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Perception of apparent motion of colored stimuli after commissurotomy
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Pergamon
PII: S0028 3932(96)00019-X
Neuropsychologia, Vol. 34, No. 11, pp. 1041-1049, 1996 Copyright © 1996 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0028-3932/96 $15.00+0.00
Perception of apparent motion of colored stimuli after commissurotomy NEELAM NAIKAR* Department of Psychology, University of Auckland, Private Bag 92019, Auckland, New Zealand (Received 7 August 1995; accepted 10 January 1996)
Abstract--One subject with complete forebrain commissurotomy (L.B.), another with posterior callosotomy (D.K.), and eight normal controls were presented with successive pairs of red and/or green lights, on either side of the retinal midline and within the
left and right visual fields. All of the subjects could discriminate the direction of apparent motion in all three locations, although L.B. was poorer on bilateral than unilateral presentations. Moreover, on bilateral presentations, L.B. was significantly poorer at identifying the color of the first light than the color of the second light. In contrast, D.K., like the control subjects, was equally good at identifying the color of either light. These and other results provide evidence that a subcortical shift in attention enables L.B. to discriminate the direction of apparent motion across the midline. On the other hand, a more robust mechanism involving the middle temporal area of the cortex must be responsible for tracking motion in D.K. and the control subjects. On the basis of these findings, it is suggested that the superior colliculus may contribute to direction sensitivity in the middle temporal area by mediating shifts in spatial attention. Copyright © 1996 Elsevier Science Ltd. Key Words: split brain; corpus callosum; superior colliculus; middle temporal area; motion; color; attention.
was only aware of a single light. In contrast, he performed perfectly within each visual field. However, Naikar and Corballis [26] failed to replicate this result in L.B. or in a subject with posterior callosotomy, D.K. These subjects had no difficulty discriminating single lights from successive pairs, regardless of whether presentation was bilateral or unilateral. Furthermore, unlike N.G. [30], they were not impaired at discriminating simultaneous from successive pairs. In addition, both subjects were able to discriminate single lights from simultaneous pairs, and leftward from rightward succession. The accuracy of the subjects on these tasks did not depend on the spatial (2 ° or 7 °) or temporal separation (33 or 133 msec) of the lights, contrary to Trevarthen's [37, 38] proposition that only long-range apparent motion is represented subcortically. The only sign of disconnection was that L.B. was slower to respond to bilateral than unilateral succession. However, further evidence of disconnection was elicited in a task involving single-light, simultaneous, and successive presentations; L.B. was significantly impaired in judging whether movement had occurred across the midline, although he could do so nearly perfectly within each visual field [26]. This difficulty seemed to be specific to discriminating single lights from successive pairs; he had no trouble identifying simultaneous presentations as
Introduction
Several studies have investigated whether apparent motion may be perceived by split-brained subjects, when two lights are flashed successively to opposite hemispheres of the disconnected brain [11, 14, 26, 30]. In one study, Ramachandran et al. [30] tested three subjects with complete section of the corpus callosum, the anterior and hippocampal commissures, and the massa intermedia if it was present (L.B., N.G., A.A.). L.B. and A.A. were able to discriminate leftward from rightward succession across the midline, and both of these from simultaneous presentations. N.G. was also able to discriminate leftward from rightward succession but she reported all simultaneous pairs to be moving. Although these results suggest that L.B. and A.A., at least, are essentially normal in perceiving apparent motion across the midline, Gazzaniga [14] reported that J.W., who had complete section of the corpus callosum but not of the anterior commissure, was unable to discriminate single lights from presentations of bilateral succession. On all of the successive presentations, J.W. responded that he saw no movement suggesting that he
* Fax: 64-9-3737450. 1041
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not moving. In addition, he continued to respond slowly to bilateral compared to unilateral succession. D.K., on the other hand, was able to judge whether movement had occurred or not, and in a subsequent task involving the same stimuli, he could also report the direction of movement on successive presentations. Corballis [11] also found evidence for disconnection when L.B. was required to discriminate simultaneous from successive pairs of lights that had a duration of only 17 msec. In the studies by Ramachandran et al. [30] and Naikar and Corballis [26] the duration of the lights was as long as 130 and 133 msec, respectively. The interstimulus interval in these studies ranged from 30 to 133 msec. Under the conditions in Corballis's task, L.B. reported nearly all bilateral successive pairs as simultaneous, although his performance in the unilateral condition was above chance. Corballis suggested that cortical commissures were necessary for fine temporal resolution across the midline. As the duration of the lights in Gazzaniga's [14] study was not reported, it is possible that J.W. was unable to discriminate succession across the midline because the duration of the lights was too short. From these studies it is evident that commissurotomy may result in some loss in the ability to perceive apparent motion across the midline. However, for the most part, split-brained subjects are able to discriminate apparent motion across the midline. The mechanism that is engaged may involve a subcortical shift in attention from the first light to the second light. The hemisphere registering the second light would be able to discriminate that movement must have been toward that light from the other side. However, a single light would also attract attention, which may explain why J.W. was unable to discriminate single lights from successive pairs [14]. That L.B. was able to perform this discrimination but had difficulty when simultaneous pairs were also involved suggests that he may have had a residual but fading trace of the first light that was relatively easy to detect in the context of simple discriminations but not when more complex discriminations were required [26]. To support the proposition that a subcortical attentional mechanism allows split-brained subjects to discriminate apparent motion across the midline, there is substantial evidence for the role of subcortical pathways in attention. For example, it has been shown that the superior colliculus of rodents is involved in the attentional components of spatial behavior [36, 22]. Furthermore, from studies with macaques, there is evidence that spotlight attention depends on the pulvinar nucleus, which receives input from the superior colliculus [27]. In addition, a study with normal human subjects has shown that the retinotectal pathway contributes to the reflex orienting of visual attention [28], and in a task with human split-brained subjects it has been shown that a spatial cue in one visual field is just as effective in directing attention to a target in the opposite visual field, as when the cue and target appear in the same visual field [17].
Another mechanism for the discrimination of apparent motion involves the middle temporal (MT) area of the cortex. This area is highly specialized for the direction, orientation, and speed of stimulus movement [20]. Moreover, it has been shown that MT neurons are involved in processing apparent motion [23]. Tracking by area MT can account for the near perfect performance of control subjects and the near perfect unilateral score of splitbrained subjects in discriminating apparent motion [26]. However, this mechanism would be incapacitated after commissurotomy, which explains why split-brained subjects may have to resort to other sources of information for discriminating apparent motion across the midline. That D.K. had little difficulty with bilateral succession [26] suggests that the cerebral commissures interconnecting MT in the two hemispheres must be intact in this subject. These commissures are thought to be located in the anterior and posterior midbody of the corpus callosum [41], areas that may well be spared in D.K. While the role of MT in the perception of visual motion has been extensively documented, the contribution of subcortical pathways to this function is less apparent. It is known that the major subcortical input to MT is from the lateral and inferior pulvinar, which receives projections from the superior colliculus [4, 5]. It has also been demonstrated that lesions to the striate cortex in macaques do not eliminate the direction sensitivity of MT neurons, whereas subsequent damage to the superior colliculus does [16, 32, 33]. The superior colliculus must therefore be able to maintain direction sensitivity in MT in the absence of the striate cortex. However, neurons in the superior colliculus are insensitive to the direction of motion [15], and any little direction sensitivity in the lateral and inferior pulvinar is eliminated by striate cortex removal [3]. Thus, visual input reaching MT by the tectopulvinar route must be nonselective [16, 32, 33], and area MT must have the capacity to produce directionally selective responses from nonselective input [16, 24, 25, 32, 331. As indicated from the results of split-brain research in the area of apparent-motion perception, the tectopulvinar input to MT may involve spatial attention. Shifts in attention directed by the superior colliculus could register in MT through several routes, including the pulvinar nucleus, striate cortex, or via lateral geniculate nucleus projections to the striate cortex and areas V2, V3, and V4 [4, 5, 6, 20]. Hence, even in the absence of striate cortex there are routes by which collicular shifts in attention could register in MT. This may explain why MT neurons remain directionally selective in the absence of the striate cortex, and why this visual responsiveness is eliminated after subsequent lesions to the superior colliculus [16, 32, 33]. The purpose of this paper is to provide further evidence that a subcortical shift in attention may allow splitbrained subjects to discriminate the direction of apparent motion across the midline. L.B., D.K., and eight control subjects were tested. In the critical tasks, spatially sep-
N. Naikar/Perception of motion of colored stimuli after commissurotomy a r a t e d pairs o f red a n d / o r green lights were presented in succession, b o t h within a n d between fields. T h e subjects were required to d i s c r i m i n a t e the direction o f a p p a r e n t m o t i o n a n d in s u b s e q u e n t tasks, to identify the c o l o r o f the first a n d second lights. It was h y p o t h e s i z e d that a l t h o u g h L.B. w o u l d be able to d i s c r i m i n a t e the direction o f a p p a r e n t m o t i o n across the midline, he w o u l d be better at identifying the c o l o r o f the second light than the c o l o r o f the first light. A shift in a t t e n t i o n from the first to the second light w o u l d allow L.B. to discriminate the direction o f a p p a r e n t m o t i o n on bilateral presentations. However, as a result o f c o m m i s s u r o t o m y , the hemisphere registering the second light w o u l d have no i n f o r m a t i o n a b o u t the c o l o r o f the first light. It has been shown that L.B. c a n n o t m a k e same/different j u d g m e n t s a b o u t colors presented on either side o f the midline [18], which indicates that there is little transfer o f c o l o r i n f o r m a t i o n in the absence o f the c o r p u s callosum. A s s u m i n g that the hemisphere registering the second light is the one controlling response, L.B. should be better at identifying the c o l o r o f the second light than the c o l o r o f the first light. In contrast, on unilateral presentations, L.B. should be equally g o o d at identifying the c o l o r o f the first a n d second lights. D . K . was also tested. If a cortical t r a c k i n g m e c h a n i s m is responsible for his ability to d i s c r i m i n a t e a p p a r e n t m o t i o n across the midline, either hemisphere should be able to identify the c o l o r o f the first or second light. P r e s u m a b l y , the c o l o r o f a light w o u l d be identified by the hemisphere registering that light. Hence, D . K . should be equally g o o d at identifying the c o l o r o f the first a n d second lights, on bilateral as well as unilateral presentations. This p a t t e r n o f p e r f o r m a n c e should also be observed in the c o n t r o l subjects. All o f the subjects were also required to identify the c o l o r o f a single light presented in the left o r right visual field, in o r d e r to d e t e r m i n e the ability o f each hemisphere to identify red a n d green colors.
