Maturation of the optokinetic response: Genetic and environmental factors

Brain Research, 71 (1974) 249-257

249

© Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands

Colloque C.N.R.S. no. 226 Comportement moteur et activit6s nerveuses programm6es Aix-en-Provence, 7-9 sept. 1973

M A T U R A T I O N OF T H E O P T O K I N E T I C E N V I R O N M E N T A L FACTORS

F. V I T A L - D U R A N D

AND M.

RESPONSE:

GENETIC

AND

JEANNEROD

Laboratoire de Neuropsychologie Expdrimentale, Unitd de Recherches U 94, INSERM, 69500 Bron (France)

SUMMARY

Oculomotor responses to displacement o f the visual field (optokinetic nystagmus, OKN) were studied in two groups of kittens. Kittens from the first group were reared in total darkness up to the 19th week o f age (dark-reared group). Kittens from the other group were reared in total darkness up to the 4th week and then exposed 1 h a day (during up to 60 h o f total exposure time) to a continuously moving visual environment. Direction of movement varied from kitten to kitten, but was constant for each individual ('unidirectional' group). At the age o f about 20 weeks all kittens were implanted with electrodes for recording eye movements, and O K N was tested with stripes o f varied orientation, moving at different speeds. Kittens from the dark-reared group, in spite o f being behaviorally blind, exhibited O K N in response to stripes moving in any direction, except downward. The response was obtained when the stripes moved slowly, and tended to be disorganized and to disappear when movement became faster. Kittens from the unidirectional group systematically exhibited a better response for stripes moving in the direction to which they had been exposed: OKN persisted as long as stimulation was maintained and was adapted to the speed o f the stripes. Contrastingly, for stripes moving in other directions, O K N was not always present and could not adapt to speed.

PJ~UM~ Les r6ponses oculomotrices au d6placement du champ visuel (nystagmus opto-

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cin6tique, NOK) ont 6t6 6tudi6es chez deux groupes de chatons. Les chatons du premier groupe ont 6t6 61ev6s darts l'obscurit6 totale jusqu'h la 19~me semaine postnatale (groupe 61ev6 au noir). Les chatons de l'autre groupe ont 6t6 61ev6s dans l'obscurit6 jusqu'~t la quatri6me semaine post-natale, puis expos6s 1 h par jour (dur6e maximum d'exposition: 60 h) h u n d6placement continu de l'environnement visuel. La direction du d6placement de l'environnement pouvait varier d'un chaton ~ l'autre, mais 6tait constante pour un chaton donn6 (groupe 'uni-directionnel'). A l'~ge de 20 semaines environ, tousles chatons ont 6t6 implant6s avec des 61ectrodes pour enregistrer les mouvements oculaires, et le NOK a 6t6 test6 ~ l'aide de bandes noires et blanches, pouvant se d6placer dans n'importe quelle direction et ~t n'importe quelle vitesse. Les chatons du groupe 61ev6 au noir, bien que comportementalement aveugles, pr6sentaient un N O K en r6ponse ~ des bandes se d6plaqant dans toutes les directions, saul vers le bas. Toutefois, cette r6ponse n'6tait obtenue que si les bandes se d6plaqaient lentement. Elle se d6sorganisait ou disparaissait quand le d6placement des bandes devenait plus rapide. Les chatons du groupe uni-directionnel pr6sentaient syst6matiquement une r6ponse meilleure pour des bandes se d6plaqant dans la direction laquelle ils avaient 6t6 expos6s: le N O K persistait alors aussi longtemps que la stimulation 6tait maintenue et sa fr6quence 6tait en corr61ation avec la vitesse du d6placement des bandes. Par contre, lorsque les bandes se d6pla~aient dans une autre direction le N O K n'apparaissait pas toujours; et lorsqu'il se produisait il ne s'adaptait pas h la vitesse du d6placement des bandes, sa fr6quence et son amplitude restant plus faibles que dans la direction correspondant ~t l'exposition.

