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Extrageniculostriate vision in the monkey. VI. Visually guided accurate reaching behavior
422
Brain Research, 152 (1978) 422428 © Elsevier/North-Holland Biomedical Press
Extrageniculostriate vision in the monkey. VI. Visually guided accurate reaching behavior
TODD E. FEINBERG, TAUBA PASIK and PEDRO PASIK Department of Neurology, Mount Sinai School of Medicine of the City University of New York, New York, N. Y 10029 (U.S.A.)
(Accepted March 9th, 1978)
In his classic article of 1942, K1/iver10 concluded that total exclusion of the geniculostriate system in monkeys leads 'to an elimination of visual space with its dimensions'. Destriated monkeys were able to reach accurately for objects only when their relative position remained constant from day to day. Such accurate reaching was confirmed in more recent studies involving two-choice discrimination situations16,1L In these investigations it was also noted that operated animals monitored the movement of their hand with appropriate head and eye movements during the performance of visual as well as tactual tasks. In addition, they recovered the ability to make smooth pursuit eye movements on tracking bright objects traversing the visual field 13, a behavior that was also seen by other investigators in monkeys which presumably have had total removal of visual cortex s. The latter studies succeeded in training these animals to grasp accurately moving as well as stationary targets and concluded that destriated monkeys were able to localize visual events in space s . However, histological reconstruction of the lesion in the subject more thoroughly examined showed that 'a small island of striate cortex was left apparently intact in the depths of the calcarine fissure' of one side with a corresponding normal region in the lateral geniculate nucleus of the same side v. The incomplete ablation decreased somewhat the significance of the study. In fact, an independent investigation showed that monkeys with up to 98 ~ of the striate cortex excised quickly mastered a 'pattern localization' task whereas monkeys with total removals failed the same problem 9. The present study re-evaluates the capacity for space localization in monkeys with total bilateral exclusion of the geniculostriate system and shows that indeed they can be trained to perform accurate reaching movements with visual guidance. A preliminary report of this work has been presented earlier 5. The subjects were 3 monkeys ( M . mulatta) with bilateral occipital lobectomies. One of them (no. 836) was a young adolescent, 2.5 kg in weight, which had previously been used in other studies involving bar orientation discrimination 14. The other two (nos. 816 and 817) were considerably older, weighing 4.5 and 6 kg, and had been received from Dr. Peter Schilder after extensive training with tests utilizing wavelength cues. The histologic reconstruction of the ablations has not been published before.
423 During testing each monkey was in a cage with the front wall made of horizontal rods, 0.6 cm in diameter and 3.5 cm apart. A 46 cm diameter white spin wheel with a protruding bolt 12.5 cm from the center was placed parallel to the cage front at arms length distance. A black circular disk, 1.5 cm thick, could be attached to the bolt and positioned in one of the 4 quadrants by rotating the wheel. All testing was conducted in an isolated room which was illuminated by fluorescent light ceiling fixtures. Care was taken to avoid spurious shadows on the wheel which measured an average luminance of 15.76 ft.L (54 cd/sq.m). During the intertrial period an opaque screen was interposed between the cage and the wheel and the position of the stimulus changed according to a random series. The reward for accurate reaching was a cube of apple, 5 mm on a side, stuck on a pin at the center of the target. A correct response was scored when the animal touched the black disk and then grasped the apple, or grasped the apple directly without ever touching the surface of the wheel. In the event the latter was touched first, the monkey was allowed to explore until the apple was found, such behavior being recorded as an incorrect response. Monkeys were given 50 trials per day, 5 days a week, until a criterion level of performance of 90 ~ correct responses in 200 consecutive trials was achieved. Prior to formal testing the animals were given 10 pretraining sessions with a black disk of 90 mm diameter and no opaque screen interposed, the experimenter placing the apple and varying the position of the disk in full view of the monkey. The formal testing consisted of 5 successive problems. In