General method Sul?iects Two commissurotomized subjects were tested on all of the tasks. L.B., who was 43 years old at the time of testing, had complete section of the corpus callosum, and anterior and hippocampal commissures, for the relief of intractable epilepsy in 1963, when he was 12 years and 11 months of age. Magnetic resonance imaging has confirmed that his corpus callosum is sectioned completely [7]. Further information regarding his neurological condition may be obtained elsewhere [8]. D.K., who was 27 years old at the time of testing, had a partial commissurotomy in the course of surgery for an arteriovenous malformation in the medial face of the right occipital lobe. He was 18 years of age at the time. A C T scan has confirmed complete section of the posterior third to half of the corpus callosum [26]. Optometric testing has indicated a defect in the upper left quadrant of the left visual field. Further details may be obtained elsewhere [12].
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Eight control subjects participated in all of the tasks. There were four males and four females. They ranged from 19 to 48 years of age, with a mean age of 29 years. Five of the subjects were right-handed and the other three were left-handed.
Equipment and sthnuli Presentation of the stimuli was controlled by an IBM-compatible computer with a fast-fade VGA screen. The subjects were required to key-in their responses on a keyboard. The stimuli were either red or green spots of light, 0.7 cm in diameter, flashed on a black background. In all of the tasks, the duration of the lights was 133 msec. In tasks involving successive presentations, the interstimulus interval was 33 msec and the spatial separation was 7 . In Task 1, the subjects were required to identify the color of a single light presented in the left or right visual field. The light was either red or green in color. Each color was presented at three levels of luminance to determine whether the subjects could discriminate the two colors independently of brightness (Red = 6.24, 8.87, 10.35 cd/m2; Green = 7.19, 9.12, 11.53 cd/m2). This was necessary as equiluminance of the red and green colors could only be approximated on subsequent tasks. The single light was presented in each of four locations: 10.5" to the left, 3.5 to the left. 3.5 t o the right, and 10.5 to the right of central fixation. Tasks 2.3, and 4 involved both bilateral and unilateral presentations of two lights in succession. The pairs of lights were presented in all four possible color combinations: red red, green-green, red green, and green-red. The colors were approximately equiluminant to prevent the subjects from discriminating them on the basis of brightness (Red = 8.87 cd/m 2, Green = 9.12 cd/m2). The successive pairs appeared in adjacent positions at the same locations as the single lights. On half of the presentations, the second light was flashed to the right of the first light so that rightward apparent motion was created. On the other half of the trials, the second light was flashed to the left of the first light so that leftward apparent motion was created. The order of the tasks for L.B. was Task 2, 4, 3, 1, whereas for D.K. it was Task 3, 4, 1,2. For the control subjects, the order of the tasks was counterbalanced. Each of the tasks consisted of four blocks of trials. L.B. and four of the control subjects responded with their left hand on the first and fourth blocks and with their right hand on the second and third blocks. D.K. and the other four control subjects responded with their right hand on the first and fourth blocks and with their left hand on the second and third blocks. Each block began with 10 practice trials which were randomly selected from the experimental trials. Task 1 consisted of 48 experimental trials per block, whereas in the remaining three tasks there were 72 experimental trials per block. Within each block, there were equal numbers of trials Jbr each stimulus condition presented in random order. When a trial was initiated by pressing the space bar, a central fixation cross appeared, which was followed 500 msec later by the appearance of the stimuli. The subjects responded by pressing either the M or N key with the forefinger and middle finger of one hand. On all of the tasks, feedback in the form of a short tone was given to incorrect responses.
Analysis Ofresults When the performance of the commissurotomized subjects fell below 95%, in either visual field or in the bilateral condition of a task, multidimensional chi-squared analyses [40] were con-
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ducted to determine the effects of stimulus condition (green vs red, leftward succession vs rightward succession), field, direction of succession, hand used for response, luminance, and their interactions. Discrimination accuracy was indexed by the interaction between stimulus condition and response selection, whereas response bias was indexed by response selection effects only. These analyses were carried out only for the commissurotomized subjects as the performance of the control subjects was at or near ceiling on all of the tasks.
Task 1: Color of single light In this task, the subjects were required to identify the color of a single red or green light presented in the left or right visual field. The purpose of the task was to establish the ability of each hemisphere to identify red and green colors. Each color was presented at three levels of luminance to determine whether the subjects could discriminate the two colors independently of brightness. The subjects were asked to press the N key if the light was green or the M key if it was red.
discrimination, as indicated by a significant effect of the color of the light on response selection [X2(1, N = 192)= 165.04, P < 0.001]. Furthermore, like L.B., his accuracy did not depend on the field of presentation of the light [22(1, N = 192)=0.02]. In addition, his performance in the left visual field was well above chance [22(1, N = 96) = 70.07, P<0.001], although it was slightly poorer than the control subjects. There were no significant effects of luminance or the hand used for response. The results of this task show that L.B., D.K. and the control subjects can identify the color of a single light presented in the left or right visual field. As none of the subjects showed significant hemispheric differences in performance, any asymmetry in subsequent tasks cannot be attributed to hemispheric differences in color-identification. Also note, that the subjects could identify the red and green colors despite being prevented from using brightness information for this purpose. It is therefore unlikely that they would rely on variances in luminance for identifying the colors on subsequent tasks.
Results and discussion
Task 2: Direction of successive pairs
L.B. Table 1 shows that L.B. was slightly better at identifying the color of a single light in the left than right visual field. L.B. had a high level of overall discrimination, as indicated by a significant effect of the color of the light on response selection [22(1, N = 192)= 114.53, P<0.001]. Moreover, his performance in the left and right visual fields was not significantly different [22(1, N = 192)= 1.34]. In addition, although L.B. was slightly less accurate than the control subjects, his performance in both visual fields was well above chance [LVF: Z2(1, N = 9 6 ) = 7 0 . 0 7 , P<0.001; RVF: 22(1, N = 9 6 ) = 4 6 . 3 6 , P < 0.001]. There were no significant effects of luminance or the hand used for response. D.K. Table 1 shows that D.K. was slightly better at identifying the color of a single light in the right than left visual field. D.K. also had a high level of overall
The results of a previous study showed that L.B. and D.K. were 100% accurate at discriminating the direction of apparent motion of white lights across the midline [26]. The purpose of this task was to determine whether they would be able to discriminate the direction of apparent motion of colored lights. Red and/or green lights were presented in succession on either side of the midline and within each visual field. The subjects were asked to press the N key if movement was to the left or the M key if it was to the right.
Results and discussion L.B. Table 1 shows that L.B.'s accuracy was markedly low in the bilateral condition. L.B. had a high level of
Table 1. Percent correct obtained by L.B., D.K. and control subjects in each task, as a function of field Task
Subjects
LVF
I. Color of single light
L.B. D.K. Controls L.B. D.K. Controls L.B. D.K. Controls L.B. D.K. Controls
92.7 92.7 98.0 100.0 100.0 98.3 68.8 68.8 97.8 74.0 78.1 97.2
2. Direction of successive pairs 3. Color of the first light 4. Color of the second light
BIL
RVF
Total
71.9 100.0 99.2 54.2 89.6 97.5 75.0 90.6 97.1
84.4 100.0 98.8 99.0 97.9 98.7 62.5 87.5 96.5 76.0 94.7 97.1
88.5 96.4 98.4 90.3 99.3 98.7 61.8 81.9 97.3 75.0 87.8 97.2
N. Naikar/Perception of motion of colored stimuli after commissurotomy overall discrimination, as indicated by a significant effect of the direction of succession on response selection [22(1, N = 288) = 186.89, P < 0.001 ]. However, his performance depended on the field of presentation [)C2(2, N=288)-19.53, P<0.001]. Paired comparisons showed that his accuracy in the bilateral condition was significantly poorer than in the left and right visual fields [BIL vs LVF: 22(1, N= 192)= 31.42, P < 0.001; BIL vs RVF: 22(2, N = 192)= 28.26, P < 0.001]. A separate analysis of L.B.'s performance on bilateral presentations, showed no significant effects or interactions between the color of the first light, the color of the second light, the direction of succession, or the hand used for response. There were also no significant effects or interactions between these variables on overall performance, Although L.B.'s performance in the bilateral condition was above chance [22( 1, N = 96) = 18.38, P < 0.001 ], it was significantly poorer than his ability to discriminate the direction of apparent motion of white lights across the midline [X2(1, N= 144)= 16.62, P<0.001] [26]. On unilateral presentations, his performance in both tasks was at or near ceiling. Earlier, it was suggested that L.B. may have discriminated the direction of apparent motion of white lights across the midline on the basis of a subcortical shift in attention from the first to the second light. In this task, his performance may have deteriorated because his attention remained focussed on the first light instead of shifting to the second light. Hence, he would have incorrectly inferred that movement had occurred towards the first light. A possible reason for attention remaining focussed on the first light is that the luminance of the colored lights was considerably lower than that of the white lights (97,5 cd/m 2) used by Naikar and Corballis [26]. Hence, the onset of the second light may not have always resulted in a shift in attention across the midline. Consistent with this suggestion are reports that blindsight performance cannot be obtained when the luminance of a target stimulus is reduced [2, 21]. It has also been observed that the latency to initiate a saccade by human subjects is greater when the target luminance is low [31]. It is unlikely that the color of the lights hampered the attentional mechanism as neurons in the primate superior colliculus are largely insensitive to color [35]. Nevertheless, L.B. was able to discriminate the direction of apparent motion on a significant proportion of bilateral presentations in this task. Therefore, if an interhemispheric attentional shift enables L.B. to discriminate the direction of apparent motion across the midline, it can still be expected that he would be better at identifying the color of the second light than the color of the first light on bilateral presentations of succession. D.K. Table 1 shows that D K . , like the control subjects, scored near ceiling at discriminating the direction of apparent motion. That the performance of these subjects was not affected by the luminance of the colored lights is consistent with the properties of MT; it has been found that neurons in this area in monkeys are active under
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conditions of low stimulus contrast [10, 13], and make the same response to moving stimuli regardless of color [1, 19].
