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Discrimination of intermittent photic stimulation in normal and brain-damaged cats
EXPERIMENTAL
NEUROLOGY
Discrimination
282-293 (1963)
7,
of
Normal
Intermittent and
Brain-Damaged
CHARLES L. TARAVELLAAND Department
of Physiology, Received
Photic
University November
Stimulation
in
Cats
GEORGE CLARK] of Buffalo,
Buffalo,
New
York
27. 1962
Cats were trained to discriminate between a flickering and a steady light and then were subjected to ablation of varying amounts of the visual cortex. The original learning curves consisted of a period of rapid learning of increased frequency of flicker, then a more or less pronounced plateau followed by a second period of more rapid learning. Following surgery those animals with virtually complete loss of striate cortex were able to relearn the discrimination and attained preoperative levels within 1000 trials. Those with slight remnants of visual cortex retained the discrimination but never (4OCO trials) reached preoperative levels while the only animal with considerable visual cortex remaining did regain preoperative performance after prolonged retraining (3500 trials). From these results it was possible to conclude that the plateau may represent the usual critical flicker fusion and that, at least in our experiments, fusion must be a central rather than a retinal event. An “interference hypothesis” is suggested which proposes that remnants of a neural system may be more damaging to performance than complete loss of the system. Introduction
The usual accounts of visual function in mammals are given in terms of two, or in some species three, processes: light intensity, form and color. It is well established that the last two of these are dependent on a functioning visual cortex while discriminations of light intensity can be made in the absenceof the visual cortex. Flicker and the fusion of a flickering light as the rate increases is another function of the visual system possibly similar to light intensity; however, knowledge of the neural correlates of flicker is meager. Schwartz and Clark (9) have 1 This investigation was aided by grant B-868, National Institutes of Health, United States Public Health Service. Present address of Dr. Taravella: Kirksville College of Osteopathy and Surgery, Kirksville, Missouri; of Dr. Clark: United States Army Research Institute of Environmental Medicine, Natick, Massachusetts. 282
PHOTIC
STIMULATION
283
shown that rats can relearn a flicker discrimination after ablation of the striate cortex and Kappauf (4) stated in an abstract that cats were able to discriminate flicker with or without a striate cortex. Since no detailed report of this work ever appeared and no histological data were offered this finding of Kappauf can hardly be considered conclusive. The development by Halstead” of a modification of the Yerkes two-choice discrimination apparatus suitable for flicker studies with cats afforded a ready technique to evaluate the report of Kappauf. Furthermore, such a study might make possible a settlement of the old controversy over whether or not the fusion resulting from an increase in the rate of flicker was a central or retinal phenomenon. Methods Apparatus: A modified Yerkes double-choice discrimination box was used. This consistedof a lightproof entry box attached to a runway which was divided by a partition at the far end into two smaller runways. Each of the smaller runways terminated in a transparent, hinged at the top, door 22 cm square. Moving the door permitted access to a food receptacle. A light was centered behind each door at a distance of 108mm. The driver unit which powered the lights was a stable electronic device designedto generate a square wave with equal on and off periods over a continuously adjustable frequency range from 10.5 to 65 cycle/set. The driver also provided a continuous direct current for the steady light. Each light had its own brightness control and the positions of the steady and flickering lights could be alternated by meansof a silent switch. Each light source consisted of a Neon glow tube (NE-32) surrounded by a conical metal reflector closed by a ground glass cover. This gave a circular light source 7 cm in diameter and of uniform intensity. Illuminance was measuredat the surface of the frosted glasswith a photographic exposure meter. The highest brightness used was arbitrarily selected and was well below the customary limits for cone vision. For this reason all training and testing were under dark-adapted conditions. Training Sequence and Testing Methods. The cat was placed in the dark starting box and left there for 20 min. An opaque sliding door was lifted allowing the animal to seeboth lights through a similar transparent door. The transparent door was lifted so that the animal could 2 Halstead,
W. C.: Personal
communication.