the first 4 (I-IV), the target was a black disk of progressively decreasing dimensions, the respective diameters being 90, 55, 35 and 15 mm (approximately 46 °, 28 °, 18° and 9 ° of visual angle). In the last problem (V) the stimulus was exclusively the apple cube (approximate visual angle of 3°) stuck directly on the bolt. The surgical and histological procedures have been described in detail elsewherO6,1L In short, bilateral one-stage occipital lobectomies at the level of the lunate sulcus and further aspiration of the remaining calcarine cortex were carried out under sodium pentobarbital anesthesia and sterile precautions. At the completion of the experiment the animals were perfused under deep narcosis with isotonic saline solution followed by 5 ~ formalin. The brains were embedded in celloidin, cut at 40 # m in either the coronal (nos. 816 and 817), or the sagittal and horizontal planes (no. 836), and stained by the K1/iver-Barrera method. Reconstructions used every 25th section for the cortical lesions and every 10th section for the retrograde degeneration in thalamic nuclei. The three monkeys became subjects of this study 42 months (nos. 816 and 817) or 8 months (no. 836) after removal of the visual cortex. By this time they all had passed the initial period of severe visual deficits 16, and had received extensive training in twochoice testing situations which amounted to a total of 5500 trials in no. 83614 and 34,000 trials in nos. 816 and 817 (Schilder, unpublished observations). The performance of the animals in the pretraining period was characterized at first by random groping movements with no visual exploration of the field. If the monkey grasped the black disk by chance, it would only explore the edges without visual fixation, and without acquiring the reward placed at its center. By the 250-300th trial, grasping of the disk's edge was consistently followed by search for the reward at its center. By the 300-350th trial, it was apparent that the monkeys were making first contact with the black disk, and
424 TABLE I
Errors through criterion for all problems Note: problems I, II, III and IV utilized black disks of 90, 55, 35 and 15 mm in diameter. In problem V, the stimulus was only the apple cube. Monkey no. Postoperative Postoperative Problems survival (months) I H
Ili
IV
V
816 817 836 Mean S.D.
56 59 14
20 17 4
19 15 3
16 14 4
41 15 11
278 286 245
14 8
12 8
11 6
22 16
270 22
on an increasing percentage of trials, clear head and eye movements toward the field were being performed in advance of the response. Thereafter the animals gradually showed increasing evidence for visual guidance. They sat at the front of the cage and slowly scanned successive quadrants. Once the disk was found they grasped the edge and searched for the reward. If they were oriented initially toward the correct quadrant, they would reach out directly and acquire the apple cube. Table 1 presents the results of the formal testing in terms of total errors, including those made on criterion trials, for all problems per individual animal. Problem I was rapidly mastered by all the monkeys in the minimum number of 200 trials required for the established criterion. This high level of performance was maintained when confronted with problems II and III. Somewhat higher mean errors were made in problem IV on the basis of the scores of monkey no. 816 which required 350 trials to reach criterion on this test. In general, it was noted that of the two types of correct responses, i.e. the touching of the black disk first or acquiring the reward directly, the monkeys tended to make the latter on an increasing number of trials from problem I to IV. This information was recorded for no. 836. The apple was contacted directly in 34%, 51%, 68% and 74% of the trials in problems I, II, III and IV, respectively. In problem V, which required the accurate grasping of a rather low contrast target (cube of apple on a white backgrond), the initial performance fell as low as 15 % correct responses in all animals. Following approximately a 10-session period, during which there was either slowly progressive or fluctuating improvement, the 3 monkeys started criterion runs and reached the established level in a total of 700 trials for no. 817, or 750 trials for nos. 816 and 836, with a mean of 270 errors. At the completion of the testing, control trials were given during which the room lights were turned off as soon as the opaque screen was removed. When the lights were returned after a period of at least 1 min, which well exceeded the time required for the response in standard trials, the animal was found sitting quietly in the cage with the reward still on the wheel Reconstructions of the lesions are illustrated in Figs. 1 and 2. The ablations included the entirety of the striate cortex on both sides, and in addition there was removal of approximately 70% of area OB and 20% of area OA 2, in nos. 836 and 817. The