Development of vision provides a convenient model for interactions between the external world and brain structures, for two principal reasons. First, the visual modality is unique in the degree to which afferent processes may be controlled experimentally. Second, the experimenter has access both to neuronal activity reflecting central processing of visual information, and to corresponding behavioral responses, such as ocular movements. Thus, experimental control (by selective restriction or enhancement) of visual information available to animals during their early life may provide cues as to how the appearance of certain visual abilities are influenced by environmental stimulation. For instance, in kittens that are permitted to view only vertical lines, cortical neurons respond exclusively to vertically oriented contours ~,2,s. Perception is also impaired by this procedure, since these kittens evidence difficulties in learning pattern discrimination 3,5. To be effective, ,this selective exposure must occur between the fourth and the sixteenth weeks of age 2,1°. Hein and Held 6 have demonstrated the importance of motor visual feedback for the development of visually guided behavior. However, one may ask whether the development of all visuo-motor responses depend on visual experience. Some types of 'elementary' behaviors appear fully organized at birth, relying upon innate reflexive mechanisms. For instance, optokinetic nystagmus (OKN), a sequence of slow pursuit movements in the direction of the stimulus motion which alternate with saccades in the opposite direction, is considered an unlearned reflex response 1~,x3.

MATURATION OF THE OPTOKINETIC RESPONSE

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In the present study, we have investigated O K N in two groups o f kittens. One group was reared in total darkness, and the other was exposed in light only when the visual field was moving in one direction. Differences in optokinetic responses between these two groups may clarify the relative contribution o f genetic and environmental factors in shaping the ocular response to visual motion. Twenty kittens from 6 litters were used in this study. During the initial stage of rearing, all kittens were kept in complete darkness. All the manipulations, including weekly weighing, were done in the dark. When they were 4 weeks old, the litters were separated into two groups. One group consisting o f two litters were kept in the dark until testing (dark-reared group). Kittens in the second group o f 4 litters were exposed individually to unidirectional motion o f the visual field, for 1 h a day, 6 days a week (unidirectional group). They spent the rest o f the time in the dark. During exposure, the animal was placed in the center o f an opaque cylinder (1 m high and 50 cm in diameter) painted with vertical black and white stripes (10 cm side), and diffusely illuminated (11.10 -4 cd/sq, cm). Some of the animals were free to move within a transparent cylindrical container which was suspended within the opaque cylinder. Other animals were restrained in a device which positioned the head at the center o f the cylinder. In both cases, the animals wore light collars to prevent view of the limbs. The cylinder was rotated at a constant speed (60°/sec). Rotation was always in the same direction for a given kitten. Nine kittens were exposed in a vertical cylinder; 5 o f them experienced rightward visual motion, and the 4 others, leftward motion. Four kittens were exposed in a horizontal cylinder: two kittens experienced upward visual motion, and the two others, downward motion. Exposure time was from 10 to 60 h and was provided between the 4th and the 17th week. Neither duration o f exposure nor age significantly affected the results. When the kittens were about 17 weeks old, they were anesthetized with pentobarbital (35 mg/kg i.p.), electrodes for recording eye movements and a head fixation device were fixed to their skulls. Several days later, O K N was tested with the head fixed. Stripes of the same visual angle were projected on a screen in front of the animal. Displacement of the stripes was obtained by moving a film loop at the focus of a projector lens. A DC motor permitted stimulation within a broad range of velocities, and immediate reversal of the direction of the movement. Additionally, single neuron activity in the superior colliculi o f 4 kittens in the unidirectional group was investigated. The animals were lightly anesthetized (pentobarbital 30 mg/kg i.p. and Novocaine infusion at the pressure points) and held in a frame. Pupils were dilated with atropine sulfate, and the eyes were protected from drying with corneal lenses. Unit activity was recorded with tungsten microelectrodes, and displayed on an oscilloscope and an audiomonitor. The screen on which luminous targets were projected was 1 m from the eyes.

