tendencies of HR rats in behavioral tasks involving a free-choice response to ... includes four components: (1) thrill and adventure-s~king characterized by the ...
0191-8869/93 $6.00 + 0.00 Copyright @J 1993 Pergamon Press Ltd
Person. iii&id. Diff. Vol. 15, No. 4, pp. 411-418, 1993 Printed in Great Britain. All rights resewed
INDIVIDUAL DIFFERENCES IN BEHAVIORAL RESPONSES TO NOVELTY IN RATS. POSSIBLE RELATIONSHIP WITH THE SENSATION-SEEKING TRAIT IN MAN F. DELLU, W. MAYO, P. V. PIAZZA,M. LE MOALand H. SIMON* Laboratoire de Psychobiologie des Comportements Adaptatifs, INSERM U.259, Universitk de Bordeaux II, Domaine de Carreire, rue Camille Saint-Sdns, 33077 Bordeaux Cedex, France (Received 17 November 1992)
Summary-Sensation-seeking is a human personality trait characterized by the need for varied, novel and complex sensations, and a general liking for risk-taking activities. Analogies can be drawn with some behavioral tendencies shown in animals. In studies on rats, certain individuals labeled as high-responders (HR), opposed to low-responders (LR), have been shown to be highly reactive in a novel environment and also predisposed to drug taking. Given that the response to novelty is the basis of the definition of sensation-seeking, the present study was designed to obtain more detailed information on the exploratory tendencies of HR rats in behavioral tasks involving a free-choice response to various novel environments differing in levels of complexity and aversiveness. The animals’ preferences for novelty and familiarity were tested in a Y-maze, and for a variety of novel places in a &arm radial maze. The animals’ exploratory tendencies in a well illu~nated area were evaluated in a dark-light emergence test. The HR rats visited one (Y-maze) or many (16-arm radial maze) novel places more frequently than the LR animals did. The visits in the lbarm radial maze by HR rats were also of shorter duration, indicating a more rapid habituation to novelty. Finally, HR rats entered more often and more rapidly an area considered as stressful. In conclusion, HR rats appear to seek novelty, variety and emotional stimulation. These characteristics may be analogous to some of the factors found in human high-sensation seekers.
INTRODUCTION
In humans, a personality trait labeled “unction-s~king” and defined by the “need for varied, novel and complex sensations and experiences” was first described by Zuckerman (Zuckerman, K&n, Price & Zoob, 1964, Zuckerman, 1969). Subsequently, it was found that sensation-seeking includes four components: (1) thrill and adventure-s~king characterized by the search for sensation through risky but exciting sports and other activities; (2) experience-seeking reflected in the search for novel experiences and a nonconfo~ing life-style; (3) disinhibition associated with the seeking of social stimulation; and (4) susceptibility to boredom or an aversion to monotonous, invariant situations, and restlessness when exposed to such situations. It is of interest that psychotropic drug experiences typically correlate with all four of these components (Zucke~an, 1983a, b, 1984, 1991). Parallels of these human personality traits or dimensions were researched in animals. From studies on social interactions in macaques, Chamove, Eysenck and Harlow (1972) isolated three factors labeled afliliative, hostile and fearful which have been related to extraversion, psychoticism and neuroticism described by Eysenck (1967), and Eysenck and Eysenck (1985). In rats, high-levels of activity and defecation in open-field tests may correspond to extraversion and neuroticism, respectively (see Garcia-Sevilla, 1984). In our laboratory, we have identified behavioral characteristics in rats which resemble some of the features of high-sensation seekers in man. Only certain indi~duals have been found to be predisposed to drug-taking. These rats defined as “high-responders” (HR) rapidly develop intravenous self-administration of amphetamine while the “low responders” (LR) do not. Moreover, these rats exhibit an enhanced locomotor response when exposed to a novel environment (Deminibre, Piazza, Le Moal & Simon, 1989; Piazza, DeminGre, Le Moal & Simon, 1989; Piazza, Maccari, Deminikre, Le Moal, Mot&de & Simon, 199la). This is attributed to a novelty effect since this behavioral response disappears after repeated exposures *To whom correspondence
should be addressed. 411
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F. DELLU et al.
to the same environment, i.e. when novelty decreases (Piazza, Maccari, Deminiere, Le Meal, Mormede & Simon, 1990). However, it is not clear whether this behavioral response is the result of increased seeking for novelty since we used a forced exploration paradigm. Given that the response to novelty is crucial to the definition of sensation-seeking (Zuckerman, 1983a, b, 1984) we decided to examine this question in more detail. The behavior of HR and LR animals was investigated in three situations that measure the free-choice response to novel environments differing in complexity and aversiveness: a Y-maze, a 16-arm radial maze, and a dark-light emergence test.
