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The effects of superior colliculus lesions on reactions to novelty in the hamster
27
Behavioural Brain Research, 36 (1990) 27-32 Elsevier BBR 00985
The effects of superior colliculus lesions on reactions to novelty in the hamster Patricia Scardigli, Jean-Claude Fabre and Catherine Thinus-Blanc C.N.R.S., Laboratoire de Neurosciences Fonctionnelles Ul bis, Marseille (France) (Received 28 November 1988) (Revised version received 16 May 1989) (Accepted 17 May 1989) Key words: Exploration; Superior colliculus; Salience of stimulus; Locomotor hyperactivity; Video-actographic system; Hamster
The aim of this experiment was to examine reactions to novelty of hamsters with large bilateral collicular lesions in an open field containing large conspicuous objects. A video-actographic system was used to quantify the contacts with the objects, the speed of the displacements and the angular head movements. Due to different evolutions of the scores in each group, most of the differences were found at the end of the experiment. Collicular animals, unlike controls, make contacts with the objects but do not habituate, which suggests that these contacts are not investigatory but fortuitous. This possibility is supported by the fact that collicular animals display hyperactive locomotion with stereotyped patterns by the end of the experiment. It is proposed that the depth of lesions and the salience of the stimulus are two modulating factors of the reaction to novelty in collicular animals.
Evidence consistent with a collicular function in exploratory behavior has been provided by a few lesion experiments. The authors report an increased locomotor activity 1,8,12 in rats with deep bilateral lesions of the superior colliculus, but this hyperactivity is not exploratory since it is not accompanied by investigatory reactions such as sniffing, head and body rearing4. In the hole-board test, designed to study reactions to novelty, rats with large lesions of the superior colliculus fail to head-dip for a long period of time 4'2, but once they have discovered the interesting features of the environment (such as the small objects placed into the holes of the floor), they show patterns of head-dipping that are similar to those of control animals 3.
However, it must be underlined that in the above-mentioned situations, the open field did not contain conspicuous objects likely to attract and focus the subjects' attention immediately; either the field was empty 5 or the attractive stimuli were hidden in holes beneath the floor of the hole-board apparatus 2,3. In a situation where sunflower seeds are widespread on the floor of the open field, colliculectomized hamsters are unsystematic in picking them up; however, the authors 6 do not mention any delay in the triggering of their search. Finally, rats with bilateral superior colliculus damage make contacts with perceivable and distinct objects in the field, but only when they approach them headlong (i.e. when no head movement is required), which indicates an ab-
Correspondence: C. Thinus-Blanc, C.N.R.S., Unit6 de Neurosciences FonctionnellesUlbis, 31 chemin J. Aiguier, 13402 Marseille Cedex 09, France. 0166-4328/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)
28 normal pattern of exploration s . These findings support the idea that rodents with superior colliculus lesions are impaired in immediately displaying adapted orienting movements toward slight or hidden sources of stimulation, but are nonetheless able to promptly detect and react to new stimulus which are conspicuous enough to draw the subject's attention. However, before concluding that animals with bilateral lesions of the superior colliculus are still able to display exploratory reactions in novel environments, it remains to be determined if the contacts with the objects are actual investigations and no mere collisions due to their hyperactive and fast locomotion. One indirect way to check the nature of the contacts is to study their evolution over time. As a matter of fact, a consistent feature of investigatory contacts in intact animals is their decrease to an asymptotic level. When observed during short periods of time, this decrease of activity cannot be related to some effect of motor fatigue but corresponds indeed to a knowledge of the features of the situation 1°. The present experiment is a replication in hamsters of Marshall's experiment 8 in rats (object exploration in the open field). Furthermore, we have analyzed the evolution over time of exploratory reactions toward objects, dissociating these reactions (contacts with the objects) from locomotor activity. For this purpose we used a computerized video-actographic system 7 designed to obtain a continuous measure of the head axis and body coordinates in freely moving animals. In addition, visual examination of the actographic charts revealed different patterns of displacements in collicular and control groups (straight versus broken line); this variable was also analyzed since it is related to information processing and reactions to the objects. Nineteen male, experimentally naive golden hamsters were used in this experiment. Since the video-detection technique required a head-marking device, all subjects were deeply anesthetized and a miniature plug-holder was sealed to the exposed skull. The surgical methods are described in detail in a previous article 12. Before this implantation, 7 hamsters received bilateral radiofrequency (RF) lesions of the superior colliculus. The electrode placements were made 1 mm lateral
~ v
Fig. 1. Reconstructions of the most extended (a) and of the most restricted (b) lesions.