284
TARAVELLA
AND
CLARK
approach the lights. The animal made a choice by touching the transparent door at the end of one of the small alleys. If correct, the door would open and the cat could obtain a small piece of fresh fish. Both doors were, of course, baited. Whether or not a correct choice was made the animal was immediately returned manually to the starting box,
FIG. 1. Serial sections through lateral geniculate nuclei of cat 2. In Figs. l-3 plete loss of large cells is indicated by cross hatching; areas with only scattered cells, by dots; normal or virtually normal areas are lined.
comlarge
Routinely such noncorrection trials were made; however in preliminary training and when motivation was low the animals were allowed to correct their choices. Such corrected choices were scored as errors. Usually sixty trials per day were made with the positions of the flickering and steady lights varied according to the Gellerman series. Training and testing were begun at 15 cycle/set. The frequency was increased by 2 cycle/set after the animal had made eight or more correct choices
PHOTIC
28.5
STIMULATION
out of a block of ten trials. Training was terminated when the animals had for 3 to 5 days successfully discriminated between 65 cycle/set and the steady light. Ablation Studies. After a successfulperiod of performance at 65 cycle/ set (the highest obtainable with the driver) varying amounts of striate
FIG. 2.
Serial
sectionsthrough
lateral
geniculate
nuclei
of cat 3.
and parastriate cortex were removed by subpial suction. In the three animals with the largest lesions the ablations extended anteriorly almost to the ansate sulcus and laterally to include the superior and posterior suprasylvian gyri. After a 2-week recovery period training and testing were resumed.At the conclusion of testing and training the animals were killed and perfused with acacia saline followed by acacia formalin (5). The brains were embedded in celloidin, sectioned at 50 u and every tenth section stained with cresyl violet acetate.
286
TARAVELLA
AND
CLARK
Since variations in nonstriate tissue ablated did not alter the behavior of the animals as assessedby the test used while variations in amount of striate cortex did, it seemedsufficient to report only the changes in the lateral geniculate nuclei. In Figs. 1, 2, and 3 are shown a series
FIG.
3.
Serial
sections
through
lateral
geniculate
nuclei
of cat
8.
of tracings through the lateral geniculate nuclei of these animals. These show the locations where intact large cells persisted. In the cat, these are the only cells which disappear following striatectomy (7). Results
When it was found that the cats were discriminating at levels much higher than anticipated (under similar conditions of dark adaptation,
PHOTIC
287
STIMULATION
light intensity, size of test patch and distance from test patch, Clark3 found critical flicker fusion levels in the low forties in a small group of humans) a series of control studies were made in an attempt to determine if the cats were utilizing extraneous cues: i. Operators were repeatedly switched to eliminate possible operator cues. ii. Fluorescent bulbs were substituted for the routinely used neon tubes. This eliminated possible high-frequency noise as a differential cue. iii. Masking noises were used to render indistinguishable the sounds normally present. iv. The steady light was driven by a second driver at 90 cycle/set. v. Since the sharp edge of the light might make possible some stroboscopic effect, the
to
20
30
40
50
60
70
60
90
DAYS 4. Preoperative (circles) Figs. 4-6 the highest frequency score indicates that performance FIG.
and postoperative (squares) scores asttained as 80% level is plotted for on that day did not reach 80% level.
of cat 2. In each day; no
test patch was redesigned to present a luminous center with no distinct margins. vi. The brightness of the steady lamp was varied so that it was at times brighter, the same or dimmer than the flickering lamp. This eliminated a brightness discrimination as a factor. Since none of these affected, more than momentarily, the performance of the animals, it was concluded that the actual negative stimulus must be the flickering light. The results of the preoperative training sessions are shown in Figs. 4, 5, 6, and 7. In the first three of these, the preoperative and postoperative scores are shown by circles and squares, respectively. In these the highest a Clark,
George:
Unpublished
work.
288
TARAVELLA
AND
CLARK
flicker frequency discriminated each day in any block of ten trials at the 80% discrimination level is shown with the time scale as abscissas. Days when performance was below the 80% level are indicated by blank spaces. There is a general similarity in the shape of the preoperative 60
IO
20
30
40
50
60
70
80
90
DAYS FIG.
5.
Preoperative
(circles)
and
postoperative
(squares)
scores
of cat
3.
80 1
. . . .. .. .. .. .*.... . ... .. ... .
l a.* .
60
IO
20
30
40
50
60
70
80
of cat
8.
DAYS
FIG. 6.
Preoperative
(circles)
and
postoperative
(squares)
scores
curves. In each, initial criterion is reached only after some days of training. Then, there is a period of rapid learning followed by several to many days with little improvement. Following this plateau, there is further and substantial improvement in the highest frequency discriminated to the maximum of 6.5 cycle/set. This maximum was deter-
PHOTIC
289
STIMULATION
mined by the driver used. It required from 3 to 9 days to reach the 80% level at the lowest frequency used and from 42 to over 60 days to reliably discriminate at the 65 cycle/set level. Cat 2 had a slight case of distemper during training and in this period there was a sharp drop in the highest frequency discriminated. Similar episodes in other animals may represent periods of otherwise symptomless illness. NUMBER 500
1000
I
80
OF TRIALS
15002000
I
I
I
. .. . . ..
