The effects of lesions of the superior colliculus on locomotor orientation and the orienting reflex in the rat

Brain Research, 88 (1975) 243-261 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands

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T H E EFFECTS OF LESIONS OF T H E SUPERIOR C O L L I C U L U S ON L O C O M O T O R O R I E N T A T I O N A N D T H E O R I E N T I N G R E F L E X IN T H E RAT

MELVYN A. GOODALE AND ROBERT C. C. MURISON* Psychological Laboratory, University of St. Andrews, St. Andrews, Fife (Great Britain)

(Accepted November 1lth, 1974)

SUMMARY The effects of bilateral removal of the superior colliculus or visual cortex on visually guided locomotor movements in rats performing a brightness discrimination task were investigated directly with the use of cine film. Rats with collicular lesions showed patterns of locomotion comparable to or more efficient than those of normal animals when approaching one of 5 small doors located at one end of a large open area. In contrast, animals with large but incomplete lesions of visual cortex were distinctly impaired in their visual control of approach responses to the same stimuli. On the other hand, rats with collicular damage showed no orienting reflex or evidence of distraction in the same task when novel visual or auditory stimuli were presented. However, both normal and visual-decorticate rats showed various components of the orienting reflex and disturbance in task performance when the same novel stimuli were presented. These results suggest that although the superior colliculus does not appear to be essential to the visual control of locomotor orientation, this midbrain structure might participate in the mediation of shifts in visual fixation and attention. Visual cortex, while contributing to visuospatial guidance of locomotor movements, might not play a significant role in the control and integration of the orienting reflex.

INTRODUCTION There is a long history of experimental work that has linked the mammalian superior colliculus with visuomotor behaviour as. However, investigations of visual * Present address: Psychology Department, University of Leicester, Leicester, Great Britain.

244 discrimination ability in animals with collicular lesions have produced contradictory findings in different species. While some investigators have reported acquisition or retention deficits in brightness and/or pattern discrimination tasks in animals with collicular damage a,4,6,11,12, a number of workers have found that collicular lesions had no effect or produced only slight impairments on similar discrimination tasks 1,13,16, 26,28,40. Despite the confused state of the empirical literature, Schneider 31-a3 has argued persuasively that the role of the superior colliculus within the mammalian visual system can be clearly differentiated from that of visual cortex. According to the 'two visual systems' hypothesis, the collicular system is directly involved in orientation behaviour, enabling the animal to localize a stimulus in visual space, whereas the geniculo-striate system participates in the identification of the visual stimulus. Support for the notion of collicular mediation of orientation behaviour is provided by Schneider's own observations that Syrian hamsters with undercut superior colliculi were unable to visually locate small food objects, such as sunflower seeds, presented by the experimenter in various parts of their visual fields. In addition, he reported that such animals could not guide themselves accurately towards visual stimuli in a two-choice discrimination apparatus even though they could discriminate the correct door from the incorrect one as indicated by their door-pushing behaviour. This latter observation, in particular, has been used by Schneider to argue that the apparent contradictions in the earlier literature can be resolved by examining the responsedemands of the visual discrimination tasks employed by different investigators. According to Schneider, discrimination tasks which require responses to be oriented towards the visual discriminanda will produce deficits in colliculectomized animals while tasks which do not require orientation will not. This interpretation has received support from the work of Barnes e t al. 2 who have shown that colliculectomized rats could not re-learn a brightness discrimination problem on a jumping stand, even though in other situations they performed quite well on brightness discriminations. Compelling as the 'two visual systems' hypothesis is, there are confusions over what precisely is meant by the term 'orientation'. In different contexts, Schneider uses this same term in reference to both (1) the head and eye movements and other postural changes constituting a shift in visual fixation towards a peripherally presented stimulus, and (2) the visually guided locomotor movements made towards visual stimuli in a discrimination task. While there is considerable evidence to suggest that the superior colliculus may be involved in shifts in visual fixationa°,89,42, the effect of coUicular lesions on visually guided locomotion has not been studied directly. Schneider's own conclusion about deficits in visually guided approach responses and those of Barnes e t al. 2 were for the most part inferred indirectly from errors to criterion on visual discrimination tasks. Therefore, the aim of the present investigation was to examine with the use of cine film, the effects of collicular lesions on both sorts of orientation behaviour. In the first experiment, the locomotor movements of colliculectomized rats performing a brightness discrimination were filmed and were compared with the