to midline, 0.5 m_m posterior to the more anterior aspect of the lambdoidal suture, and 3 mm below the cortical surface. The current was increased progressively for 20 s, till the tip temperature reached 60 °C, then maintained for 40 sec. Reconstructions of the least and most extended lesions are displayed in Fig. 1. In all 7 hamsters the superior colliculus was extensively damaged but not completely destroyed, Invasion of the central gray was observed in 5 cases. The overlying cortex was not affected by the lesion. The recording technique has been detaitg~l elsewhere 7'12 so that only its main features will be described here. At the beginning of each daily session a small plastic bar, 27 mm long with lightemitting-diodes (LEDs) at both ends was fixed to the plug-holder so that the 'front' LED was approximately at interocular level and the 'rear' one above the fu'st cervical vertebrae. These LEDs provided an input signal to a TV camera installed directly overhead and connected to a microprocessor through a hardware interface. A subroutine detected the bright spots in the TV field and addressed their X - Y coordinates into
29 memory. The acquisition process was controlled by a main program which stored the data on disk. Intermittent LED activation was controlled by an electronic device on an alternate cycle - 20 ms on, 10 ms o f f - to allow memory effects of the camera tube to dissipate, The sampling rate was 5 frames/s.
\\k~~'f
'"
:G \
\
\\ Fig. 2. The concentric circles represent an object and the surrounding zone delimited to record the contacts. The bars represent the successive positions of the head axis. Each recording is separated by a 0.20-s interval, a: example of the recording of one contact, b: representation of the calculation of the distance covered. A displacement is measured by joining the middle of adjacent vectors, c: example of the measurement of angular displacements. All the angles made during each block are summed without regard for change in direction. On the example, angles alpha 1 to alpha 7 are summed. The other displacements (forward movements in the same axis and translations) and the immobilities are not taken into account as they are parallel or anterior translation.
The open field was oval, 90 and 50 cm in long and short axes respectively with walls 30 cm high. The inside of the apparatus was painted matt black. Three objects were placed in the field as shown in Fig. 4. The experiment consisted of three 10-min sessions separated by about 6-8 h where the animals could explore the open field with the 3 objects. Only the first and last 3 min of activity were recorded. The use of the computer-video actograms allowed the analysis (Fig. 2) of the length and pattern of the animals' displacements, the number of contacts with the objects, and the number of consecutive samples of the position of the head axis which made an angle; this last measure provided an index of the head movements usually related to orienting and scanning activities. A repeated measure analysis of variance for paired comparisons (VAR 3 Program 11) was carried out on the different variables recorded during each three minute phase. The main factors were Group (collicular and control), Sessions (S 1, $2, $3) and Blocks within sessions (B 1, B2). The analysis of variance on the number of investigatory contacts with the objects revealed a significant main effect of the factors Group (Fl,17 = 4.48, P < 0.05), Session (F1,17 = 6.39, P < 0.01) and of the interaction Session x Block (/72,34 = 3.53, P < 0.05). According to detailed comparisons, collicular hamsters made more contacts than controls during the second block of $3 (F],17 = 7.90, P < 0.05; cf. Fig. 3a). The factor Session was found to have a significant effect only within the control group, with a decrease in the number of contacts (habituation) from S 1 to $2 (F1.11=6.02, P < 0 . 0 5 ) and from S1 to $3 (F1,11 = 12.67, P < 0.001). Concerning the distances covered and speed of the displacements, it is obvious from Fig. 4 that, unlike controls, collicular hamsters display a hyperactive locomotion which does not decrease over time. The analysis of variance revealed a main effect of the factor Group (F1.~7 = 8.55, P < 0.001). Detailed comparisons showed that the difference between the two groups was significant for the second block of each session (F].]7 = 8.77, 9.69 and 8.77 for S1, $2 and $3,
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Fig. 4. Examples of actographic charts with representation of the simple distance covered (a) and of the positions of the head axis (b) for a control (left side) and a representative collicular hamster (right side) during the first 3 min of the experiment (B 1S 1) and the last 3 rain of the last session
(B2s3).