425
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I00
150
200
250
200
250
300
350
320
350
400
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300
Fig. 1. Reconstruction of lesions in monkey 836. Absence of occipital lobes indicated by dashed lines. Absence of cortex is shown by black in the surface views and by a fine line in the sections. Intact cortex in the sections is represented by the thicker black shading. In the framed enlargement, degeneration with dense gliosis is shown by stippling. Numbers identify serial sections which were cut at 40/~m. LGd, lateral geniculate nucleus, pars dorsalis; LGv, lateral geniculate nucleus, pars ventralis; OT, optic tract; OR, optic radiations; MG, medial geniculate nucleus; IC, inferior colliculus; Pul, pulvinar; Pal, pallidum; Put, putarnen; Cau, caudate nucleus (tail); SNc, substantia nigra, pars compacta; SNr, substantia nigra, pars reticulata. Top: convexity and base views of posterior half of left hemisphere; sections are in the sagittal plane. Bottom: lateral and medial aspects of posterior half of right hemisphere; sections are in the horizontal plane. Note that the occipital lobes and the cortex at the banks of the remaining calcarine fissures are absent on both sides. Degeneration with heavy gliosis is present bilaterally in the entirety of the LGd and optic radiations. The pulvinars also show circumscribed areas of retrograde degeneration. lateral geniculate nuclei showed c o m p l e t e d i s a p p e a r a n c e o f principal cells with few i n t e r n e u r o n s r e m a i n i n g in the m i d s t o f the glial proliferationaL The pulvinars exhibited areas o f r e t r o g r a d e d e g e n e r a t i o n p a r t i c u l a r l y in nucleus pulvinaris lateralis a n d inferior. M o n k e y 816 showed a m i n u t e r e m n a n t o f striate cortex at the rostral end o f the s u p e r i o r lip o f the calcarine fissure on the left side. Layers V a n d VI o f this cortex were gliotic a n d with only few n e u r o n s left. The v o l u m e o f the r e m n a n t was calculated f r o m its a r e a m e a s u r e d in serial sections, and was f o u n d to be 2.4 cu.mm. This a m o u n t represents 0 . 1 7 ~ o f the t o t a l v o l u m e o f striate cortex present in one hemisphere of
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Fig. 2. Reconstruction of lesions in monkeys 816 and 817. Notations as in Fig. 1. R and L indicate right and left side for all drawings. Note the completeness of the ablations except for a minute remnant of striate cortex in the left hemisphere of no. 816 between sections 330 and 380 (arrows). similarly processed normal brains (Pasik and Pasik, unpublished observations). The left lateral geniculate nucleus contained few principal cells in locations corresponding to the 6 layers but never clustering in a group involving all the layers in a single section. It is clear from the preceding results that monkeys with histologically confirmed complete bilateral removal of striate cortex and partial damage to circumstriate cortex can make visually guided accurate reaching movements. A similar conclusion had been reached earlier from studies in other species including the rat 6, hamster z3 and tree shrew 4, as well as from the observations made most notably on one monkey with incomplete lesions 7,s. Although the influence of the striate cortex remnant in the latter investigation cannot be ruled out, the present findings suggest that it was not essential. The significance of our results in terms of understanding the visual system of primates is emphasized by the observations made in humans who have sustained brain damage. Traditionally, the condition of patients with 'cortical blindness' due to total