METHODS
Animals Male Sprague-Dawley rats, weighing between 280 and 300 g at the start of the experiment were used. They were housed singly in a temperature (22°C) and humidity controlled room (60%) on a 12 hr light-dark (08:0&20:00) schedule. They had free access to food and water throughout the experiments. Apparatus
and behavioral
testing
Novelty-induced locomotor activity. The novel environment consisted of a circular corridor (10 cm wide and 70 cm in diameter). Four photoelectric cells placed at the perpendicular axes of this apparatus automatically recorded locomotion. The locomotor response was recorded over a period of 2 hr between 16:00 and 18:00 hr. The score of each animal (mean number of photocell counts) cumulated over the 2 hr of testing in the circular corridor was chosen as the variable indicating the individual’s reactivity to the novel environment. Two groups of rats were used: one was tested in the Y-maze, and the other in the 16-arm radial maze and the dark-light emergence test. For the first one, the animals (n = 14) were split into two groups on the basis of their locomotor reactivity to the novel environment. The first group (HR) contained all the animals with an activity score above the median (n = 7), and the second (LR) contained the remainder (n = 7). In the second experiment, 40 rats were split into these two groups (HR: n = 20; LR: n = 20) on the basis of their locomotor response in the novel environment as described above. Exploration in a Y-maze. The two-trial task developed in this maze has been recently validated in our laboratory (Dellu, Mayo, Cherkaoui, Le Moal & Simon, 1992). The apparatus was a Y-maze made of grey plastic, each arm was 50 cm long, 16 cm wide and 32 cm high and was equipped with 2 infrared beams 22 cm apart crossing each arm 3 cm above the floor. The beams were located 47 and 25 cm from the ends of the arms. A visit to an arm was recorded only when the proximal and the distal beams were interrupted in succession. Interruption of these infrared beams was recorded on a micro-computer (IBM-PC) outside the testing room. The floor of the maze was covered with rat odor-saturated sawdust. After each trial, the sawdust was mixed in order to eliminate olfactory stimuli. The maze was placed in a sound-attenuated room under dim illumination. Numerous visual cues were placed on the walls of the testing room and were kept constant during the behavioral testing sessions. An experiment consisted of two trials separated by a 30 min interval. In the first trial, one arm of the Y-maze was closed with a guillotine door. Rats were placed in an arm, their head pointing away from the center of the maze, and they were allowed to visit the two arms for 10 min. During the second trial, animals had free access to the three arms, and were allowed to explore the maze for 10 min. The number and duration of explorations of each arm were recorded during the first 5 min of the second trial. The percentage of visits in the novel arm with respect to the total number of visits in the three arms during the first 2 min of the test was calculated. Exploration in a 16-arm radial maze. The apparatus made of grey plastic consisted of 16 arms (63 cm long x 7 cm wide x 21 cm high) projecting from a central platform (35 cm in diameter). Each arm was equipped with one infrared beam 50 cm from the center and 3 cm above the floor. A visit to an arm was recorded when the beam was interrupted. Interruption of these infrared beams was recorded on a micro-computer (IBM-PC) outside the testing room. The apparatus was placed in a defined position in a room with numerous visual cues placed on the walls. The rat was
Behavioral responses to novelty in rats
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placed in the central area and was allowed to explore the maze for 15 min. Number and duration of visits were recorded. Dark-light emergence test. The apparatus (40 cm long x 40 cm wide x 35 cm high) consisted of a box with two equal compartments. A door (12 x 31 cm) enabled the rats to pass from one compartment to the other. One of the compartments was completely enclosed by black opaque plastic sides with a lid of the same material, while the other was made of white plastic and had no lid. The white compartment was illuminated by a 60 W lamp placed 70 cm above it. The experiment was carried out between 10:00 and 16:00 hr. The rat was placed in the illuminated compartment facing the wall opposite the door. The latencies to enter and then emerge from the dark compartment were recorded. The number of visits and the total and mean times spent in the illuminated compartment after the first entry into the dark box were also recorded. Emergence was taken to be when the animal placed all four paws in the illuminated compartment. The rats were observed for 10 min, and if a rat did not emerge from the darkened compartment within 10 min from the start of test, the trial was stopped, and the emergence latency was recorded as 600 sec. Statistics
