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Head-dipping by rats with lesions of superior colliculus during extended testing in hole-board
Behavioural Brain Research, 8 (1983) 309-316
309
Elsevier Biomedical Press
H E A D - D I P P I N G BY RATS WITH LESIONS OF SUPERIOR COLLICULUS D U R I N G E X T E N D E D T E S T I N G IN HOLE-BOARD
PAUL DEAN and PETER R E D G R A V E
Department of Psvchology, University of Sheffield, Sheffield, SIO 2TN (U.K.) (Received October 25th, 1982) (Accepted January 4th, 1983)
Key words." superior colliculus - hole-board - exploration - novelty - rats
SUMMARY
It has previously been shown that rats with large lesions of the superior colliculus fail to head-dip during a 5 min hole-board test. To investigate whether this was a permanent deficit in exploratory behaviour arising from inability to produce the appropriate responses, collicular rats were tested in a hole-board for 60 min or more. The period before their first head-dip (mean 27 min 40 sec) was much longer than for unoperated animals (mean 22 sec), but subsequently the collicular rats showed a pattern of head-dipping that was similar (although not identical) to that of the control rats. It appears that rats with lesions of the superior colliculus are not permanently prevented from exploring the hole-board by inability to produce the required response, but rather that they may have difficulty in discovering certain features of novel environments.
INTRODUCTION
When tested for a brief period in the open-field, rats with large lesions of the superior colliculus rear, sniff and raise their heads less than normal animals [ 13, 19, 22, 24]. These observations suggest that the superior colliculus might be important for the production of exploratory responses. Support for this suggestion was provided by an experiment that investigated the effect of lesions of the superior colliculus on head-dipping in the hole-board. The hole-board is essentially an open-field with holes in the floor beneath which small objects can be placed. Normal rats investigate these holes by dipping their heads down then, a conspi0166-4328/83/0000-0000/$03.00 © 1983 Elsevier Science Publishers
310 cuous response whose frequency, duration and target can easily be measured (e.g. ref. 11). During a 5 min test, rats with control lesions spent on average 26 sec head-dipping, whereas 14 of 15 rats with large lesions of the superior colliculus failed to head-dip at all [7]. This is a particularly clear example of a collicular deficit in the exploration of a novel environment, and raises the question of which aspect of exploratory behaviour is affected. One suggestion is that rats with collicular lesions have difficulty in actually producing certain kinds of investigatory response [7]. This suggestion was prompted by the finding that rats or hamsters with lesions of the superior colliculus make many fewer head-scanning movements than normal animals in a variety of visual learning tasks, even when tested in highly familiar environments several months after operation [4, 5, 12, 20]. If this explanation were correct, then it might be expected that collicular animals would fail to head-dip even if left in the hole-board for extended periods; or, if head-dipping did occur, it would be grossly abnormal. We therefore observed the behaviour of rats with lesions of the superior colliculus and control rats in the hole-board for 60 min or longer. MATERIALS AND M E T H O D S
The animals used were 14 male hooded Lister rats (weight about 300 g) that had not taken part in any previous experiment. Seven of the rats were given one-stage bilateral electrolytic lesions of the superior colliculus. They were anaesthetized with 10 ml/kg of 4~o chloral hydrate, and an 00-gauge stainless steel anode, insulated apart from the cross sectional area of its tip, was placed with its tip at the stereotaxic coordinates 5 mm posterior to bregrna, 4.25 mm deep to the cortical surface, and 1.5 mm on either side of the midline (incisor bar 5 mm above the ear bars). The lesions were made by a current that was raised from 0 to 3 mA over 10 sec, maintained at 3 mA for 20 sec, then reduced to 0 over 5 sec. At least 2 weeks after surgery, the rats were tested in a hole-board adapted from File and Wardill [11 ]. Walls 45 cm high surrounded a raised square floor (60 cm side), which