Task 3: Color of the first light
In this task, the subjects were required to identify the color of the first of two lights presented in succession. Pairs of red and/or green lights were presented within each visual field and on either side of the midline. The subjects were instructed to press the N key if the color of the first light was green or the M key if it was red.
Results and discussion L.B. Table 1 shows that L.B. performed more poorly than the control subjects in all three field conditions. Although the effect of field on response selection failed to reach significance [22(2, N = 288)---4.14], paired comparisons showed that L.B.'s performance in the bilateral condition was significantly poorer than in the combined unilateral condition (left and right visual fields) [g2(1, N = 288) = 4.84, P < 0.05]. Moreover, his performance in the bilateral condition did not exceed chance, although it was well above this level in the left and right visual fields [BIL: 22(1, N=96)=0.67; LVF: 22(1, N = 9 6 ) = 13.89, P<0.001; RVF: 22(1, N=96)=6.00, P<0.025]. These results indicate that response on bilateral presentations must have been controlled by the hemisphere registering the second light; as a result of commissurotomy, this hemisphere would have no information about the color of the first light. Another significant effect was the color of the second light on response selection [22(1, N=288)=4.53, P < 0.05]. Paired comparisons showed that this effect was significant in the bilateral condition but not in the left or right visual fields [BIL: 22(1, N=96)=4.20, P<0.05; LVF: Z2(1, N = 9 6 ) = 1.54; RVF: 22(1, N=96)=0.17]. An examination of L.B.'s responses on bilateral presentations showed that he had a significant tendency to report that the color of the first light was what the color of the second light had been (58/96). This result is consistent with the proposal that on presentations of bilateral succession, L.B.'s attention must shift from the first to the second light. The hemisphere registering the second light would have no knowledge of the color of the first light, and may therefore simply report the color of the second light instead. D.K. Table 1 shows that in contrast to L.B., D.K.'s accuracy was highest in the bilateral condition. Although D.K. had a high level of overall discrimination, as indicated by a significant effect of the color of the first light on response selection [22(1, N = 288) = 120.37, P < 0.001], his performance depended on the field of presentation [~(2(2, N=288)=10.35, P<0.01]. Paired comparisons
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showed that D.K.'s accuracy in the left visual field was significantly poorer than in the bilateral condition and right visual field [LVF vs BIL: ;(2(1, N = 192)= 12.63, P < 0.001; LVF vs RVF: ;(2(1, N = 192)=9.87, P < 0.005], Nevertheless, his performance in the left visual field was above chance [;(2(1, N = 96) = 14.11, P < 0.001 ]. There was no significant difference in accuracy between the bilateral condition and the right visual field [;(2(1, N = 192)= 0.21], and his performance in both of these locations was well above chance [BIL: ;(2(1, N = 96) = 60.17, P < 0.001; RVF: ;(2(1, N = 9 6 ) = 57.60, P<0.001]. D.K.'s poor score in the left visual field may be due to a defect in the upper-left quadrant of this field, as a result of right occipital lobe damage. This damage may be in area V4, which is located in the inferior occipital lobe in humans [39]. Unpublished tasks in our laboratory show that on a simple reaction time task, D.K. is impaired in detecting a grey target when it is flashed on a yellow background of equal luminance on presentations in the left but not in the right visual field. In contrast, he is not impaired at detecting a white target flashed on a black background in either visual field.
Task 4: Color of the second light In this task, the subjects were required to identify the color of the second of two lights presented in succession. Pairs of red and/or green lights were presented on either side of the midline and within each visual field. The subjects were instructed to press the N key if the color of the second light was green or the M key if it was red.
Results and discussion L.B. Table 1 shows that L.B.'s performance was similar in all three fields. He had a high level of overall discrimination, as indicated by a significant effect of the color of the second light on response selection [;(2(1, N=288)=72.06, P<0.001]. His ability to identify the color of the second light did not depend on the field of presentation of the lights [;(2(2, N=288)=0.08], and his performance was above chance in all three field conditions [LVF: ;(2(1, N=96)=22.13, P<0.001; BIL: ;(2(1, N=96)=24.04, P<0.001; RVF: ;(2(1, N=96)=26.14, P<0.001]. As hypothesized, on bilateral presentations L.B. was significantly better at identifying the color of the second light than the color of the first light [;(2(1, N = 192) = 9.12, P < 0.005]. In the left visual field, there was no difference in his ability to identify the color of the two lights [;(2(1, N = 192)=0.64], although in the right visual field he was slightly better at identifying the color of the second light than the first light [~2(1, N=192)=4.14, P<0.05]. However, in the combined unilateral condition (left and
right visual fields), there was no significant difference in his ability to identify the color of the first and second lights [;(2(1, N = 288)= 1.6]. These results suggest that on bilateral presentations, L.B.'s attention must shift from the first to the second light of a successive pair. The hemisphere registering the second light would be able to identify the color of that light but as a result of commissurotomy, it would have no access to the color of the first light. This explains why L.B. was better at identifying the color of the second light than the first light on bilateral presentations. Another significant effect was the color of the first light on response selection [Z2(1, N = 2 8 8 ) = 10.90, P<0.001]. Paired comparisons showed that this effect was significant in the bilateral condition but not in the left or right visual fields [BIL: ;(2(1, N=96)=4.17, P<0.05; LVF: ;(2(1, N=96)=3.39; RVF: ;(2(1, N=96)=3.39]. An examination of L.B.'s responses on bilateral presentations showed that he had a significant tendency to report that the color of the second light was what the color of the first light had been (58/96). Hence, on some of the bilateral presentations, his attention must have remained focussed in the hemisphere that registered the first light. This explanation is consistent with the proposal that L.B. performed poorly at discriminating the direction of apparent motion of colored lights across the midline (Task 2) because he incorrectly inferred that movement had occurred towards the first light on which his attention was focussed. D.K. Table 1 shows D.K.'s accuracy in each visual field. D.K. had a high level of overall discrimination, as indicated by a significant effect of the color of the second light on response selection [;(2(1, N=288)=165.40, P < 0.001]. However, his accuracy depended on the field of presentation [;(2(2, N=288)=5.99, P<0.05]. Paired comparisons showed that D.K. performed more poorly in the left visual field compared to the bilateral condition and the right visual field [LVF vs BIL: )~2(1, N=192)=5.69, P<0.025; LVF vs RVF: ;(2(1, N = 192)= 11.39, P<0.001]. As in Task 3, this may be due to a defect in the upper-left quadrant of the left visual field. Nevertheless, D.K.'s performance in the left visual field was significantly above chance [LVF: ;(2(1, N = 96) = 30.39, P < 0.001]. In addition, his performance in the bilateral condition and the right visual field was not significantly different [;(2(1, N = 192)= 1.23], and it exceeded chance in both of these locations [BIL: )~2(1, N=96)=63.62, P<0.001; RVF: ;(2(1, N=96)=77.89, P<0.00I]. As hypothesized, D.K. was equally good at identifying the color of the first and second lights, regardless of whether presentation was bilateral or unilateral [LVF: ;(2(1, N = 192) =2.16; BIL: Z2(1, N = 192) =0.06; RVF: ;(2(1, N = 192) = 3.16]. Hence, on bilateral presentations, either hemisphere must be able to identify the color of the first or second light. Presumably, the color of each light was identified by the hemisphere registering that light.
N. Naikar/Perception of motion of colored stimuli after commissurotomy General discussion Both L.B. and D.K. were able to discriminate the direction of apparent motion of colored lights, in either visual field and across the midline. However, L.B. performed more poorly on bilateral than unilateral presentations. Furthermore, on bilateral presentations, L.B. was significantly poorer at identifying the color of the first light than the color of the second light. In contrast, D.K. was equally good at identifying the color of either light, regardless of location. The control subjects performed near ceiling on all of the tasks. These results suggest that L.B. uses a different mechanism from D.K. or the control subjects to discriminate the direction of apparent motion across the midline. The results of this study support the hypothesis that a subcortically mediated shift in attention may allow L.B. to discriminate the direction of apparent motion across the midline. On bilateral presentations of two lights in succession, a shift in attention may occur from the first to the second light. The hemisphere registering the second light would be able to discriminate that movement must have been toward that light from the other side. However, as a result of commissurotomy, this hemisphere would have no information about the color of the first light. Hence, L.B. was better at identifying the color of the second light than the color of the first light on presentations of bilateral succession. This does not mean that the first light was undetected by the hemisphere registering the second light. It has been shown that L.B. is able to discriminate single-light from successive presentations across the midline, suggesting that the hemisphere registering the second light must have some trace of the first light [26]. Rather, the results indicate that subcortical pathways cannot transfer information about color between the disconnected hemispheres. The findings of this study therefore show a dissociation between the interhemispheric integration of motion and color. While it is possible that L.B. may have discriminated apparent motion across the midline on the basis of the transfer of simple perceptual information, given that there is some indication that the hemisphere registering the second light had some trace of the first light [26], the most parsimonious explanation for his ability to discriminate apparent motion across the midline involves an attentional mechanism. First, the results reported in this paper indicate that an attentional shift from the location of the first light to the location of the second light did occur. Second, the attentional mechanism can explain J.W.'s [14] performance. This subject was unable to discriminate single lights from successive pairs presented bilaterally, indicating that perceptual transfer did not occur under this condition. J.W. may have been unable to use attentional information to discriminate the two types of presentations because a single light may also induce a shift in attention across the midline. Third, the attentional mechanism can explain how neurons in the superior colliculus contribute to direction selectivity in
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area M T in the absence of the striate cortex. Note that there is no reason to suppose that L.B. has conscious access to information about the direction of the subcortical attentional shift. Shifts in attention mediated subcortically may register in area MT which is believed to have the capacity to produce directionally selective responses from nonselective input [16, 24, 25, 32, 33]. Most probably, then, it is the activity of area MT which gives rise to the conscious perception of motion. On the other hand, cortical area MT must have been responsible for tracking motion across the midline in D.K. This subject was equally proficient at identifying the color of the first and second lights on bilateral presentations, suggesting that either hemisphere must have been able to respond to either light. Presumably, response was controlled by the hemisphere registering the light that had to be identified. Tracking by MT can also account for the near ceiling performance of the control subjects in discriminating the direction of apparent motion on both bilateral and unilateral presentations of colored lights. In addition, intact intrahemispheric MT connections must be responsible for L.B.'s near perfect unilateral performance in discriminating the direction of apparent motion of colored lights. Although L.B. was also able to discriminate the direction of apparent motion of colored lights on bilateral presentations, his performance was poorer than in the unilateral condition. In the same task with white lights, L.B. scored near ceiling on both bilateral and unilateral presentations [26]. The critical difference between the two tasks is that the luminance of the colored lights was considerably lower than that of the white lights. This suggests that subcortical pathways may be less effective at shifting attention across the midline under conditions of low stimulus luminance. In addition, the results of previous studies indicate that the efficiency of subcortical pathways may also be compromised in cases of increased stimulus complexity [26] and stringent temporal parameters [11]. In contrast, D.K. and/or control subjects have little difficulty discriminating apparent motion under these conditions [26, I 1]. Furthermore, D.K. and control subjects are faster than L.B. at discriminating succession across the midline, and L.B. himself responds more quickly to within-field than bilateral presentations of succession [26]. These findings show that area MT is more highly developed for visual motion than subcortical pathways. The results of this study are therefore consistent with the notion that the tectopulvinar pathway has the capacity for considerable visuospatial function, although its role has been augmented by the development of the neocortex [34, 36]. In addition, the dissociation between the interhemispheric transfer of motion and color observed in this study support the position that forebrain mechanisms are necessary for the analysis of object features but not for visuospatial function [34, 36]. This study also sheds light on the nature of subcortical input to area MT. Although neurons in the superior
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colliculus and the pulvinar nucleus have little direction selectivity [3, 15], the tectopulvinar pathway may contribute to direction sensitivity in MT by mediating shifts in spatial attention. As MT receives projections from the superior colliculus through a number of routes [4, 5, 6, 20], these shifts in attention may very well register in MT. This may explain why considerable direction sensitivity is found in area MT in the absence of the striate cortex, and why this visual responsiveness is eliminated after subsequent lesions to the superior colliculus [16, 32, 33]. In conclusion, this research identifies two processes for motion detection. Specifically, apparent motion may be detected by directionally selective neurons in cortical regions of the brain and by a subcortical attentional mechanism. On the other hand, Cavanagh [9] has distinguished between a passive process, which involves lowlevel motion detectors, and an active process, whereby the visible features of a stimulus, such as its color, are tracked with voluntary attention. As the active process is object-specific, it is probably mediated by higher cortical systems such as those involved in object-based attention [29]. In contrast, the subcortical attentional mechanism is insensitive to object features, as indicated by the dissociation between the interhemispheric integration of motion and color. Taken together, this and Cavanagh's study suggest that there are two attentional processes that can mediate motion perception; a subcortical, involuntary process that is insensitive to object features, and a cortical, voluntary process that tracks visible stimulus features.