427 interference with the geniculostriate system has usually precluded adequate testing. In two such recent cases the subjects could distinguish the 'sudden illumination of a dark r o o m from sudden darkening of a light one', but no clear sign of other visual capacities including space localization could be elicited 3. On the other hand, information has been obtained from patients with visual field defects due to partial destruction of the geniculostriate system. It has long been known that such cases may localize the source of flashes as brief as 40 msec within perimetrically defined hemianopic fields 1,28. Similar observations were repeated more recently 19,27, and additionally a certain degree of correlation between target position and eye fixation could also be demonstrated 2°,27. The present results showing that space localization is possible in the total absence of striate cortex raise the important question of which structures in the remaining brain are responsible for this residual ability. There is some evidence that the superior colliculi may be crucial in the hamster 23 where a double dissociation of deficits and locus of lesion 25 led to the theory that the retinotectal input mediates visual spatial localization, whereas the retinogeniculostriate system subserves visual discriminating capacities 2a,26. Earlier results in the monkey do not support this view, Destriated monkeys not only retain some capacity for space localization as demonstrated in this study, but also exhibit discriminative abilities under certain testing conditionsg,15,~l,2L Whether total superior colliculi ablations will eliminate the capacity to localize in space both in the presence of the striate cortex or in its complete absence, is at present an empirical question answerable by further experimentation. It has recently been shown that monkeys with partial striate and collicular lesions resulting in overlapping scotomata could not make accurate saccades to points within the field defect 11. Since these animals could not even detect light flashes within the scotoma, it is possible that the residual vision was highly taxed by the stimuli used which were only 15 minutes of arc in visual angle and exposed for 200 msec. We have shownin the past tha t monkeys with total bilateral removal of striate cortex and superior colliculi not only can detect a luminous source given sufficient time, but can also master a discrimination based on differences in total luminous flux 17. They fail only when the targets are equated for this dimension is. This work was supported in part by N.I.M.H. G r a n t MH-02261. The skillful assistance of Jorge Balbastro, Victor Rodriguez and Minerva Travieso is gratefully acknowledged.
1 Bender, M. B. and Krieger, H. P., Visual function in perimetrically blind fields, Arch. Neurol. Psychiat., 65 (1951) 72-79. 2 Bonin, G. v. and Bailey, P., The Neocortex ofMacaca mulatta, Univ. of Illinois Press, Urbana, II1., 1947. 3 Brindley, G. S., Gautier-Smith, P. C. and Lewin, W., Cortical blindness and the functions of the non-geniculate fibres of the optic tracts, J. Neurol. Neurosurg. Psychiat., 32 (1969) 259-264. 4 Diamond, I. T. and Hall, W. C., Evolution of neocortex, Science, 164 (1969) 251-262. 5 Feinberg, T., Pasik, P. and Pasik, T., Visually mediated space localization in monkeys without striate cortex, Fed. Proc., 36 (1977) 507. 6 Ferrier, R. J. and Cooper, R. M., Striate cortex ablation and spatial vision, Brain Research, 106 (1967) 71-85.
428 7 Humphrey, N. K., Vision in a monkey without striate cortex: a case study, Perception, 3 (1974) 241-255. 8 Humphrey, N. K. and Weiskrantz, L., Vision in monkeys after removal of the striate cortex, Nature (Lond.), 215 (1967) 595-597. 9 Keating, E. G., Effects of prestriate and striate lesions on the monkey's ability to locate and discriminate visual forms, Exp. Neurol., 47 (1975) 16-25. 10 Kliiver, H., Functional significance of the geniculostriate system, BioL Syrup., 7 (1942) 253-299. 11 Mohler, C. W. and Wurtz, R. H., Role of striate cortex and superior colliculus in visual guidance of saccadic eye movements in monkeys, J. Neurophysiol., 40 (1977) 74-94. 12 Pasik, P., Pasik, T., H~imori, J. and Szentfigothai, J., Golgi type II interneurons in the neuronal circuit of the monkey lateral geniculate nucleus, Exp. Brain Res., 17 (1973) 18-34. 13 Pasik, P., Pasik, T. and Krieger, H. P., Effects of cerebral lesions upon optokinetic nystagmus in monkeys, J. NeurophysioL, 22 (1959) 297-304. 14 Pasik, P,, Pasik, T., Nolan, J. T. and Solomon, S. J., Bar orientation discrimination in normal and destriated monkeys, Neurosci. Abstr., 2 (1976) 1130. 15 Pasik, P,, Pasik, T. and Schilder, P., Extrageniculostriate vision in the monkey: discrimination of luminous flux-equated figures, Exp. Neurol., 24 (1969) 421-437. 16 Pasik, T. and Pasik, P., The visual world of monkeys deprived of striate cortex: effective stimulus parameters and the importance of the accessory optic system. In T. Shipley and J. E. Dowling (Eds.), Visual Processes in Vertebrates, Vision Res., Suppl. 3, (1971) 419-435. 17 Pasik, T. and Pasik, P., Extrageniculostriate vision in the monkey. IV. Critical structures for light vs. no-light discrimination, Brain Research, 56 (1973) 165-182. 