0
. .,
.
60
z !i 40 0 ii l.L 20
2To I 750I
12Y0
PRE-OPERATIVE
z
500
2500
l
.
5
POST-OPERATIVE .. . . . .
.
..
. .
.* . . .
.
..‘* .
.
. ..-
l
*
.
.
.
.
: .
. .
PAUSE IN TRAINING-A
I IO
I 20
I 30
E I
40
5b
60
SURGICAL -RECOVERY
r&--z
DAYS FIG.
training operation
7.
Preoperative, was of 2 weeks and testing.
retention duration
and postoperative scores on cat 10. The pause in corresponding to the 2-week routine delay between
Postoperative testing and training are shown graphically in the same figures. In the caseof cat 10, preoperative, postoperative and, in addition, training after a delay period of 2 weeks are shown in a single figure (Fig. 7). Since 2 weeks was the interval between operation and retraining in all the animals, this delay period (in cat 10) serves to give some measure of the possible loss in ability to discriminate simply as a result of cessation of training. The graphs of postoperative performance fall into three distinct groups. There is only one animal (cat 3) in the first of these. This animal was able to discriminate at a high level (43 cycle/set) on the first day of testing. Nevertheless, it was more than 60 days and almost 3500 trials later before it was able to discriminate at the preoperative level. Cats 2
290
TARAVELLA
AND
CLARK
and 4 also discriminated at relatively high levels on the first day of testing (32 and 39 cycle/set, respectively). However, even after more than 80 days of training and over 4000 trials, neither ever reliably attained preoperative levels of discrimination. The other three animals (cats 8, 9, and 10) have decidedly different records. Only one of these discriminated between the flickering and steady light on the first day of testing but within 10 days and 500 trials all had discriminated at 6 5 cycle/set . The diagrams of the destruction in the lateral geniculate nuclei in Figs. 1, 2 and 3 make it apparent that the animals all had varying amounts of intact striate cortex remaining. This ranged from considerable (cat 3) to slight (cat 2) to virtually none (cat 8). The lesion and the degeneration in the lateral geniculate nuclei in cat 4 was very similar to that in cat 2, while the lesions and the degeneration in the lateral geniculates in cats 8, 9, and 10 were much the same. In the figures (1, 2, and 3) showing the lateral geniculate nuclei areas of complete disappearance of large cells are indicated by cross hatching, areas where scattered large cells remained are dotted and normal or virtually normal areas are lined. This separation of the animals into three groups on the basis of the histological findings is identical with that based on their postoperative records. In cat 10, who was run subsequent to the others, there was interposed a 2-week delay period between original training and operating during which no training or testing occurred. Testing began after this pause. The animal reached over 30 cps on the first day and attained 65 cps on the seventh day (Fig. 7). The slope of the curve of this performance is very similar to the postoperative curve in the same animal and to that of the other two animals with virtually complete striate removals (cats 8 and 9). However, it should be noted that after the delay period there was retention of the discrimination, while after operation performance was below the 80% level until the fourth day of retraining. The postoperative loss in ability to discriminate was thus considerable despite the subsequent rapid relearning. Discussion
We have thus confirmed the incomplete report of Kappauf (4) and have extended the findings of Schwartz and Clark (9) to another species. Discrimination of intermittent photic stimulation like the discrimination of light intensity can be relearned following removal of the striate cortex.
PHOTIC
STIMULATION
291
In both of these discriminations some nonstriate mechanism must be present which can mediate the discrimination. Since photic stimuli can activate the reticular formation it is tempting to assume that this may be another of the myriad of functions of this overworked region. However, the nature and locus of this nonstriate mechanism must remain for future work to determine. The relationship of these results to critical flicker fusion in humans is also largely conjectural. The possibility of adequate verbal directions and familiarity with various forms of flicker in the human makes unnecessary the long learning period during which each increase in frequency may be presumed to present a new problem to the animal. However, if the early rapid rise in frequency discriminable represents striatal learning and the subsequent rapid rise nonstriatal learning, then the intervening plateau might be comparable to critical flicker fusion frequency (CFF) in man. Some support for this concept can be derived from several sources. This rate is only slightly above the human fusion level found by Clark” who used the same driver and lights used for the cats. Schwartz4 using a go-no-go procedure for the study of flicker in cats found a CFF at about the average rate during the plateau. This average rate is also in the range found by Lindsley (6) in the cat for maximum cortical following of an intermittent photic stimulation. Again, however, more work is needed to settle this issue. An explanation for the three types of postoperative curves obtained is difficult and is definitely limited by the small number of animals used in this experiment. However, since histological findings resulted in the same three groups it seems appropriate to assume that the grouping reflects the varying amounts of damage to the geniculostriate system. If this be so then the plateau may represent a period when fusion is present at the striate level and when the animal is making a shift to some nonstriate mechanism which is able to handle the higher frequencies. It would seem, too, that retention of the discrimination and a very slow shifting to the nonstriate mechanism could occur with considerable striate tissue remaining, and that retention of the discrimination and an inability to shift to the nonstriate mechanism might also occur. Finally either no retention or retention with only use of the nonstriate mechanism might occur. This is, of course, only a restatement of the results of the 4 Schwartz,
A.:
Personal
communication.