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9. 10.
11.
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Acknowledgements--This research was supported by a grant from the New Zealand Neurological Foundation. I thank Professor Michael Corballis from the University of Auckland for his valuable advice. I am also grateful to Dahlia and Evan Zaidel and Joseph E. Bogen for arranging for L.B. to be tested in Los Angeles, and to all of the subjects, especially L.B. and D.K., for their cheerful and willingparticipation.
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References
1. Albright, T. D., Desimone, R. and Gross, C. G. Columnar organisation of directionally selective cells in visual area MT of the macaque. Journal of Neurophysiology 51, 16-31, 1984. 2. Barbur, J. L., Ruddock, K. H. and Waterfield, V. A. Human visual responses in the absence of the geniculo-calcarine projection. Brain 103, 905 928, 1980. 3. Bender, D. B. Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Research 279, 258 261, 1983. 4. Benevento, L. A. and Fallon, J. H. The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). Journal of Comparative Neurology 160, 339-362, 1975. 5. Benevento, L. A. and Standage, G. P. The organisation of projections of the retinorecipient and non-
17.
18. 19.
20.
retinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. Journal of Comparative Neurology 217, 307-336, 1983. Benevento, L. A. and Yoshida, K. The afferent and efferent organisation of the lateral geniculo-prestriate pathways in the macaque monkey. Journal of Comparative Neurology 203, 455-474, 1981. Bogen, J. E., Schultz, D. H. and Vogel, P. J. Completeness of callosotomy shown by magnetic resonance imaging in the long term. Archives of Neurology 45, 1203-1205, 1988. Bogen, J. E., and Vogel, P. J. Neurologic status in the long term following complete cerebral commissurotomy. In Les Syndromes de Disconnexion Calleuse chez l'Homme, F. Michel and B. Schott (Editors), pp. 227 251. Hopital Neurologique, Lyon, 1975. Cavanagh, P. Attention-based motion perception. Science 257, 1563-1565, 1992. Cheng, K., Hasegawa, T., Saleem, K. S. and Tanaka, K. Comparison of neuronal selectivity for stimulus speed, length, and contrast in the prestriate visual cortical area V4 and MT of the macaque monkey. Journal of Neurophysiology 71, 2269 2280, 1994. Corballis, M. C. Hemispheric interactions in temporal judgements about spatially separated stimuli. Neuropsychology, in press. Corballis, M. C. and Trudel, C. I. The role of the forebrain commissures in interhemispheric integration. Neuropsychology 7, 1 19, 1993. Dobkins, K. R. and Albright, T. D. Color, luminance, and the detection of visual motion. Current Directories in Psychol. Science 2, 189 193, 1993. Gazzaniga, M. S. Perceptual and attentional processes following callosal section in humans. Neuropsychologia 25, 119-133, 1987. Goldberg, M. and Wurtz, R. H. Activity of the superior colliculus in the behaving monkey. I. Visual receptive fields of single neurons. Journal of Neurophysiology 35, 542 596, 1972. Gross, C. G. Contribution of striate cortex and the superior colliculus to visual function in area MT, the superior temporal polysensory area and the inferior temporal cortex. Neuropsychologia 25, 497-515, 1991. Holtzman, J. D., Sidtis, J. J., Volpe, B. T., Wilson, D. H. and Gazzaniga, M. S. Dissociation of spatial information for stimulus localisation and the control of attention. Brain 104, 861-872, 1981. Johnson, L. E. Bilateral visual cross-integration by human forebrain commissurotomy subjects. Neuropsychologia 22, 167-175, 1984. Maunsell, J. H. R. and Van Essen, D. C. The connections of the middle temporal visual area (MT) and their relationship to cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 25632586, 1983. Maunsell, J. H. R. and Van Essen, D. C. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. Journal of Neurophysiology 49, 1127 1147, 1983.
N. Naikar/Perception of motion of colored stimuli after commissurotomy 21. Meienberg, O., Zangemeister, W. H., Rosenberg, M., Hoyt, W. F. and Stark, L. Saccadic eye movement strategies in patients with homonymous hemianopia. Annals of Neurology 9, 537-544, 1981. 22. Midgley, G. C. and Tees, R. C. Reinstatement of orienting behavior by d-amphetamine in rats with superior colliculus lesions. Behavioral Neuroscience 100, 246-255, 1986. 23. Mikami, A. Direction selective neurons respond to short-range and long-range apparent motion stimuli in macaque visual area MT. International Journal of Neuroscience 61, 101 112, 1991. 24. Mikami, A., Newsome, W. T. and Wurtz, R. H. Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extra° striate area MT. Journal of Neurophysiology 55, 1308 1327, 1986. 25. Mikami, A., Newsome, W. T. and Wurtz, R. H. Motion selectivity in macaque visual cortex. II. Spatio-temporal range of directional interactions in MT and VI. Journal of Neurophysiology 55, 1328 1339, 1986. 26. Naikar, N. and Corballis, M. C. The perception of apparent motion across the retinal midline after commissurotomy. Neuropsychologia 34, 297-309, 1996. 27. Petersen, S. E., Robinson, D. L. and Morris, J. D. Contributions of the pulvinar to visual spatial attention. Neuropsychologia 25, 97-106, 1987. 28. Rafal, R., Henik, A. and Smith, J. Extrageniculate contributions to reflex visual orienting in normal humans: A temporal hemifield advantage. Journal of Cognitive Neuroscience 3, 322-328, 1991. 29. Rafal, R. and Robertson, L. The neurology of visual attention. In The Cognitive Neurosciences, M. S. Gazzaniga (Editor), pp. 625-648. MIT Press, Cambridge, MA, 1995. 30. Ramachandran, V. S., Cronin-Golomb, A. and Myers, J. J. Perception of apparent motion by commissurotomy patients. Nature 320, 358 359, 1986. 31. Reuter-Lorenz, P. A., Hughes, H. C. and Fendrich, R. The reduction of saccadic latency by prior offset
32.
33.
34. 35.
36.
37. 38.
39.
40. 41.
1049
of the fxation point: An analysis of the gap effect. Perception and Psychology 49, 165-175, 1991. Rodman, H. R., Gross, C. G. and Albright, T. D. Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal. Journal of Neuroscience 9, 2033-2050, 1989. Rodman, H. R., Gross, C. G. and Albright, T. D. Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal. Journal of Neuroscience 10, 1154-1164, 1990. Schneider, G. E. The two visual systems. Science 163, 895-902, 1969. Sprague, J. M., Berlucchi, G. and Rizzolatti, G. The role of the superior colliculus and pretectum in vision and visually guided behavior. In Handbook of Sens. Physiology, R. Jung (Editor), Vol. II/3B, pp. 27 101. Springer, Berlin, 1973. Thinus-Blanc, C., Scardigli, P. and Buhot, M.-C. The effects of superior colliculus lesions in hamsters: Feature detection versus spatial localisation. Physi0/09)' and Behavior 49, 1-6, 1991. Trevarthen, C. B. Two mechanisms of vision in primates. Psychologische Forschung 31,299-337, 1968. Trevarthen, C. B. Integrative functions of the cerebral commissures. In Handbook of Neuropsychology: Vol. 4. The Commissurotomized Brain, R. D. Nebes (Editor), pp. 49-83, Elsevier Science, Oxford, 1991. Truett, A., Begleiter, A., McCarthy, G., Roessler, E., Nobre, A. C. and Spencer, D. D. Electrophysiological studies of color processing in human visual cortex. Electro. and Clinical Neurophysiology 88, 343-355, 1993. Winer, B. J. Statistical Principles in Experimental Design. Wiley, New York, 1971. Zaidel, E. In Interhemispheric transfer in the split brain: Long-term status following complete cerebral commissurotomy. In Brain Asymmetry, R. J. Davidson and K. Hugdahl (Editors), pp. 491 532. MIT Press, Cambridge, MA, 1995.
