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Influence of novelty on locomotor hyperactivity after lesions of superior colliculus in rats
Behavioural Brain Research, 5 (1982) 213-218
213
Elsevier Biomedical Press
Influence of novelty on locomotor hyperactivity after lesions of superior colliculus in rats
PAUL DEAN, SIAN G. POPE and PETER REDGRAVE
Department of Psychology, University of Sheffield, Sheffield SIO 2TN (U.K.) (Received June 24th, 1981) (Accepted January 29th, 1982)
Key words: superior colliculus - activity - novelty - rat
Rats given large lesions of the superior colliculus that were adequate to produce locomotor hyperactivity in 2 min open-field tests did not show increased running in their running-wheel home cages. This result is consistent with the suggestion that lesions of the superior colliculus cause hyperactivity in novel not familiar surroundings. The suggestion was also supported by two additional results: (i) a further group of rats with lesions of the superior colliculus did show increased activity in the running wheel when they were first put in it, an effect that occurred mainly during the first 10 min of testing, and (ii) the open-field hyperactivity of these rats similarly declined sharply after the first 10 min of testing.
In rats, large lesions of the superior colliculus (which typically damage parts of adjacent central grey and midbrain reticular formation) increase locomotor activity in the open-field, the holeboard and on an elevated maze [3-5, 8, 10, 13, 14]. In contrast, activity in the home cage appears not to be increased after lesions of the superior colliculus [1 ] (also Goodale and Carson, cited in refs. 8 and 9). This pattern of results has given rise to the suggestion that rats with collicular lesions are hyperactive because they respond abnormally to novel surroundings [8]. However, home cages differ from the pieces of apparatus producing collicular hyperactivity not only in being more familiar, but also in being smaller and so affording less opportunity for running. We report here 3 experiments designed to assess more precisely the role of novelty in the locomotor activity produced by lesions of the superior colliculus. In the first, the effects of collicular lesions were examined on the activity of rats housed in cages attached to running wheels. Twelve male hooded Lister rats (320--520 g) were housed in their normal keeping room in running-wheel cages of standard design (similar to Fig. 1 of ref. 7). A small cage (18.5 cm wide x 26 cm long x 18 cm high, provided with ad libitum food and water) was attached to a wire mesh wheel (40cm diameter x 12.5 cm wide). The wheel could revolve freely (for more than one 0166-4328/82/0000-0000/$02.75 © Elsevier Biomedical Press
214 revolution) in one direction only, and its revolutions were recorded by a mechanical counter. Readings of the counter were taken 5 or 6 days each week. The animals were kept in the running wheel cages for at least 7 weeks before operation, during which time their running scores became relatively stable [7]. The rats were also tested preoperatively in a standard open-field [2]. The field was lit by four 150 W bulbs, giving 220 lux at floor level, and masking white noise was provided. Two tests each 2 min long were given, approximately 3 weeks and 1 week before operation. The number of squares crossed during the tests was recorded. Using standard surgical procedures (see, e.g., ref. 10) 7 of the rats were given bilateral lesions of the superior colliculus. The coordinates (with incisor bar 5 mm above the ear bars) were 4.8 mm posterior to bregma, 1.6 mm lateral to midline, and 4.5 mm below the cortical surface. The lesions were made by passing direct anodal current through a 4-gauge stainless steel insect pin, insulated except for a 0.5 mm tip. The current was increased from 0 to 4 mA over 10 sec, held at 4 mA for a further 20 sec, then reduced from 4 mA to 0 over the final 5 sec. The remaining 5 rats were given sham operations in which the electrode was lowered 3 mm below the cortical surface and no current passed. Subsequent histological processing showed that the collicular lesions had produced extensive destruction in rostral superior colliculus, with some sparing of caudal colliculus, and slight invasion of central grey, midbrain reticular formation, and overlying cerebral cortex (similar to the lesions shown in Fig. 1 of ref. 11). When the animals had recovered from the immediate effects of surgery they were returned to the running wheel cages and observed there for up to 10 weeks. They were also tested in the open-field 30 and 60 days after operation.