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Fig. 3. Evolution within each group of: (a) the number of contacts, (b)the distance covered and (c)the angularity of the displacements. *P < 0.05; **P < 0.01.
respectively, P < 0.01 for all; cf. Fig. 3b) where collicular hamsters run more distance than control ones. The speeds (cm/s, obtained by calculating the ratio: total number of centimeter/180 s of recording for each block) ranged from 11.06 to 15.43 cm/s (mean speed = 12.98 cm/s) and from 7.40 to 11.19 cm/s (mean speed = 8.56 cm/s) in the collicular and control groups, respectively. Finally, the rough examiaation of the actographic charts (Fig. 4) showed that collicular animals' patterns of displacements were more rectilinear than those in the control group. This difference is particularly marked at the end of the experiment (of. Fig. 3c). The analysis of variance calculated on the number of angular head dis-
placements revealed a significant effect of the factor Group (/1,17 --- 7.16, P < 0.05) that detailed comparisons allowed to locate at both blocks of $3 (Block 1:Fl,17 = 11.86, P < 0 . 0 1 ; Block 2: Fla 7 = 6.22, P < 0.05). Furthermore, there was a within-group evolution in opposite direction: the number of angular head movements increased in the control group from $2 to $3 (Fl.l~ = 5.28, P < 0.05) and decreased in the collicular one from S1 to $3 (F1. 6 = 8.36, P < 0.05). It is of interest to note that for the 3 considered variables the statistically significant differences between groups apl~ar at the end of each session (lentrda of the displacements) or only during the third session (number of contacts and angularity of the displacements). Therefore, collicutar and control subjects' behavior d o not appear to be intrinsically different per se, but rather in their evolution, at least with regard to the considered variables.
31 This experiment provides evidence that collicular hamsters, like rats, do make contact with conspicuous objects and more than control animals by the very end of the experiment, due to a lack of habituation in the operated group. In contrast, a clear habituation is observed in the control group as early as the second session. The lack of habituation in the collicular group does not support the hypothesis of the investigatory nature of those contacts which would rather be fortuitous encounters of the objects. Such an interpretation does not fit with the behavior of collicular rats in the hole-board apparatus 3 where animals displayed delayed, but normal, exploratory reactions. However, in view of the hyperactive and fast locomotion of our operated hamsters (their average speed of displacements was 51.63 ~o superior to that of control hamsters), it is unlikely that they may have been able to inhibit this strong tendency in order to stop and investigate the holes. The depth of the lesions may have been responsible for differences in locomotion, the deeper the lesions (damaging parts of the central grey and midbrain reticular formation), the more exaggerated the locomotor activity2'5"9"13. In addition, we have found that the speed of locomotion and distance covered by the coUicular hamsters do not decrease over time. However, the period along which the present experiment extended may not have been long enough to allow collicular animals to fully familiarize themselves with this new environment. Finally, we have found that the pattern of displacement of operated hamsters are more rectilinear than those of control subjects. An evolution of the collicular group's score is recorded only for this variable, with a decrease of angular head movements between the first and the last session. These data and the mere visual examination of the charts of displacement, suggest that by the end of the experiment some kind of stereotypic behavior would have prevailed over any other type of activity in collicular animals. In conclusion, the implication of the superior colliculus in reactions to novelty and in the organization of information picking up is undisputable. However, our view is that the different effects of the collicular lesions upon exploration
can be accounted for by considering two kinds of competing factors. (1) The salience of the stimulus; the more salient and significant they are, the less pronounced will be the effects of the lesion. (2) The depth of the lesion. The deeper it is, the more accentuated will be the hyperactive locomotion, preventing the animals from stopping to investigate new stimulus. Therefore, this hypothesis predicts that animals with superficial lesions would not show impairment in reacting to new, very salient, stimuli; whereas, in the other extreme, deep damage should induce a total neglect of inconspicuous stimuli. In between, behavior would result in the balance between the two competing and modulating factors. The resuits of this experience provide an example of an intermediate case (deep lesions with exaggerated locomotion and conspicuous objects inducing perturbation of the reactions to novelty without neglect).