18 Pasik, T., Pasik, P., Schilder, P. and Wininger, J., Extrageniculostriate vision in the monkey: effect of circumstriate cortex or superior colliculi ablations. In Excerpta Medica, Int. Congr. Series No. 286, Excerpta Medica, Amsterdam, 1973, pp. 201-202. 19 Perenin, M. T. and Jeannerod, M,, Residual vision in cortically blind hemiphields. Neuropsychologia, 13 (1975) 1-7. 20 P6ppel, E., Held, R. and Frost, D., Residual visual function after brain wounds involving the central visual pathways in man, Nature (Lond.), 243 (1973) 295-296. 21 Schilder, P., Pasik, P, and Pasik, T., Extrageniculostriate vision in the monkey. III. Circle vs triangle and 'red vs. green' discrimination, Exp. Brain Res., 14 (1972) 436~48. 22 Schilder, P., Pasik, T. and Pasik, P., Extrageniculostriate vision in the monkey. If. Demonstration of brightness discrimination, Brain Research, 32 (1971) 383-398. ~ 23 Schneider, G. E., Contrasting visuomotor functions of tectum and cortex in the golden hamster, PsychoL Forsch., 31 (1967) 52-62. 24 Schneider, G. E., The two visual systems, Science, 163 (1969) 895-902. 25 Teuber, H.-L., Physiological psychology, Ann. Rev. Psychol., 6 (1955) 267-296. 26 Trevarthen, C. B., Two mechanisms of vision in primates, PsychoL Forsch., 31 (1968) 299-337. 27 Weiskrantz, L., Warrington, E. K., Sanders, M. D. and Marshall, J., Visual capacity in the hemianopic field following a restricted occipital ablation, Brain, 97 (1974) 709-728. 28 Williams, D. and Gassel, M. M., Visual function in patients with homonymous hemianopia. Part I: The visual fields, Brain, 85 (1962) 175-250.
Note added inproof. Since original submission of this paper in autumn 1977, the article by Weiskrantz et al. (Brain, 100 (1977) 655-670) has appeared in the literature, showing that one monkey with total removal of striate cortex succeeded in reaching accurately to the source of a 110 msec flash.
Brain Research, 152 (1978) 422428 © Elsevier/North-Holland Biomedical Press
Extrageniculostriate vision in the monkey. VI. Visually guided accurate reaching behavior
TODD E. FEINBERG, TAUBA PASIK and PEDRO PASIK Department of Neurology, Mount Sinai School of Medicine of the City University of New York, New York, N. Y 10029 (U.S.A.)
(Accepted March 9th, 1978)
In his classic article of 1942, K1/iver10 concluded that total exclusion of the geniculostriate system in monkeys leads 'to an elimination of visual space with its dimensions'. Destriated monkeys were able to reach accurately for objects only when their relative position remained constant from day to day. Such accurate reaching was confirmed in more recent studies involving two-choice discrimination situations16,1L In these investigations it was also noted that operated animals monitored the movement of their hand with appropriate head and eye movements during the performance of visual as well as tactual tasks. In addition, they recovered the ability to make smooth pursuit eye movements on tracking bright objects traversing the visual field 13, a behavior that was also seen by other investigators in monkeys which presumably have had total removal of visual cortex s. The latter studies succeeded in training these animals to grasp accurately moving as well as stationary targets and concluded that destriated monkeys were able to localize visual events in space s . However, histological reconstruction of the lesion in the subject more thoroughly examined showed that 'a small island of striate cortex was left apparently intact in the depths of the calcarine fissure' of one side with a corresponding normal region in the lateral geniculate nucleus of the same side v. The incomplete ablation decreased somewhat the significance of the study. In fact, an independent investigation showed that monkeys with up to 98 ~ of the striate cortex excised quickly mastered a 'pattern localization' task whereas monkeys with total removals failed the same problem 9. The present study re-evaluates the capacity for space localization in monkeys with total bilateral exclusion of the geniculostriate system and shows that indeed they can be trained to perform accurate reaching movements with visual guidance. A preliminary report of this work has been presented earlier 5. The subjects were 3 monkeys ( M . mulatta) with bilateral occipital lobectomies. One of them (no. 836) was a young adolescent, 2.5 kg in weight, which had previously been used in other studies involving bar orientation discrimination 14. The other two (nos. 816 and 817) were considerably older, weighing 4.5 and 6 kg, and had been received from Dr. Peter Schilder after extensive training with tests utilizing wavelength cues. The histologic reconstruction of the ablations has not been published before.