292
TARAVELLA
AND
CLARK
experiment, but it does suggest the concept that perhaps remnants of a functional area might be more damaging to the animal than complete ablation in that the remnants might inhibit the functioning of subsidiary mechanisms. Such an interference hypothesis would require substantiation. The question of whether fusion is a retinal or a central phenomenon probably dates at least from Sherrington (10) but is still unanswered. Ireland (3) stated “the results of the present investigation are regarded as offering definite evidence for the importance of central factors in the phenomena of flicker and fusion.” On the other hand Enroth (l), who makes no mention of Ireland’s work, states that it “seems likely that flicker fusion takes place in the retina.” Our data definitely support the position of Ireland (3). As shown above there were three types of postoperative scores in our animals. The crucial group consists of cats 2 and 4. Preoperatively they could discriminate between 65 cycle/set and a steady light so they must have had a CFF greater than 6.5 cycle/set. Their failure, postoperatively, to discriminate at levels below 65 cycle/ set indicates a postoperative fusion level less than 65 cycle/set. The fact that with more complete removals of striate cortex preoperative levels were attained postoperatively rules out the use of retrograde retinal damage as the cause of the loss in fusion levels. At the very least these findings in our experiments show that central elements are concerned in fusion and that fusion is not a strictly retinal phenomenon. There are two other reports on effects of brain damage on CFF in subhuman vertebrates. Goldzband and Clark (2) found little effect on CFF as a result of frontal lesions in rats. Mishkin and Weiskrantz (8) compared the effects of frontal, infratemporal and occipital lesions on CFF in monkeys. No anatomical details are given but reference is made to similar lesions in two earlier papers. In these earlier papers the diagrams of the lateral geniculate nuclei are so small as to be worthless. For this reason, despite the evident impairment of their occipital animals, no comparison with our animals would be fruitful. References I.
2.
ENROTH, C. 1952. The mechanism of flicker and fusion studied on single retinal elements in the dark-adapted eye of the cat. Acta Pltysiol. Stand. 27 (Suppl. 100): l-67. GOLDZBAND, M. G., and G. CLARK. 1955. Flicker fusion in the rat. /. &net. Psychol. 87: 257-264.
PHOTIC
3.
5.
6. 7.
8. 9.
10.
293
F. H. 1950. A comparison of critical flicker frequencies under conof monocular and binocular stimulation. /. Erptl. Psych. 40: 282-286. KAPPAUF, W. E. 1940. The foundation of the visual cortex in relation to level of brightness adaptation. Psychol. Bull. 37: 495-496. KOENIG, H., R. A. GROAT, and W. F. WINDLE. 1945. A physiological approach to perfusion-fixation of tissues with formalin. Stain Technol. 20: 13-22. LINDSLEY, D. B. 1954. Electrical response to photic stimulation in visual pathways of the cat. Electroencephalog. and Clin. Neurophysiol. 6: 690-691. MIXKOWSKI, M. 1913. Experimentelle Untersuchungen iiber die Beziehungen der grosshirnrinde und der Netzhaut zii den primLren optischen Zentren, besonders zum Corpus Geniculatum externum. Arb. Hirnandt. Inst. Ziirich. 7: 257-361. MISHICIN, M., and L. WEISKRANTZ. 1959. Effects of cortical lesion in monkeys on critical flicker frequency. J. Camp. and Physiol. Psychol. 62: 660-666. SCHWARTZ, A., and G. CLARK. 1957. Discrimination of intermittent photic stimulation in the rat without its striate cortex. J. Corn@. and Physiol. Psychol. 46: 119-126. SHERRINCTON, C. 1904. On binocular flicker and the correlation of activity of “corresponding” retinal points. Brit. J. Psychol. 1: 26-60. IRELAND,
ditions
4.