245 movements of normal and visual-decorticate rats in the same situation. In the second experiment, film records were made of shifts in visual fixation and other responses made by all 3 groups of rats to novel visual and auditory stimuli presented during the performance of the same discrimination task. Running times (latencies) on discrimination trials were also measured as an index of the amount of disruption produced in ongoing behaviour by the sudden introduction of a novel stimulus. METHODS

Apparatus The discrimination apparatus consisted of two large open boxes (hereafter referred to as box A and box B) each with a floor space of 91.4 cm × 91.4 cm with walls 42.5 cm high. Boxes A and B were interconnected by a short 10.2-cm tunnel centred in one wall of each box at floor level. The openings leading into the tunnel from each box measured 9 cm x 9 cm and a photoelectric beam intersected the tunnel halfway along its length. Five circular holes, 5.1 cm in diameter and 15.2 cm apart, were located in each box 6 mm above the floor in the wall opposite the tunnel opening. Behind each hole was a translucent white perspex door hinged at the top which, when pushed aside, gave access to a small feeding hole through which a condensed milk solution could be presented by means of a dipper mechanism (Campden Instruments, London). In addition, a 3.5-V light bulb which could be independently illuminated was located directly behind each door. Except for the doors themselves, the entire apparatus was painted matt grey. General illumination was provided by a 100-W light bulb mounted 1.5 m above the floor of the apparatus. External noises were masked with white noise emitted from an overhead loudspeaker. A Bolex 16-mm cine camera fitted with a wide angle lens and a remote control electric motor was centred 1.5 m above the floor of box B. The field of view of the camera included the entire floor of box B with the tunnel opening and 5 circular openings in the opposite wall clearly visible. The discrimination apparatus and camera were automatically controlled by electromechanical and solid state logic modules. Correct responses and errors were recorded on electromechanical counters.

Experiment 1 Locomotor orientation Pre-operative training. Nine male hooded rats weighing approximately 300 g at the beginning of the experiment were maintained on a 23-h food deprivation schedule. Each rat was first pre-trained in box A (with the tunnel entrance blocked) to push open one of the 5 doors that was illuminated. If the illuminated door was pushed open the dipper mechanism was activated allowing the rat access to the condensed milk solution for 2 sec. The light behind the door remained on during the 2-sec reinforcement period. At the end of the reinforcement period the light went out and there was a 10-see intertrial interval before another door was illuminated. The position of the illuminated

246 door was changed in a pseudo-random sequence. Pushing open a door that was not illuminated would not result in a reinforcement. After a rat had pushed open each door correctly at least 20 times, it was transferred to box B and was trained in a similar fashion to push open the 5 doors in that box. After each rat had responded correctly at least 20 times to each of the 5 doors in the second box, the block in front of the tunnel entrance was removed and training proper was started. During training the rat was placed initially in box A in which none of the 5 doors was illuminated. If the rat entered the inter-connecting tunnel and broke the photoelectric beam, the light behind one of the 5 doors in box B was illuminated. If the rat pushed open the illuminated door, the dipper presented the milk solution for 2 sec. At the end of the reinforcement period the light went out, and no light came on again until the rat entered the tunnel and broke the photoelectric beam in which case one of the 5 doors in box A was then illuminated. In this way, one of the 5 doors in either box A or B was illuminated in an alternating fashion, and to obtain reinforcement the rat was forced to run from one end of the apparatus to the other via the inter-connecting tunnel. The position of the illuminated door in both box A and B was varied according to a pseudo-random sequence. An error was defined as a response to a darkened door in that box in which one of the doors was illuminated. If the rat re-entered the box in which none of the doors was illuminated, no door-push errors were recorded. Each rat received 40 trials/day (20 in each box) for 10 days. After an animal was tested, both boxes were thoroughly cleaned with a 2 ~o acetic acid solution before another animal was placed in the apparatus. On day 10 the locomotor movements of each rat on the last 10 trials in box B were filmed at I0 frames/sec with the overhead cine camera. The camera was switched on as soon as the rat broke the photoelectric beam and continued to operate until the rat either pushed the correct door or until 7 sec had elapsed. I f 7 sec had not elapsed by the end of the 2-sec reinforcement period, the camera was again switched on until the 7 sec had run out or the rat had re-entered the tunnel. During the period of filming, each of the 5 doors in box B was illuminated twice. Surgery. After filming, the 9 rats were divided into 3 groups: 3 animals received bilateral lesions of the superior colliculus, 3 animals received bilateral ablations of visual cortex, and 3 control animals received sham operations. Surgery was performed under deep sodium pentobarbitone anaesthesia. Collicular lesions were made stereotaxically with an RF lesion-maker using an electrode tip exposure of 1 mm. With the inter-aural line and upper edge of the incisor bar in the same horizontal plane, the electrode placements were made 1.8 m m on each side of the midline, 2.9 m m anterior to the most posterior aspect of the lambdoidal suture, and 3.7 m m below the cortical surface. The RF current was applied for 90 sec with a tip temperature of 70 °C. The cortical ablations were made by aspirating tissue under direct visual guidance. An attempt was made to remove bilaterally all cortical tissue within area 17 as designated by Krieg 25. In the sham operations, the skin overlying the skull was incised and then the wound was simply closed with silk sutures.