423 During testing each monkey was in a cage with the front wall made of horizontal rods, 0.6 cm in diameter and 3.5 cm apart. A 46 cm diameter white spin wheel with a protruding bolt 12.5 cm from the center was placed parallel to the cage front at arms length distance. A black circular disk, 1.5 cm thick, could be attached to the bolt and positioned in one of the 4 quadrants by rotating the wheel. All testing was conducted in an isolated room which was illuminated by fluorescent light ceiling fixtures. Care was taken to avoid spurious shadows on the wheel which measured an average luminance of 15.76 ft.L (54 cd/sq.m). During the intertrial period an opaque screen was interposed between the cage and the wheel and the position of the stimulus changed according to a random series. The reward for accurate reaching was a cube of apple, 5 mm on a side, stuck on a pin at the center of the target. A correct response was scored when the animal touched the black disk and then grasped the apple, or grasped the apple directly without ever touching the surface of the wheel. In the event the latter was touched first, the monkey was allowed to explore until the apple was found, such behavior being recorded as an incorrect response. Monkeys were given 50 trials per day, 5 days a week, until a criterion level of performance of 90 ~ correct responses in 200 consecutive trials was achieved. Prior to formal testing the animals were given 10 pretraining sessions with a black disk of 90 mm diameter and no opaque screen interposed, the experimenter placing the apple and varying the position of the disk in full view of the monkey. The formal testing consisted of 5 successive problems. In the first 4 (I-IV), the target was a black disk of progressively decreasing dimensions, the respective diameters being 90, 55, 35 and 15 mm (approximately 46 °, 28 °, 18° and 9 ° of visual angle). In the last problem (V) the stimulus was exclusively the apple cube (approximate visual angle of 3°) stuck directly on the bolt. The surgical and histological procedures have been described in detail elsewherO6,1L In short, bilateral one-stage occipital lobectomies at the level of the lunate sulcus and further aspiration of the remaining calcarine cortex were carried out under sodium pentobarbital anesthesia and sterile precautions. At the completion of the experiment the animals were perfused under deep narcosis with isotonic saline solution followed by 5 ~ formalin. The brains were embedded in celloidin, cut at 40 # m in either the coronal (nos. 816 and 817), or the sagittal and horizontal planes (no. 836), and stained by the K1/iver-Barrera method. Reconstructions used every 25th section for the cortical lesions and every 10th section for the retrograde degeneration in thalamic nuclei. The three monkeys became subjects of this study 42 months (nos. 816 and 817) or 8 months (no. 836) after removal of the visual cortex. By this time they all had passed the initial period of severe visual deficits 16, and had received extensive training in twochoice testing situations which amounted to a total of 5500 trials in no. 83614 and 34,000 trials in nos. 816 and 817 (Schilder, unpublished observations). The performance of the animals in the pretraining period was characterized at first by random groping movements with no visual exploration of the field. If the monkey grasped the black disk by chance, it would only explore the edges without visual fixation, and without acquiring the reward placed at its center. By the 250-300th trial, grasping of the disk's edge was consistently followed by search for the reward at its center. By the 300-350th trial, it was apparent that the monkeys were making first contact with the black disk, and
424 TABLE I
Errors through criterion for all problems Note: problems I, II, III and IV utilized black disks of 90, 55, 35 and 15 mm in diameter. In problem V, the stimulus was only the apple cube. Monkey no. Postoperative Postoperative Problems survival (months) I H
Ili
IV
V
816 817 836 Mean S.D.