Running Wheel
Open Field
+400
"1-20
+300
+15
+200
+10 -I-5
+100 I.W i-
0
SHAM
II
SC
B
SHAM
0 SC
--100
--5
-- 200
-10
--300
-15
--400
--20
¢D
Fig. 1. Change in activity (postoperative score minus preoperative score - see text) after lesions of superior colliculus or s h a m lesions in running-wheel h o m e cages (left) and open-field (right).
215 Change in activity after operation (postoperative score minus preoperative score) is shown for both running wheel and open-field in Fig. 1. The preoperative score for the running wheel was the mean number of wheel turns per week for the 5 weeks prior to operation; the postoperative score was the mean number of turns per week for the first 8 weeks spent in the wheel after operation. For the open field, the preoperative score was the total number of squares crossed in the two preoperative testing sessions; the postoperative score the total for the two postoperative tests. In the running wheel, the activity of the control rats declined slightly; two rats showed a clear decrease, one an increase, and the remaining two showed little change. The activity of the collicular animals also declined, with 5 out the 7 rats showing a clear decrease. However, the effects of coUicular and sham lesions were not significantly different, whether assessed by analysis of variance (two-factor, the interaction Nature of Lesion x Time of Test F (1,10) -- 0.36 non-significant), or by comparing the differences in pre- and postoperative scores with the Mann-Whitney U-test (n~ = 5, n2 = 7, U = 15, P = 0.38 one-tailed). In contrast, the activity of the collicular animals in the open-field increased (6 of 7 rats) whereas for the control rats it declined (4 of 5 rats), possibly because of habituation. This difference between the groups was significant (analysis of variance, interaction Nature of Lesion x Time of Test, F (1,10)= 5.13, P < 0.05: Mann-Whitney U-test on differences between preand postoperative scores, U = 5, P = 0.048, two-tailed). Thus, collicular lesions adequate to change activity in the open field did not produce effects on home-cage activity, even when the home-cage allowed opportunity for extensive running. Further evidence that for these animals the running wheel and open-field were measuring different aspects of activity was provided by the correlations between the two sets of scores. These were negative, though not significantly so, both before and after operation (Spearman's rank correlation, n = 12; before operation r = -0.13, P > 0.1; after operation, r = -0.32, P > 0.1). This finding is consistent with previous results suggesting that lesions of the superior colliculus in rats increase locomotor activity only in novel environments (see above). However, it was still possible that rats with collicular lesions were not hyperactive in the running wheel because of some (unknown) aspect of the running response required, rather than because the wheels were very familiar. To test this possibility, we observed the behaviour of rats with lesions of the superior colliculus exposed to a running wheel cage for the first time. The animals used were 14 male hooded Lister rats, weighing about 300 g at the start of the experiment, kept in conventional home cages with ad libitum food and water. Seven of the rats were given large lesions of the superior colliculus similar to those of the first experiment (data are given for 6 rats only, because the seventh was found to have a massive diencephalic tumour). The remaining 7 rats were unoperated controls. Testing in the running wheel was carried out about 3 months after opera-
216 tion, during which period the animals were observed for 1 or 2 h in a holeboard (Dean and Redgrave, in preparation). The running wheel was identical to those used in the first experiment, except that no food or water was provided. It was situated in the same experimental room as the holeboard. Lighting was provided by ceiling mounted fluorescent tubes supplemented with a 150 W bulb, giving an illumination level of about 60 lux. The animals were placed one at a time in the running wheel for 1 h, and their behaviour filmed with an overhead-mounted videoeamera onto videotape. Two measures of running wheel activity were taken, one from the mechanical counter as in the first experiment, and the other from the videotape by writing down the time and magnitude of each wheel movement, scored to the nearest 1/8th of a turn in either direction. The animals with lesions of the superior colliculus (SC) were more active than the unoperated ( U N O P ) controls on either measure (mechanical counts, SC group mean 13 turns, range 2-39; U N O P group mean 0.14 turns, range 0-1; Mann-Whitney U-test, n, = 6, n2 = 7, U = 0, P = 0.002 two-tailed; and score from videotape, SC group mean 18.7 turns, range 6.9--44.8; U N O P group mean 1.6 turns, range 0.33-4.13; U = 0, P = 0.002 two-tailed). This result is consistent with the view that the collicular rats in the first experiment showed normal levels of activity in the wheel, not because of the nature of the wheel-running response, but because the wheels were familiar. The influence of novelty on wheel-running by rats with lesions of the superior colliculus is further illustrated by more detailed analysis of the data recorded on the videotapes (Fig. 2a). Although the difference in wheel-running between the groups over the last 20 min of testing was significant (score from videotape, SC group mean 1.27 turns, range 0-3.8; U N O P group mean 0.086 turns, range 0--0.5; U = 4.5, P = 0.018 two-tailed), the bulk of the (a) Running Wheel
(b) Open
15
150
10
e
Field
eSC oUNOP
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(J
i
"o s0
\
0 10
20
30
40
Time (min)
50
60
10
20
30
40
50
60
Time (min)
Fig. 2. a: wheel turns (as recorded on videotape - see text) made in successive 5 min periods by rats with lesions of superior colliculus or unoperated controls when put in running wheel for first time. b: squares crossed in open field in successive 5 min periods by rats with lesions of superior colliculus or unoperated controls put in open field for first time.
