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Impaired orientation after primate tectal lesions
538
Brain Research, 67 (1974) 538-541 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Impaired orientation after primate tectal lesions
E. G R E G O R Y K E A T I N G
Departments of Neurology and Anatomy, S.U.N.Y. Upstate Medical Center, Syracuse, N.Y. 13210
(u.s.a.) (Accepted November 14th, 1973)
Removal of the superior colliculus in the monkey causes some deficits such as impaired discrimination of stimulus velocity and slowed initiations of eye movements 1,s, but most laboratories working with primates report nothing like the visual neglect caused by lesion of this area in other species. This is surprising since unit recording and stimulation studies describe neurons in the monkey tectum which as in other animals seem tuned to orienting the animal to particular points of his visual field ~,5. One laboratory reported an interesting class of neurons that selectively attended to relevant stimuli, that is, it responded only to those lights appearing in its receptive field which the monkey was required to fixate for reward 3. The authors theorized that the superior colliculus sifts out those visual events which deserve further attention and guides the monkey's orientation to the proper point in space. Two lesion studies which tested the theory measured orienting movements o f the eyes, which are slowed but probably not otherwise impaired by tectal removal 4,8. I tried to measure a different orienting response and to design a behavioral task which determined whether lesions impaired a monkey's accuracy in reaching toward the important one o f two stimuli appearing briefly in its visual field. The attempt resulted in the following procedures. The door of a standard primate testing box opened and the monkey faced the array of 24 food bins shown in Fig. 1. The apparatus subtended about 100° of visual field. The door covering each bin was made of half-ground translucent plexiglass which served as a screen for rear-projected visual stimuli. Two spots o f light flashed simultaneously and briefly for 200 msec, one on each of two of the doors. One light spot was half as bright as the other and the monkey had to locate the position o f the dimmer spot by reaching through that door to obtain a raisin. If he misreached, the trial ended and the position o f each error was recorded. Over the 50 trials o f a daily session the spots changed positions according to a sequence that was random except for the restriction that the correct (dimmer) spot should fall on each door twice in a session. I selected a stimulus duration of 200 msec since that interval is probably too short for a monkey to complete a fixating saccade a. This would enable the test to measure the monkey's orientation to peripheral as well as central targets since the animal could not scan the array until the lights fell within its fovea. Since normal eye movements were not required to solve the
SHORT COMMUNICATIONS
539
Fig. 1. Array of covered food bins used for orientation task. Circles represent rear-projected spots of light which flashed simultaneously for 200 msec on two of the doors. The monkey had to locate the door which had held the dimmer spot. task the short stimulus time minimized the postoperative influence o f impaired eye movements caused by poorly contained tectal lesions. Six rhesus monkeys were shaped on components of this task and then trained to criterion on its final f o r m as described above. Criterion performance was 90 correct in a single session or 80 ~ correct on two successive sessions. In addition all monkeys were trained on a flux discrimination that was identical to the orientation task except that the stimulus lights remained on for the duration of the trial. They were also trained on a pattern discrimination between two doors with vertical v e r s u s horizontal stripes. After testing, the superior colliculi o f all 6 monkeys were removed bilaterally by visually monitored aspiration. One week later the monkeys received one session of pattern retesting as a control for generalized trauma or inadvertent occipital damage and their group performance averaged 8 4 ~ correct. The following day testing on the 200 msec light orientation test began. Table I records the effect of tectal removal on the monkey's ability to target the rewarded one of two lights appearing briefly in its visual field. The monkeys t o o k from 1-10 times the number of preopera-
540 TABLE
SHORT COMMUNICATIONS
I
TRIALS AND ERRORS TO CRITERION ON ORIENTATION TASK
A nimal
59 66 69 70 73 74 Mean
Preoperative
Postoperative
Trials
Errors
Trials
Errors
200 775 205 416 613 200 402
47 245 47 137 208 57 124
1050 750 550 1282 636 450 786
425 262 182 436 220 156 280
