies in dark-reared animals are shorter than in the normal kitten, and than in normal adult cats (about 170 msec. Sakai 1973) recorded in the same conditions. We have no explanation of this difference.
In the dark-reared kittens, shifting from dark to light induced a change in background EEG activity of the visual cortex. Background amplitude and frequency tended to increase, and the activity was more "synchronized". Although eye movements were still present, and even at a greater rate than in the dark, EMPs were hardly detectable; they were present, however, but with a considerably reduced amplitude (Fig. 2). For this reason, latencies were not measured under this condition. On returning to darkness, EMPs reappeared immediately (Fig. 2, B). In control kittens, as in normal adult cats, changes in background illumination have the reverse effect: EMPs are generally of greater amplitude in the light than in the dark. Visual cortex responses to flashes of light were obtained in all four dark-reared kittens, with flicker fusion at frequencies around 15 flashes/sec. The mean latency of responses (to the peak of the initial positivity) was about 35 msec.
TABLE 1 Peak latencies in milliseconds for EMPs in one control and four dark-reared kittens. Each value is an average of 50 individual latencies. All animals in the dark.
Control
Peak latency S.D.
188.4 51
Dark-reared 1
2
3
4
104.6 24.5
157.4 63.2
143.9 42.8
131,8 50.5
S.D. : standard deviation.
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Fig, 3. Sleep-waking cycle in one dark-reared kitten, aged 18 weeks. Upper row: waking stage, animal in the dark. S e c o n d row: slow wave sleep. Note slow rolling of the eyes and unusually high voltage activity of the visual cortex. Two lower rows: continuous tracing. Note onset of paradoxical sleep episode. Within a few seconds, rapid eye movements, ponto-geniculooccipital activity in the visual cortex and muscular twitches (EMG from the neck muscles) are clearly observed.
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Fig. 4. Paradoxical sleep episode in one normally reared (A) and one dark-reared kitten (B). In both cases the episode begins about 40 sec after the beginning of the tracing. In A and B, the two rows are continuous. Note similar patterns of rapid eye movements,isolated or in bursts. Also note ponto-geniculo-occipitalactivity in the visual cortex in both kittens. Paradoxical sleep Transition from waking to slow wave sleep was marked, in dark-reared kittens, by the occurrence of sporadic high voltage positivenegative spikes, recorded synchronously from both visual cortices, but absent from the sensorimotor cortex. They were not related to eye movements or to muscular twitches. These "spikes" might correspond to the so-called pseudooccipital foci described in the EEG of children born blind (Kellaway et al. 1955; Jeannerod and Courjon 1964; Harrison et al. 1970). During slow wave sleep, the EEG of darkreared kittens was not different from that of normals. Slow rolling of the eyes was clearly present in the records when the EOG could he recorded with DC amplifiers (Fig. 3). At the onset of paradoxical sleep, the activity
of the visual cortex tended to become progressively desynchronized. However, bursts of slow activity persisted throughout the entire episode. PGO spiking was present but, because of this incomplete desynchronization, was less conspicuous than in control kittens (Fig. 4). On the other hand, rapid eye movements, isolated or in bursts, were present in the dark-reared kittens during each paradoxical sleep episode. Fig. 4 shows the lack of significant difference between paradoxical sleep episodes in a normal (Fig. 4, A), and in a dark-reared kitten (Fig. 4, B). DISCUSSION
One important point made by this study is that EMPs are present in animals totally devoid of visual experience. The appearance of EMPs