was marked by a grid of lines into 36 squares. There were 4 holes in the floor, 3.8 cm in diameter and 15 cm from each corner. Objects that had previously been shown to elicit investigation from normal rats (e.g. balls of silver paper on a watch glass) were placed 2-4 cm beneath each hole. Lighting was provided by a 150 W bulb in a metal reflector mounted about 1 m above the holeboard floor. The animals' behaviour was filmed with an overhead mounted video camera and recorded on video tape. Each animal was tested for 1 h in the hole board. Two animals, one from each group, were tested per day, always between 12.00 h and 16.30 h. Order of testing was counterbalanced over days. No observer was present in the experimental room during the test period. The videotapes were analyzed for (a) the duration
311 and location of each head-dip, and (b) locomotor activity (the number of squares crossed), during successive 10 min periods. One collicular animal failed to headdip during the hour, and was therefore given a second hour's test in the holeboard, 16 days after the first. After further behavioural testing, reported elsewhere [6], the animals with lesions were anaesthetized with chloroform then killed by cervical dislocation. Their brains were removed and frozen at -18 ° C. Coronal sections (24 or 48 #m) were cut in a cryostat, and stained with either iron hematoxylin or cresyl fast violet. Each animal's lesion was reconstructed onto diagrams taken from the stereotaxic atlas of K0nig and Klippel [ 17]. RESULTS One collicular rat was found to have a massive diencephalic tumour: therefore, behavioural data for only the 6 remaining rats with lesions are presented below. Reconstruction of a representative collicular lesion is shown in Fig. 1A. In all 6 animals the superior colliculus was extensively damaged but not completely destroyed. Spared tissue was found in the caudal one-third of the colliculus (5 animals) or rostral sections near the boundary with the pretectum (4 animals). In every case the lesions invaded overlying cerebral cortex and, much less estensively, dorsal central grey. They probably also invaded the mesencephalic reticular formation underlying the superior colliculus, although because of the indistinctness of the boundary between the two structures (cf. ref. 10) it was difficult to be certain. Comparison of the behaviour of the two groups obtained by analysis of the video tapes revealed the following four points. (i) The rats with lesions of the superior colliculus did eventually head-dip, but took much longer to start than the control animals (latency to first head-dip, SC group mean 1660 sec, range 384-4625 sec; N group mean 22 sec, range 9- 3 6 sec; Mann-Whitney U-test, nl = 6, n2 = 7, U = 0, P -- 0.002, two-tailed P values given throughout). (ii) Once the rats with lesions of the superior colliculus had started to head-dip, their subsequent head-dipping was not significantly different from that of the normal animals on a number of measures. For example, the time spent in head-dipping differed between the two groups only for the first two 10 min periods (Fig. lb: 0-10 rain, U = 1, P = 0.002; 10-20 min, U = 3, P = 0.008; for other periods, P > 0.3). Analysis of each animal's head-dips in the 30 min beginning at the start of its first head-dip showed no significant difference between the groups in total number (U = 11, P -- 0.18), total duration (U = 17, P = 0.63), or mean duration (U = 14, P -- 0.37). (iii) There were nonetheless some minor abnormalities in the head-dipping of the collicular rats during this period (30 min starting at first head-dip). It was
312 B 60. OU~P •SC
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~ 20 10 10
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"~ 300 o 200
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Time ( ~ n ) Fig. 1. A: reconstruction of representative lesion of superior colliculus onto coronal sections redrawn from atlas of KOnig and Klippel [ 16]. B: head-dipping (time dipped in a 10 min period) plotted against time in hole-board. Group median scores are shown. One animal with a lesion of the superior colliculus failed to head-dip during the 60 min period shown on the graph (see text). C: locomotor activity (squares crossed in a 10 min period) plotted against time in hole-board. Group median scores are shown.