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Neuropsychologia, Vol. 34, No. 11, pp. 1041-1049, 1996 Copyright © 1996 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0028-3932/96 $15.00+0.00
Perception of apparent motion of colored stimuli after commissurotomy NEELAM NAIKAR* Department of Psychology, University of Auckland, Private Bag 92019, Auckland, New Zealand (Received 7 August 1995; accepted 10 January 1996)
Abstract--One subject with complete forebrain commissurotomy (L.B.), another with posterior callosotomy (D.K.), and eight normal controls were presented with successive pairs of red and/or green lights, on either side of the retinal midline and within the
left and right visual fields. All of the subjects could discriminate the direction of apparent motion in all three locations, although L.B. was poorer on bilateral than unilateral presentations. Moreover, on bilateral presentations, L.B. was significantly poorer at identifying the color of the first light than the color of the second light. In contrast, D.K., like the control subjects, was equally good at identifying the color of either light. These and other results provide evidence that a subcortical shift in attention enables L.B. to discriminate the direction of apparent motion across the midline. On the other hand, a more robust mechanism involving the middle temporal area of the cortex must be responsible for tracking motion in D.K. and the control subjects. On the basis of these findings, it is suggested that the superior colliculus may contribute to direction sensitivity in the middle temporal area by mediating shifts in spatial attention. Copyright © 1996 Elsevier Science Ltd. Key Words: split brain; corpus callosum; superior colliculus; middle temporal area; motion; color; attention.
was only aware of a single light. In contrast, he performed perfectly within each visual field. However, Naikar and Corballis [26] failed to replicate this result in L.B. or in a subject with posterior callosotomy, D.K. These subjects had no difficulty discriminating single lights from successive pairs, regardless of whether presentation was bilateral or unilateral. Furthermore, unlike N.G. [30], they were not impaired at discriminating simultaneous from successive pairs. In addition, both subjects were able to discriminate single lights from simultaneous pairs, and leftward from rightward succession. The accuracy of the subjects on these tasks did not depend on the spatial (2 ° or 7 °) or temporal separation (33 or 133 msec) of the lights, contrary to Trevarthen's [37, 38] proposition that only long-range apparent motion is represented subcortically. The only sign of disconnection was that L.B. was slower to respond to bilateral than unilateral succession. However, further evidence of disconnection was elicited in a task involving single-light, simultaneous, and successive presentations; L.B. was significantly impaired in judging whether movement had occurred across the midline, although he could do so nearly perfectly within each visual field [26]. This difficulty seemed to be specific to discriminating single lights from successive pairs; he had no trouble identifying simultaneous presentations as
Introduction
Several studies have investigated whether apparent motion may be perceived by split-brained subjects, when two lights are flashed successively to opposite hemispheres of the disconnected brain [11, 14, 26, 30]. In one study, Ramachandran et al. [30] tested three subjects with complete section of the corpus callosum, the anterior and hippocampal commissures, and the massa intermedia if it was present (L.B., N.G., A.A.). L.B. and A.A. were able to discriminate leftward from rightward succession across the midline, and both of these from simultaneous presentations. N.G. was also able to discriminate leftward from rightward succession but she reported all simultaneous pairs to be moving. Although these results suggest that L.B. and A.A., at least, are essentially normal in perceiving apparent motion across the midline, Gazzaniga [14] reported that J.W., who had complete section of the corpus callosum but not of the anterior commissure, was unable to discriminate single lights from presentations of bilateral succession. On all of the successive presentations, J.W. responded that he saw no movement suggesting that he
* Fax: 64-9-3737450. 1041
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not moving. In addition, he continued to respond slowly to bilateral compared to unilateral succession. D.K., on the other hand, was able to judge whether movement had occurred or not, and in a subsequent task involving the same stimuli, he could also report the direction of movement on successive presentations. Corballis [11] also found evidence for disconnection when L.B. was required to discriminate simultaneous from successive pairs of lights that had a duration of only 17 msec. In the studies by Ramachandran et al. [30] and Naikar and Corballis [26] the duration of the lights was as long as 130 and 133 msec, respectively. The interstimulus interval in these studies ranged from 30 to 133 msec. Under the conditions in Corballis's task, L.B. reported nearly all bilateral successive pairs as simultaneous, although his performance in the unilateral condition was above chance. Corballis suggested that cortical commissures were necessary for fine temporal resolution across the midline. As the duration of the lights in Gazzaniga's [14] study was not reported, it is possible that J.W. was unable to discriminate succession across the midline because the duration of the lights was too short. From these studies it is evident that commissurotomy may result in some loss in the ability to perceive apparent motion across the midline. However, for the most part, split-brained subjects are able to discriminate apparent motion across the midline. The mechanism that is engaged may involve a subcortical shift in attention from the first light to the second light. The hemisphere registering the second light would be able to discriminate that movement must have been toward that light from the other side. However, a single light would also attract attention, which may explain why J.W. was unable to discriminate single lights from successive pairs [14]. That L.B. was able to perform this discrimination but had difficulty when simultaneous pairs were also involved suggests that he may have had a residual but fading trace of the first light that was relatively easy to detect in the context of simple discriminations but not when more complex discriminations were required [26]. To support the proposition that a subcortical attentional mechanism allows split-brained subjects to discriminate apparent motion across the midline, there is substantial evidence for the role of subcortical pathways in attention. For example, it has been shown that the superior colliculus of rodents is involved in the attentional components of spatial behavior [36, 22]. Furthermore, from studies with macaques, there is evidence that spotlight attention depends on the pulvinar nucleus, which receives input from the superior colliculus [27]. In addition, a study with normal human subjects has shown that the retinotectal pathway contributes to the reflex orienting of visual attention [28], and in a task with human split-brained subjects it has been shown that a spatial cue in one visual field is just as effective in directing attention to a target in the opposite visual field, as when the cue and target appear in the same visual field [17].
Another mechanism for the discrimination of apparent motion involves the middle temporal (MT) area of the cortex. This area is highly specialized for the direction, orientation, and speed of stimulus movement [20]. Moreover, it has been shown that MT neurons are involved in processing apparent motion [23]. Tracking by area MT can account for the near perfect performance of control subjects and the near perfect unilateral score of splitbrained subjects in discriminating apparent motion [26]. However, this mechanism would be incapacitated after commissurotomy, which explains why split-brained subjects may have to resort to other sources of information for discriminating apparent motion across the midline. That D.K. had little difficulty with bilateral succession [26] suggests that the cerebral commissures interconnecting MT in the two hemispheres must be intact in this subject. These commissures are thought to be located in the anterior and posterior midbody of the corpus callosum [41], areas that may well be spared in D.K. While the role of MT in the perception of visual motion has been extensively documented, the contribution of subcortical pathways to this function is less apparent. It is known that the major subcortical input to MT is from the lateral and inferior pulvinar, which receives projections from the superior colliculus [4, 5]. It has also been demonstrated that lesions to the striate cortex in macaques do not eliminate the direction sensitivity of MT neurons, whereas subsequent damage to the superior colliculus does [16, 32, 33]. The superior colliculus must therefore be able to maintain direction sensitivity in MT in the absence of the striate cortex. However, neurons in the superior colliculus are insensitive to the direction of motion [15], and any little direction sensitivity in the lateral and inferior pulvinar is eliminated by striate cortex removal [3]. Thus, visual input reaching MT by the tectopulvinar route must be nonselective [16, 32, 33], and area MT must have the capacity to produce directionally selective responses from nonselective input [16, 24, 25, 32, 331. As indicated from the results of split-brain research in the area of apparent-motion perception, the tectopulvinar input to MT may involve spatial attention. Shifts in attention directed by the superior colliculus could register in MT through several routes, including the pulvinar nucleus, striate cortex, or via lateral geniculate nucleus projections to the striate cortex and areas V2, V3, and V4 [4, 5, 6, 20]. Hence, even in the absence of striate cortex there are routes by which collicular shifts in attention could register in MT. This may explain why MT neurons remain directionally selective in the absence of the striate cortex, and why this visual responsiveness is eliminated after subsequent lesions to the superior colliculus [16, 32, 33]. The purpose of this paper is to provide further evidence that a subcortical shift in attention may allow splitbrained subjects to discriminate the direction of apparent motion across the midline. L.B., D.K., and eight control subjects were tested. In the critical tasks, spatially sep-
N. Naikar/Perception of motion of colored stimuli after commissurotomy a r a t e d pairs o f red a n d / o r green lights were presented in succession, b o t h within a n d between fields. T h e subjects were required to d i s c r i m i n a t e the direction o f a p p a r e n t m o t i o n a n d in s u b s e q u e n t tasks, to identify the c o l o r o f the first a n d second lights. It was h y p o t h e s i z e d that a l t h o u g h L.B. w o u l d be able to d i s c r i m i n a t e the direction o f a p p a r e n t m o t i o n across the midline, he w o u l d be better at identifying the c o l o r o f the second light than the c o l o r o f the first light. A shift in a t t e n t i o n from the first to the second light w o u l d allow L.B. to discriminate the direction o f a p p a r e n t m o t i o n on bilateral presentations. However, as a result o f c o m m i s s u r o t o m y , the hemisphere registering the second light w o u l d have no i n f o r m a t i o n a b o u t the c o l o r o f the first light. It has been shown that L.B. c a n n o t m a k e same/different j u d g m e n t s a b o u t colors presented on either side o f the midline [18], which indicates that there is little transfer o f c o l o r i n f o r m a t i o n in the absence o f the c o r p u s callosum. A s s u m i n g that the hemisphere registering the second light is the one controlling response, L.B. should be better at identifying the c o l o r o f the second light than the c o l o r o f the first light. In contrast, on unilateral presentations, L.B. should be equally g o o d at identifying the c o l o r o f the first a n d second lights. D . K . was also tested. If a cortical t r a c k i n g m e c h a n i s m is responsible for his ability to d i s c r i m i n a t e a p p a r e n t m o t i o n across the midline, either hemisphere should be able to identify the c o l o r o f the first or second light. P r e s u m a b l y , the c o l o r o f a light w o u l d be identified by the hemisphere registering that light. Hence, D . K . should be equally g o o d at identifying the c o l o r o f the first a n d second lights, on bilateral as well as unilateral presentations. This p a t t e r n o f p e r f o r m a n c e should also be observed in the c o n t r o l subjects. All o f the subjects were also required to identify the c o l o r o f a single light presented in the left o r right visual field, in o r d e r to d e t e r m i n e the ability o f each hemisphere to identify red a n d green colors.
