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Modification of direction selectivity of neurons in the visual cortex of kittens
Brain Research, 84 (1975) 143-149 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
143
Modification of direction selectivity of neurons in the visual cortex of kittens
F. TRETTER, M. CYNADER AND W. SINGER Max Planck Institute for Psychiatry, 8000 Munich 40 (G.F.R.)
(Accepted October 21st, 1974)
Accumulating evidence suggests that the development of the cat visual system is dependent on visual experience. Visual deprivation results in the loss of functional specificity in cortical neurons6,10, 22 and it is possible to cause specific and long lasting changes in the functional properties of cortical neurons 2,3,7,8,11-13,~7,21 by brief selective exposure during the critical period. In particular, it has been shown that cortical neurons become orientation-selective in the same axis as the visual stimuli presented during exposure3,8,13. If exposed to stimuli which lack orientation cues, cortical cells lose or fail to develop orientation specificity H. Cortical units in mature cats are sensitive not only to specific shapes but also selective for the speed and the direction of moving contrasts. It has recently been shown as well, that stimulus movement is a crucial parameter in the development of such normal cortical selectivity 4. With these considerations in mind, we therefore attempted to determine the extent to which dynamic R F properties such as direction selectivity and velocity tuning can be modified by selective visual exposure. Kittens which had been reared with both eyes occluded from birth were exposed, beginning at the age of 4 weeks, to vertically oriented stripes which covered the entire visual field and moved in only one direction. The kittens were placed in a restraining chair which prevented them from rotating or inclining their heads. The chair was mounted in the center of a rotating drum the walls of which were covered with a grating. The pattern had a uniform spatial frequency (0.1 c/°) and moved from left to right with an angular velocity of 15°/sec. This speed was chosen since in the adult cat it reliably activates both sustained and transient L G N cells 15. The exposure time varied from 3 to 12 h and was segmented in daily sessions of 3 h. The recordings from single units in areas 17 and 18 were performed 4-6 weeks after exposure. For surgery the kittens were anesthetized with ether and for recording the animals were curarized and anesthetized with nitrous oxide. The pupils were dilated with atropine and the corneae protected with contact lenses containing artificial pupils of 2 m m diameter. Refractive errors were measured with a Rhodenstock refractometer and corrected if necessary. The neuron samples obtained from each of the 4 kittens ranged
144
B
A 100.
100
x ~ X ~ x
3'h
6'h
3"h
12' h
6'h
C
12'h
D
90
60
20 10
60
90
~
0
Fig. 1. A: the effect of exposure time (abscissa) on the frequency of occurrence of asymmetrical RFs. Ordinate: percentage of units. © ©, units unresponsive to light stimulation; • 0 , units with direction-selective fields; x ×, units with orientation-selective fields. The interrupted horizontal lines indicate the respective percentages in adult cats. B: the effect of exposure time (abscissa) on the formation of stimulus specific RFs. × - - - - x, percentage of vertically oriented RFs v e r s u s horizontally oriented RFs; 0 - - - • , percentage of direction-selective units for rightward movements v e r s u s direction-selective units for leftward movements. The interrupted horizontal line at 50 ~ indicates the respective level for a symmetrical distribution; • • , percentage of directionselective units for rightward movement v e r s u s direction-selective units for movements in the 3 other directions (vertical up and down and horizontal leftward). The interrupted horizontal line at 25 indicates the level for symmetrical distributions. C: polar distribution of oriented RFs of the whole sample. Abscissa: horizontal orientations; ordinate: vertical orientations. D: polar distribution of direction-selective RFs. The axes correspond to the 4 determined directions of movement. between 30 a n d 64 cells. A total o f 128 cells was analyzed from that hemisphere for which the experienced m o v e m e n t was towards the vertical meridian. After the receptive fields were m a p p e d using h a n d held stimuli, at least 2 histograms were compiled for every cell: one for a vertically oriented a n d the other for a horizontally oriented m o v i n g stimulus. F r o m these histograms it was determined whether the cell preferred 1 o f the 4 directions. W h e n a cell reacted equally well in 2 or m o r e directions, a d d i t i o n a l histograms were compiled for the oblique orientations. O r i e n t a t i o n selectivity was tested with slits o f variable length. It t u r n e d out that the great m a j o r i t y o f orientation-selective units had their preferred axes either closer to the vertical or to the horizontal meridian. F o r the numerical evaluation we classified fields with somewhat oblique o r i e n t a t i o n s as vertical or horizontal according to their respective affinities. The same was done for direction selectivity. D u r i n g exposure all kittens showed a n i m m e d i a t e vigorous optokinetic nystagmus a n d when the head was u n r e s t r a i n e d a m a r k e d head r o t a t i o n i n the direction o f