217 collicular hyperactivity occurred in the first 10 min of testing. Analysis of variance showed that the interaction Groups x Time in Apparatus was highly significant ( F ( l l , l l 0 ) = 3.08, P = 0.0012; data from the unoperated rat with the median activity score of its group was discarded to give equal numbers of subjects in the two groups). The result shown in Fig. 2a suggests not only that novelty is an important influence on the locomotor hyperactivity shown by rats with lesions of the superior colliculus, but also that the time course of its effects may be relatively fast. It is interesting that rats with collicular lesions have previously been tested in the open field only for short periods of time, 10 rain or less [4, 8, 10, 13, 14]. Perhaps if testing were carded out for longer periods, collicular hyperactivity might be seen to decline sharply, as in the running wheel. The animals from the second experiment were therefore tested in the open-field for 1 h. The apparatus and procedure were as in the first experiment, except for the duration of the test, and for the use of a video camera instead of an observer. The pattern of results obtained in the open-field was very similar to that seen in the running wheel. Although the collicular rats were significantly more active than controls during the trma120 min of the test (squares crossed, SC group mean 61.8, range 17-126; U N O P group mean 6.1, range 0-18, U = 1, P -- 0.002), their hyperactivity was particularly marked during the first 10 min of testing (Fig. 2b; interaction Group x Time in Apparatus, F(11,110) = 17.2, P < 0.0001, 6 rats in each group as before). The similarity of the animals' behaviour in the running wheel and open-field in the second and third experiments is indicated by the correlation between the two sets of scores (wheel turns and squares crossed in 1 h; Spearman's rank, n = 13, r = 0.86, P < 0.02). This is in marked contrast to the small negative correlation obtained in the first experiment when the runningwheel served as a home cage. Thus, to summarize the present results, rats with lesions of the superior colliculus showed increased locomotor activity in a novel open-field (2 rain test), but not in a familiar running-wheel (home cage). In either an unfamiliar runningwheel, or an unfamiliar open-field, their hyperactivity was much more marked during the first 10 min than thereafter. These results are therefore consistent with Foreman et al.'s [8] suggestion concerning the importance of novelty in producing the locomotor hyperactivity observed after lesions of the superior colliculus in rats. The results do not show that novelty is the only factor capable of causing this hyperactivity, nor do they indicate which of the cues associated with transfer to a novel environment (for example, handling, absence of colony noises and smells, change in illumination, new sights and smells) are important. One possibility is that any change in surroundings which produces systematic exploration in normal animals will give rise to locomotor hyperactivity in collicular rats, since there is some evidence that the hyperactivity is symptomatic of disorganized exploratory behaviour [ 5, 8, 10 ]. This possibility requires further testing. In any case, it appears that there are at least some circumstances in which the structures destroyed by large lesions of the