300 during ontogeny is thus independent of visual stimulation, and particularly of changes in visual afferentation produced by saccades. This finding fits the hypothesis, already put forward by several authors, that EMPs are related to central mechanisms controlling the execution of saccades (Brooks 1968; Cohen and Feldman 1968; Jeannerod and Sakai 1970). The fact that these signals propagate exclusively to the visual system (lateral geniculate body and visual cortex) leads to the further interpretation that they are part of a visuo-motor process, integrating some characteristics of the saccades (e.g., speed, amplitude) and the resulting visual input. This process would result in adequate localization and stabilization of visual objects. However, the finding that the presence of EMPs is not influenced by visual experience suggests that they should be involved in more elementary mechanisms, such as signalling the occurrence ofa saccade to the visual system (Jung's "timing", 1972) and clearing the visual pathways at the time when new visual information is arriving (Jung's "cancellation", 1972). Decrease in amplitude, or almost complete disappearance, of EMPs in dark-reared animals when they are in the light, is more intriguing. Although we have no direct explanation for this phenomenon, we can suggest that sudden illumination in these animals may produce considerable changes in retinal activity which, in turn, may alter the excitability of cortical neurons and their responsiveness to non-visual inputs. Persistence of PGO waves after visual deprivation from birth is in accordance with the present understanding of this activity, which is known to originate in the brain-stem and to reach the visual system through the lateral geniculate body (Jouvet 1972). In normal kittens, PGO activity appears (in the geniculate) around the third week of age (Bowe-Anders et aL 1974). Deprivation of visual input in adult cats (by enucleation of both eyes)does not prevent cortical PGO waves to occur during paradoxical sleep episodes (Jeannerod et al. 1965). It is thus not surprising that rapid movements, .which are behavioral correlates of PGO activity, are still present in our kittens. This is in accordance with previous studies in monkeys deprived
1:. V H , M . - D U R A N D AND M, JEANNEROI)
of pattern vision: at the age of 18 months these animals have almost normal rapid eye movements (Berger and Meier 1969). A similar result (though more controversial) has also been reported in human subjects born blind (Amadeo and Gomez 1966). SUMMARY
Kittens reared in total darkness from birth were found to be behaviorally blind, when tested at the age of 15 20 weeks. Visual cortex EEGs were recorded with transcortical electrodes. During waking, potentials related to saccadic eye movements (EMPs) were present in the dark. though they were depressed in amplitude in the light. During paradoxical sleep, rapid eye movements, isolated or in bursts, were present at a normal rate, as were occipital waves related to ponto~geniculo-oecipital activity. It is concluded that EMPs during waking and phasic bursts during paradoxical sleep represent central "built in" events uninfluenced by visual experience, RESUME
ACTIVITES
EN RAPPORT
AVEC DES MOUVEMENTS
OCULAIRES. RECUEILLIES DANS LE CORTEX VISUEL DE CHATONS ELEVEg A L'OBSCURITE
Des chatons 61eves dans l'obscurite totale depuis [a naissance paraissent totalement aveugles lorsqu'ils sont test6s vers l"~ge de 15 20 semaines. Chez ces animaux, l'activit6 61ectrique du cortex visuel a 6t~ enregistr6e fi l'aide d'61ectrodes transcorticales. Pendant l'6veil, les potentiels lies aux saccades oculaires [EMPs} 6taient enregistr6s lorsque l'animal ~tait dans l'obscurit6: lorsque l'animal 6tait ~ la lumiere, par contre. leur amplitude 6tait diminu~e. Pendant le sommeil paradoxal, les mo uvements oculaires rapides, isol6s ou en bouff~es. 6taient pr6sents avec une fr6quence normale: de m~me, les pointes occipitales correspondant fi l'activit6 ponto-g6niculooccipitale 6taient pr6sentes. On conclut que les EMPs pendant l'6veil, comme les manifestations phasiques du sommeil paradoxal repr6sentent des ph6nom6nescentraux"pr~programm~s", non influenc6s par l'exp6rience visueUe
EEG IN VISUALLY DEPRIVED KITTENS Thanks are due to Dr. K. Sakai who kindly participated in some of these experiments.