56 59 14
20 17 4
19 15 3
16 14 4
41 15 11
278 286 245
14 8
12 8
11 6
22 16
270 22
on an increasing percentage of trials, clear head and eye movements toward the field were being performed in advance of the response. Thereafter the animals gradually showed increasing evidence for visual guidance. They sat at the front of the cage and slowly scanned successive quadrants. Once the disk was found they grasped the edge and searched for the reward. If they were oriented initially toward the correct quadrant, they would reach out directly and acquire the apple cube. Table 1 presents the results of the formal testing in terms of total errors, including those made on criterion trials, for all problems per individual animal. Problem I was rapidly mastered by all the monkeys in the minimum number of 200 trials required for the established criterion. This high level of performance was maintained when confronted with problems II and III. Somewhat higher mean errors were made in problem IV on the basis of the scores of monkey no. 816 which required 350 trials to reach criterion on this test. In general, it was noted that of the two types of correct responses, i.e. the touching of the black disk first or acquiring the reward directly, the monkeys tended to make the latter on an increasing number of trials from problem I to IV. This information was recorded for no. 836. The apple was contacted directly in 34%, 51%, 68% and 74% of the trials in problems I, II, III and IV, respectively. In problem V, which required the accurate grasping of a rather low contrast target (cube of apple on a white backgrond), the initial performance fell as low as 15 % correct responses in all animals. Following approximately a 10-session period, during which there was either slowly progressive or fluctuating improvement, the 3 monkeys started criterion runs and reached the established level in a total of 700 trials for no. 817, or 750 trials for nos. 816 and 836, with a mean of 270 errors. At the completion of the testing, control trials were given during which the room lights were turned off as soon as the opaque screen was removed. When the lights were returned after a period of at least 1 min, which well exceeded the time required for the response in standard trials, the animal was found sitting quietly in the cage with the reward still on the wheel Reconstructions of the lesions are illustrated in Figs. 1 and 2. The ablations included the entirety of the striate cortex on both sides, and in addition there was removal of approximately 70% of area OB and 20% of area OA 2, in nos. 836 and 817. The
425
I
2 2 3 3 4 4
0 5 0 5 0 5
I
I00
150
200
250
200
250
300
350
320
350
400
0 - 0 - 0 - 0 - 0 - 0 - -
300
Fig. 1. Reconstruction of lesions in monkey 836. Absence of occipital lobes indicated by dashed lines. Absence of cortex is shown by black in the surface views and by a fine line in the sections. Intact cortex in the sections is represented by the thicker black shading. In the framed enlargement, degeneration with dense gliosis is shown by stippling. Numbers identify serial sections which were cut at 40/~m. LGd, lateral geniculate nucleus, pars dorsalis; LGv, lateral geniculate nucleus, pars ventralis; OT, optic tract; OR, optic radiations; MG, medial geniculate nucleus; IC, inferior colliculus; Pul, pulvinar; Pal, pallidum; Put, putarnen; Cau, caudate nucleus (tail); SNc, substantia nigra, pars compacta; SNr, substantia nigra, pars reticulata. Top: convexity and base views of posterior half of left hemisphere; sections are in the sagittal plane. Bottom: lateral and medial aspects of posterior half of right hemisphere; sections are in the horizontal plane. Note that the occipital lobes and the cortex at the banks of the remaining calcarine fissures are absent on both sides. Degeneration with heavy gliosis is present bilaterally in the entirety of the LGd and optic radiations. The pulvinars also show circumscribed areas of retrograde degeneration. lateral geniculate nuclei showed c o m p l e t e d i s a p p e a r a n c e o f principal cells with few i n t e r n e u r o n s r e m a i n i n g in the m i d s t o f the glial proliferationaL The pulvinars exhibited areas o f r e t r o g r a d e d e g e n e r a t i o n p a r t i c u l a r l y in nucleus pulvinaris lateralis a n d inferior. M o n k e y 816 showed a m i n u t e r e m n a n t o f striate cortex at the rostral end o f the s u p e r i o r lip o f the calcarine fissure on the left side. Layers V a n d VI o f this cortex were gliotic a n d with only few n e u r o n s left. The v o l u m e o f the r e m n a n t was calculated f r o m its a r e a m e a s u r e d in serial sections, and was f o u n d to be 2.4 cu.mm. This a m o u n t represents 0 . 1 7 ~ o f the t o t a l v o l u m e o f striate cortex present in one hemisphere of