(I) Dark-reared kittens Kittens from the dark-reared group were tested between the fifteenth and the

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nineteenth weeks of age. When placed in a lighted environment the animals appeared blind. They explored the surrounds with their vibrissae, bumped into stationary obstacles, and would not descend from a small platform only 10 cm high. This effect of dark rearing has been reported by a number of authors 4,13,ts together with inability to learn a pattern discrimination task. Our kittens, however, clearly displayed motion detection. They were able to fixate a small visual target and showed refixation movements of their head and eyes and occasionally struck at it with a forepaw if the target was moved at moderate speed. Yet, they lost the target quite frequently and apparently could not estimate depth, since they reached for distant and close targets alike. O K N was easily obtained in all 7 kittens, and persisted with no sign of habituation for testing periods of up to 20 min. The frequency of ocular saccades was correlated to the velocity of moving stripes in a range from 0.5 to about 1.6 black stripes/sec (5 degrees to about 15 degrees/sec). At higher velocities the nystagmus became disorganized, slowed, and tended to vanish. When stripes were vertical, reversing the direction of movement was promptly followed by a reversal of the direction of saccades. When stripes were horizontal, only stripes moving upward could elicit nystagmus t7 (Fig. 1).

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Fig. 1. Evaluation of optokinetic responses to stimuli moving in different directions, in 5 different kittens from the two experimental groups. Insert on the right of each diagram indicates the rearing condition of the corresponding kitten: DR, dark-reared. For the 4 others, direction of the arrow indicates the direction of visual motion experienced during exposure sessions. The mean number of saccades per 25 sec epoch is plotted for each direction of stimulation (R, rightward, L, leftward, U, upward, D, downward). Epochs from different stimulation velocities are cumulated.

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Fig. 2. Relationship of saccade frequency in optokinetic nystagmus, and velocity of passing stripes in one kitten from the unidirectional group. In this and the following figure, eye movements are recorded on a polygraph, with a 0.24 see time constant; upper deflexion indicates a movement to the right. Animal has its head fixed. Upper row: stripes move in the 'experienced' direction (rightward). Note increase in saccade frequency when the stripe velocity is increased (S, frequency of stripes recorded by a photocell). Lower row: stripes move in the opposite direction. Note decrease in saccade frequency when the stripe velocity is increased. Diagram on the right: plot of saccad¢ frequency (N) during 25 sec epochs, against the frequency of passing stripes (F). In our experiments, an increase in stripe frequency corresponds to an increase in stripe velocity. Black circles: saccade frequency when the stripes move in the 'experienced' direction at various velocities. The heavy line represents the corresponding regression line (r, 0.80, P > 0.001). Open circles: saccade frequency when the stripes move in the opposite direction, at various velocities. Dotted line, corresponding regression line (r, 0.36, n.s.).

(II) Kittens exposed to unidirectional visual motion Optokinetic responses Animals were tested a r o u n d the 18th week o f age. Several characteristics o f the O K N were differentiated by the direction o f stripes movement. Kittens which had been exposed to horizontal m o t i o n readily exhibited O K N when they were stimulated with stripes moving in the direction (i.e., rightward or leftward) that they had experienced. Frequency o f nystagmic saccades increased as stripe velocity increased and the relation held up to 5 stripes/sec for most kittens, and even to 8 stripes/sec for two o f them. These velocities exceed that presented during exposure sessions (Fig. 2). In addition, O K N persisted as long as stimulation was maintained. W h e n the animals were presented with stripes moving in the direction opposite to the 'experienced' direction, the initial saccades were erratic and oriented in all directions. After some time, the animals displayed rhythmic saccades with normal orientation but low amplitude and frequency. These rhythmic saccades were elicited only by low stripe velocities (Fig. 2). Fig. 3 represents the effects o f sudden reversals o f stripes movement. When m o v e m e n t was shifted f r o m the 'experienced' direction to its opposite, O K N did not stop immediately; saccades with the same orientation and at a similar fre-

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Fig. 3. Effects of reversal of the stripes motion on optokinetic responses, in two kittens from the unidirectional group. ÷ Signs below the tracings refer to stimulation by stripes moving in the 'experienced' direction, and -- signs, by stripes moving in the opposite direction. Arrows indicate the exact time of reversal. Upper row: two lines of continuous recording from one kitten exposed for 60 h to a leftward visual motion. Lower row: recording from one kitten exposed for 25 h to a rightward visual motion. Note difference in time scale between the two rows. Frequency of stripes is indicated below each row.