145 drum rotation. The optokinetic response fatigued during the initial 20 min of the daily session. The kittens would then stare at the moving grating and only occasionally pursued the stripes. When they fell asleep and had to be woken up, optokinetic nystagmus reappeared for several minutes. After the sessions, when the eyes were again occluded, the kittens would quite frequently rotate around themselves or walk in circles, the direction of this movement usually being opposite to the direction of movement of the drum. Immediately before the neurophysiological experiment, the kittens were again briefly tested behaviorally. When exposed to the rotating grating, they again showed optokinetic nystagmus and head pursuit movements to stripes moving in either direction. When tested for following responses to small hand held objects, the kittens would try to catch the stimuli as soon as they moved. They were apparently unable, however, to estimate distance or perceive stationary objects. They performed 'catching' responses irrespective of stimulus distance and bumped into stationary obstacles. The results of the single unit analysis show that an exposure time of 3 h is sufficient to produce a bias in favor of units responding optimally to vertically oriented stimuli (Fig. 1B). Out of 28 oriented RFs, 69 ~ were classified as vertical. Correspondingly, most units (68 ~ of direction-selective cells) preferred horizontally moving stimuli, but with 3 h exposure there was no preference for either of the horizontal directions. Increasing the time of exposure above 6 h, however, resulted in a clear predominance of direction selectivity in the direction of previously experienced movement. This bias increased with exposure time. Further effects of prolonged exposure were a slight reduction of unresponsive cells (Fig. 1A) and an increase of the orientation bias (Fig. 1B). There was, however, no clear change in the ratios of direction-selective v e r s u s nondirection-selective units and orientationselective v e r s u s nonoriented units (Fig. 1A). As there are no data from mature cortices where every cell has been analyzed with histograms it is difficult to compare the absolute sensitivity to light stimuli. Judging from our manual field analysis, even with 12 h exposure, the kitten cells responded in a much less selective way than cells in experienced cortices. In addition, the response amplitudes were, on the average, smaller and the percentage of cells rated as unresponsive to manual field analysis was found to be higher than in normal adult cortices. Judging from the histograms, however, 91 ~ of the cells responded to the light stimuli and the percentages of cells with asymmetrical RFs preferring a certain stimulus orientation or direction were similar to those observed in our studies of adult cats16, TM (Fig. 1A). For further comparison with adult cortices, the spontaneous activity of the cells was rated in 4 categories. Comparison with the corresponding data from adult cats16,18 showed that the spontaneous activity of the kitten cells was significantly higher (P < 0.001) than that of neurons in adult cats. The velocity preference of the kitten neurons was difficult to determine since they would respond over a wider range than in the adult. This implies that the striate cells of kittens could follow faster movements than most cells in the striate cortex of adult cats. In spite of the generally weak responses, there were, however, cells which were
146
A
C
~qo"'T
B
E
0'ssec
D
1,,ec
lsec
F
05sec
lsec
Fig. 2. Responses of 2 direction-selective units encountered in area 17 of a kitten after 12 h exposure to vertical stripes moving from left to right. A-D : PSTHs (10 sweeps) to moving (A, B) and stationary (C, D) light bars (width 1°; length 10°, speed of movement 10°/sec) in a cell with a vertically oriented RF which is direction-selective for rightward movements. The bar is moving orthogonal to its longitudinal axis, the arrows in A and B indicate the respective directions of movement. C and D: responses of the same cell to the vertically oriented stationary flashing slit (duration 1 sec, repetition rate 0.3/sec). The RF consists of 2 elongated, vertically oriented and spatially separate on and off bands. In C and D, the stimuli are placed in the off and on bands respectively. The off band is to the left of the on band. E and F: averaged response of another unit with an orientation- and direction-selective RF encountered in the same animal. The RF axis is horizontal and the preferred direction of movement is upward. Stimulus configuration and PSTH parameters are the same as in A-D. The sharpness of tuning is similar in the two units even though horizontally oriented contrasts moving up and down have not been experienced during exposure.