STIMULATION
NEUROLOGY
Discrimination
282-293 (1963)
7,
of
Normal
Intermittent and
Brain-Damaged
CHARLES L. TARAVELLAAND Department
of Physiology, Received
Photic
University November
Stimulation
in
Cats
GEORGE CLARK] of Buffalo,
Buffalo,
New
York
27. 1962
Cats were trained to discriminate between a flickering and a steady light and then were subjected to ablation of varying amounts of the visual cortex. The original learning curves consisted of a period of rapid learning of increased frequency of flicker, then a more or less pronounced plateau followed by a second period of more rapid learning. Following surgery those animals with virtually complete loss of striate cortex were able to relearn the discrimination and attained preoperative levels within 1000 trials. Those with slight remnants of visual cortex retained the discrimination but never (4OCO trials) reached preoperative levels while the only animal with considerable visual cortex remaining did regain preoperative performance after prolonged retraining (3500 trials). From these results it was possible to conclude that the plateau may represent the usual critical flicker fusion and that, at least in our experiments, fusion must be a central rather than a retinal event. An “interference hypothesis” is suggested which proposes that remnants of a neural system may be more damaging to performance than complete loss of the system. Introduction
The usual accounts of visual function in mammals are given in terms of two, or in some species three, processes: light intensity, form and color. It is well established that the last two of these are dependent on a functioning visual cortex while discriminations of light intensity can be made in the absenceof the visual cortex. Flicker and the fusion of a flickering light as the rate increases is another function of the visual system possibly similar to light intensity; however, knowledge of the neural correlates of flicker is meager. Schwartz and Clark (9) have 1 This investigation was aided by grant B-868, National Institutes of Health, United States Public Health Service. Present address of Dr. Taravella: Kirksville College of Osteopathy and Surgery, Kirksville, Missouri; of Dr. Clark: United States Army Research Institute of Environmental Medicine, Natick, Massachusetts. 282
PHOTIC
STIMULATION
283
shown that rats can relearn a flicker discrimination after ablation of the striate cortex and Kappauf (4) stated in an abstract that cats were able to discriminate flicker with or without a striate cortex. Since no detailed report of this work ever appeared and no histological data were offered this finding of Kappauf can hardly be considered conclusive. The development by Halstead” of a modification of the Yerkes two-choice discrimination apparatus suitable for flicker studies with cats afforded a ready technique to evaluate the report of Kappauf. Furthermore, such a study might make possible a settlement of the old controversy over whether or not the fusion resulting from an increase in the rate of flicker was a central or retinal phenomenon. Methods Apparatus: A modified Yerkes double-choice discrimination box was used. This consistedof a lightproof entry box attached to a runway which was divided by a partition at the far end into two smaller runways. Each of the smaller runways terminated in a transparent, hinged at the top, door 22 cm square. Moving the door permitted access to a food receptacle. A light was centered behind each door at a distance of 108mm. The driver unit which powered the lights was a stable electronic device designedto generate a square wave with equal on and off periods over a continuously adjustable frequency range from 10.5 to 65 cycle/set. The driver also provided a continuous direct current for the steady light. Each light had its own brightness control and the positions of the steady and flickering lights could be alternated by meansof a silent switch. Each light source consisted of a Neon glow tube (NE-32) surrounded by a conical metal reflector closed by a ground glass cover. This gave a circular light source 7 cm in diameter and of uniform intensity. Illuminance was measuredat the surface of the frosted glasswith a photographic exposure meter. The highest brightness used was arbitrarily selected and was well below the customary limits for cone vision. For this reason all training and testing were under dark-adapted conditions. Training Sequence and Testing Methods. The cat was placed in the dark starting box and left there for 20 min. An opaque sliding door was lifted allowing the animal to seeboth lights through a similar transparent door. The transparent door was lifted so that the animal could 2 Halstead,
W. C.: Personal
communication.