218 superior colliculus are less important for detecting that the surroundings have changed, than for organizing the appropriate responses to them. Finally, the present experiments were concerned with the nature o f the behavioural changes following large collicular lesions, rather than the precise anatomical substrates underlying those changes. Other evidence suggests that hyperactivity in the open-field is found after damage to the deep but not superficial layers of the superior colliculus (see ref. 8), or after damage anywhere in the mesencephalic reticular formation (see ref. 12). Recent arguments have emphasized the similarity o f the deep layers of the superior colliculus to the mesencephalic reticular formation [6], and perhaps both structures are involved in organizing appropriate exploratory behaviour in novel surroundings. Supported in part by S.R.C. G r a n t G R / B / 2 4 7 0 7 . S.G.P. was an M.R.C. research student. It is a pleasure to thank I o n a H o d g e s for histological assistance. 1 Altman, J., Diurnal activity rhythm of rats with lesions of superior colliculus and visual cortex, Arner. J. Physiol., 202 (1962) 1205-1207. 2 Broadhurst, P.L., Applications of biometrical genetics to the inheritance of behaviour. In H.J. Eysenck(Ed.), Experiments in Personality Vol. 1, Routledge and Kegan Paul, 1960, pp. 3-102. 3 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. 4 Dean, P. and Pope, S.G., Visual discrimination learning in rats with lesions of superior colliculus: door-push and approach errors in modified jumping stand, Quart. J. exp. Psychol., 33B (1981) 141-157 5 Dean, P., Pope, S.G., Redgrave, P. and Donohoe, T.P., Superior colliculus lesions in rat abolish exploratory head-dipping in holeboard test, Brain Res., 197 (1980) 571-576. 6 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. 7 Finger, F.W., Measuring behavioral activity. In R.D. Myers (Ed.), Methods in Psychobiology Vol. 2, Academic Press, London, 1972, pp. 1-19. 8 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. 9 Murison, R.C.C., The Effects of Lesions of the Superior Colliculus on Visually Guided Behaviour and GeneralActivity in the Rat, unpublished Ph.D. Dissertation, Univ. of Leicester, U.K., 1977. 10 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. 11 Pope, S.G., Dean, P. and Redgrave, P., Dissociation of D-amphetamine induced locomotor activity and stereotyped behaviour by lesions of the superior colliculus, Psychopharmacology, 70 (1980) 297-302. 12 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. 13 Smith, C.J. and Weldon, D.A., Hyperactivity and deficits in problem solving followingsuperior colliculus lesions in the rat, Physiol. Behav., 16 (1976) 381-385. 14 Weldon, D.A. and Smith, C.J., Superior colliculus lesions and environmental experience: nonvisual effects on problem solving and locomotor activity, Physiol. Behav., 23 (1979) 159-163.
213
Elsevier Biomedical Press
Influence of novelty on locomotor hyperactivity after lesions of superior colliculus in rats
PAUL DEAN, SIAN G. POPE and PETER REDGRAVE
Department of Psychology, University of Sheffield, Sheffield SIO 2TN (U.K.) (Received June 24th, 1981) (Accepted January 29th, 1982)
Key words: superior colliculus - activity - novelty - rat
Rats given large lesions of the superior colliculus that were adequate to produce locomotor hyperactivity in 2 min open-field tests did not show increased running in their running-wheel home cages. This result is consistent with the suggestion that lesions of the superior colliculus cause hyperactivity in novel not familiar surroundings. The suggestion was also supported by two additional results: (i) a further group of rats with lesions of the superior colliculus did show increased activity in the running wheel when they were first put in it, an effect that occurred mainly during the first 10 min of testing, and (ii) the open-field hyperactivity of these rats similarly declined sharply after the first 10 min of testing.