REFERENCES AMADEO, M. and GOMEZ, E. Eye movements, attention and dreaming in subjects with life-long blindness. Canad. psychiat. Ass. J., 1966, II : 501-507. BAXTER, B. Effect of visual deprivation during postnatal maturation on the electroencephalogram of the cat. Exp. Neurol., 1966, 14: 224-237. BEGGER. R. J. and MEIER, G. W. Eye movements during sleep and waking in infant monkeys (Maeaca mulatta) deprived of patterned vision. Develop. Psyehobiol., 1969, 1 : 266-275. BOWE-ANDERS. C., ADRIEN, J. and ROFFWARG, H. Ontogenesis of PGO waves in the lateral geniculate nucleus of the developing kitten, Exp. Neurol., 1974, 43: 242-260. BROOKS, D. C. Waves associated with eye movements in the awake and sleeping cat. Eleetroenceph. elin. Neurophysiol., 1968, 24: 532-541. COHEN. B. and FELDMAN, M. Relationship of electrical activity in pontine reticular formation and lateral geniculate body to rapid eye movements. J. Neurophysiol., 1968, 31: 806-817. GLoaus, A. and SCHEIBEL,A. B. The effect of visual deprivation on cortical neurons. A Golgi study. Exp. Neurol., 1967, 19: 331-345. HARRISON~A., LAIRY,G. C. et LEGER,E. M. EEG et privation visuelle. Electroenceph. clin. NeurophysioL, 1970, 29: 20-37. JEANNEROD, M. et COURJON, J. Les pointes occipitales survenant pendant le sommeil chez l'enfant amblyope. Rev. neurol., 1964, 111: 346-350. JEANNEROD, M. and SAKAL K. Occipital and geniculate potentials related to eye movements in the unanesthetized cat. Brain Res., 1970, 19: 361-377. JEANNEROD,M., MOURET,J. et JOUVET.M. Effets secondaires de la d6-aff6rentation visuelle sur l'activit6 61ectrique
301 phasique ponto-geniculo-occipitale. J. Physiol. (Paris), 1965, 57: 255-256. JOUVET, M. The role of monoamines and acetylcholine containing neurones in the regulation of the sleep-waking cycle. Ergbn. Physiol., 1972, 64: 166-307. JUNG, R. Neurophysiological and psychophysical correlates in vision research. In A. G. KARCZMARand J. C. ECCLES (Eds.), Brain and human behavior. Spinger-Verlag, Berlin, 1972: 209-258. KELLAWAY,P., BLOXSOM,A. and MACGREGOR,M. Occipital spike foci associated with retro-lental fibroplasia and other forms of retinal loss in children. Electroenceph. clin. NeurophysioL, 1955, 7: 469-470. LUND, J. S. and LUND, R. D. The effects of varying periods of visual deprivation on synaptogenesis in the superior colliculus of the rat. Brain Res., 1972, 42: 21-32. ORBAN, G., VANDENBUSSCHE, E. and CALLENS, M. Electrophysiological evidence for the existence of connections between the brainstem oculomotor areas and the visual system in the cat. Brain Res., 1972, 41: 225-229. RtESEN, A. H. Effects of visual deprivation on perceptual functions and the neural substrate. In J. DE AJURIAGUERRA(Ed.), Desaff&entation exp&imentale et clinique. Masson, Paris, 1965: 47~56. SAKAI, K. Phasic electrical activity in the brain associated with eye movement in waking cats. Brain Res., 1973, 56: 135-150. VITAL-DURAND, F., PUTKONEN,P. T. S. and JEANNEROD, M. Motion detection and optokinetic responses in darkreared kittens. Vision Res., 1974, 14: 141-142. WEISKRAr~TZ, L. Sensory deprivation and the cat's optic nervous system. Nature (Lond.), 1958, 181: 1047-1050. W1ESEL,T. N. and HUBEL,D. H. Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. J. Neurophysiol., 1963a, 26: 978-993. WIESEL, T. N. and HUBEL, D. H. Single cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol., 1963b, 26: 1003-1017.