quency usually persisted for several seconds (as if the animal had not 'noticed' the shift in direction). This resembles optokinetic after-nystagmus, which may be observed in normal animals when the light is suddenly turned off during stimulation by moving stripes 9. O K N of correct orientation reappeared almost immediately with a fast rise in saccade frequency when the direction o f the stripes was returned to the experienced direction 16. Kittens reared with exposure to horizontal visual motion exhibited O K N when stimulated by stripes moving upward but not downward. This absence of O K N in response to downward motion was the same as noted in the dark-reared group. The same asymmetry in response to vertically moving stripes was observed in the kittens from the group exposed to vertical visual motion either upward or downward. All animals in this group displayed O K N when stimulated by stripes moving upward but failed to respond to downward motion (Fig. 1).

Neuronal responses in the superior colliculi Neurons from both colliculi were investigated in 4 of the kittens exposed to rightward visual motion. Retinotopic projection of these neurons on the collicular surface was normal, as were the characteristics o f their receptive fields. Among the

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MATURATION OF THE OPTOKINETIC RESPONSE

LEFT

RIGHT

Fig. 4. Preferred directions of collicular neurons in 4 kittens from the unidirectional group (exposed to rightward motion). The two circles represent the right and the left superior colliculus, respectively. Each arrow indicates the direction of a moving stimulus preferred by a single neuron. Results from the 4 kittens are cumulated.

104 neurons studied, 43 displayed a strong preference to one direction o f movement. Of the 24 directionally selective neurons recorded from the right colliculus, 20 responded maximally to leftward movements within 45 ° from horizontal (Fig. 4). In the left colliculus, 19 neurons were directionally selective; 11 responded to stimuli moving toward the left and 4 to stimuli moving upward. Only 4 preferred the rightward direction (Fig. 4). In normal cats14,1~, as in our experimental animals, units in the right colliculus are directionally selective for leftward movements. Units recorded in the left colliculus o f normal animals are maximally responsive to rightward movement in contrast to our experimental animals in which the units preferred leftward movements. We expected that, in kittens that had been exposed to rightward visual motion, the predominant neural response would be to rightward motion. However, 75 ~o of the units preferred leftward movement. It is possible that long exposure to rightward motion would elicit more saccadic eye and head movements to the left than to the right. If so, our findings suggest that collicular neurons could have been more influenced by displacements o f the visual field during saccades than during slow ocular pursuit. Deprivation of visual input during the neonatal period is one technique which helps to clarify the contribution of genetic factors to the development of visuo-motor behavior. From the present experiments, we conclude that the neural substrates for motion detection and oculomotor response to moving stimuli can mature without visual experience (see also ref. 13). However, the anomalies in the O K N observed in all members o f our experimental groups reveal that development o f these capacities is not totally independent o f early experience. The observed asymmetry of O K N

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c a n n o t be explained by a defect in visual acuity, since a reduction o f acuity would alter responses in all directions o f movement. Neuronal correlates o f the asymmetrical O K N displayed by our kittens might be f o u n d in the visual system. F o r instance, a retarded maturation o f detectors for m o v e m e n t in one direction in the corresponding colliculus could explain the absence o f accuracy o f O K N in this direction. There is no direct support for this explanation in our results, since a similar n u m b e r o f directional neurons are found in both colliculi. The findings are more compatible with the one that neurons with direction potentiality have been altered by the early exposure, or that neurons devoid o f potentiality have been specified by this pressure 12. However, the small n u m b e r o f units recorded does not allow the elimination o f the possibility that there has been loss o f detectors for m o v e m e n t in one direction is. A series o f studies utilizing neonatal kittens indicate that visually coordinated behavior may be segregated into separated components by the technique o f selective exposure to light 7. F o r example, Hein and Held 6 demonstrated that visual placing o f the forelimbs to a broad surface can be elicited in an animal that has never previously seen its limbs, but precise guidance o f the paw to a small target requires a history o f exposure with opportunity to view the moving limbs. The results o f the present experiment reveal ability to respond (presence o f O K N , as in the dark-reared group) and ability to adapt (accuracy o f O K N ) as two additional components o f the visually coordinated behavior. We wish to thank Prof. A. Hein, D e p a r t m e n t o f Psychology, M.I.T., Cambridge, U.S.A., for carefully reading and commenting on our manuscript. This study was sponsored by I N S E R M and F R M F , Paris.