247 The animals were given one week to recover with free access to food and water, before being re-introduced to the 23-h food deprivation schedule. Post-operative training. Two weeks after surgery, each animal was given 40 trials/ day in the discrimination apparatus for 8 consecutive days. On days 1, 4 and 8, the last 10 trials in box B were filmed in a manner identical to that used in pre-operative training.

Experiment 2 Distracting stimuli For this experiment, the apparatus was modified slightly. A loudspeaker and a 12-V lamp were mounted on top of each of the side walls of box B. The loudspeakers and the lamps were located in a plane mid-way between the tunnel opening and the 5 stimulus doors. Five days after experiment 1 was completed, each rat was given 30 trials/day (15 in each box) for 2 days in the modified apparatus. During the last 5 trials irt box B on the first day, one of the 12-V lamps was flashed at 2 flashes/sec for 5 sec, 400 msec after the rat had broken the photoelectric beam in the tunnel. The position of the flashing light alternated from trial to trial. On both days, a record was kept of the elapsed time between breaking the photoelectric beam and pushing the correct door on each of the 15 trials in box B. In addition, the cine camera was used to film each rat's behaviour on the 5 trials in which the flashing light was presented. On the following day, each rat was given a similar set of trials except that on the last 5 trials in box B, instead of a flashing light, a 5-sec burst of loud clicks was presented at the rate of 2 clicks/sec over one of the two loudspeakers. The loudspeaker used to present the clicks was alternated from trial to trial. Histology. At the end of this experiment, the 6 rats with brain lesions were killed with sodium pentobarbital and were perfused with 10~o formalin. Their brains were removed and fixed in 10 % formalin for 6 days and sucrose formalin for 4 days. Coronal sections were cut at 40/~m through the midbrain of the 3 rats with collicular lesions and through the lateral geniculate nuclei of the 3 rats with cortical lesions. Every fifth section was stained with cresyl fast violet. The extent of each collicular lesion was plotted on brain section diagrams taken from KSnig and Klippe124 and the extent of the damage to area 17 in each cortical lesion was estimated from the amount of retrograde degeneration in pars dorsalis of the lateral geniculate nucleus. RESULTS

Histology The superior colliculi in the animals with mid-brain lesions were almost completely destroyed except for a small amount of tissue in the intermediate and deeper layer of the rostro-medial portion of the colliculi in all 3 animals (Fig. 1). Within these areas of apparently intact tissue, there was extensive gliosis and neuronal degeneration. The lesions invaded the rostral edge of the inferior colliculus in two animals, and in all