as responsive a n d as s h a r p l y t u n e d as cells in m a t u r e cortices (Fig. 2). A l t h o u g h the m a j o r i t y o f these sharply t u n e d cells h a d vertically oriented fields which were direction selective for r i g h t w a r d m o v e m e n t s , 6 cells with p r o p e r t i e s o f m a t u r e cells were enc o u n t e r e d with h o r i z o n t a l fields a n d 4 cells with vertical fields sensitive to leftward m o v e m e n t . S o m e o f these cells were r e c o r d e d d u r i n g the first h o u r s o f the r e c o r d i n g session. Since Pettigrew a n d G a r e y lz have shown t h a t the c o n s o l i d a t i o n o f R F specificity takes at least several hours after exposure, it is unlikely t h a t these units h a d been t u n e d b y the stimuli which we used to elicit responses d u r i n g the r e c o r d i n g session. The c o m p a r i s o n between the quality o f a light response a n d the level o f s p o n t a neous activity suggests a negative c o r r e l a t i o n between these 2 p a r a m e t e r s . The quality o f a light response was d e t e r m i n e d f r o m the h i s t o g r a m s b y considering the a m p l i t u d e o f the response a n d the sharpness o f the peak. F r o m these p a r a m e t e r s responses were g r o u p e d into 10 classes (0 = no responses, 10 ~ very g o o d responses). There was a clear t e n d e n c y f o r cells r a t e d in classes 7-10 to have lower s p o n t a n e o u s activity t h a n units in the o t h e r classes. This t e n d e n c y was significant at the P < 0.01 level when tested with g 2. A few cells (n = 3) w h i c h we h a d never o b s e r v e d in a d u l t cats r e s p o n d e d equally well to all stimuli b u t were selectively i n h i b i t e d b y a vertical b a r m o v i n g
147 opposite to the experienced direction. Eleven cells were inhibited by stimuli oriented orthogonal to the excitatory stimulus. Seven cells had exclusive inhibitory fields which were neither orientation nor direction selective. In 2 cats with 12 h exposure, penetrations were also made in area 18. The results were identical to those obtained from area 17 as far as the bias for vertical orientation selective units with preference for rightward movement is concerned. Just as in the adult cat 16,1s, however, the cells in area 18 responded preferentially to rapidly moving stimuli (/> 15°/sec). Twenty-three of the orientation- and direction-selective RFs were analyzed with stationary slits. Six of them consisted of elongated, spatially adjacent, on and off areas and thus closely resembled simple fields 9. It was, however, not possible to predict from the spatial arrangement of on and off bands which direction of movement would be preferred. In addition to these simple units we also observed more complex fields, from which only mixed on/off responses could be obtained with stationary stimuli. Two recent studies bear on the results reported here: Cynader et al. 5 have raised cats in a unidirectionally moving environment, but using spots instead of elongated slits as the moving stimuli, and employing a markedly differing luminance level, field of view, and exposure duration. The results of this experiment, which demonstrates similar alterations in cortical receptive field properties, corroborate the results reported here. Vital-Durand and Jeannerod 19 have recorded from collicular units in cats reared in an environment composed of a rightward-moving grating. They report that units in both colliculi responded optimally to leftward moving stimuli, i.e. stimuli moving in the direction opposite to the direction of the training environment. Since the direction selectivity of cat collicular units appears to depend partially upon corticofugal input1,14, 20, it may be considered that the observed asymmetries at the collicular level are due to an asymmetrical distribution of cortical direction selectivity. This question is currently under investigation. The