1 BLAKEMORE,C., Environmental constraints on development in the visual system. In R. A. HINDE

ANDJ. STEVENSON-HINDE(Eds.), Constraints on Learning, Academic Press, London, 1973,pp. 51-73. 2 BLAKEMORE,C., AND COOPER, G. F., Development of the brain depends on the visual environment,

Nature (Lond.), 228 (1970) 477-478. 3 DEWS, P. B., AND WIESEL, T. N., Consequences of monocular deprivation on visual behavior in kittens, J. Physiol. (Lond.), 206 (1970) 437-455. 4 GANZ, L., AND FITCH, M., The effect of visual deprivation on perceptual behavior, Exp. Neurol., 22 (1968) 638-660. 5 GANZ, L., HIRSCH,H. V. B., AND BLISS=TIEMAN, S., The nature of perceptual deficits in visually deprived cats, Brain Research, 44 (1972) 547-568. 6 HEIN, A., AND HELD, R., Dissociation of the visual placing response into elicited and guided components, Science, 158 (1967) 390-392. 7 HEIN, A., AND DIAMOND, R., Locomotory space as a prerequisite for acquiring visually guided reaching in kittens, J. comp. physiol. Psychol., 81 (1972) 394-398. 8 HIRSCH,H. V. B., AND SP1NELLI, D. N., Modification of the distribution of receptive field orientation in cats by selective visual exposure during development, Exp. Brain Res., 13 (1971) 509-527. 9 HONRUBIA,V,, SCOTT,B. J., AND WARD, P. H., Experimental studies on optokinetic nystagmus, I. Normal cats, Acta oto-laryng. (Stockh.), 64 (1967) 388-402. 10 HUrtLE, D. H., AND WIESEL, T . N . , The period of susceptibility to the physiological effects of unilateral eye closure in kittens, J. Physiol. (Lond.), 206 (1970) 419-436. 11 PASIK,T., AND PASIK,P., Optokinetic nystagmus: an unlearned response altered by section of chiasma and corpus callosum in monkeys, Nature (Lond.), 203 (1964) 609-611.

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12 PETTIGREW,J. D., OLSON,C., AND HIRSCH, H. V. B., Cortical effect of selective visual experience: degeneration or reorganization? Brain Research, 51 (1973) 345-351. 13 RIESEN,A. H., Effects of visual deprivation on perceptual functions and the neural substrate. In J. DE AJURIAGUERRAtEd.), Ddsaffdrentation expdrimentale et clinique, Masson, Paris, 1965, pp. 47-66. 14 STERLINO,P., AND WICKELGREN,B. G., Visual receptive fields in the superior coIliculus in the cat, J. Neurophysiol., 32 (1969) 1-15. 15 STRASCHILL,M., AND HOFFMANN,K. P., Relationship between localization and functional properties of movement sensitive neurons of the cat's tectum opticum, Brain Research, 8 (1968) 382-385. 16 VITAL-DURAND,F., AND JEANNEROD,M., Role of visual experience in the development of optokinetic responses in kittens, Exp. Brain Res., (1974) in press. 17 VITAL-DURAND,F., PUTKONEN, P. T. S., AND JEANNEROD,M., Motion detection and optokinetic responses in dark reared kittens, Vision Rex., 14 (1974) 141-142. 18 WIESEL,T. N., AND HUBEL, O. H., Single cell responses in striate cortex of kittens deprived of vision in one eye, J. Neurophysiol., 26 (1963) 1003-1019.