284
TARAVELLA
AND
CLARK
approach the lights. The animal made a choice by touching the transparent door at the end of one of the small alleys. If correct, the door would open and the cat could obtain a small piece of fresh fish. Both doors were, of course, baited. Whether or not a correct choice was made the animal was immediately returned manually to the starting box,
FIG. 1. Serial sections through lateral geniculate nuclei of cat 2. In Figs. l-3 plete loss of large cells is indicated by cross hatching; areas with only scattered cells, by dots; normal or virtually normal areas are lined.
comlarge
Routinely such noncorrection trials were made; however in preliminary training and when motivation was low the animals were allowed to correct their choices. Such corrected choices were scored as errors. Usually sixty trials per day were made with the positions of the flickering and steady lights varied according to the Gellerman series. Training and testing were begun at 15 cycle/set. The frequency was increased by 2 cycle/set after the animal had made eight or more correct choices
PHOTIC
28.5
STIMULATION
out of a block of ten trials. Training was terminated when the animals had for 3 to 5 days successfully discriminated between 65 cycle/set and the steady light. Ablation Studies. After a successfulperiod of performance at 65 cycle/ set (the highest obtainable with the driver) varying amounts of striate
FIG. 2.
Serial
sectionsthrough
lateral
geniculate
nuclei
of cat 3.
and parastriate cortex were removed by subpial suction. In the three animals with the largest lesions the ablations extended anteriorly almost to the ansate sulcus and laterally to include the superior and posterior suprasylvian gyri. After a 2-week recovery period training and testing were resumed.At the conclusion of testing and training the animals were killed and perfused with acacia saline followed by acacia formalin (5). The brains were embedded in celloidin, sectioned at 50 u and every tenth section stained with cresyl violet acetate.
286
TARAVELLA
AND
CLARK
Since variations in nonstriate tissue ablated did not alter the behavior of the animals as assessedby the test used while variations in amount of striate cortex did, it seemedsufficient to report only the changes in the lateral geniculate nuclei. In Figs. 1, 2, and 3 are shown a series
FIG.
3.
Serial
sections
through
lateral
geniculate
nuclei
of cat
8.
of tracings through the lateral geniculate nuclei of these animals. These show the locations where intact large cells persisted. In the cat, these are the only cells which disappear following striatectomy (7). Results
When it was found that the cats were discriminating at levels much higher than anticipated (under similar conditions of dark adaptation,
PHOTIC
287
STIMULATION
light intensity, size of test patch and distance from test patch, Clark3 found critical flicker fusion levels in the low forties in a small group of humans) a series of control studies were made in an attempt to determine if the cats were utilizing extraneous cues: i. Operators were repeatedly switched to eliminate possible operator cues. ii. Fluorescent bulbs were substituted for the routinely used neon tubes. This eliminated possible high-frequency noise as a differential cue. iii. Masking noises were used to render indistinguishable the sounds normally present. iv. The steady light was driven by a second driver at 90 cycle/set. v. Since the sharp edge of the light might make possible some stroboscopic effect, the
to
20
30
40
50
60
70
60
90
DAYS 4. Preoperative (circles) Figs. 4-6 the highest frequency score indicates that performance FIG.
and postoperative (squares) scores asttained as 80% level is plotted for on that day did not reach 80% level.
of cat 2. In each day; no
test patch was redesigned to present a luminous center with no distinct margins. vi. The brightness of the steady lamp was varied so that it was at times brighter, the same or dimmer than the flickering lamp. This eliminated a brightness discrimination as a factor. Since none of these affected, more than momentarily, the performance of the animals, it was concluded that the actual negative stimulus must be the flickering light. The results of the preoperative training sessions are shown in Figs. 4, 5, 6, and 7. In the first three of these, the preoperative and postoperative scores are shown by circles and squares, respectively. In these the highest a Clark,
George:
Unpublished
work.
288
TARAVELLA
AND
CLARK
flicker frequency discriminated each day in any block of ten trials at the 80% discrimination level is shown with the time scale as abscissas. Days when performance was below the 80% level are indicated by blank spaces. There is a general similarity in the shape of the preoperative 60
IO
20
30
40
50
60
70
80
90
DAYS FIG.
5.
Preoperative
(circles)
and
postoperative
(squares)
scores
of cat
3.
80 1
. . . .. .. .. .. .*.... . ... .. ... .
l a.* .
60
IO
20
30
40
50
60
70
80
of cat
8.
DAYS
FIG. 6.
Preoperative
(circles)
and
postoperative
(squares)
scores
curves. In each, initial criterion is reached only after some days of training. Then, there is a period of rapid learning followed by several to many days with little improvement. Following this plateau, there is further and substantial improvement in the highest frequency discriminated to the maximum of 6.5 cycle/set. This maximum was deter-
PHOTIC
289
STIMULATION
mined by the driver used. It required from 3 to 9 days to reach the 80% level at the lowest frequency used and from 42 to over 60 days to reliably discriminate at the 65 cycle/set level. Cat 2 had a slight case of distemper during training and in this period there was a sharp drop in the highest frequency discriminated. Similar episodes in other animals may represent periods of otherwise symptomless illness. NUMBER 500
1000
I
80
OF TRIALS
15002000
I
I
I
. .. . . ..