observed that normal animals either put their heads deep into the hole (up to their ears), or more shallowly, up to about the level of the eyes. The collicular animals had a much higher proportion of shallow head-dips (SC group, mean proportion of shallow dip s 0.71, range 0.51-0.94; N group, mean proportion of shallow dips 0.38, range 0.23-0.52; U = 1, P = 0.002), and made significantly fewer deep dips (SC group, mean number of deep dips 12.5, range 1-25; N group, mean number of deep dips 34.4, range10-58 : U = 2, P = 0.004). Also, for the normal group, the mean duration of head-dips (both kinds taken together) clustered closely round the mean of 2.23 sec (range 1.89-2.63 sec). The mean durations of the collicular group were in every case outside this range: two collicular rats had shorter durations, 1.07 and 1.55 sec, whereas the other 4 collicular rats had longer
313 durations, range 2.96-12.9 sec. Finally, there was a tendency for the rats with lesions of the superior colliculus to explore less efficiently, in the sense of making more head-dips in the first three holes sampled before making the first head-dip in the fourth. Three of the collicular rats made more of these dips than any normal animal, and two of the three in fact failed to find the fourth hole in the time available. However, the difference between the groups as a whole fell short of significance because of the much better performance of the other three rats with collicular lesions (U = 9, P = 0.102). (iv) The rats with collicular lesions had significantly higher locomotor activity scores than the control animals during the first three 10 min periods (Fig. 1C: 0-10 min, U = 0, P = 0.002; 10-20 min, U = 0, P = 0.002; 20-30 min, U = 2, P = 0.004), but not subsequently. During the first 10 min in particular their behaviour was as described previously [7]: they spent much of their time running around the walls of the hole-board, rarely rearing, grooming or freezing. Examination of individual cases, however, did not suggest any simple relationship between the increased locomotor activity and the failure to head-dip. For example, the animal with a lesion of the superior colliculus that was most active (535 squares in the first 10 rain) had the shortest latency to head-dip (384 sec), whereas the collicular rat that took longest to head-dip (4625 sec) covered only 12 squares during the last 30 min of its test session. In fact the correlation between activity during the first 10 min and latency to head-dip was negative, though not significantly so (Spearman's rank r = -0.6, n = 6, P > 0.05). The results of the present experiment thus replicate those obtained previously [7], and in addition show that rats with lesions of the superior colliculus do head-dip if left in the hole-board long enough. The suggestion that their initial failure to head-dip can be ascribed to an inability to produce the required exploratory response [7] is therefore incorrect. DISCUSSION
What is required is an explanation of why the rats with lesions of the superior colliculus took much longer than normal to begin head-dipping. One possibility is that they discovered the holes as soon as normal animals, but their locomotor hyperactivity, which other experiments suggest only occurs in novel environments [4, 13, 24], competed with and prevented exploratory head-dipping. This possibility is consistent with ~the observations that collicular rats show normal amounts of activity [1, 6, 21 ] and of sniffing, head-raising and rearing (Goodale and Carson, unpublished, cited in ref. 13) in their home cages. However, there are a number of findings that indicate that the locomotor hyperactivity and lack of exploratory responding are at least partly independent. (i) In the present experiment the predicted relationship between amount of hyperactivity and latency to head-dip was not obtained. (ii) Small injections of kainic acid within the superior