General method Sul?iects Two commissurotomized subjects were tested on all of the tasks. L.B., who was 43 years old at the time of testing, had complete section of the corpus callosum, and anterior and hippocampal commissures, for the relief of intractable epilepsy in 1963, when he was 12 years and 11 months of age. Magnetic resonance imaging has confirmed that his corpus callosum is sectioned completely [7]. Further information regarding his neurological condition may be obtained elsewhere [8]. D.K., who was 27 years old at the time of testing, had a partial commissurotomy in the course of surgery for an arteriovenous malformation in the medial face of the right occipital lobe. He was 18 years of age at the time. A C T scan has confirmed complete section of the posterior third to half of the corpus callosum [26]. Optometric testing has indicated a defect in the upper left quadrant of the left visual field. Further details may be obtained elsewhere [12].
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Eight control subjects participated in all of the tasks. There were four males and four females. They ranged from 19 to 48 years of age, with a mean age of 29 years. Five of the subjects were right-handed and the other three were left-handed.
Equipment and sthnuli Presentation of the stimuli was controlled by an IBM-compatible computer with a fast-fade VGA screen. The subjects were required to key-in their responses on a keyboard. The stimuli were either red or green spots of light, 0.7 cm in diameter, flashed on a black background. In all of the tasks, the duration of the lights was 133 msec. In tasks involving successive presentations, the interstimulus interval was 33 msec and the spatial separation was 7 . In Task 1, the subjects were required to identify the color of a single light presented in the left or right visual field. The light was either red or green in color. Each color was presented at three levels of luminance to determine whether the subjects could discriminate the two colors independently of brightness (Red = 6.24, 8.87, 10.35 cd/m2; Green = 7.19, 9.12, 11.53 cd/m2). This was necessary as equiluminance of the red and green colors could only be approximated on subsequent tasks. The single light was presented in each of four locations: 10.5" to the left, 3.5 to the left. 3.5 t o the right, and 10.5 to the right of central fixation. Tasks 2.3, and 4 involved both bilateral and unilateral presentations of two lights in succession. The pairs of lights were presented in all four possible color combinations: red red, green-green, red green, and green-red. The colors were approximately equiluminant to prevent the subjects from discriminating them on the basis of brightness (Red = 8.87 cd/m 2, Green = 9.12 cd/m2). The successive pairs appeared in adjacent positions at the same locations as the single lights. On half of the presentations, the second light was flashed to the right of the first light so that rightward apparent motion was created. On the other half of the trials, the second light was flashed to the left of the first light so that leftward apparent motion was created. The order of the tasks for L.B. was Task 2, 4, 3, 1, whereas for D.K. it was Task 3, 4, 1,2. For the control subjects, the order of the tasks was counterbalanced. Each of the tasks consisted of four blocks of trials. L.B. and four of the control subjects responded with their left hand on the first and fourth blocks and with their right hand on the second and third blocks. D.K. and the other four control subjects responded with their right hand on the first and fourth blocks and with their left hand on the second and third blocks. Each block began with 10 practice trials which were randomly selected from the experimental trials. Task 1 consisted of 48 experimental trials per block, whereas in the remaining three tasks there were 72 experimental trials per block. Within each block, there were equal numbers of trials Jbr each stimulus condition presented in random order. When a trial was initiated by pressing the space bar, a central fixation cross appeared, which was followed 500 msec later by the appearance of the stimuli. The subjects responded by pressing either the M or N key with the forefinger and middle finger of one hand. On all of the tasks, feedback in the form of a short tone was given to incorrect responses.
Analysis Ofresults When the performance of the commissurotomized subjects fell below 95%, in either visual field or in the bilateral condition of a task, multidimensional chi-squared analyses [40] were con-
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N. Naikar/Perception of motion of colored stimuli after commissurotomy
ducted to determine the effects of stimulus condition (green vs red, leftward succession vs rightward succession), field, direction of succession, hand used for response, luminance, and their interactions. Discrimination accuracy was indexed by the interaction between stimulus condition and response selection, whereas response bias was indexed by response selection effects only. These analyses were carried out only for the commissurotomized subjects as the performance of the control subjects was at or near ceiling on all of the tasks.
Task 1: Color of single light In this task, the subjects were required to identify the color of a single red or green light presented in the left or right visual field. The purpose of the task was to establish the ability of each hemisphere to identify red and green colors. Each color was presented at three levels of luminance to determine whether the subjects could discriminate the two colors independently of brightness. The subjects were asked to press the N key if the light was green or the M key if it was red.
discrimination, as indicated by a significant effect of the color of the light on response selection [X2(1, N = 192)= 165.04, P < 0.001]. Furthermore, like L.B., his accuracy did not depend on the field of presentation of the light [22(1, N = 192)=0.02]. In addition, his performance in the left visual field was well above chance [22(1, N = 96) = 70.07, P<0.001], although it was slightly poorer than the control subjects. There were no significant effects of luminance or the hand used for response. The results of this task show that L.B., D.K. and the control subjects can identify the color of a single light presented in the left or right visual field. As none of the subjects showed significant hemispheric differences in performance, any asymmetry in subsequent tasks cannot be attributed to hemispheric differences in color-identification. Also note, that the subjects could identify the red and green colors despite being prevented from using brightness information for this purpose. It is therefore unlikely that they would rely on variances in luminance for identifying the colors on subsequent tasks.
Results and discussion
Task 2: Direction of successive pairs
L.B. Table 1 shows that L.B. was slightly better at identifying the color of a single light in the left than right visual field. L.B. had a high level of overall discrimination, as indicated by a significant effect of the color of the light on response selection [22(1, N = 192)= 114.53, P<0.001]. Moreover, his performance in the left and right visual fields was not significantly different [22(1, N = 192)= 1.34]. In addition, although L.B. was slightly less accurate than the control subjects, his performance in both visual fields was well above chance [LVF: Z2(1, N = 9 6 ) = 7 0 . 0 7 , P<0.001; RVF: 22(1, N = 9 6 ) = 4 6 . 3 6 , P < 0.001]. There were no significant effects of luminance or the hand used for response. D.K. Table 1 shows that D.K. was slightly better at identifying the color of a single light in the right than left visual field. D.K. also had a high level of overall
The results of a previous study showed that L.B. and D.K. were 100% accurate at discriminating the direction of apparent motion of white lights across the midline [26]. The purpose of this task was to determine whether they would be able to discriminate the direction of apparent motion of colored lights. Red and/or green lights were presented in succession on either side of the midline and within each visual field. The subjects were asked to press the N key if movement was to the left or the M key if it was to the right.
Results and discussion L.B. Table 1 shows that L.B.'s accuracy was markedly low in the bilateral condition. L.B. had a high level of
Table 1. Percent correct obtained by L.B., D.K. and control subjects in each task, as a function of field Task
Subjects
LVF
I. Color of single light
L.B. D.K. Controls L.B. D.K. Controls L.B. D.K. Controls L.B. D.K. Controls
92.7 92.7 98.0 100.0 100.0 98.3 68.8 68.8 97.8 74.0 78.1 97.2
2. Direction of successive pairs 3. Color of the first light 4. Color of the second light
BIL
RVF
Total
71.9 100.0 99.2 54.2 89.6 97.5 75.0 90.6 97.1
84.4 100.0 98.8 99.0 97.9 98.7 62.5 87.5 96.5 76.0 94.7 97.1
88.5 96.4 98.4 90.3 99.3 98.7 61.8 81.9 97.3 75.0 87.8 97.2
N. Naikar/Perception of motion of colored stimuli after commissurotomy overall discrimination, as indicated by a significant effect of the direction of succession on response selection [22(1, N = 288) = 186.89, P < 0.001 ]. However, his performance depended on the field of presentation [)C2(2, N=288)-19.53, P<0.001]. Paired comparisons showed that his accuracy in the bilateral condition was significantly poorer than in the left and right visual fields [BIL vs LVF: 22(1, N= 192)= 31.42, P < 0.001; BIL vs RVF: 22(2, N = 192)= 28.26, P < 0.001]. A separate analysis of L.B.'s performance on bilateral presentations, showed no significant effects or interactions between the color of the first light, the color of the second light, the direction of succession, or the hand used for response. There were also no significant effects or interactions between these variables on overall performance, Although L.B.'s performance in the bilateral condition was above chance [22( 1, N = 96) = 18.38, P < 0.001 ], it was significantly poorer than his ability to discriminate the direction of apparent motion of white lights across the midline [X2(1, N= 144)= 16.62, P<0.001] [26]. On unilateral presentations, his performance in both tasks was at or near ceiling. Earlier, it was suggested that L.B. may have discriminated the direction of apparent motion of white lights across the midline on the basis of a subcortical shift in attention from the first to the second light. In this task, his performance may have deteriorated because his attention remained focussed on the first light instead of shifting to the second light. Hence, he would have incorrectly inferred that movement had occurred towards the first light. A possible reason for attention remaining focussed on the first light is that the luminance of the colored lights was considerably lower than that of the white lights (97,5 cd/m 2) used by Naikar and Corballis [26]. Hence, the onset of the second light may not have always resulted in a shift in attention across the midline. Consistent with this suggestion are reports that blindsight performance cannot be obtained when the luminance of a target stimulus is reduced [2, 21]. It has also been observed that the latency to initiate a saccade by human subjects is greater when the target luminance is low [31]. It is unlikely that the color of the lights hampered the attentional mechanism as neurons in the primate superior colliculus are largely insensitive to color [35]. Nevertheless, L.B. was able to discriminate the direction of apparent motion on a significant proportion of bilateral presentations in this task. Therefore, if an interhemispheric attentional shift enables L.B. to discriminate the direction of apparent motion across the midline, it can still be expected that he would be better at identifying the color of the second light than the color of the first light on bilateral presentations of succession. D.K. Table 1 shows that D K . , like the control subjects, scored near ceiling at discriminating the direction of apparent motion. That the performance of these subjects was not affected by the luminance of the colored lights is consistent with the properties of MT; it has been found that neurons in this area in monkeys are active under
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conditions of low stimulus contrast [10, 13], and make the same response to moving stimuli regardless of color [1, 19].
Task 3: Color of the first light
In this task, the subjects were required to identify the color of the first of two lights presented in succession. Pairs of red and/or green lights were presented within each visual field and on either side of the midline. The subjects were instructed to press the N key if the color of the first light was green or the M key if it was red.