0
. .,
.
60
z !i 40 0 ii l.L 20
2To I 750I
12Y0
PRE-OPERATIVE
z
500
2500
l
.
5
POST-OPERATIVE .. . . . .
.
..
. .
.* . . .
.
..‘* .
.
. ..-
l
*
.
.
.
.
: .
. .
PAUSE IN TRAINING-A
I IO
I 20
I 30
E I
40
5b
60
SURGICAL -RECOVERY
r&--z
DAYS FIG.
training operation
7.
Preoperative, was of 2 weeks and testing.
retention duration
and postoperative scores on cat 10. The pause in corresponding to the 2-week routine delay between
Postoperative testing and training are shown graphically in the same figures. In the caseof cat 10, preoperative, postoperative and, in addition, training after a delay period of 2 weeks are shown in a single figure (Fig. 7). Since 2 weeks was the interval between operation and retraining in all the animals, this delay period (in cat 10) serves to give some measure of the possible loss in ability to discriminate simply as a result of cessation of training. The graphs of postoperative performance fall into three distinct groups. There is only one animal (cat 3) in the first of these. This animal was able to discriminate at a high level (43 cycle/set) on the first day of testing. Nevertheless, it was more than 60 days and almost 3500 trials later before it was able to discriminate at the preoperative level. Cats 2
290
TARAVELLA
AND
CLARK
and 4 also discriminated at relatively high levels on the first day of testing (32 and 39 cycle/set, respectively). However, even after more than 80 days of training and over 4000 trials, neither ever reliably attained preoperative levels of discrimination. The other three animals (cats 8, 9, and 10) have decidedly different records. Only one of these discriminated between the flickering and steady light on the first day of testing but within 10 days and 500 trials all had discriminated at 6 5 cycle/set . The diagrams of the destruction in the lateral geniculate nuclei in Figs. 1, 2 and 3 make it apparent that the animals all had varying amounts of intact striate cortex remaining. This ranged from considerable (cat 3) to slight (cat 2) to virtually none (cat 8). The lesion and the degeneration in the lateral geniculate nuclei in cat 4 was very similar to that in cat 2, while the lesions and the degeneration in the lateral geniculates in cats 8, 9, and 10 were much the same. In the figures (1, 2, and 3) showing the lateral geniculate nuclei areas of complete disappearance of large cells are indicated by cross hatching, areas where scattered large cells remained are dotted and normal or virtually normal areas are lined. This separation of the animals into three groups on the basis of the histological findings is identical with that based on their postoperative records. In cat 10, who was run subsequent to the others, there was interposed a 2-week delay period between original training and operating during which no training or testing occurred. Testing began after this pause. The animal reached over 30 cps on the first day and attained 65 cps on the seventh day (Fig. 7). The slope of the curve of this performance is very similar to the postoperative curve in the same animal and to that of the other two animals with virtually complete striate removals (cats 8 and 9). However, it should be noted that after the delay period there was retention of the discrimination, while after operation performance was below the 80% level until the fourth day of retraining. The postoperative loss in ability to discriminate was thus considerable despite the subsequent rapid relearning. Discussion
We have thus confirmed the incomplete report of Kappauf (4) and have extended the findings of Schwartz and Clark (9) to another species. Discrimination of intermittent photic stimulation like the discrimination of light intensity can be relearned following removal of the striate cortex.