tive errors to regain criterion after midbrain surgery. Except for monkey no. 74, they also committed a different kind o f error postoperatively. Normal monkeys when they erred reached into the other lighted door 88 ~ of the time. That accounted for only 53 ~ of the errors postoperatively; the other 4 7 ~ of misreaches missed both lighted doors. The effect was thus not simply a failure to distinguish flux differences. Furthermore, I directly tested luminance discrimination on 4 animals during a single session in which the light spots were left on for the entire trial. Their performance averaged 88 ~ correct. The deficit was probably not oculomotor. All the monkeys displayed the 'reluctance' to make large angular eye shifts that is often reported after tectal lesions. One monkey, no. 69, had dilated pupils and forced downward gaze. The posterior commissure of this animal was found to be sectioned and the pretectal region damaged anteriorly up into the thalamus. However, eye movements in 5 of the 6 monkeys were otherwise normal and the histology available for 4 of them verified that the lesions did not invade the posterior commissure and adjacent nuclei. A second interesting finding is that the monkeys were never completely unable to perform the task. Their performance never dropped below 40 ~ correct - - considerably better than chance for an array of 24 choices. Tectal lesions were incomplete in all cases, but lesion size did not entirely predict the degree of deficit. Bilateral removal was least complete in monkeys no. 73 and 74 and greater than 80 ~ complete in the other animals. I could not consistently relate the pattern o f each monkey's errors to the known visual field topography of its spared tectum. For example, they did not consistently neglect the side o f the array that was contralateral to the more complete tectal removal. Nor did sparing of the lateral boundary of the tectum which receives optic fibers controlling lower field vision predict a strong tendency to perform better on the lower half of the array. However, observation o f the monkeys during testing did reveal one interesting pattern to their errors. Most misreaches occurred when the stimulus fell on the opposite half o f the array from where the animal's head was pointing at the start o f a trial. Particularly if a train o f 2-3 trials in a row fell on one half o f the array the animal was poor at finding the next stimulus if it flashed on the opposite half. In other words, assuming that his eyes were pointed in the same
SHORT COMMUNICATIONS
541
direction as his head, the monkey's performance was poorest for stimuli falling in the peripheral visual field. I f more formal test confirms it, this observation may explain the partial sparing of function on this task and the negative effects o f tectal removal on other behavioral measures. Tectal lesions combined with even partial striate cortex lesions severely disrupt performance of some visual tasks1, 7. T h a t result and the rather mild effects of tectal lesion alone have suggested an overlapping function for the primate midbrain and geniculostriate systems. The overlap may separate into different topographic sectors of influence. Lesion o f the superior colliculus will cause a deficit only to the extent that the monkey is forced to solve the task with his peripheral field. It will have no effect if the geniculostriate system is able to foveate a stimulus and use central visual field mechanisms to discern its relevance. It is interesting in this regard that the central receptive fields frequently recorded from tectal neurons seem specified by indirect connections from some other system, since the foveal retina sends no direct projections to primate superior colliculus ~. Furthermore to produce the severe deficits o f combined striate and tectal lesions it is necessary to remove only the foveal portion o f the striate cortex 1. F r o m experiments on other species it is said that the tectal visual system answers the question 'where it is' for a stimulus appearing in the visual field, while the geniculostriate pathways determines 'what it is'. Electrophysiological evidence2,3, 8 and the present results extend the function of the tectum to include both questions. In the visual world where not two, but thousands o f stimuli simultaneously compete for attention, the rectum must make some preliminary judgment about what these events are in order to orient the animal accurately to the few that deserve further scrutiny. I wish to thank Mrs. Karen Webster for her considerable help in this study. The work was supported by Syracuse V.A. Hospital Research funds and by U.S. Public Health Service G r a n t RR5402.
1 ANDERSON,K. V., AND SYMMES,D., The superior colliculus and higher visual functions in the monkey, Brain Research, 13 (1969) 37-52. 2 GOLDBERG, i . E . , AND WURTZ, R.H., Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons, J. Neurophysiol., 35 (1972) 542-559. 3 GOLDBERG,i . E., AND WURTZ, R.H., Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses, J. Neurophysiol., 35 (1972) 560-574. 4 SCHILLER,P. H., Some functional characteristics of the superior colliculus of the rhesus monkey, Bibl. ophthal. (Basel), 82 (1972) 122-129. 5 SCmLLER,P. H., AND STRYKER,i . , Single unit recording and stimulation in superior colliculus of the alert rhesus monkey, J. Neurophysiol., 35 (1972) 915-924. 6 WILSON,M. E., ANDTOYNE,M. J., Retino-tectal and cortico-tectal projections in Macaca mulatta, Brain Research, 24 (1970) 395-406. 7 WININGER,J., PASIK,P., AND PASlK, T., Effect of superior colliculus lesions on discrimination of luminous flux-equated figures by monkeys deprived of striate cortex, Soc. Neurosci. Abstracts, 2
(1973) 100. 8 WURTZ, R. H., AND GOLDBERG,M.E., Activity of superior colliculus in behaving monkey. IV. Effects of lesions on eye movements, J. Neurophysiol., 35 (1972) 587-596.