In rats, large lesions of the superior colliculus (which typically damage parts of adjacent central grey and midbrain reticular formation) increase locomotor activity in the open-field, the holeboard and on an elevated maze [3-5, 8, 10, 13, 14]. In contrast, activity in the home cage appears not to be increased after lesions of the superior colliculus [1 ] (also Goodale and Carson, cited in refs. 8 and 9). This pattern of results has given rise to the suggestion that rats with collicular lesions are hyperactive because they respond abnormally to novel surroundings [8]. However, home cages differ from the pieces of apparatus producing collicular hyperactivity not only in being more familiar, but also in being smaller and so affording less opportunity for running. We report here 3 experiments designed to assess more precisely the role of novelty in the locomotor activity produced by lesions of the superior colliculus. In the first, the effects of collicular lesions were examined on the activity of rats housed in cages attached to running wheels. Twelve male hooded Lister rats (320--520 g) were housed in their normal keeping room in running-wheel cages of standard design (similar to Fig. 1 of ref. 7). A small cage (18.5 cm wide x 26 cm long x 18 cm high, provided with ad libitum food and water) was attached to a wire mesh wheel (40cm diameter x 12.5 cm wide). The wheel could revolve freely (for more than one 0166-4328/82/0000-0000/$02.75 © Elsevier Biomedical Press
214 revolution) in one direction only, and its revolutions were recorded by a mechanical counter. Readings of the counter were taken 5 or 6 days each week. The animals were kept in the running wheel cages for at least 7 weeks before operation, during which time their running scores became relatively stable [7]. The rats were also tested preoperatively in a standard open-field [2]. The field was lit by four 150 W bulbs, giving 220 lux at floor level, and masking white noise was provided. Two tests each 2 min long were given, approximately 3 weeks and 1 week before operation. The number of squares crossed during the tests was recorded. Using standard surgical procedures (see, e.g., ref. 10) 7 of the rats were given bilateral lesions of the superior colliculus. The coordinates (with incisor bar 5 mm above the ear bars) were 4.8 mm posterior to bregma, 1.6 mm lateral to midline, and 4.5 mm below the cortical surface. The lesions were made by passing direct anodal current through a 4-gauge stainless steel insect pin, insulated except for a 0.5 mm tip. The current was increased from 0 to 4 mA over 10 sec, held at 4 mA for a further 20 sec, then reduced from 4 mA to 0 over the final 5 sec. The remaining 5 rats were given sham operations in which the electrode was lowered 3 mm below the cortical surface and no current passed. Subsequent histological processing showed that the collicular lesions had produced extensive destruction in rostral superior colliculus, with some sparing of caudal colliculus, and slight invasion of central grey, midbrain reticular formation, and overlying cerebral cortex (similar to the lesions shown in Fig. 1 of ref. 11). When the animals had recovered from the immediate effects of surgery they were returned to the running wheel cages and observed there for up to 10 weeks. They were also tested in the open-field 30 and 60 days after operation.
Running Wheel
Open Field
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0
SHAM
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0 SC
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--5
-- 200
-10
--300
-15
--400
--20
¢D
Fig. 1. Change in activity (postoperative score minus preoperative score - see text) after lesions of superior colliculus or s h a m lesions in running-wheel h o m e cages (left) and open-field (right).
215 Change in activity after operation (postoperative score minus preoperative score) is shown for both running wheel and open-field in Fig. 1. The preoperative score for the running wheel was the mean number of wheel turns per week for the 5 weeks prior to operation; the postoperative score was the mean number of turns per week for the first 8 weeks spent in the wheel after operation. For the open field, the preoperative score was the total number of squares crossed in the two preoperative testing sessions; the postoperative score the total for the two postoperative tests. In the running wheel, the activity of the control rats declined slightly; two rats showed a clear decrease, one an increase, and the remaining two showed little change. The activity of the collicular animals also declined, with 5 out the 7 rats showing a clear decrease. However, the effects of coUicular and sham lesions were not significantly different, whether assessed by analysis of variance (two-factor, the interaction Nature of Lesion x Time of Test F (1,10) -- 0.36 non-significant), or by comparing the differences in pre- and postoperative scores with the Mann-Whitney U-test (n~ = 5, n2 = 7, U = 15, P = 0.38 one-tailed). In contrast, the activity of the collicular animals in the open-field increased (6 of 7 rats) whereas for the control rats it declined (4 of 5 rats), possibly because of habituation. This difference between the groups was significant (analysis of variance, interaction