REFERENCES 1 Dean, P., Pope, S.G. and Redgrave, P., Influence of novelty on locomotor hyperactivity after lesions of superior colliculus in rats, Behav. Brain Res., 5 (1982) 213-218. 2 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. 3 Dean, P. and Redgrave, P., Head-dipping by rats with lesions of superior colliculus during extended testing in hole-board, Behav. Brain Res., 8 (1983) 309-316. 4 Foreman, N.P., Head-dipping in rats with superior collicular, medial frontal cortical and hippocampal lesions, Physiol. Behav., 30 (1983) 711-717. 5 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. 6 Keselika, J.J. and Rosinski, R.R., Spatial perception in colliculectomized and normal golden hamsters (Mesocricetus auratus ), Physiol. Psychol. , 4 (1976) 511-514. 7 Lecas, J.C. and Dutrieux, G., Head movements and actographic recordings in free-moving animals, using computer analysis of video images, J. Neurosci. Methods, 9 (1983) 357-366. 8 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.
32 9 Pope, S.G. and Dean, P., Hyperactivity, aphagia and motor disturbance following lesions of superior colliculus and underlying tegmentum in rats, Behav. Neurol. Biol., 27 (1979) 433-453. 10 Poucet, B., Chapuis, N., Durup, M. and Thinus-Blanc, C., A study of exploratory behavior as an index of spatial knowledge in hamsters, AnOn. Learning Behav., 14 (1986) 93-100. 11 Rouanet, H. and Lepine, D., Comparisons between treatments in a repeated measurement design; ANOVA and
multivariate methods, Brit. J. Math. Stat. P.s~vchol., 23 (1970) 147-163. 12 Thinus-Blanc, C. and Lecas, J.C., Effects of collicular lesions in the hamster during visual discrimination. An analysis from computer-video actograms, Q. J. Exp. PsvchoL, 37B (1985) 212-233. 13 Weldon, D.A. and Smith, C.J., Superior colliculus lesions and environmental experience: non-visual effects on problem-solving and locomotor activity, Physiol. Behav., 23 (1979) 159-165.
Behavioural Brain Research, 36 (1990) 27-32 Elsevier BBR 00985
The effects of superior colliculus lesions on reactions to novelty in the hamster Patricia Scardigli, Jean-Claude Fabre and Catherine Thinus-Blanc C.N.R.S., Laboratoire de Neurosciences Fonctionnelles Ul bis, Marseille (France) (Received 28 November 1988) (Revised version received 16 May 1989) (Accepted 17 May 1989) Key words: Exploration; Superior colliculus; Salience of stimulus; Locomotor hyperactivity; Video-actographic system; Hamster
The aim of this experiment was to examine reactions to novelty of hamsters with large bilateral collicular lesions in an open field containing large conspicuous objects. A video-actographic system was used to quantify the contacts with the objects, the speed of the displacements and the angular head movements. Due to different evolutions of the scores in each group, most of the differences were found at the end of the experiment. Collicular animals, unlike controls, make contacts with the objects but do not habituate, which suggests that these contacts are not investigatory but fortuitous. This possibility is supported by the fact that collicular animals display hyperactive locomotion with stereotyped patterns by the end of the experiment. It is proposed that the depth of lesions and the salience of the stimulus are two modulating factors of the reaction to novelty in collicular animals.