The normality of the 2 sample distributions was verified using Shapiro-Wilk’s test. Student’s between the groups, together with analysis of variance (ANOVA) for repeated measures followed by post hoc comparisons by the Newman-Keuls test (NK). The behavioral data were correlated using Bravais-Pearson’s correlation test. t-test was employed for the comparisons
RESULTS Novelty-induced locomotor activity
The normality of the 2 sample distribution was verified: first experiment: w = 0.97, P = 0.8; second experiment: w = 0.95, P = 0.1. The two groups of rats were selected on the basis of their locomotor responses to novelty in a circular corridor. The locomotor response scores over 2 hr were: HR = 810.1 f 92.2, LR = 504.9 f 32.3 photocell counts for the first experiment, and HR = 759.6 f 34.1, LR = 455.3 + 20.4 photocell counts for the second experiment (Fig. 1). Exploration in a Y-maze
The time course of the number of explorations in the three arms during the first 5 min of the second trial is shown in Fig. 2. The number of visits for HR rats [Fig. 2(A)] was significantly different between the three arms throughout the first 2 min. More visits were made in the novel arm [ANOVA: F(2,12) = 21.04, P < 0.001, novel arm vs arm 1 (NK, P < 0.01) and vs arm 2 (NK, P < O.Ol)]. The percentage of visits in the novel arm (57.3 f 4.8%) was significantly above chance (33.3%) (t = 5.00, df = 6, P < 0.01). For the LR rats [Fig. 2(B)], there was no difference between the number of visits in the novel arm and the other two arms throughout the first 2 min of exploration [F(2,12) = 3.00, NS]. Over the first minute, the number of visits was higher in the novel arm than in arm 2 (NK, P < 0.05) but not in arm 1 (NK, NS). The percentage of visits in the novel arm (40.9 + 4.8%) was not different from chance (t = 2.45, df = 6, NS). This percentage was significantly higher for the HR rats compared to the LR rats (t = 2.87, df = 12, P < 0.05). The HR group made fewer total visits in the three arms during the first 2 min (7.0 + 1.2 visits) than did the LR group (11.7 + 1.55 visits) (t = 2.40, df = 12, P < 0.05). Six HR rats and 5 LR rats (out of 7 in each case) made their first choice in the novel arm during the second trial. The total duration of visits did not show the same characteristics as the number of visits (Table 1). The duration of visits for HR rats was significantly higher in the novel arm than in the other two arms throughout the first 2 min [ANOVA: F(2,12) = 9.13, P < 0.01; novel arm vs arm 1 (NK, P < 0.01) and vs arm 2 (NK, P < O.Ol)]. The greatest difference was observed during the first minute [ANOVA: F(2,12) = 15.8, P < 0.001, novel arm vs arm 1 (NK, P < 0.001) vs arm 2 (NK, P < O.OOl)]. For the LR rats, the duration of visits was significantly different between the three arms throughout the first 2 min [F(2,12) = 5.65, P < 0.05; novel arm vs arm 1 (NK, P c 0.05) vs arm 2 (NK, P < O.OS)].The greatest difference was observed during the second minute [ANOVA: F(2,12) = 4.46, P < 0.05, novel arm vs arm 1 (NK, P -C0.05) and vs arm 2 (NK, P < O.OS)].
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Exploration in a l&arm radial maze
Over the 15 min of the experiment, the exploratory behavior of HR and LR animals in the 16-arm radial maze differed both in number and mean duration of visits (Fig. 3). Compared to LR rats, HR rats made more visits [Fig. 3(A)] (t = 3.5, df = 38, P c 0.001). The duration of the visits was also around 50% shorter than that of the visits made by the LR rats (t = 2.34, df = 38, P < 0.05) [Fig. 3(B)]. Over all rats, there was a positive correlation between number of visits in the 16-arm radial maze and the novelty-induced locomotor activity (r = 0.43, P c 0.01). The number of visits made before the rats returned to a previously visited arm was the same in the HR and LR groups: (HR rats: 6.07 f 0.74 visits, LR rats: 6.53 ) 0.76 visits; t = 0.43, df = 38, NS), but the number of nonvisited arms during the experiment was significantly lower with the HR rats: (0.60 f 0.19) than with the LR rats: (1.73 + 0.33) (t = 2.97, df = 38, P < 0.01). Dark-light
emergence
test
The latency to emerge from the dark compartment differed significantly between the HR and LR rats. The HR animals entered the illuminated compartment with less delay than did the LR rats [Fig. 4(A)] [HR = 76.5 f 29 set, LR = 292.0 + 47.37 set (t = 3.88, df = 38, P < O.OOl)]. The HR rats also made more visits than the LR rats in the illuminated compartment over the first 5 min of the experiment (HR = 2.8 + 0.42 visits, LR = 1.5 + 0.36 visits) [Fig. 4(B)] (t = 2.35, df = 38, P < 0.05), although the total number of visits over 10 min did not differ between the two groups (t = 0.84, df = 38, NS). Over all rats, there was a negative correlation between the latency to emerge and the novelty-induced locomotor activity (r = -0.44, P c 0.01) and a positive correlation
NOVELTY-INDUCED LOCOMOTION
1000
900
00
800
0
HR (n=20) Z=759.6
ii
700
8
600
A-500
%
400
1 El
300
0 0
LR (n=20) x=455.3
0 200
Fig. 1. Individual values of novelty-induced locomotion (number of photocell counts) measured in a circular corridor over 2 hr for the second experiment. The horizontal line represents the median separating the HR from the LR.