Results and discussion L.B. Table 1 shows that L.B. performed more poorly than the control subjects in all three field conditions. Although the effect of field on response selection failed to reach significance [22(2, N = 288)---4.14], paired comparisons showed that L.B.'s performance in the bilateral condition was significantly poorer than in the combined unilateral condition (left and right visual fields) [g2(1, N = 288) = 4.84, P < 0.05]. Moreover, his performance in the bilateral condition did not exceed chance, although it was well above this level in the left and right visual fields [BIL: 22(1, N=96)=0.67; LVF: 22(1, N = 9 6 ) = 13.89, P<0.001; RVF: 22(1, N=96)=6.00, P<0.025]. These results indicate that response on bilateral presentations must have been controlled by the hemisphere registering the second light; as a result of commissurotomy, this hemisphere would have no information about the color of the first light. Another significant effect was the color of the second light on response selection [22(1, N=288)=4.53, P < 0.05]. Paired comparisons showed that this effect was significant in the bilateral condition but not in the left or right visual fields [BIL: 22(1, N=96)=4.20, P<0.05; LVF: Z2(1, N = 9 6 ) = 1.54; RVF: 22(1, N=96)=0.17]. An examination of L.B.'s responses on bilateral presentations showed that he had a significant tendency to report that the color of the first light was what the color of the second light had been (58/96). This result is consistent with the proposal that on presentations of bilateral succession, L.B.'s attention must shift from the first to the second light. The hemisphere registering the second light would have no knowledge of the color of the first light, and may therefore simply report the color of the second light instead. D.K. Table 1 shows that in contrast to L.B., D.K.'s accuracy was highest in the bilateral condition. Although D.K. had a high level of overall discrimination, as indicated by a significant effect of the color of the first light on response selection [22(1, N = 288) = 120.37, P < 0.001], his performance depended on the field of presentation [~(2(2, N=288)=10.35, P<0.01]. Paired comparisons
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N. Naikar/Perception of motion of colored stimuli after commissurotomy
showed that D.K.'s accuracy in the left visual field was significantly poorer than in the bilateral condition and right visual field [LVF vs BIL: ;(2(1, N = 192)= 12.63, P < 0.001; LVF vs RVF: ;(2(1, N = 192)=9.87, P < 0.005], Nevertheless, his performance in the left visual field was above chance [;(2(1, N = 96) = 14.11, P < 0.001 ]. There was no significant difference in accuracy between the bilateral condition and the right visual field [;(2(1, N = 192)= 0.21], and his performance in both of these locations was well above chance [BIL: ;(2(1, N = 96) = 60.17, P < 0.001; RVF: ;(2(1, N = 9 6 ) = 57.60, P<0.001]. D.K.'s poor score in the left visual field may be due to a defect in the upper-left quadrant of this field, as a result of right occipital lobe damage. This damage may be in area V4, which is located in the inferior occipital lobe in humans [39]. Unpublished tasks in our laboratory show that on a simple reaction time task, D.K. is impaired in detecting a grey target when it is flashed on a yellow background of equal luminance on presentations in the left but not in the right visual field. In contrast, he is not impaired at detecting a white target flashed on a black background in either visual field.
Task 4: Color of the second light In this task, the subjects were required to identify the color of the second of two lights presented in succession. Pairs of red and/or green lights were presented on either side of the midline and within each visual field. The subjects were instructed to press the N key if the color of the second light was green or the M key if it was red.
Results and discussion L.B. Table 1 shows that L.B.'s performance was similar in all three fields. He had a high level of overall discrimination, as indicated by a significant effect of the color of the second light on response selection [;(2(1, N=288)=72.06, P<0.001]. His ability to identify the color of the second light did not depend on the field of presentation of the lights [;(2(2, N=288)=0.08], and his performance was above chance in all three field conditions [LVF: ;(2(1, N=96)=22.13, P<0.001; BIL: ;(2(1, N=96)=24.04, P<0.001; RVF: ;(2(1, N=96)=26.14, P<0.001]. As hypothesized, on bilateral presentations L.B. was significantly better at identifying the color of the second light than the color of the first light [;(2(1, N = 192) = 9.12, P < 0.005]. In the left visual field, there was no difference in his ability to identify the color of the two lights [;(2(1, N = 192)=0.64], although in the right visual field he was slightly better at identifying the color of the second light than the first light [~2(1, N=192)=4.14, P<0.05]. However, in the combined unilateral condition (left and
right visual fields), there was no significant difference in his ability to identify the color of the first and second lights [;(2(1, N = 288)= 1.6]. These results suggest that on bilateral presentations, L.B.'s attention must shift from the first to the second light of a successive pair. The hemisphere registering the second light would be able to identify the color of that light but as a result of commissurotomy, it would have no access to the color of the first light. This explains why L.B. was better at identifying the color of the second light than the first light on bilateral presentations. Another significant effect was the color of the first light on response selection [Z2(1, N = 2 8 8 ) = 10.90, P<0.001]. Paired comparisons showed that this effect was significant in the bilateral condition but not in the left or right visual fields [BIL: ;(2(1, N=96)=4.17, P<0.05; LVF: ;(2(1, N=96)=3.39; RVF: ;(2(1, N=96)=3.39]. An examination of L.B.'s responses on bilateral presentations showed that he had a significant tendency to report that the color of the second light was what the color of the first light had been (58/96). Hence, on some of the bilateral presentations, his attention must have remained focussed in the hemisphere that registered the first light. This explanation is consistent with the proposal that L.B. performed poorly at discriminating the direction of apparent motion of colored lights across the midline (Task 2) because he incorrectly inferred that movement had occurred towards the first light on which his attention was focussed. D.K. Table 1 shows D.K.'s accuracy in each visual field. D.K. had a high level of overall discrimination, as indicated by a significant effect of the color of the second light on response selection [;(2(1, N=288)=165.40, P < 0.001]. However, his accuracy depended on the field of presentation [;(2(2, N=288)=5.99, P<0.05]. Paired comparisons showed that D.K. performed more poorly in the left visual field compared to the bilateral condition and the right visual field [LVF vs BIL: )~2(1, N=192)=5.69, P<0.025; LVF vs RVF: ;(2(1, N = 192)= 11.39, P<0.001]. As in Task 3, this may be due to a defect in the upper-left quadrant of the left visual field. Nevertheless, D.K.'s performance in the left visual field was significantly above chance [LVF: ;(2(1, N = 96) = 30.39, P < 0.001]. In addition, his performance in the bilateral condition and the right visual field was not significantly different [;(2(1, N = 192)= 1.23], and it exceeded chance in both of these locations [BIL: )~2(1, N=96)=63.62, P<0.001; RVF: ;(2(1, N=96)=77.89, P<0.00I]. As hypothesized, D.K. was equally good at identifying the color of the first and second lights, regardless of whether presentation was bilateral or unilateral [LVF: ;(2(1, N = 192) =2.16; BIL: Z2(1, N = 192) =0.06; RVF: ;(2(1, N = 192) = 3.16]. Hence, on bilateral presentations, either hemisphere must be able to identify the color of the first or second light. Presumably, the color of each light was identified by the hemisphere registering that light.
N. Naikar/Perception of motion of colored stimuli after commissurotomy General discussion Both L.B. and D.K. were able to discriminate the direction of apparent motion of colored lights, in either visual field and across the midline. However, L.B. performed more poorly on bilateral than unilateral presentations. Furthermore, on bilateral presentations, L.B. was significantly poorer at identifying the color of the first light than the color of the second light. In contrast, D.K. was equally good at identifying the color of either light, regardless of location. The control subjects performed near ceiling on all of the tasks. These results suggest that L.B. uses a different mechanism from D.K. or the control subjects to discriminate the direction of apparent motion across the midline. The results of this study support the hypothesis that a subcortically mediated shift in attention may allow L.B. to discriminate the direction of apparent motion across the midline. On bilateral presentations of two lights in succession, a shift in attention may occur from the first to the second light. The hemisphere registering the second light would be able to discriminate that movement must have been toward that light from the other side. However, as a result of commissurotomy, this hemisphere would have no information about the color of the first light. Hence, L.B. was better at identifying the color of the second light than the color of the first light on presentations of bilateral succession. This does not mean that the first light was undetected by the hemisphere registering the second light. It has been shown that L.B. is able to discriminate single-light from successive presentations across the midline, suggesting that the hemisphere registering the second light must have some trace of the first light [26]. Rather, the results indicate that subcortical pathways cannot transfer information about color between the disconnected hemispheres. The findings of this study therefore show a dissociation between the interhemispheric integration of motion and color. While it is possible that L.B. may have discriminated apparent motion across the midline on the basis of the transfer of simple perceptual information, given that there is some indication that the hemisphere registering the second light had some trace of the first light [26], the most parsimonious explanation for his ability to discriminate apparent motion across the midline involves an attentional mechanism. First, the results reported in this paper indicate that an attentional shift from the location of the first light to the location of the second light did occur. Second, the attentional mechanism can explain J.W.'s [14] performance. This subject was unable to discriminate single lights from successive pairs presented bilaterally, indicating that perceptual transfer did not occur under this condition. J.W. may have been unable to use attentional information to discriminate the two types of presentations because a single light may also induce a shift in attention across the midline. Third, the attentional mechanism can explain how neurons in the superior colliculus contribute to direction selectivity in
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area M T in the absence of the striate cortex. Note that there is no reason to suppose that L.B. has conscious access to information about the direction of the subcortical attentional shift. Shifts in attention mediated subcortically may register in area MT which is believed to have the capacity to produce directionally selective responses from nonselective input [16, 24, 25, 32, 33]. Most probably, then, it is the activity of area MT which gives rise to the conscious perception of motion. On the other hand, cortical area MT must have been responsible for tracking motion across the midline in D.K. This subject was equally proficient at identifying the color of the first and second lights on bilateral presentations, suggesting that either hemisphere must have been able to respond to either light. Presumably, response was controlled by the hemisphere registering the light that had to be identified. Tracking by MT can also account for the near ceiling performance of the control subjects in discriminating the direction of apparent motion on both bilateral and unilateral presentations of colored lights. In addition, intact intrahemispheric MT connections must be responsible for L.B.'s near perfect unilateral performance in discriminating the direction of apparent motion of colored lights. Although L.B. was also able to discriminate the direction of apparent motion of colored lights on bilateral presentations, his performance was poorer than in the unilateral condition. In the same task with white lights, L.B. scored near ceiling on both bilateral and unilateral presentations [26]. The critical difference between the two tasks is that the luminance of the colored lights was considerably lower than that of the white lights. This suggests that subcortical pathways may be less effective at shifting attention across the midline under conditions of low stimulus luminance. In addition, the results of previous studies indicate that the efficiency of subcortical pathways may also be compromised in cases of increased stimulus complexity [26] and stringent temporal parameters [11]. In contrast, D.K. and/or control subjects have little difficulty discriminating apparent motion under these conditions [26, I 1]. Furthermore, D.K. and control subjects are faster than L.B. at discriminating succession across the midline, and L.B. himself responds more quickly to within-field than bilateral presentations of succession [26]. These findings show that area MT is more highly developed for visual motion than subcortical pathways. The results of this study are therefore consistent with the notion that the tectopulvinar pathway has the capacity for considerable visuospatial function, although its role has been augmented by the development of the neocortex [34, 36]. In addition, the dissociation between the interhemispheric transfer of motion and color observed in this study support the position that forebrain mechanisms are necessary for the analysis of object features but not for visuospatial function [34, 36]. This study also sheds light on the nature of subcortical input to area MT. Although neurons in the superior
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colliculus and the pulvinar nucleus have little direction selectivity [3, 15], the tectopulvinar pathway may contribute to direction sensitivity in MT by mediating shifts in spatial attention. As MT receives projections from the superior colliculus through a number of routes [4, 5, 6, 20], these shifts in attention may very well register in MT. This may explain why considerable direction sensitivity is found in area MT in the absence of the striate cortex, and why this visual responsiveness is eliminated after subsequent lesions to the superior colliculus [16, 32, 33]. In conclusion, this research identifies two processes for motion detection. Specifically, apparent motion may be detected by directionally selective neurons in cortical regions of the brain and by a subcortical attentional mechanism. On the other hand, Cavanagh [9] has distinguished between a passive process, which involves lowlevel motion detectors, and an active process, whereby the visible features of a stimulus, such as its color, are tracked with voluntary attention. As the active process is object-specific, it is probably mediated by higher cortical systems such as those involved in object-based attention [29]. In contrast, the subcortical attentional mechanism is insensitive to object features, as indicated by the dissociation between the interhemispheric integration of motion and color. Taken together, this and Cavanagh's study suggest that there are two attentional processes that can mediate motion perception; a subcortical, involuntary process that is insensitive to object features, and a cortical, voluntary process that tracks visible stimulus features.