Evidence consistent with a collicular function in exploratory behavior has been provided by a few lesion experiments. The authors report an increased locomotor activity 1,8,12 in rats with deep bilateral lesions of the superior colliculus, but this hyperactivity is not exploratory since it is not accompanied by investigatory reactions such as sniffing, head and body rearing4. In the hole-board test, designed to study reactions to novelty, rats with large lesions of the superior colliculus fail to head-dip for a long period of time 4'2, but once they have discovered the interesting features of the environment (such as the small objects placed into the holes of the floor), they show patterns of head-dipping that are similar to those of control animals 3.
However, it must be underlined that in the above-mentioned situations, the open field did not contain conspicuous objects likely to attract and focus the subjects' attention immediately; either the field was empty 5 or the attractive stimuli were hidden in holes beneath the floor of the hole-board apparatus 2,3. In a situation where sunflower seeds are widespread on the floor of the open field, colliculectomized hamsters are unsystematic in picking them up; however, the authors 6 do not mention any delay in the triggering of their search. Finally, rats with bilateral superior colliculus damage make contacts with perceivable and distinct objects in the field, but only when they approach them headlong (i.e. when no head movement is required), which indicates an ab-
Correspondence: C. Thinus-Blanc, C.N.R.S., Unit6 de Neurosciences FonctionnellesUlbis, 31 chemin J. Aiguier, 13402 Marseille Cedex 09, France. 0166-4328/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)
28 normal pattern of exploration s . These findings support the idea that rodents with superior colliculus lesions are impaired in immediately displaying adapted orienting movements toward slight or hidden sources of stimulation, but are nonetheless able to promptly detect and react to new stimulus which are conspicuous enough to draw the subject's attention. However, before concluding that animals with bilateral lesions of the superior colliculus are still able to display exploratory reactions in novel environments, it remains to be determined if the contacts with the objects are actual investigations and no mere collisions due to their hyperactive and fast locomotion. One indirect way to check the nature of the contacts is to study their evolution over time. As a matter of fact, a consistent feature of investigatory contacts in intact animals is their decrease to an asymptotic level. When observed during short periods of time, this decrease of activity cannot be related to some effect of motor fatigue but corresponds indeed to a knowledge of the features of the situation 1°. The present experiment is a replication in hamsters of Marshall's experiment 8 in rats (object exploration in the open field). Furthermore, we have analyzed the evolution over time of exploratory reactions toward objects, dissociating these reactions (contacts with the objects) from locomotor activity. For this purpose we used a computerized video-actographic system 7 designed to obtain a continuous measure of the head axis and body coordinates in freely moving animals. In addition, visual examination of the actographic charts revealed different patterns of displacements in collicular and control groups (straight versus broken line); this variable was also analyzed since it is related to information processing and reactions to the objects. Nineteen male, experimentally naive golden hamsters were used in this experiment. Since the video-detection technique required a head-marking device, all subjects were deeply anesthetized and a miniature plug-holder was sealed to the exposed skull. The surgical methods are described in detail in a previous article 12. Before this implantation, 7 hamsters received bilateral radiofrequency (RF) lesions of the superior colliculus. The electrode placements were made 1 mm lateral
~ v
Fig. 1. Reconstructions of the most extended (a) and of the most restricted (b) lesions.