Nature of Lesion x Time of Test, F (1,10)= 5.13, P < 0.05: Mann-Whitney U-test on differences between preand postoperative scores, U = 5, P = 0.048, two-tailed). Thus, collicular lesions adequate to change activity in the open field did not produce effects on home-cage activity, even when the home-cage allowed opportunity for extensive running. Further evidence that for these animals the running wheel and open-field were measuring different aspects of activity was provided by the correlations between the two sets of scores. These were negative, though not significantly so, both before and after operation (Spearman's rank correlation, n = 12; before operation r = -0.13, P > 0.1; after operation, r = -0.32, P > 0.1). This finding is consistent with previous results suggesting that lesions of the superior colliculus in rats increase locomotor activity only in novel environments (see above). However, it was still possible that rats with collicular lesions were not hyperactive in the running wheel because of some (unknown) aspect of the running response required, rather than because the wheels were very familiar. To test this possibility, we observed the behaviour of rats with lesions of the superior colliculus exposed to a running wheel cage for the first time. The animals used were 14 male hooded Lister rats, weighing about 300 g at the start of the experiment, kept in conventional home cages with ad libitum food and water. Seven of the rats were given large lesions of the superior colliculus similar to those of the first experiment (data are given for 6 rats only, because the seventh was found to have a massive diencephalic tumour). The remaining 7 rats were unoperated controls. Testing in the running wheel was carried out about 3 months after opera-
216 tion, during which period the animals were observed for 1 or 2 h in a holeboard (Dean and Redgrave, in preparation). The running wheel was identical to those used in the first experiment, except that no food or water was provided. It was situated in the same experimental room as the holeboard. Lighting was provided by ceiling mounted fluorescent tubes supplemented with a 150 W bulb, giving an illumination level of about 60 lux. The animals were placed one at a time in the running wheel for 1 h, and their behaviour filmed with an overhead-mounted videoeamera onto videotape. Two measures of running wheel activity were taken, one from the mechanical counter as in the first experiment, and the other from the videotape by writing down the time and magnitude of each wheel movement, scored to the nearest 1/8th of a turn in either direction. The animals with lesions of the superior colliculus (SC) were more active than the unoperated ( U N O P ) controls on either measure (mechanical counts, SC group mean 13 turns, range 2-39; U N O P group mean 0.14 turns, range 0-1; Mann-Whitney U-test, n, = 6, n2 = 7, U = 0, P = 0.002 two-tailed; and score from videotape, SC group mean 18.7 turns, range 6.9--44.8; U N O P group mean 1.6 turns, range 0.33-4.13; U = 0, P = 0.002 two-tailed). This result is consistent with the view that the collicular rats in the first experiment showed normal levels of activity in the wheel, not because of the nature of the wheel-running response, but because the wheels were familiar. The influence of novelty on wheel-running by rats with lesions of the superior colliculus is further illustrated by more detailed analysis of the data recorded on the videotapes (Fig. 2a). Although the difference in wheel-running between the groups over the last 20 min of testing was significant (score from videotape, SC group mean 1.27 turns, range 0-3.8; U N O P group mean 0.086 turns, range 0--0.5; U = 4.5, P = 0.018 two-tailed), the bulk of the (a) Running Wheel
(b) Open
15
150
10
e
Field
eSC oUNOP
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i
"o s0
\
0 10
20
30
40
Time (min)
50
60
10
20
30
40
50
60
Time (min)
Fig. 2. a: wheel turns (as recorded on videotape - see text) made in successive 5 min periods by rats with lesions of superior colliculus or unoperated controls when put in running wheel for first time. b: squares crossed in open field in successive 5 min periods by rats with lesions of superior colliculus or unoperated controls put in open field for first time.
217 collicular hyperactivity occurred in the first 10 min of testing. Analysis of variance showed that the interaction Groups x Time in Apparatus was highly significant ( F ( l l , l l 0 ) = 3.08, P = 0.0012; data from the unoperated rat with the median activity score of its group was discarded to give equal numbers of subjects in the two groups). The result shown in Fig. 2a suggests not only that novelty is an important influence on the locomotor hyperactivity shown by rats with lesions of the superior colliculus, but also that the time course of its effects may be relatively fast. It is interesting that rats with collicular lesions have previously been tested in the open field only for short periods of time, 10 rain or less [4, 8, 10, 13, 14]. Perhaps if testing were carded out for longer periods, collicular hyperactivity might be seen to decline sharply, as in the running wheel. The animals from the second experiment were therefore tested in the open-field for 1 h. The