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Fig. 1. Reconstructions of the collicular lesions. The extent of the lesion in each animal was plotted from histological material onto outlines taken from K6nig and Klippe124. The solid black areas represent complete tissue destruction. The surrounding stippled area indicates incomplete cellular necrosis and extensive gliosis. 3 animals there was minimal damage to the periaqueductal grey and subjacent tegmenturn. Gross inspection of the lesions in the 3 animals with cortical ablations indicated that although a large amount of neocortex had been aspirated, it was possible that some of area 17 could have been spared. This conclusion was confirmed by the amount of retrograde degeneration in the lateral geniculate nuclei. As Fig. 2 illustrates, degeneration in pars dorsalis was incomplete in all 3 animals with variable numbers of normal cells scattered throughout the dorso-lateral portion of the nuclei. In all 3 animals there was extensive bilateral damage to area 18a (as described by Krieg~5). While area 18 was also probably invaded in all the animals, only No. 98 appeared to have extensive damage medial to area 17. This animal also showed a slight amount of gliosis in the ventral nucleus of the thalamus on one side indicating that there was some invasion of somaesthetic cortex. In none of the animals did the lesions appear to extend into motor cortex.

Experiment 1 Brightness discrimination performance During pre-operative training all the animals learned the brightness discrimination very rapidly. The rapid acquisition was undoubtedly a direct result of pre-training

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Fig. 2. Reconstructions of the cortical lesions and the extent of retrograde degeneration in the lateral geniculate nuclei. The extent of the cortical lesion in each animal is indicated by the solid black area on the outline of the dorsal view of the brain. The amount of retrograde degeneration in pars dorsalis of the lateral geniculate nuclei in each animal is also shown as solid black areas.

with an illuminated door. After only 4 days of training, each of the 9 rats was pushing open the correct door first on at least 36 of the 40 daily trials. Thus, since they were given 10 days of training, each rat effectively received at least 240 'over-training' trials at a performance level of 90 % or better. As Fig. 3 shows, the percentage of correct trials for each group of 3 rats on the last day of pre-operative training was well above 90%. On the first test day following surgery, unlike the sham-operated rats, the 3 animals with cortical ablations and the 3 with collicular lesions showed a marked impairment in their performance of the discrimination task (Fig. 3). Although both groups improved rapidly over the next 7 days of training, the performance of the 3 colliculectomized rats improved significantly faster than that of the animals with cortical ablations (P < 0.01). As Fig. 3 shows, by day 7 all 3 groups of rats were scoring 90 % or better. Locomotor orientation The films made of the pre- and post-operative locomotor behaviour of the 3 different groups of animals were examined frame by frame on a microfilm reader. The routes that each animal followed from the tunnel opening to one of the 5 doors in box B were plotted using the tip of the animal's nose as a reference point. The lengths of the paths were measured and transformed to a common relative scale to compensate

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Fig. 3. P~t-operative retention on the brightness discrimination task averaged over the 3 animals in each group. The mean percentage of correct trials is plotted for each post-operative test day. The performance of the normal animals is shown by solid lines and open squares. The performances of the visual-dccortieateand the collieulectomizedanimals are shown as dotted lines with closed circles and dashed lines with open circlesrespectively.Performance of each group on the last day of prc-opcrative training is shown on the left-hand side of the graph.

for small differences in the absolute distance between the tunnel opening and each of the 5 doors. Analysis of the pre-operative film records revealed that there were no significant differences in the length of the routes followed by the 3 groups of rats and that all 9 animals showed good evidence of visual guidance by running almost directly from the tunnel exit to the correct door. The post-operative film records also indicated that all 3 groups of rats were capable of visually guided locomotor movements in this situation. None of the animals moved aimlessly around the apparatus or regularly followed the walls of the box in order to find the correct door, However, when the length of the paths followed on correct trials was measured for each rat on post-operative days 1, 4 and 8, and was compared with the length of the paths that same animal followed pre-operatively, it was found that the 3 visual-decorticate rats showed a significant post-operative increase in the length of the path they took from the tunnel to the correct door. In contrast, after surgery, the rats with collicular lesions were more efficient, and followed paths that were 5-10% shorter than those they had taken on the last day of preoperative training. Although this improvement might seem quite small, in fact, the pathlengths of the colliculectomized group were approaching the minimum distance between the tunnel opening and the correct doors. The post-operative changes in