to midline, 0.5 m_m posterior to the more anterior aspect of the lambdoidal suture, and 3 mm below the cortical surface. The current was increased progressively for 20 s, till the tip temperature reached 60 °C, then maintained for 40 sec. Reconstructions of the least and most extended lesions are displayed in Fig. 1. In all 7 hamsters the superior colliculus was extensively damaged but not completely destroyed, Invasion of the central gray was observed in 5 cases. The overlying cortex was not affected by the lesion. The recording technique has been detaitg~l elsewhere 7'12 so that only its main features will be described here. At the beginning of each daily session a small plastic bar, 27 mm long with lightemitting-diodes (LEDs) at both ends was fixed to the plug-holder so that the 'front' LED was approximately at interocular level and the 'rear' one above the fu'st cervical vertebrae. These LEDs provided an input signal to a TV camera installed directly overhead and connected to a microprocessor through a hardware interface. A subroutine detected the bright spots in the TV field and addressed their X - Y coordinates into
29 memory. The acquisition process was controlled by a main program which stored the data on disk. Intermittent LED activation was controlled by an electronic device on an alternate cycle - 20 ms on, 10 ms o f f - to allow memory effects of the camera tube to dissipate, The sampling rate was 5 frames/s.
\\k~~'f
'"
:G \
\
\\ Fig. 2. The concentric circles represent an object and the surrounding zone delimited to record the contacts. The bars represent the successive positions of the head axis. Each recording is separated by a 0.20-s interval, a: example of the recording of one contact, b: representation of the calculation of the distance covered. A displacement is measured by joining the middle of adjacent vectors, c: example of the measurement of angular displacements. All the angles made during each block are summed without regard for change in direction. On the example, angles alpha 1 to alpha 7 are summed. The other displacements (forward movements in the same axis and translations) and the immobilities are not taken into account as they are parallel or anterior translation.
The open field was oval, 90 and 50 cm in long and short axes respectively with walls 30 cm high. The inside of the apparatus was painted matt black. Three objects were placed in the field as shown in Fig. 4. The experiment consisted of three 10-min sessions separated by about 6-8 h where the animals could explore the open field with the 3 objects. Only the first and last 3 min of activity were recorded. The use of the computer-video actograms allowed the analysis (Fig. 2) of the length and pattern of the animals' displacements, the number of contacts with the objects, and the number of consecutive samples of the position of the head axis which made an angle; this last measure provided an index of the head movements usually related to orienting and scanning activities. A repeated measure analysis of variance for paired comparisons (VAR 3 Program 11) was carried out on the different variables recorded during each three minute phase. The main factors were Group (collicular and control), Sessions (S 1, $2, $3) and Blocks within sessions (B 1, B2). The analysis of variance on the number of investigatory contacts with the objects revealed a significant main effect of the factors Group (Fl,17 = 4.48, P < 0.05), Session (F1,17 = 6.39, P < 0.01) and of the interaction Session x Block (/72,34 = 3.53, P < 0.05). According to detailed comparisons, collicular hamsters made more contacts than controls during the second block of $3 (F],17 = 7.90, P < 0.05; cf. Fig. 3a). The factor Session was found to have a significant effect only within the control group, with a decrease in the number of contacts (habituation) from S 1 to $2 (F1.11=6.02, P < 0 . 0 5 ) and from S1 to $3 (F1,11 = 12.67, P < 0.001). Concerning the distances covered and speed of the displacements, it is obvious from Fig. 4 that, unlike controls, collicular hamsters display a hyperactive locomotion which does not decrease over time. The analysis of variance revealed a main effect of the factor Group (F1.~7 = 8.55, P < 0.001). Detailed comparisons showed that the difference between the two groups was significant for the second block of each session (F].]7 = 8.77, 9.69 and 8.77 for S1, $2 and $3,
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Fig. 4. Examples of actographic charts with representation of the simple distance covered (a) and of the positions of the head axis (b) for a control (left side) and a representative collicular hamster (right side) during the first 3 min of the experiment (B 1S 1) and the last 3 rain of the last session
(B2s3).