314 colliculus can increase locomotor activity without affecting head-dipping [9]. (iii) Damage confined to the superficial and intermediate layers of the colliculus does not increase activity, but does reduce the frequency of some exploratory responses [ 19]. (iv) Microinjection of the GABA agonist muscimol, or the local anaesthetic procaine, within the superior colliculus reduce both exploratory responding and locomotor activity [2, 8]. An alternative explanation is that the animals with collicular lesions actually took longer to discover that holes were present in the apparatus. This could have occurred because of, for example, (a) a sensory deficit, (b) an attentional deficit made apparent in a situation containing many novel cues in a variety of modalities, or (c) a subtle motor impairment, for example of vibrissa movement, that was undetectable with the quality of recording available in the present study. Further experiments are required to distinguish between these possibilities, and to establish how coUicular 'neglect' of a static feature of the environment is related to the neglect of briefly presented stimuli known to occur in rats with collicular lesions [14, 16, 18]. The greatly extended latencies of the collicular rats to begin exploration of the holes contrasted strongly with their subsequent almost normal pattern of investigation. However, this relative normality may reflect only that exploring 4 holes is a simple task. In similar situations involving systematic search for food at 8 or more locations, collicular lesions can produce clear deficits in search efficiency [3, 4, 15 ], and preliminary results with a 16-hole apparatus suggest that similar deficits may be found in the hole-board. How far these collicular impairments in exploration of discovered features can be attributed to problems in response-production remains to be determined. Finally, the present experiment was concerned with the nature of the behavioural changes that follow large collicular lesions, rather than with the precise anatomical substrates underlying those changes. Other evidence suggests that disruption of exploratory behaviour in highly novel environments can be caused by damage either to the superficial layers of the superior colliculus, or to the deep layers, or to the mesencephalic reticular formation underlying the colliculus (e.g. refs. 8, 13, 19, 23). How these different areas cooperate in producing normal exploration is not known. However, it is clear from the results described here that the superior colliculus can be important for normal exploration without being necessary for the production of a particular exploratory response. ACKNOWLEDGEMENTS
This work was supported by S.R.C. grant GR/B/24707. We thank Iona Hodges for help with histology, and Catherine Quail for testing the animals.
315 REFERENCES 1 Altman, J., Diurnal activity rhythm of rats with lesions of superior colliculus and visual cortex, Amer J. Physiol., 202 (1962) 1205-1207. 2 Collingridge, G.L., Kilpatrick, I.C. and Starr, M.S., Pharmacological manipulations of tectal GAB A systems affect posture and locomotion in the rat, Brit. J. Pharmacol., 73 (1981) 271P. 3 Collins, M.J., Role of Frontal Eye-Fields and Superior Colliculi in the Visual Behaviour of Rats and Monkeys, Unpublished Thesis, University of Oxford, 1977. 4 Dean, P. and Key, C., Spatial deficits on radial maze after large tectal lesions in rats: possible role of impaired scanning, Behav. Neural Biol., 32 (1981) 170-190. 5 Dean, P. and Pope, S.G., Visual discriminationlearning in rats with lesions of superior colliculus: door-push and approach errors in modified jumping stand, Quart. J. exp. Psvchol., 338 (1981) 141-157. 6 Dean, P., Pope, S.G. and Redgrave, P., Influence of novelty on locomotor hyperactivity after lesions of superior colliculus in rats, Behav. Bra#~ Res., 5 (1982) 213-218. 7 Dean, P., Pope, S.G., Redgrave, P. and Donohoe, T.P., Superior colliculus lesions in rat abolish exploratory head-dipping in hole-board test, Brain Res., 197 (1980) 571-576. 8 Dean, P., Redgrave, P. and Lewis, G., Locomotor activity of rats in open field after microinjection of procaine into superior colliculus or underlying reticular formation, Behav. Brain Res., 5(1982) 175 187. 