results of this study suggest several preliminary conclusions. (1) Optokinetic nystagmus, pursuit movements and movement after-effects are elicitable in 4-week-old visually inexperienced kittens. (2) Three hours of visual exposure to unidirectionally moving vertical stripes are sufficient to produce a bias in the orientation of cortical RFs. This bias increases with exposure time at least up to 12 h. (3) With exposure times above 6 h, the direction selectivity of cortical cells is also modifiable. (4) Sharply tuned adult-like RFs may also occur for orientations and directions which have never been seen before the experiment. (5) With exposure to unidirectional movement, atypical RFs develop, which show selective inhibition only for one direction of movement. (6) The percentage of units with asymmetric RFs appears to be similar to that in the adult irrespective of 3 or 12 h exposure. But even with 12 h exposure the selectivity and the amplitude of the majority of responses are considerably lower than in the adult.
148 (7) The average spontaneous activity of the kitten cells is higher than in the adult. There is a negative correlation between the spontaneous discharge rate of a cell and the 'quality' or strength of its visual response. (8) The response characteristics of cells in cortical area 18 are also subject to modification by selective visual exposure. (9) Velocity tuning and preferred stimulus velocity in cortical units appear to be more resistant to environmental modification than other properties. As in normal cats, units in area 18 prefer high velocity stimuli while those in area 17 respond to lower velocities. M. Cynader was supported by Grant No. MA 5201 from the Medical Research Council of Canada. This work was partially supported by the 'Deutsche Forschungsgemeinschaft', SFB 50, Kybernetik.
1 BERMAN,N., AND CYNADER,M., Comparison of receptive field organization of the superior colliculus in Siamese and normal cats, J. Physiol. (Lond.), 224 (1972) 363-389. 2 BLAKEMORE,C., AND COOPER, G. F., Development of the brain depends on the visual environment, Nature (Lond.), 228 (1970) 477-478. 3 BLAKEMORE,C., AND MITCHELL, M., Environmental modification of the visual cortex and the neural basis of learning and memory, Nature (Lond.), 241 (1973) 467-468. 4 CYNADER,M., BERMAN,N., AND HEIN, A., Cats reared in stroboscopic illumination: effects on receptive fields in cat visual cortex, Proc. nat. Acad. Sci. (Wash.), 70 (1973) 1353-1354. 5 CYNADER,M., BERMAN, N., AND HEIN, A., Cats raised in a one-directional world: effects on receptive fields in visual system, in preparation. 6 CYNADER, M., BERMAN, N., AND HEIN, A., Recovery of function in cat visual cortex following prolonged pattern deprivation, in preparation. 7 HIRSCH, U. V. B., Visual perception in cats after environmental surgery, Exp. Brain Res., 15 (1972) 405-423. 8 HIRSeH, U. V. B., AND SPINELLI, D. N., Modification of the distribution of receptive field orientation in cats by selective visual exposure during development, Exp. Brahl Res, 13 (1971) 509-527. 9 I-]UBEL,D. H., AND WIESEL,T. N., Receptive fields, binocular interaction and functional architecture in the cat's visual cortex, J. PhysioL (Lond.), 160 0962) 106-154. l0 HUBEL,D. H., AND WIESEL,T. N., Receptive fields of cells in striate cortex of very young, visually inexperienced kittens, J. Neurophysiol., 26 (1963) 994-1002. 11 PETTIGREW, J.O., AND BARLOW, U.B., Kitten visual cortex: short-term, stimulus-induced changes in connectivity, Science, 180 (1973) 1202-1203. 12 PETTIGREW, J. O., AND FREEMAN, R. D., Visual experience without lines: effect on developing cortical neurons, Science, 182 (1973) 599-601. 13 PETTIGREW, J. O., AND GAREY, L.J., Selective modification of single neuron properties in the visual cortex of kittens, Brain Research, 66 (1974) 160-164. 14 ROSENQUIST, A. C., AND PALMER,L., Visual receptive field properties of cells in the superior colliculus after cortical lesions in the cat, Exp. Neurol., 33 (1971) 629-652. 