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Fig. 4. The post-operative changes in pathlength on correct trials for each group on test days 1, 4, and 8. The change in pathlength for each animal is plotted as a ratio: E-M/O--M, where E = average length of the path from the tunnel opening to the correct door on the last day of pre-operative testing, O = average length of the path on correct trials on each post-operative test day, and M = length of a straight line (i.e. the theoretical minimum pathlength) between the tunnel opening and the correct door. (In all cases the pathlengths were transformed to a common relative scale.) A ratio of I indicates no change; a ratio greater than 1, a decrease in pathlength; and a ratio less than 1, an increase in pathlength. The ratios for individual animals on each test day are shown thus: normal animals, open squares; visual-decorticate animals, solid circles; and colliculectomized animals, open circles. The mean ratios for each group on each test day are joined by straight lines; the normal group is represented by a solid line, the visual-decorticate group by a dotted line, and the colliculectomized group by a dashed line.

p a t h l e n g t h in b o t h these g r o u p s were significantly greater t h a n the small changes in the length o f the p a t h s followed b y the 3 animals t h a t received s h a m - o p e r a t i o n s (P < 0.05). M o r e o v e r , as Fig. 4 shows, these differences were a p p a r e n t on d a y 1 o f p o s t - o p e r a t i v e testing a n d persisted t h r o u g h o u t the testing period. A l t h o u g h the differences in the efficiency o f the 3 g r o u p s are s u m m a r i z e d in Fig. 4, these differences are also clearly visible in Fig. 5 which illustrates the routes followed b y each g r o u p on every correct trial filmed d u r i n g p o s t - o p e r a t i v e testing. A t the e n d o f some trials, the r e t u r n runs f r o m the stimulus d o o r s to the tunnel were filmed. A l t h o u g h the n u m b e r o f c o m p l e t e runs t h a t were filmed was very small,

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Fig. 5. The paths followed on all the correct trials filmed during post-operative testing. The tunnel opening is indicated by the large opening at the top of each outline of the floor of box B; the correct door by the smaller opening at the bottom of each outlined square. The paths of the visual.decorticate group towards each of the 5 doors are shown in the left-hand column; those of the group of normal animals in the centre column; and those of the colliculectomized group in the right-hand column. The points on an individual path represent the tip of an animal's nose plotted on successive frames of film separated by 0.1 sec.

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it was clear that all 3 groups showed evidence of visually guided locomotion. However, the available data again suggest that the visual-decorticate rats did not run as directly towards the tunnel openings as did the colliculectomized and normal animals. The paths followed by different animals on incorrect trials were difficult to compare meaningfully since almost no errors had been recorded on film for any of the groups pre-operatively. In post-operative testing, only the visual decorticate animal made many errors after day 1. Certainly there were no large differences on day 1 between the paths followed by colliculectomized and decorticate rats on error trials, and animals in both groups ran from the tunnel opening in the direction of the stimulus doors. However, the darkened doors pushed by the colliculectomized animals on error trials were on average significantly closer (P < 0.05) to the correct illuminated door than were those pushed by the visual-decorticate rats. Informal observations of the animals' behaviour during a few trials in which no filming took place suggested that the experimenter's presence in the test room often disturbed or distracted the normal and visual-decorticate rats, but never the animals with collicular lesions. This observation was tested formally in experiment 2.

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Fig. 7. The mean running times (latencies) for each group in experiment 2. On each test day the novel stimulus was first presented on trial 11. The latencies of the normal group are represented by open squares joined by solid lines; those of the visual-decorticate group by solid circles joined by dotted lines; and those of the colliculectomized group by open circles joined by dashed lines.

Experiment 2 The films of each animal's behaviour on those trials in which a flashing light or train of clicks had been presented as a distracting stimulus were examined frame by frame on the microfilm reader. The paths were plotted and measured, and the responses to the novel stimuli were recorded. These records, some of which are reproduced in Fig. 6, clearly show that both normal rats and rats with lesions of visual cortex exhibited pronounced head-raising, turning, rearing, approach responses, and freezing responses to both visual and auditory novel stimuli. Although these responses were shown throughout all 5 trials on both test days, the responses were more vigorous and persistent on the first presentation of the novel stimulus on both days than they were on later trials: One of the normal animals, No. 86, was so disturbed by the introduction of the flashing light that it immediately ran back into the tunnel, and it could not be induced to re-enter box B on this or the next test day. During the trials on which loud clicks were used as novel stimuli, the normal and visual-decorticate animals commonly froze immediately after leaving the tunnel and remained in that position for several seconds after the 5-sec train of clicks had terminated. However, when the flashing light was presented, rearing and approach responses were often observed. In contrast to the behaviour of normal and visual-decorticate rats, the animals with collicular lesions showed no responses at all to either the novel visual or auditory stimulus. As Fig. 6 shows, the colliculectomized rats ran directly from the tunnel