0 BI
02 SI
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SISSIONS
Fig. 3. Evolution within each group of: (a) the number of contacts, (b)the distance covered and (c)the angularity of the displacements. *P < 0.05; **P < 0.01.
respectively, P < 0.01 for all; cf. Fig. 3b) where collicular hamsters run more distance than control ones. The speeds (cm/s, obtained by calculating the ratio: total number of centimeter/180 s of recording for each block) ranged from 11.06 to 15.43 cm/s (mean speed = 12.98 cm/s) and from 7.40 to 11.19 cm/s (mean speed = 8.56 cm/s) in the collicular and control groups, respectively. Finally, the rough examiaation of the actographic charts (Fig. 4) showed that collicular animals' patterns of displacements were more rectilinear than those in the control group. This difference is particularly marked at the end of the experiment (of. Fig. 3c). The analysis of variance calculated on the number of angular head dis-
placements revealed a significant effect of the factor Group (/1,17 --- 7.16, P < 0.05) that detailed comparisons allowed to locate at both blocks of $3 (Block 1:Fl,17 = 11.86, P < 0 . 0 1 ; Block 2: Fla 7 = 6.22, P < 0.05). Furthermore, there was a within-group evolution in opposite direction: the number of angular head movements increased in the control group from $2 to $3 (Fl.l~ = 5.28, P < 0.05) and decreased in the collicular one from S1 to $3 (F1. 6 = 8.36, P < 0.05). It is of interest to note that for the 3 considered variables the statistically significant differences between groups apl~ar at the end of each session (lentrda of the displacements) or only during the third session (number of contacts and angularity of the displacements). Therefore, collicutar and control subjects' behavior d o not appear to be intrinsically different per se, but rather in their evolution, at least with regard to the considered variables.
31 This experiment provides evidence that collicular hamsters, like rats, do make contact with conspicuous objects and more than control animals by the very end of the experiment, due to a lack of habituation in the operated group. In contrast, a clear habituation is observed in the control group as early as the second session. The lack of habituation in the collicular group does not support the hypothesis of the investigatory nature of those contacts which would rather be fortuitous encounters of the objects. Such an interpretation does not fit with the behavior of collicular rats in the hole-board apparatus 3 where animals displayed delayed, but normal, exploratory reactions. However, in view of the hyperactive and fast locomotion of our operated hamsters (their average speed of displacements was 51.63 ~o superior to that of control hamsters), it is unlikely that they may have been able to inhibit this strong tendency in order to stop and investigate the holes. The depth of the lesions may have been responsible for differences in locomotion, the deeper the lesions (damaging parts of the central grey and midbrain reticular formation), the more exaggerated the locomotor activity2'5"9"13. In addition, we have found that the speed of locomotion and distance covered by the coUicular hamsters do not decrease over time. However, the period along which the present experiment extended may not have been long enough to allow collicular animals to fully familiarize themselves with this new environment. Finally, we have found that the pattern of displacement of operated hamsters are more rectilinear than those of control subjects. An evolution of the collicular group's score is recorded only for this variable, with a decrease of angular head movements between the first and the last session. These data and the mere visual examination of the charts of displacement, suggest that by the end of the experiment some kind of stereotypic behavior would have prevailed over any other type of activity in collicular animals. In conclusion, the implication of the superior colliculus in reactions to novelty and in the organization of information picking up is undisputable. However, our view is that the different effects of the collicular lesions upon exploration
can be accounted for by considering two kinds of competing factors. (1) The salience of the stimulus; the more salient and significant they are, the less pronounced will be the effects of the lesion. (2) The depth of the lesion. The deeper it is, the more accentuated will be the hyperactive locomotion, preventing the animals from stopping to investigate new stimulus. Therefore, this hypothesis predicts that animals with superficial lesions would not show impairment in reacting to new, very salient, stimuli; whereas, in the other extreme, deep damage should induce a total neglect of inconspicuous stimuli. In between, behavior would result in the balance between the two competing and modulating factors. The resuits of this experience provide an example of an intermediate case (deep lesions with exaggerated locomotion and conspicuous objects inducing perturbation of the reactions to novelty without neglect).
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