15 SINGER, W., AND BEDWORTH,N., Inhibitory interaction between X and Y units in the cat lateral geniculate nucleus, Brain Research, 49 (1973) 291-307. 16 SINGER, W., CYNADER,M., AND TRETTER,F., On the organization of cat striate cortex, a correlation of receptive field properties with afferent and efferent connections, in preparation. 17 SPINELLI, D . N . , HIRSCN, U. V. B., PHELPS, R.W., AND METZLER, J., Visual experience as a determinant of the response characteristics of cortical receptive fields in cats, Exp. Brain Res., 15 0972) 289-304. 18 TRETTER,F., CYNADER,M., AND SINGER,W,, The cat parastriate cortex, a primary or secondary visual area?, In preparation. 19 VITAL-DURAND,F., AND JEANNEROD, M., Maturation of the optokinetic response: genetic and environmental factors, Brabz Research, 71 (1974) 249-257.
149 20 WICKELGREN,B. G., AND STERLING, P., Influence of visual cortex on receptive fields in the superior colliculus of the cat, J. Neurophysiol., 32 (1969) 16-23. 21 WIESEL, T., AND HUBEL, D. H., Single cell responses in striate cortex of kittens deprived of vision in one eye, J. Neurophysiol., 26 (1963) 1003-1017. 22 WIESEL, T. N., AND HUBEL, D. H., Extent of recovery from the effects of visual deprivation in kittens, J. Neurophysiol., 28 (1965) 1060-1072.
143
Modification of direction selectivity of neurons in the visual cortex of kittens
F. TRETTER, M. CYNADER AND W. SINGER Max Planck Institute for Psychiatry, 8000 Munich 40 (G.F.R.)
(Accepted October 21st, 1974)
Accumulating evidence suggests that the development of the cat visual system is dependent on visual experience. Visual deprivation results in the loss of functional specificity in cortical neurons6,10, 22 and it is possible to cause specific and long lasting changes in the functional properties of cortical neurons 2,3,7,8,11-13,~7,21 by brief selective exposure during the critical period. In particular, it has been shown that cortical neurons become orientation-selective in the same axis as the visual stimuli presented during exposure3,8,13. If exposed to stimuli which lack orientation cues, cortical cells lose or fail to develop orientation specificity H. Cortical units in mature cats are sensitive not only to specific shapes but also selective for the speed and the direction of moving contrasts. It has recently been shown as well, that stimulus movement is a crucial parameter in the development of such normal cortical selectivity 4. With these considerations in mind, we therefore attempted to determine the extent to which dynamic R F properties such as direction selectivity and velocity tuning can be modified by selective visual exposure. Kittens which had been reared with both eyes occluded from birth were exposed, beginning at the age of 4 weeks, to vertically oriented stripes which covered the entire visual field and moved in only one direction. The kittens were placed in a restraining chair which prevented them from rotating or inclining their heads. The chair was mounted in the center of a rotating drum the walls of which were covered with a grating. The pattern had a uniform spatial frequency (0.1 c/°) and moved from left to right with an angular velocity of 15°/sec. This speed was chosen since in the adult cat it reliably activates both sustained and transient L G N cells 15. The exposure time varied from 3 to 12 h and was segmented in daily sessions of 3 h. The recordings from single units in areas 17 and 18 were performed 4-6 weeks after exposure. For surgery the kittens were anesthetized with ether and for recording the animals were curarized and anesthetized with nitrous oxide. The pupils were dilated with atropine and the corneae protected with contact lenses containing artificial pupils of 2 m m diameter. Refractive errors were measured with a Rhodenstock refractometer and corrected if necessary. The neuron samples obtained from each of the 4 kittens ranged
144
B
A 100.