9 Dean, P., Redgrave, P., Pope, S. and Donohoe, T., Behavioural effects of kainic acid microinjected into the superior colliculus of rats, Neurosci. Lett., Suppl. 3 (1979) $302. 10 Edwards, S.B., The deep cell layers of the superior colliculus: their reticular characteristics and structural organization. In J.A. Hobson and M.A.B. Brazier (Eds.), The Reticular Formation Revisited, Raven Press, New York, (1980), pp. 193-209. 11 File, S.E. and Wardill, A.G., Validity of head-dipping as a measure of exploration in a modified hole-board, Psychopharmacologia, 44 (1975) 53-59. 12 Finlay, B.L., Sengelaub, D.R., Berg, A.T. and Cairns, S.J., A neuroethological approach to hamster vision, Behav. Brain Res., 1 (1980) 479-496. 13 Foreman, N.P., Goodale, M.A. and Milner, A.D., Nature of postoperative hyperactivity following lesions of the superior colliculus in the rat, Physiol. Behav., 21 (1978) 157-160. 14 Goodale, M.A. and Murison, R.C.C., The effects of lesions of the superior colliculus on locomotor orientation and the orienting reflex in the rat, Brain Res., 88 (1975) 243-261. 15 Keselica, J.J. and Rosinski, R.R., Spatial perception in colliculectomized and normal golden hamsters (Mesocricetus auratus), Physiol. Psychol., 4 (1976) 511-514. 16 Kirvel, R.D., Sensorimotor responsiveness in rats with unilateral superior collicular and amygdaloid lesions, J. comp. physiol. Psychol., 89 (1975) 882-891. 17 K6nig, J.F.R. and Klippel, R.A., The Rat Brain. A Stereotaxic Atlas of the Forebrain and Lower Parts of the Brain Stem, Williams and Wilkins, Baltimore, MD, 1963, 162 pp. 18 Marshall, J.F., Comparison of the sensorimotor dysfunctions produced by damage to lateral hypothalamus or superior colliculus in the rat, Exp. Neurol., 58 (1978) 203-217. 19 Midgley, G.C., Prkachin, K.M. and Tees, R.C., Exploratory behavior of rats following visual cortical and subcortical lesions, Physiol. Psychol., 9 (1981) 152-156. 20 Mort, E., Cairns, S., Hersch, H. and Finlay, B., The role of the superior colliculus in visually guided locomotion and visual orienting in the hamster, Physiol. Psvchol., 8 (1980) 20-28. 21 Murison, R.C.C., The Effects of Lesions of the Superior Colliculus on Visually Guided Behaviour and General Activity in the Rat, Unpublished Thesis, University of Leicester, 1977. 22 Pope, S.G. and Dean, P., Hyperactivity, aphagia, and motor disturbance following lesions of superior colliculus and underlying tegmentum in rats, Behav. Neural Biol., 27 (1979) 433-453.
316 23
Pope, S.G., Dean, P. and Redgrave, P., Hyperactivity, aphagia and motor disturbance following restricted lesions of midbrain in rats, Behav. Neural Biol., 34 (1982) 63-74. 24 Smith, C.J. and Weldon, D.A., Hyperactivity and deficits in problem solving following superior colliculus lesions in the rat, Physiol. Behav., 16 (1976) 381-385.
309
Elsevier Biomedical Press
H E A D - D I P P I N G BY RATS WITH LESIONS OF SUPERIOR COLLICULUS D U R I N G E X T E N D E D T E S T I N G IN HOLE-BOARD
PAUL DEAN and PETER R E D G R A V E
Department of Psvchology, University of Sheffield, Sheffield, SIO 2TN (U.K.) (Received October 25th, 1982) (Accepted January 4th, 1983)
Key words." superior colliculus - hole-board - exploration - novelty - rats
SUMMARY
It has previously been shown that rats with large lesions of the superior colliculus fail to head-dip during a 5 min hole-board test. To investigate whether this was a permanent deficit in exploratory behaviour arising from inability to produce the appropriate responses, collicular rats were tested in a hole-board for 60 min or more. The period before their first head-dip (mean 27 min 40 sec) was much longer than for unoperated animals (mean 22 sec), but subsequently the collicular rats showed a pattern of head-dipping that was similar (although not identical) to that of the control rats. It appears that rats with lesions of the superior colliculus are not permanently prevented from exploring the hole-board by inability to produce the required response, but rather that they may have difficulty in discovering certain features of novel environments.