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In both of these discriminations some nonstriate mechanism must be present which can mediate the discrimination. Since photic stimuli can activate the reticular formation it is tempting to assume that this may be another of the myriad of functions of this overworked region. However, the nature and locus of this nonstriate mechanism must remain for future work to determine. The relationship of these results to critical flicker fusion in humans is also largely conjectural. The possibility of adequate verbal directions and familiarity with various forms of flicker in the human makes unnecessary the long learning period during which each increase in frequency may be presumed to present a new problem to the animal. However, if the early rapid rise in frequency discriminable represents striatal learning and the subsequent rapid rise nonstriatal learning, then the intervening plateau might be comparable to critical flicker fusion frequency (CFF) in man. Some support for this concept can be derived from several sources. This rate is only slightly above the human fusion level found by Clark” who used the same driver and lights used for the cats. Schwartz4 using a go-no-go procedure for the study of flicker in cats found a CFF at about the average rate during the plateau. This average rate is also in the range found by Lindsley (6) in the cat for maximum cortical following of an intermittent photic stimulation. Again, however, more work is needed to settle this issue. An explanation for the three types of postoperative curves obtained is difficult and is definitely limited by the small number of animals used in this experiment. However, since histological findings resulted in the same three groups it seems appropriate to assume that the grouping reflects the varying amounts of damage to the geniculostriate system. If this be so then the plateau may represent a period when fusion is present at the striate level and when the animal is making a shift to some nonstriate mechanism which is able to handle the higher frequencies. It would seem, too, that retention of the discrimination and a very slow shifting to the nonstriate mechanism could occur with considerable striate tissue remaining, and that retention of the discrimination and an inability to shift to the nonstriate mechanism might also occur. Finally either no retention or retention with only use of the nonstriate mechanism might occur. This is, of course, only a restatement of the results of the 4 Schwartz,
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experiment, but it does suggest the concept that perhaps remnants of a functional area might be more damaging to the animal than complete ablation in that the remnants might inhibit the functioning of subsidiary mechanisms. Such an interference hypothesis would require substantiation. The question of whether fusion is a retinal or a central phenomenon probably dates at least from Sherrington (10) but is still unanswered. Ireland (3) stated “the results of the present investigation are regarded as offering definite evidence for the importance of central factors in the phenomena of flicker and fusion.” On the other hand Enroth (l), who makes no mention of Ireland’s work, states that it “seems likely that flicker fusion takes place in the retina.” Our data definitely support the position of Ireland (3). As shown above there were three types of postoperative scores in our animals. The crucial group consists of cats 2 and 4. Preoperatively they could discriminate between 65 cycle/set and a steady light so they must have had a CFF greater than 6.5 cycle/set. Their failure, postoperatively, to discriminate at levels below 65 cycle/ set indicates a postoperative fusion level less than 65 cycle/set. The fact that with more complete removals of striate cortex preoperative levels were attained postoperatively rules out the use of retrograde retinal damage as the cause of the loss in fusion levels. At the very least these findings in our experiments show that central elements are concerned in fusion and that fusion is not a strictly retinal phenomenon. There are two other reports on effects of brain damage on CFF in subhuman vertebrates. Goldzband and Clark (2) found little effect on CFF as a result of frontal lesions in rats. Mishkin and Weiskrantz (8) compared the effects of frontal, infratemporal and occipital lesions on CFF in monkeys. No anatomical details are given but reference is made to similar lesions in two earlier papers. In these earlier papers the diagrams of the lateral geniculate nuclei are so small as to be worthless. For this reason, despite the evident impairment of their occipital animals, no comparison with our animals would be fruitful. References I.
2.
ENROTH, C. 1952. The mechanism of flicker and fusion studied on single retinal elements in the dark-adapted eye of the cat. Acta Pltysiol. Stand. 27 (Suppl. 100): l-67. GOLDZBAND, M. G., and G. CLARK. 1955. Flicker fusion in the rat. /. &net. Psychol. 87: 257-264.
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F. H. 1950. A comparison of critical flicker frequencies under conof monocular and binocular stimulation. /. Erptl. Psych. 40: 282-286. KAPPAUF, W. E. 1940. The foundation of the visual cortex in relation to level of brightness adaptation. Psychol. Bull. 37: 495-496. KOENIG, H., R. A. GROAT, and W. F. WINDLE. 1945. A physiological approach to perfusion-fixation of tissues with formalin. Stain Technol. 20: 13-22. LINDSLEY, D. B. 1954. Electrical response to photic stimulation in visual pathways of the cat. Electroencephalog. and Clin. Neurophysiol. 6: 690-691. MIXKOWSKI, M. 1913. Experimentelle Untersuchungen iiber die Beziehungen der grosshirnrinde und der Netzhaut zii den primLren optischen Zentren, besonders zum Corpus Geniculatum externum. Arb. Hirnandt. Inst. Ziirich. 7: 257-361. MISHICIN, M., and L. WEISKRANTZ. 1959. Effects of cortical lesion in monkeys on critical flicker frequency. J. Camp. and Physiol. Psychol. 62: 660-666. SCHWARTZ, A., and G. CLARK. 1957. Discrimination of intermittent photic stimulation in the rat without its striate cortex. J. Corn@. and Physiol. Psychol. 46: 119-126. SHERRINCTON, C. 1904. On binocular flicker and the correlation of activity of “corresponding” retinal points. Brit. J. Psychol. 1: 26-60. IRELAND,
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