100
x ~ X ~ x
3'h
6'h
3"h
12' h
6'h
C
12'h
D
90
60
20 10
60
90
~
0
Fig. 1. A: the effect of exposure time (abscissa) on the frequency of occurrence of asymmetrical RFs. Ordinate: percentage of units. © ©, units unresponsive to light stimulation; • 0 , units with direction-selective fields; x ×, units with orientation-selective fields. The interrupted horizontal lines indicate the respective percentages in adult cats. B: the effect of exposure time (abscissa) on the formation of stimulus specific RFs. × - - - - x, percentage of vertically oriented RFs v e r s u s horizontally oriented RFs; 0 - - - • , percentage of direction-selective units for rightward movements v e r s u s direction-selective units for leftward movements. The interrupted horizontal line at 50 ~ indicates the respective level for a symmetrical distribution; • • , percentage of directionselective units for rightward movement v e r s u s direction-selective units for movements in the 3 other directions (vertical up and down and horizontal leftward). The interrupted horizontal line at 25 indicates the level for symmetrical distributions. C: polar distribution of oriented RFs of the whole sample. Abscissa: horizontal orientations; ordinate: vertical orientations. D: polar distribution of direction-selective RFs. The axes correspond to the 4 determined directions of movement. between 30 a n d 64 cells. A total o f 128 cells was analyzed from that hemisphere for which the experienced m o v e m e n t was towards the vertical meridian. After the receptive fields were m a p p e d using h a n d held stimuli, at least 2 histograms were compiled for every cell: one for a vertically oriented a n d the other for a horizontally oriented m o v i n g stimulus. F r o m these histograms it was determined whether the cell preferred 1 o f the 4 directions. W h e n a cell reacted equally well in 2 or m o r e directions, a d d i t i o n a l histograms were compiled for the oblique orientations. O r i e n t a t i o n selectivity was tested with slits o f variable length. It t u r n e d out that the great m a j o r i t y o f orientation-selective units had their preferred axes either closer to the vertical or to the horizontal meridian. F o r the numerical evaluation we classified fields with somewhat oblique o r i e n t a t i o n s as vertical or horizontal according to their respective affinities. The same was done for direction selectivity. D u r i n g exposure all kittens showed a n i m m e d i a t e vigorous optokinetic nystagmus a n d when the head was u n r e s t r a i n e d a m a r k e d head r o t a t i o n i n the direction o f
145 drum rotation. The optokinetic response fatigued during the initial 20 min of the daily session. The kittens would then stare at the moving grating and only occasionally pursued the stripes. When they fell asleep and had to be woken up, optokinetic nystagmus reappeared for several minutes. After the sessions, when the eyes were again occluded, the kittens would quite frequently rotate around themselves or walk in circles, the direction of this movement usually being opposite to the direction of movement of the drum. Immediately before the neurophysiological experiment, the kittens were again briefly tested behaviorally. When exposed to the rotating grating, they again showed optokinetic nystagmus and head pursuit movements to stripes moving in either direction. When tested for following responses to small hand held objects, the kittens would try to catch the stimuli as soon as they moved. They were apparently unable, however, to estimate distance or perceive stationary objects. They performed 'catching' responses irrespective of stimulus distance and bumped into stationary