255 opening to the correct door without showing any of the responses to the novel stimulus that were observed in the other two groups of animals. The failure of the flashing light or the train of loud clicks to disturb the performance of the animals with collicular lesions can also be seen in Fig. 7, which shows the mean running time (latency) in box B for each group on each of the 15 trials on both test days. While both the normal and visual-decorticate animals showed a massive increase in latency on the 5 trials in which novel stimuli were presented, the colliculectomized rats showed no change whatsoever. Excluding the results of No. 86 which did not complete the testing session, the difference between the test trial latencies of the normal and visual-decorticate groups was not significant on either test day. However, the test trial latencies of both groups on both days were significantly different (P < 0.001) from the latencies of the animals with collicular lesions. It is also apparent in Fig. 7 that the latencies of the normal and visual-decorticate rats on the initial trials in the apparatus when no distracting stimuli were presented were much longer than those of the colliculectomized animals. This difference was much more apparent on the second day of testing after the animals had already experienced the presentation of a novel stimulus the day before. DISCUSSION

The results of experiment 1 clearly indicate that rats with complete bilateral lesions of the superior colliculus show excellent visual control of their locomotor movements in a brightness discrimination task. The routes followed by rats with collieular lesions when approaching correct stimuli or initiating a new trial were comparable to, and often more efficient, than those of normal animals. None of the 'peculiar path habits' described by Schneiders2 in his hamsters with undercut superior colliculi were observed in any of the colliculectomized rats. Although the apparent discrepancy in the results of the two experiments could be due to species differences or differences in the discrimination apparatus and surgical techniques, it is interesting to note that of the 4 hamsters with damaged superior colliculi in Schneider's experiment, only one of them (M-7) failed to learn to approach the correct door under visual control and that was only during a horizontal-vertical discriminational,SL Yet this same animal had made only slightly more 'approach errors' than normal animals on an earlier black-white discrimination problem. Thus, the deficit in visual control of approach responses in the hamsters was not absolute and indeed, at least in one animal, appeared to be stimulus-dependent. Even normal hamsters make many approach errors in apparatus of only slightly different designa3, and similar sorts of approach errors have been observed in normal rats in a comparable two-choice discrimination apparatus (Goodale and Milner, unpublished observations). The work of Barnes e t al. z who investigated the behaviour of rats with collicular lesions in a brightness discrimination problem is also difficult to evaluate. The rats in their experiment were required to jump from a central platform through the aperture of one of 6 boxes for food reinforcement. The correct box was dark and the 5 incorrect boxes were illuminated. The rats were given only 30 post-operative training trials on

256 the jumping stand in contrast to the 320 trials each animal received in the present investigation. Although the rats had not re-learned the brightness discrimination within these 30 trials, they nevertheless jumped accurately towards the apertures of the boxes and never hit the partition between adjacent apertures. When it was made possible for the rats to walk towards the boxes from the central platform, the animals with collicular lesions did re-learn the problem. Barnes e t al. 2 interpreted these results as evidence for a deficit in 'orientation' to brightness cues as distinct from a deficit in orientation to visual forms. However, the poor performance of their rats may have been due to factors other than difficulties in orientation. In experiment 1 of the present investigation, even though the rats with collicular damage made many errors in the first 40 post-operative trials on the brightness discrimination, they showed rapid improvement over the next few days of testing, and throughout all their post-operative training the visual control of their approach responses to the correct door was comparable to or superior to that of normal animals. The transient deficit in discrimination performance observed in the initial post-operative trials is difficult to interpret, but it does not seem to be due to any disturbance in visuospatial control of locomotion. Although the collicular lesions in the 3 animals in the present experiment were very large, it might possibly be argued that some small remnant of coilicular tissue was mediating the visual control of locomotion that was observed. This explanation is unlikely since if the superior colliculus were directly involved in visual guidance of locomotor movements, some initial post-operative deficit would be expected with such large lesions, even if the animals eventually did manage to utilize the small remnants of collicular tissue that remained. No such deficit was observed. Moreover, in recent unpublished experiments, rats with even larger midbrain lesions that included the superior colliculus and extended slightly into the pretectum were nevertheless capable of good visual control of ambulation. Unfortunately, there has been little direct investigation of the effect of lesions of the superior colliculus on locomotor orientation in any other species. However, the visual control of the limb movements of reaching has received some attention, and the published observations are consistent with the results of the present investigation. Sprague and his co-workers a7 have reported that cats with large bilateral collicular lesions can localize objects in visual space rather well if judged by accuracy of reaching. In the macaque, Schiller and Koerner 3° have found that although ablation of the superior colliculus results in a persistent inability to locate visual targets accurately by saccadic eye movements, the animals can learn to turn their heads towards and reach for objects accurately. In contrast to the colliculectomized rats, the animals which had received cortical lesions in the present investigation did show a significant deficit in visually guided locomotor movements. The length of the paths each of these animals followed from the tunnel exit to the correct doors in experiment 1 increased after aspiration of most of the tissue in area 17, with some damage to neighbouring visual areas 18 and 18a. It might be argued that these longer paths were a result of an increase in distractibility similar to that reported in the tree shrew ~a following lesions of area 17. However, this