INTRODUCTION
When tested for a brief period in the open-field, rats with large lesions of the superior colliculus rear, sniff and raise their heads less than normal animals [ 13, 19, 22, 24]. These observations suggest that the superior colliculus might be important for the production of exploratory responses. Support for this suggestion was provided by an experiment that investigated the effect of lesions of the superior colliculus on head-dipping in the hole-board. The hole-board is essentially an open-field with holes in the floor beneath which small objects can be placed. Normal rats investigate these holes by dipping their heads down then, a conspi0166-4328/83/0000-0000/$03.00 © 1983 Elsevier Science Publishers
310 cuous response whose frequency, duration and target can easily be measured (e.g. ref. 11). During a 5 min test, rats with control lesions spent on average 26 sec head-dipping, whereas 14 of 15 rats with large lesions of the superior colliculus failed to head-dip at all [7]. This is a particularly clear example of a collicular deficit in the exploration of a novel environment, and raises the question of which aspect of exploratory behaviour is affected. One suggestion is that rats with collicular lesions have difficulty in actually producing certain kinds of investigatory response [7]. This suggestion was prompted by the finding that rats or hamsters with lesions of the superior colliculus make many fewer head-scanning movements than normal animals in a variety of visual learning tasks, even when tested in highly familiar environments several months after operation [4, 5, 12, 20]. If this explanation were correct, then it might be expected that collicular animals would fail to head-dip even if left in the hole-board for extended periods; or, if head-dipping did occur, it would be grossly abnormal. We therefore observed the behaviour of rats with lesions of the superior colliculus and control rats in the hole-board for 60 min or longer. MATERIALS AND M E T H O D S
The animals used were 14 male hooded Lister rats (weight about 300 g) that had not taken part in any previous experiment. Seven of the rats were given one-stage bilateral electrolytic lesions of the superior colliculus. They were anaesthetized with 10 ml/kg of 4~o chloral hydrate, and an 00-gauge stainless steel anode, insulated apart from the cross sectional area of its tip, was placed with its tip at the stereotaxic coordinates 5 mm posterior to bregrna, 4.25 mm deep to the cortical surface, and 1.5 mm on either side of the midline (incisor bar 5 mm above the ear bars). The lesions were made by a current that was raised from 0 to 3 mA over 10 sec, maintained at 3 mA for 20 sec, then reduced to 0 over 5 sec. At least 2 weeks after surgery, the rats were tested in a hole-board adapted from File and Wardill [11 ]. Walls 45 cm high surrounded a raised square floor (60 cm side), which was marked by a grid of lines into 36 squares. There were 4 holes in the floor, 3.8 cm in diameter and 15 cm from each corner. Objects that had previously been shown to elicit investigation from normal rats (e.g. balls of silver paper on a watch glass) were placed 2-4 cm beneath each hole. Lighting was provided by a 150 W bulb in a metal reflector mounted about 1 m above the holeboard floor. The animals' behaviour was filmed with an overhead mounted video camera and recorded on video tape. Each animal was tested for 1 h in the hole board. Two animals, one from each group, were tested per day, always between 12.00 h and 16.30 h. Order of testing was counterbalanced over days. No observer was present in the experimental room during the test period. The videotapes were analyzed for (a) the duration
311 and location of each head-dip, and (b) locomotor activity (the number of squares crossed), during successive 10 min periods. One collicular animal failed to headdip during the hour, and was therefore given a second hour's test in the holeboard, 16 days after the first. After further behavioural testing, reported elsewhere [6], the animals with lesions were anaesthetized with chloroform then killed by cervical dislocation. Their brains were removed and frozen at -18 ° C. Coronal sections (24 or 48 #m) were cut in a cryostat, and stained with either iron hematoxylin or cresyl fast violet. Each animal's lesion was reconstructed onto diagrams taken from the stereotaxic atlas of K0nig and Klippel [ 17]. RESULTS One collicular rat was found to have a massive diencephalic tumour: therefore, behavioural data for only the 6 remaining rats with lesions are presented below. Reconstruction of a representative collicular lesion is shown in Fig. 1A. In all 6 animals the superior