6.
7.
8.
9. 10.
11.
12.
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Acknowledgements--This research was supported by a grant from the New Zealand Neurological Foundation. I thank Professor Michael Corballis from the University of Auckland for his valuable advice. I am also grateful to Dahlia and Evan Zaidel and Joseph E. Bogen for arranging for L.B. to be tested in Los Angeles, and to all of the subjects, especially L.B. and D.K., for their cheerful and willingparticipation.
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References
1. Albright, T. D., Desimone, R. and Gross, C. G. Columnar organisation of directionally selective cells in visual area MT of the macaque. Journal of Neurophysiology 51, 16-31, 1984. 2. Barbur, J. L., Ruddock, K. H. and Waterfield, V. A. Human visual responses in the absence of the geniculo-calcarine projection. Brain 103, 905 928, 1980. 3. Bender, D. B. Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Research 279, 258 261, 1983. 4. Benevento, L. A. and Fallon, J. H. The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). Journal of Comparative Neurology 160, 339-362, 1975. 5. Benevento, L. A. and Standage, G. P. The organisation of projections of the retinorecipient and non-
17.
18. 19.
20.
retinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. Journal of Comparative Neurology 217, 307-336, 1983. Benevento, L. A. and Yoshida, K. The afferent and efferent organisation of the lateral geniculo-prestriate pathways in the macaque monkey. Journal of Comparative Neurology 203, 455-474, 1981. Bogen, J. E., Schultz, D. H. and Vogel, P. J. Completeness of callosotomy shown by magnetic resonance imaging in the long term. Archives of Neurology 45, 1203-1205, 1988. Bogen, J. E., and Vogel, P. J. Neurologic status in the long term following complete cerebral commissurotomy. In Les Syndromes de Disconnexion Calleuse chez l'Homme, F. Michel and B. Schott (Editors), pp. 227 251. Hopital Neurologique, Lyon, 1975. Cavanagh, P. Attention-based motion perception. Science 257, 1563-1565, 1992. Cheng, K., Hasegawa, T., Saleem, K. S. and Tanaka, K. Comparison of neuronal selectivity for stimulus speed, length, and contrast in the prestriate visual cortical area V4 and MT of the macaque monkey. Journal of Neurophysiology 71, 2269 2280, 1994. Corballis, M. C. Hemispheric interactions in temporal judgements about spatially separated stimuli. Neuropsychology, in press. Corballis, M. C. and Trudel, C. I. The role of the forebrain commissures in interhemispheric integration. Neuropsychology 7, 1 19, 1993. Dobkins, K. R. and Albright, T. D. Color, luminance, and the detection of visual motion. Current Directories in Psychol. Science 2, 189 193, 1993. Gazzaniga, M. S. Perceptual and attentional processes following callosal section in humans. Neuropsychologia 25, 119-133, 1987. Goldberg, M. and Wurtz, R. H. Activity of the superior colliculus in the behaving monkey. I. Visual receptive fields of single neurons. Journal of Neurophysiology 35, 542 596, 1972. Gross, C. G. Contribution of striate cortex and the superior colliculus to visual function in area MT, the superior temporal polysensory area and the inferior temporal cortex. Neuropsychologia 25, 497-515, 1991. Holtzman, J. D., Sidtis, J. J., Volpe, B. T., Wilson, D. H. and Gazzaniga, M. S. Dissociation of spatial information for stimulus localisation and the control of attention. Brain 104, 861-872, 1981. Johnson, L. E. Bilateral visual cross-integration by human forebrain commissurotomy subjects. Neuropsychologia 22, 167-175, 1984. Maunsell, J. H. R. and Van Essen, D. C. The connections of the middle temporal visual area (MT) and their relationship to cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 25632586, 1983. Maunsell, J. H. R. and Van Essen, D. C. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. Journal of Neurophysiology 49, 1127 1147, 1983.
N. Naikar/Perception of motion of colored stimuli after commissurotomy 21. Meienberg, O., Zangemeister, W. H., Rosenberg, M., Hoyt, W. F. and Stark, L. Saccadic eye movement strategies in patients with homonymous hemianopia. Annals of Neurology 9, 537-544, 1981. 22. Midgley, G. C. and Tees, R. C. Reinstatement of orienting behavior by d-amphetamine in rats with superior colliculus lesions. Behavioral Neuroscience 100, 246-255, 1986. 23. Mikami, A. Direction selective neurons respond to short-range and long-range apparent motion stimuli in macaque visual area MT. International Journal of Neuroscience 61, 101 112, 1991. 24. Mikami, A., Newsome, W. T. and Wurtz, R. H. Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extra° striate area MT. Journal of Neurophysiology 55, 1308 1327, 1986. 25. Mikami, A., Newsome, W. T. and Wurtz, R. H. Motion selectivity in macaque visual cortex. II. Spatio-temporal range of directional interactions in MT and VI. Journal of Neurophysiology 55, 1328 1339, 1986. 26. Naikar, N. and Corballis, M. C. The perception of apparent motion across the retinal midline after commissurotomy. Neuropsychologia 34, 297-309, 1996. 27. Petersen, S. E., Robinson, D. L. and Morris, J. D. Contributions of the pulvinar to visual spatial attention. Neuropsychologia 25, 97-106, 1987. 28. Rafal, R., Henik, A. and Smith, J. Extrageniculate contributions to reflex visual orienting in normal humans: A temporal hemifield advantage. Journal of Cognitive Neuroscience 3, 322-328, 1991. 29. Rafal, R. and Robertson, L. The neurology of visual attention. In The Cognitive Neurosciences, M. S. Gazzaniga (Editor), pp. 625-648. MIT Press, Cambridge, MA, 1995. 30. Ramachandran, V. S., Cronin-Golomb, A. and Myers, J. J. Perception of apparent motion by commissurotomy patients. Nature 320, 358 359, 1986. 31. Reuter-Lorenz, P. A., Hughes, H. C. and Fendrich, R. The reduction of saccadic latency by prior offset
32.
33.
34. 35.
36.
37. 38.
39.
40. 41.
1049
of the fxation point: An analysis of the gap effect. Perception and Psychology 49, 165-175, 1991. Rodman, H. R., Gross, C. G. and Albright, T. D. Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal. Journal of Neuroscience 9, 2033-2050, 1989. Rodman, H. R., Gross, C. G. and Albright, T. D. Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal. Journal of Neuroscience 10, 1154-1164, 1990. Schneider, G. E. The two visual systems. Science 163, 895-902, 1969. Sprague, J. M., Berlucchi, G. and Rizzolatti, G. The role of the superior colliculus and pretectum in vision and visually guided behavior. In Handbook of Sens. Physiology, R. Jung (Editor), Vol. II/3B, pp. 27 101. Springer, Berlin, 1973. Thinus-Blanc, C., Scardigli, P. and Buhot, M.-C. The effects of superior colliculus lesions in hamsters: Feature detection versus spatial localisation. Physi0/09)' and Behavior 49, 1-6, 1991. Trevarthen, C. B. Two mechanisms of vision in primates. Psychologische Forschung 31,299-337, 1968. Trevarthen, C. B. Integrative functions of the cerebral commissures. In Handbook of Neuropsychology: Vol. 4. The Commissurotomized Brain, R. D. Nebes (Editor), pp. 49-83, Elsevier Science, Oxford, 1991. Truett, A., Begleiter, A., McCarthy, G., Roessler, E., Nobre, A. C. and Spencer, D. D. Electrophysiological studies of color processing in human visual cortex. Electro. and Clinical Neurophysiology 88, 343-355, 1993. Winer, B. J. Statistical Principles in Experimental Design. Wiley, New York, 1971. Zaidel, E. In Interhemispheric transfer in the split brain: Long-term status following complete cerebral commissurotomy. In Brain Asymmetry, R. J. Davidson and K. Hugdahl (Editors), pp. 491 532. MIT Press, Cambridge, MA, 1995.