Brain Research, 67 (1974) 538-541 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Impaired orientation after primate tectal lesions
E. G R E G O R Y K E A T I N G
Departments of Neurology and Anatomy, S.U.N.Y. Upstate Medical Center, Syracuse, N.Y. 13210
(u.s.a.) (Accepted November 14th, 1973)
Removal of the superior colliculus in the monkey causes some deficits such as impaired discrimination of stimulus velocity and slowed initiations of eye movements 1,s, but most laboratories working with primates report nothing like the visual neglect caused by lesion of this area in other species. This is surprising since unit recording and stimulation studies describe neurons in the monkey tectum which as in other animals seem tuned to orienting the animal to particular points of his visual field ~,5. One laboratory reported an interesting class of neurons that selectively attended to relevant stimuli, that is, it responded only to those lights appearing in its receptive field which the monkey was required to fixate for reward 3. The authors theorized that the superior colliculus sifts out those visual events which deserve further attention and guides the monkey's orientation to the proper point in space. Two lesion studies which tested the theory measured orienting movements o f the eyes, which are slowed but probably not otherwise impaired by tectal removal 4,8. I tried to measure a different orienting response and to design a behavioral task which determined whether lesions impaired a monkey's accuracy in reaching toward the important one o f two stimuli appearing briefly in its visual field. The attempt resulted in the following procedures. The door of a standard primate testing box opened and the monkey faced the array of 24 food bins shown in Fig. 1. The apparatus subtended about 100° of visual field. The door covering each bin was made of half-ground translucent plexiglass which served as a screen for rear-projected visual stimuli. Two spots o f light flashed simultaneously and briefly for 200 msec, one on each of two of the doors. One light spot was half as bright as the other and the monkey had to locate the position o f the dimmer spot by reaching through that door to obtain a raisin. If he misreached, the trial ended and the position o f each error was recorded. Over the 50 trials o f a daily session the spots changed positions according to a sequence that was random except for the restriction that the correct (dimmer) spot should fall on each door twice in a session. I selected a stimulus duration of 200 msec since that interval is probably too short for a monkey to complete a fixating saccade a. This would enable the test to measure the monkey's orientation to peripheral as well as central targets since the animal could not scan the array until the lights fell within its fovea. Since normal eye movements were not required to solve the
SHORT COMMUNICATIONS
539
Fig. 1. Array of covered food bins used for orientation task. Circles represent rear-projected spots of light which flashed simultaneously for 200 msec on two of the doors. The monkey had to locate the door which had held the dimmer spot. task the short stimulus time minimized the postoperative influence o f impaired eye movements caused by poorly contained tectal lesions. Six rhesus monkeys were shaped on components of this task and then trained to criterion on its final f o r m as described above. Criterion performance was 90 correct in a single session or 80 ~ correct on two successive sessions. In addition all monkeys were trained on a flux discrimination that was identical to the orientation task except that the stimulus lights remained on for the duration of the trial. They were also trained on a pattern discrimination between two doors with vertical v e r s u s horizontal stripes. After testing, the superior colliculi o f all 6 monkeys were removed bilaterally by visually monitored aspiration. One week later the monkeys received one session of pattern retesting as a control for generalized trauma or inadvertent occipital damage and their group performance averaged 8 4 ~ correct. The following day testing on the 200 msec light orientation test began. Table I records the effect of tectal removal on the monkey's ability to target the rewarded one of two lights appearing briefly in its visual field. The monkeys t o o k from 1-10 times the number of preopera-
540 TABLE
SHORT COMMUNICATIONS
I
TRIALS AND ERRORS TO CRITERION ON ORIENTATION TASK
A nimal
59 66 69 70 73 74 Mean
Preoperative
Postoperative
Trials
Errors
Trials
Errors
200 775 205 416 613 200 402
47 245 47 137 208 57 124
1050 750 550 1282 636 450 786
425 262 182 436 220 156 280