257 suggestion is not supported by the results of experiment 2 in which the 3 animals with cortical lesions seemed to be no more disturbed by the introduction of novel visual or auditory stimuli than were the normal rats. The observed increase in path length in the present experiment is not inconsistent with the observations of a number of investigators who have described deficits in visually guided responses following geniculostriate lesions. Avoiding unexpected obstacles while walking and visually guided placing are severely impaired following ablation of area 17 in the macaque, and areas 17, 18 and 19 in the cat, although with long post-operative survival some recovery does occur 8,1°,11,21,35,41. In a recent investigation using a task similar to that used in the present study, Marks and Jane 2v reported that both cats and squirrel monkeys were severely impaired in their visually guided locomotor movements following bilateral lesions in areas 17, 18 and 19. These authors22, ~v make an important distinction between static localization or'attention' and ambulatory localization which involves readjustment and coordination of the visual field with each movement toward the goal, and they suggest that the deficit in the visual-decorticate animal is one of ambulatory rather than static localization. However, in the present study, the rats with cortical lesions, although impaired, did show evidence of some visual control of locomotor behaviour. None of the 3 animals in this group wandered aimlessly about the apparatus, nor did they hug the walls when approaching the discriminanda as did the cats and squirrel monkeys in the experiments by Marks and Jane 27. The absence in the present experiment of the absolute deficit in ambulatory localization described by these authors could be due to the fact that the cortical lesions in the rats were much less extensive than those in the cats and squirrel monkeys. On the other hand, it might also mean that visual cortex, while making some contribution to visual control of locomotion in the normal rat, is not essential for the performance of such behaviour. Despite their deficit in locomotor orientation, in experiment 2 the 3 animals with cortical lesions showed shifts in visual fixation, rearing, and freezing responses as often as normal animals when either novel auditory or visual stimuli were suddenly presented during the performance of the discrimination task. Shifts in fixation and other gross behavioural components of the 'orienting reflexTM have also been reported as surviving large and often total ablations of area 17 in the macaque 20,21, the cata6, and the hamster31-33. Unlike the rats with cortical lesions, the 3 colliculectomized animals did not respond at all to the presentation of novel stimuli. In these animals, the flashing light and the train of loud clicks evoked none of the components of the orienting reflex or freezing responses that had been observed in the other two groups. Moreover, the failure to turn towards and visually fixate a novel stimulus in the periphery was not simply a result of a deficit in the control and integration of the constituent responses, since there was no discernible disturbance of any kind in on-going behaviour on any of the discrimination trials in which a distracting stimulus was introduced. If the failure to orient were simply a result of visuomotor impairments, some other disturbance in on-going behaviour such as freezing, or at least a modification of their running hehaviour, would be expected to occur. In short, the rats with collicular lesions did not