apparatus and procedure were as in the first experiment, except for the duration of the test, and for the use of a video camera instead of an observer. The pattern of results obtained in the open-field was very similar to that seen in the running wheel. Although the collicular rats were significantly more active than controls during the trma120 min of the test (squares crossed, SC group mean 61.8, range 17-126; U N O P group mean 6.1, range 0-18, U = 1, P -- 0.002), their hyperactivity was particularly marked during the first 10 min of testing (Fig. 2b; interaction Group x Time in Apparatus, F(11,110) = 17.2, P < 0.0001, 6 rats in each group as before). The similarity of the animals' behaviour in the running wheel and open-field in the second and third experiments is indicated by the correlation between the two sets of scores (wheel turns and squares crossed in 1 h; Spearman's rank, n = 13, r = 0.86, P < 0.02). This is in marked contrast to the small negative correlation obtained in the first experiment when the runningwheel served as a home cage. Thus, to summarize the present results, rats with lesions of the superior colliculus showed increased locomotor activity in a novel open-field (2 rain test), but not in a familiar running-wheel (home cage). In either an unfamiliar runningwheel, or an unfamiliar open-field, their hyperactivity was much more marked during the first 10 min than thereafter. These results are therefore consistent with Foreman et al.'s [8] suggestion concerning the importance of novelty in producing the locomotor hyperactivity observed after lesions of the superior colliculus in rats. The results do not show that novelty is the only factor capable of causing this hyperactivity, nor do they indicate which of the cues associated with transfer to a novel environment (for example, handling, absence of colony noises and smells, change in illumination, new sights and smells) are important. One possibility is that any change in surroundings which produces systematic exploration in normal animals will give rise to locomotor hyperactivity in collicular rats, since there is some evidence that the hyperactivity is symptomatic of disorganized exploratory behaviour [ 5, 8, 10 ]. This possibility requires further testing. In any case, it appears that there are at least some circumstances in which the structures destroyed by large lesions of the
218 superior colliculus are less important for detecting that the surroundings have changed, than for organizing the appropriate responses to them. Finally, the present experiments were concerned with the nature o f the behavioural changes following large collicular lesions, rather than the precise anatomical substrates underlying those changes. Other evidence suggests that hyperactivity in the open-field is found after damage to the deep but not superficial layers of the superior colliculus (see ref. 8), or after damage anywhere in the mesencephalic reticular formation (see ref. 12). Recent arguments have emphasized the similarity o f the deep layers of the superior colliculus to the mesencephalic reticular formation [6], and perhaps both structures are involved in organizing appropriate exploratory behaviour in novel surroundings. Supported in part by S.R.C. G r a n t G R / B / 2 4 7 0 7 . S.G.P. was an M.R.C. research student. It is a pleasure to thank I o n a H o d g e s for histological assistance. 1 Altman, J., Diurnal activity rhythm of rats with lesions of superior colliculus and visual cortex, Arner. J. Physiol., 202 (1962) 1205-1207. 2 Broadhurst, P.L., Applications of biometrical genetics to the inheritance of behaviour. In H.J. Eysenck(Ed.), Experiments in Personality Vol. 1, Routledge and Kegan Paul, 1960, pp. 3-102. 3 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. 4 Dean, P. and Pope, S.G., Visual discrimination learning in rats with lesions of superior colliculus: door-push and approach errors in modified jumping stand, Quart. J. exp. Psychol., 33B (1981) 141-157 5 Dean, P., Pope, S.G., Redgrave, P. and Donohoe, T.P., Superior colliculus lesions in rat abolish exploratory head-dipping in holeboard test, Brain Res., 197 (1980) 571-576. 6 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. 7 Finger, F.W., Measuring behavioral activity. In R.D. Myers (Ed.), Methods in Psychobiology Vol. 2, Academic Press, London, 1972, pp. 1-19. 8 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. 9 Murison, R.C.C., The Effects of Lesions of the Superior Colliculus on Visually Guided Behaviour and GeneralActivity in the Rat, unpublished Ph.D. Dissertation, Univ. of Leicester, U.K., 1977. 10 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. 11 Pope, S.G., Dean, P. and Redgrave, P., Dissociation of D-amphetamine induced locomotor activity and stereotyped behaviour by lesions of the superior colliculus, Psychopharmacology, 70 (1980) 297-302. 12 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. 13 Smith, C.J. and Weldon, D.A., Hyperactivity and deficits in problem solving followingsuperior colliculus lesions in the rat, Physiol. Behav., 16 (1976) 381-385. 14 Weldon, D.A. and Smith, C.J., Superior colliculus lesions and environmental experience: nonvisual effects on problem solving and locomotor activity, Physiol. Behav., 23 (1979) 159-163.