obstacles. The results of the single unit analysis show that an exposure time of 3 h is sufficient to produce a bias in favor of units responding optimally to vertically oriented stimuli (Fig. 1B). Out of 28 oriented RFs, 69 ~ were classified as vertical. Correspondingly, most units (68 ~ of direction-selective cells) preferred horizontally moving stimuli, but with 3 h exposure there was no preference for either of the horizontal directions. Increasing the time of exposure above 6 h, however, resulted in a clear predominance of direction selectivity in the direction of previously experienced movement. This bias increased with exposure time. Further effects of prolonged exposure were a slight reduction of unresponsive cells (Fig. 1A) and an increase of the orientation bias (Fig. 1B). There was, however, no clear change in the ratios of direction-selective v e r s u s nondirection-selective units and orientationselective v e r s u s nonoriented units (Fig. 1A). As there are no data from mature cortices where every cell has been analyzed with histograms it is difficult to compare the absolute sensitivity to light stimuli. Judging from our manual field analysis, even with 12 h exposure, the kitten cells responded in a much less selective way than cells in experienced cortices. In addition, the response amplitudes were, on the average, smaller and the percentage of cells rated as unresponsive to manual field analysis was found to be higher than in normal adult cortices. Judging from the histograms, however, 91 ~ of the cells responded to the light stimuli and the percentages of cells with asymmetrical RFs preferring a certain stimulus orientation or direction were similar to those observed in our studies of adult cats16, TM (Fig. 1A). For further comparison with adult cortices, the spontaneous activity of the cells was rated in 4 categories. Comparison with the corresponding data from adult cats16,18 showed that the spontaneous activity of the kitten cells was significantly higher (P < 0.001) than that of neurons in adult cats. The velocity preference of the kitten neurons was difficult to determine since they would respond over a wider range than in the adult. This implies that the striate cells of kittens could follow faster movements than most cells in the striate cortex of adult cats. In spite of the generally weak responses, there were, however, cells which were
146
A
C
~qo"'T
B
E
0'ssec
D
1,,ec
lsec
F
05sec
lsec
Fig. 2. Responses of 2 direction-selective units encountered in area 17 of a kitten after 12 h exposure to vertical stripes moving from left to right. A-D : PSTHs (10 sweeps) to moving (A, B) and stationary (C, D) light bars (width 1°; length 10°, speed of movement 10°/sec) in a cell with a vertically oriented RF which is direction-selective for rightward movements. The bar is moving orthogonal to its longitudinal axis, the arrows in A and B indicate the respective directions of movement. C and D: responses of the same cell to the vertically oriented stationary flashing slit (duration 1 sec, repetition rate 0.3/sec). The RF consists of 2 elongated, vertically oriented and spatially separate on and off bands. In C and D, the stimuli are placed in the off and on bands respectively. The off band is to the left of the on band. E and F: averaged response of another unit with an orientation- and direction-selective RF encountered in the same animal. The RF axis is horizontal and the preferred direction of movement is upward. Stimulus configuration and PSTH parameters are the same as in A-D. The sharpness of tuning is similar in the two units even though horizontally oriented contrasts moving up and down have not been experienced during exposure.