colliculus was extensively damaged but not completely destroyed. Spared tissue was found in the caudal one-third of the colliculus (5 animals) or rostral sections near the boundary with the pretectum (4 animals). In every case the lesions invaded overlying cerebral cortex and, much less estensively, dorsal central grey. They probably also invaded the mesencephalic reticular formation underlying the superior colliculus, although because of the indistinctness of the boundary between the two structures (cf. ref. 10) it was difficult to be certain. Comparison of the behaviour of the two groups obtained by analysis of the video tapes revealed the following four points. (i) The rats with lesions of the superior colliculus did eventually head-dip, but took much longer to start than the control animals (latency to first head-dip, SC group mean 1660 sec, range 384-4625 sec; N group mean 22 sec, range 9- 3 6 sec; Mann-Whitney U-test, nl = 6, n2 = 7, U = 0, P -- 0.002, two-tailed P values given throughout). (ii) Once the rats with lesions of the superior colliculus had started to head-dip, their subsequent head-dipping was not significantly different from that of the normal animals on a number of measures. For example, the time spent in head-dipping differed between the two groups only for the first two 10 min periods (Fig. lb: 0-10 rain, U = 1, P = 0.002; 10-20 min, U = 3, P = 0.008; for other periods, P > 0.3). Analysis of each animal's head-dips in the 30 min beginning at the start of its first head-dip showed no significant difference between the groups in total number (U = 11, P -- 0.18), total duration (U = 17, P = 0.63), or mean duration (U = 14, P -- 0.37). (iii) There were nonetheless some minor abnormalities in the head-dipping of the collicular rats during this period (30 min starting at first head-dip). It was
312 B 60. OU~P •SC
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~ 20 10 10
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30 40 ~ Time (min)
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Time ( ~ n ) Fig. 1. A: reconstruction of representative lesion of superior colliculus onto coronal sections redrawn from atlas of KOnig and Klippel [ 16]. B: head-dipping (time dipped in a 10 min period) plotted against time in hole-board. Group median scores are shown. One animal with a lesion of the superior colliculus failed to head-dip during the 60 min period shown on the graph (see text). C: locomotor activity (squares crossed in a 10 min period) plotted against time in hole-board. Group median scores are shown.
observed that normal animals either put their heads deep into the hole (up to their ears), or more shallowly, up to about the level of the eyes. The collicular animals had a much higher proportion of shallow head-dips (SC group, mean proportion of shallow dip s 0.71, range 0.51-0.94; N group, mean proportion of shallow dips 0.38, range 0.23-0.52; U = 1, P = 0.002), and made significantly fewer deep dips (SC group, mean number of deep dips 12.5, range 1-25; N group, mean number of deep dips 34.4, range10-58 : U = 2, P = 0.004). Also, for the normal group, the mean duration of head-dips (both kinds taken together) clustered closely round the mean of 2.23 sec (range 1.89-2.63 sec). The mean durations of the collicular group were in every case outside this range: two collicular rats had shorter durations, 1.07 and 1.55 sec, whereas the other 4 collicular rats had longer
313 durations, range 2.96-12.9 sec. Finally, there was a tendency for the rats with lesions of the superior colliculus to explore less efficiently, in the sense of making more head-dips in the first three holes sampled before making the first head-dip in the fourth. Three of the collicular rats made more of these dips than any normal animal, and two of the three in fact failed to find the fourth hole in the time available. However, the difference between the groups as a whole fell short of significance because of the much better performance of the other three rats with collicular lesions (U = 9, P = 0.102). (iv) The rats with collicular lesions had significantly higher locomotor activity scores than the control animals during the first three 10 min periods (Fig. 1C: 0-10 min, U = 0, P = 0.002; 10-20 min, U = 0, P = 0.002; 20-30 min, U = 2, P = 0.004), but not subsequently. During the first 10 min in particular their behaviour was as described previously [7]: they spent much of their time running around the walls of the hole-board, rarely rearing, grooming or freezing. Examination of individual cases, however, did not suggest any simple relationship between the increased locomotor activity and the failure to head-dip. For