258 appear to attend to the new stimulus. This lack of distractibility might help to account for the puzzling observation in experiment 1 that the colliculectomized animals followed paths that were shorter and more efficient than those they had taken pre-operatively. It might also explain why this group showed running times that were much shorter than those of the other two groups on the initial trials of experiment 2. A similar lack of attention to novel stimuli was observed in an earlier study 1'~,, in which rats with sub-total collicular lesions showed less response suppression than normal animals on an appetitive bar-pressing task when a novel visual, auditory, or tactile stimulus was suddenly presented. These observations are consistent with reports from a number of investigators who have described deficits in attention in animals with lesions of the superior colliculus or pretectum 1,6,7,39 although most of these accounts are based on gross observations of the general neurological status of such animals. On the whole, the results of the earlier work together with the findings of the present study suggest that the attentional deficit in the colliculectomized animal is not one of failing to maintain attention to a particular set of stimuli, but one of failing to shift attention to a new stimulus. Thus, while the superior colliculus might participate in the initiation, control and integration of the responses constituting a shift in visual fixation towards a peripheral stimulus, it might at the same time mediate a shift in the animal's attention to this new stimulus. However, it is not yet clear whether there are any circumstances in which stimuli of the sort used in experiment 2 could control the behaviour of rats with collicular lesions, or whether such rats would be disturbed by similar novel stimuli introduced into the immediate vicinity of the visual stimuli controlling their on-going behaviour. The failure to shift attention to new stimuli following collicular damage in the rat may be similar to the deficit described by Killackey e t al. 23 in tree shrews with extrastriate visual cortical lesions. Their animals found it difficult to perform discrimination tasks in which they were required to shift attention from a previously rewarded stimulus dimension to a different dimension in order to obtain reinforcement. The extrastriate visual cortex of the tree shrew does receive a significant input from the superior colliculus via the lateral posterior nucleus of the thalamus 9, and the observed deficits in their animals 23 could be interpreted as a disruption of the cortical elaboration and integration of this input. The effect of comparable cortical lesions in the rat on attentional shifts is unknown. Several investigators have implicated notions of attention in attempting to account for the results of electrophysiological recordings from single neurones in the colliculus. Horn and Hill is have recorded the activity of single cells in the rabbit superior colliculus which are responsive to stimuli in 2 or 3 sensory modalities. Moreover, many of these multimodal units show rapid habituation to the repeated presentation of a particular stimulus, even though they remain very responsive to a novel stimulus. On the basis of these and similar findings Horn 17 and Humphrey 19,~° have suggested that the superior colliculus might be involved in switching attention to novel stimuli; that is, stimuli of potential ecological importance to the animal. More recently, Camarda et al. 5 have reported that the response of single units in the superior colliculus of the cat to a moving slit of light are strongly inhibited

259 when a second moving stimulus is introduced far outside the excitatory part of the unit receptive field. Camarda and his colleagues have interpreted these findings as evidence for the possible participation of the superior colliculus in selective attention to visual stimuli. Using alert monkeys, Goldberg and Wurtz 14 have demonstrated that the activity of a single cell in the superior colliculus will often show an enhanced response to a receptive field stimulus immediately before the animal makes a saccade to that stimulus. Furthermore, the observed enhancement is not always followed by an eye movement although habituation of the enhanced response does occur during the period when the animal has ceased to use the stimulus as the target of a saccade. Goldberg and Wurtz have suggested that the response enhancement is a reflection of the neural processes underlying shifts in selective attention which are to some extent independent of the neural control of eye movements. The results of the present study are in good agreement with the electrophysiological data. Rats with complete lesions of the superior colliculus did not shift fixation towards novel visual and auditory stimuli to which normal and visual-decorticate rats showed brisk and strong responses. Furthermore, they did not appear to shift their attention to these stimuli but continued their on-going behaviour without disturbance. Paradoxically, these same animals showed excellent visuospatial control of their running behaviour in a situation in which rats with lesions in visual cortex were distinctly impaired. This double dissociation of deficits suggests that while the superior colliculus may be important in the mediation of the orienting reflex in the rat, it is not essential to visuospatial orientation of locomotion. Visual cortex, on the other hand, appears to participate in locomotor orientation, but may not be a significant part of the neural system controlling the orienting reflex. ACKNOWLEDGEMENTS

The authors would like to thank David Milner, Frank Quinault, and Brian Rogers for their helpful suggestions during the preparation of the manuscript, and Christopher Barman for his technical assistance in carrying out the experiments.

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