as responsive a n d as s h a r p l y t u n e d as cells in m a t u r e cortices (Fig. 2). A l t h o u g h the m a j o r i t y o f these sharply t u n e d cells h a d vertically oriented fields which were direction selective for r i g h t w a r d m o v e m e n t s , 6 cells with p r o p e r t i e s o f m a t u r e cells were enc o u n t e r e d with h o r i z o n t a l fields a n d 4 cells with vertical fields sensitive to leftward m o v e m e n t . S o m e o f these cells were r e c o r d e d d u r i n g the first h o u r s o f the r e c o r d i n g session. Since Pettigrew a n d G a r e y lz have shown t h a t the c o n s o l i d a t i o n o f R F specificity takes at least several hours after exposure, it is unlikely t h a t these units h a d been t u n e d b y the stimuli which we used to elicit responses d u r i n g the r e c o r d i n g session. The c o m p a r i s o n between the quality o f a light response a n d the level o f s p o n t a neous activity suggests a negative c o r r e l a t i o n between these 2 p a r a m e t e r s . The quality o f a light response was d e t e r m i n e d f r o m the h i s t o g r a m s b y considering the a m p l i t u d e o f the response a n d the sharpness o f the peak. F r o m these p a r a m e t e r s responses were g r o u p e d into 10 classes (0 = no responses, 10 ~ very g o o d responses). There was a clear t e n d e n c y f o r cells r a t e d in classes 7-10 to have lower s p o n t a n e o u s activity t h a n units in the o t h e r classes. This t e n d e n c y was significant at the P < 0.01 level when tested with g 2. A few cells (n = 3) w h i c h we h a d never o b s e r v e d in a d u l t cats r e s p o n d e d equally well to all stimuli b u t were selectively i n h i b i t e d b y a vertical b a r m o v i n g
147 opposite to the experienced direction. Eleven cells were inhibited by stimuli oriented orthogonal to the excitatory stimulus. Seven cells had exclusive inhibitory fields which were neither orientation nor direction selective. In 2 cats with 12 h exposure, penetrations were also made in area 18. The results were identical to those obtained from area 17 as far as the bias for vertical orientation selective units with preference for rightward movement is concerned. Just as in the adult cat 16,1s, however, the cells in area 18 responded preferentially to rapidly moving stimuli (/> 15°/sec). Twenty-three of the orientation- and direction-selective RFs were analyzed with stationary slits. Six of them consisted of elongated, spatially adjacent, on and off areas and thus closely resembled simple fields 9. It was, however, not possible to predict from the spatial arrangement of on and off bands which direction of movement would be preferred. In addition to these simple units we also observed more complex fields, from which only mixed on/off responses could be obtained with stationary stimuli. Two recent studies bear on the results reported here: Cynader et al. 5 have raised cats in a unidirectionally moving environment, but using spots instead of elongated slits as the moving stimuli, and employing a markedly differing luminance level, field of view, and exposure duration. The results of this experiment, which demonstrates similar alterations in cortical receptive field properties, corroborate the results reported here. Vital-Durand and Jeannerod 19 have recorded from collicular units in cats reared in an environment composed of a rightward-moving grating. They report that units in both colliculi responded optimally to leftward moving stimuli, i.e. stimuli moving in the direction opposite to the direction of the training environment. Since the direction selectivity of cat collicular units appears to depend partially upon corticofugal input1,14, 20, it may be considered that the observed asymmetries at the collicular level are due to an asymmetrical distribution of cortical direction selectivity. This question is currently under investigation. The results of this study suggest several preliminary conclusions. (1) Optokinetic nystagmus, pursuit movements and movement after-effects are elicitable in 4-week-old visually inexperienced kittens. (2) Three hours of visual exposure to unidirectionally moving vertical stripes are sufficient to produce a bias in the orientation of cortical RFs. This bias increases with exposure time at least up to 12 h. (3) With exposure times above 6 h, the direction selectivity of cortical cells is also modifiable. (4) Sharply tuned adult-like RFs may also occur for orientations and directions which have never been seen before the experiment. (5) With exposure to unidirectional movement, atypical RFs develop, which show selective inhibition only for one direction of movement. (6) The percentage of units with asymmetric RFs appears to be similar to that in the adult irrespective of 3 or 12 h exposure. But even with 12 h exposure the selectivity and the amplitude of the majority of responses are considerably lower than in the adult.
148 (7) The average spontaneous activity of the kitten cells is higher than in the adult. There is a negative correlation between the spontaneous discharge rate of a cell and the 'quality' or strength of its visual response. (8) The response characteristics of cells in cortical area 18 are also subject to modification by selective visual exposure. (9) Velocity tuning and preferred stimulus velocity in cortical units appear to be more resistant to environmental modification than other properties. As in normal cats, units in area 18 prefer high velocity stimuli while those in area 17 respond to lower velocities. M. Cynader was supported by Grant No. MA 5201 from the Medical Research Council of Canada. This work was partially supported by the 'Deutsche Forschungsgemeinschaft', SFB 50, Kybernetik.
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