example, the animal with a lesion of the superior colliculus that was most active (535 squares in the first 10 rain) had the shortest latency to head-dip (384 sec), whereas the collicular rat that took longest to head-dip (4625 sec) covered only 12 squares during the last 30 min of its test session. In fact the correlation between activity during the first 10 min and latency to head-dip was negative, though not significantly so (Spearman's rank r = -0.6, n = 6, P > 0.05). The results of the present experiment thus replicate those obtained previously [7], and in addition show that rats with lesions of the superior colliculus do head-dip if left in the hole-board long enough. The suggestion that their initial failure to head-dip can be ascribed to an inability to produce the required exploratory response [7] is therefore incorrect. DISCUSSION
What is required is an explanation of why the rats with lesions of the superior colliculus took much longer than normal to begin head-dipping. One possibility is that they discovered the holes as soon as normal animals, but their locomotor hyperactivity, which other experiments suggest only occurs in novel environments [4, 13, 24], competed with and prevented exploratory head-dipping. This possibility is consistent with ~the observations that collicular rats show normal amounts of activity [1, 6, 21 ] and of sniffing, head-raising and rearing (Goodale and Carson, unpublished, cited in ref. 13) in their home cages. However, there are a number of findings that indicate that the locomotor hyperactivity and lack of exploratory responding are at least partly independent. (i) In the present experiment the predicted relationship between amount of hyperactivity and latency to head-dip was not obtained. (ii) Small injections of kainic acid within the superior
314 colliculus can increase locomotor activity without affecting head-dipping [9]. (iii) Damage confined to the superficial and intermediate layers of the colliculus does not increase activity, but does reduce the frequency of some exploratory responses [ 19]. (iv) Microinjection of the GABA agonist muscimol, or the local anaesthetic procaine, within the superior colliculus reduce both exploratory responding and locomotor activity [2, 8]. An alternative explanation is that the animals with collicular lesions actually took longer to discover that holes were present in the apparatus. This could have occurred because of, for example, (a) a sensory deficit, (b) an attentional deficit made apparent in a situation containing many novel cues in a variety of modalities, or (c) a subtle motor impairment, for example of vibrissa movement, that was undetectable with the quality of recording available in the present study. Further experiments are required to distinguish between these possibilities, and to establish how coUicular 'neglect' of a static feature of the environment is related to the neglect of briefly presented stimuli known to occur in rats with collicular lesions [14, 16, 18]. The greatly extended latencies of the collicular rats to begin exploration of the holes contrasted strongly with their subsequent almost normal pattern of investigation. However, this relative normality may reflect only that exploring 4 holes is a simple task. In similar situations involving systematic search for food at 8 or more locations, collicular lesions can produce clear deficits in search efficiency [3, 4, 15 ], and preliminary results with a 16-hole apparatus suggest that similar deficits may be found in the hole-board. How far these collicular impairments in exploration of discovered features can be attributed to problems in response-production remains to be determined. Finally, the present experiment was concerned with the nature of the behavioural changes that follow large collicular lesions, rather than with the precise anatomical substrates underlying those changes. Other evidence suggests that disruption of exploratory behaviour in highly novel environments can be caused by damage either to the superficial layers of the superior colliculus, or to the deep layers, or to the mesencephalic reticular formation underlying the colliculus (e.g. refs. 8, 13, 19, 23). How these different areas cooperate in producing normal exploration is not known. However, it is clear from the results described here that the superior colliculus can be important for normal exploration without being necessary for the production of a particular exploratory response. ACKNOWLEDGEMENTS
This work was supported by S.R.C. grant GR/B/24707. We thank Iona Hodges for help with histology, and Catherine Quail for testing the animals.
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