tive errors to regain criterion after midbrain surgery. Except for monkey no. 74, they also committed a different kind o f error postoperatively. Normal monkeys when they erred reached into the other lighted door 88 ~ of the time. That accounted for only 53 ~ of the errors postoperatively; the other 4 7 ~ of misreaches missed both lighted doors. The effect was thus not simply a failure to distinguish flux differences. Furthermore, I directly tested luminance discrimination on 4 animals during a single session in which the light spots were left on for the entire trial. Their performance averaged 88 ~ correct. The deficit was probably not oculomotor. All the monkeys displayed the 'reluctance' to make large angular eye shifts that is often reported after tectal lesions. One monkey, no. 69, had dilated pupils and forced downward gaze. The posterior commissure of this animal was found to be sectioned and the pretectal region damaged anteriorly up into the thalamus. However, eye movements in 5 of the 6 monkeys were otherwise normal and the histology available for 4 of them verified that the lesions did not invade the posterior commissure and adjacent nuclei. A second interesting finding is that the monkeys were never completely unable to perform the task. Their performance never dropped below 40 ~ correct - - considerably better than chance for an array of 24 choices. Tectal lesions were incomplete in all cases, but lesion size did not entirely predict the degree of deficit. Bilateral removal was least complete in monkeys no. 73 and 74 and greater than 80 ~ complete in the other animals. I could not consistently relate the pattern o f each monkey's errors to the known visual field topography of its spared tectum. For example, they did not consistently neglect the side o f the array that was contralateral to the more complete tectal removal. Nor did sparing of the lateral boundary of the tectum which receives optic fibers controlling lower field vision predict a strong tendency to perform better on the lower half of the array. However, observation o f the monkeys during testing did reveal one interesting pattern to their errors. Most misreaches occurred when the stimulus fell on the opposite half o f the array from where the animal's head was pointing at the start o f a trial. Particularly if a train o f 2-3 trials in a row fell on one half o f the array the animal was poor at finding the next stimulus if it flashed on the opposite half. In other words, assuming that his eyes were pointed in the same
SHORT COMMUNICATIONS
541
direction as his head, the monkey's performance was poorest for stimuli falling in the peripheral visual field. I f more formal test confirms it, this observation may explain the partial sparing of function on this task and the negative effects o f tectal removal on other behavioral measures. Tectal lesions combined with even partial striate cortex lesions severely disrupt performance of some visual tasks1, 7. T h a t result and the rather mild effects of tectal lesion alone have suggested an overlapping function for the primate midbrain and geniculostriate systems. The overlap may separate into different topographic sectors of influence. Lesion o f the superior colliculus will cause a deficit only to the extent that the monkey is forced to solve the task with his peripheral field. It will have no effect if the geniculostriate system is able to foveate a stimulus and use central visual field mechanisms to discern its relevance. It is interesting in this regard that the central receptive fields frequently recorded from tectal neurons seem specified by indirect connections from some other system, since the foveal retina sends no direct projections to primate superior colliculus ~. Furthermore to produce the severe deficits o f combined striate and tectal lesions it is necessary to remove only the foveal portion o f the striate cortex 1. F r o m experiments on other species it is said that the tectal visual system answers the question 'where it is' for a stimulus appearing in the visual field, while the geniculostriate pathways determines 'what it is'. Electrophysiological evidence2,3, 8 and the present results extend the function of the tectum to include both questions. In the visual world where not two, but thousands o f stimuli simultaneously compete for attention, the rectum must make some preliminary judgment about what these events are in order to orient the animal accurately to the few that deserve further scrutiny. I wish to thank Mrs. Karen Webster for her considerable help in this study. The work was supported by Syracuse V.A. Hospital Research funds and by U.S. Public Health Service G r a n t RR5402.
1 ANDERSON,K. V., AND SYMMES,D., The superior colliculus and higher visual functions in the monkey, Brain Research, 13 (1969) 37-52. 2 GOLDBERG, i . E . , AND WURTZ, R.H., Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons, J. Neurophysiol., 35 (1972) 542-559. 3 GOLDBERG,i . E., AND WURTZ, R.H., Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses, J. Neurophysiol., 35 (1972) 560-574. 4 SCHILLER,P. H., Some functional characteristics of the superior colliculus of the rhesus monkey, Bibl. ophthal. (Basel), 82 (1972) 122-129. 5 SCmLLER,P. H., AND STRYKER,i . , Single unit recording and stimulation in superior colliculus of the alert rhesus monkey, J. Neurophysiol., 35 (1972) 915-924. 6 WILSON,M. E., ANDTOYNE,M. J., Retino-tectal and cortico-tectal projections in Macaca mulatta, Brain Research, 24 (1970) 395-406. 7 WININGER,J., PASIK,P., AND PASlK, T., Effect of superior colliculus lesions on discrimination of luminous flux-equated figures by monkeys deprived of striate cortex, Soc. Neurosci. Abstracts, 2
(1973) 100. 8 WURTZ, R. H., AND GOLDBERG,M.E., Activity of superior colliculus in behaving monkey. IV. Effects of lesions on eye movements, J. Neurophysiol., 35 (1972) 587-596.