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Fig. 2. Reconstruction of lesions in monkeys 816 and 817. Notations as in Fig. 1. R and L indicate right and left side for all drawings. Note the completeness of the ablations except for a minute remnant of striate cortex in the left hemisphere of no. 816 between sections 330 and 380 (arrows). similarly processed normal brains (Pasik and Pasik, unpublished observations). The left lateral geniculate nucleus contained few principal cells in locations corresponding to the 6 layers but never clustering in a group involving all the layers in a single section. It is clear from the preceding results that monkeys with histologically confirmed complete bilateral removal of striate cortex and partial damage to circumstriate cortex can make visually guided accurate reaching movements. A similar conclusion had been reached earlier from studies in other species including the rat 6, hamster z3 and tree shrew 4, as well as from the observations made most notably on one monkey with incomplete lesions 7,s. Although the influence of the striate cortex remnant in the latter investigation cannot be ruled out, the present findings suggest that it was not essential. The significance of our results in terms of understanding the visual system of primates is emphasized by the observations made in humans who have sustained brain damage. Traditionally, the condition of patients with 'cortical blindness' due to total
427 interference with the geniculostriate system has usually precluded adequate testing. In two such recent cases the subjects could distinguish the 'sudden illumination of a dark r o o m from sudden darkening of a light one', but no clear sign of other visual capacities including space localization could be elicited 3. On the other hand, information has been obtained from patients with visual field defects due to partial destruction of the geniculostriate system. It has long been known that such cases may localize the source of flashes as brief as 40 msec within perimetrically defined hemianopic fields 1,28. Similar observations were repeated more recently 19,27, and additionally a certain degree of correlation between target position and eye fixation could also be demonstrated 2°,27. The present results showing that space localization is possible in the total absence of striate cortex raise the important question of which structures in the remaining brain are responsible for this residual ability. There is some evidence that the superior colliculi may be crucial in the hamster 23 where a double dissociation of deficits and locus of lesion 25 led to the theory that the retinotectal input mediates visual spatial localization, whereas the retinogeniculostriate system subserves visual discriminating capacities 2a,26. Earlier results in the monkey do not support this view, Destriated monkeys not only retain some capacity for space localization as demonstrated in this study, but also exhibit discriminative abilities under certain testing conditionsg,15,~l,2L Whether total superior colliculi ablations will eliminate the capacity to localize in space both in the presence of the striate cortex or in its complete absence, is at present an empirical question answerable by further experimentation. It has recently been shown that monkeys with partial striate and collicular lesions resulting in overlapping scotomata could not make accurate saccades to points within the field defect 11. Since these animals could not even detect light flashes within the scotoma, it is possible that the residual vision was highly taxed by the stimuli used which were only 15 minutes of arc in visual angle and exposed for 200 msec. We have shownin the past tha t monkeys with total bilateral removal of striate cortex and superior colliculi not only can detect a luminous source given sufficient time, but can also master a discrimination based on differences in total luminous flux 17. They fail only when the targets are equated for this dimension is. This work was supported in part by N.I.M.H. G r a n t MH-02261. The skillful assistance of Jorge Balbastro, Victor Rodriguez and Minerva Travieso is gratefully acknowledged.
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Note added inproof. Since original submission of this paper in autumn 1977, the article by Weiskrantz et al. (Brain, 100 (1977) 655-670) has appeared in the literature, showing that one monkey with total removal of striate cortex succeeded in reaching accurately to the source of a 110 msec flash.