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Behavioral responses to novelty in rats
00
3.0
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..._.__.._ .-----._.--i ;I ? feo
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2.5 F t; 5
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HR RATS
*
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2.5 g t; F
2.0
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AIM 3 (NOV2L)
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2 TIME
(MIN)
Fig. 2. Time course of exploration in a Y-maze. Number of visits in the three arms and percentages of number of visits in the novel arm by HR (A) and LR (B) rats. The measures were recorded during the first 5 min of the second trial (free access to the three arms) that followed the first 10 min trial (access only to arms 1 and 2) by a time interval of 30min. Statistical significances: HR rats, first min, l**P < 0.001; second, *P < 0.05. Percentage number of visits in the novel arm over the first 2 min of the second trial (inserts) were compared to chance (33.3%). Statistical significances: HR rats, “P -C0.01.
between the number of visits in the illuminated compartment novelty-induced locomotor activity (r = 0.3, P < 0.05).
over the first 5 min and the
DISCUSSION
Rats differing in their locomotor reactivity to novelty (HR and LR rats) were compared in three behavioral tasks involving a free-choice response to various novel environments. In the Y-maze, the animal’s preference between novelty and familiarity was evaluated, while in the radial maze, the animal’s choices between several novel places, the 16 arms of the maze, were determined. These two experimental designs combine specificity and sensitivity to novelty. In the dark-light emergence
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F. DELLU et al. Table
I. Time course of exploration Duration
I
Time (min) HR Novel Arm Arm2 LR Novel Arm Arm2
in a Y-maze of exploration
2
(xc)
3
4
5
arm
33.40 f 3.60’” 5.26 k 2.10 10.70 f 4.02
24.41 5 6.11 18.81 f 5.73 5.76 5 2.24
30.66 f 10.91 8.09 _+4.35 20.31 + 14.89
8.51 f 5.08 4.81 f 2.29 13.73 * 7.40
21.03 k 5.96 5.17 * 3.73 18.94 & 16.95
arm
21.03f4.14 12.61 + 3.84 9.51 f 2.14
54.00 + 20.96’ 13.71 k2.16 7.71 t 2.35
10.97 * 3.10 16.23 f 5.58 6.43 T 2.33
23.54 i 9.30 25.70 k 10.59 6.07 i 3.31
6.67 k 4.33 13.49 f 4.41 10.86 f 5.26
I
I
Duration of visits (in seconds) in the three arms by HR and LR rats (mean i SEM). The measures were recorded during the 5 min of the second trial. Statistical significance: *P i 0.05; l**P < 0.001.
test, since rats are naturally photophobic, the emotional value of novelty-inducing effects was assessed. In the Y-maze, HR rats made more visits in the novel than in the familiar arms. This was not the case for LR rats. This result cannot be attributed to locomotor hyperactivity of HR rats nor to a deficit in recognition processes of the LR rats since (1) the measure is based on a choice between a novel place and a familiar one, and the HR animals made less overall visits in the three arms of the maze than did the LR. In other words, their “hyperactivity” was selectively associated with novelty, (2) the two groups of animals did not differ in discriminating novelty from familiarity as the first arm they chose to visit was the novel one. With respect to the duration of novelty exploration, the HR and LR rats behaved in a similar way i.e. they explored the novel arm longer than they did the other two arms in the first 2 min of the test. However, while the duration of exploration in the novel arm was longer at the start of the test (first minute) and subsequently declined for the HR rats, it reached a maximum during the second minute for the LR rats. This may indicate that LR animals are more fearful of novelty. Overall, the dissociation of results between the number and the duration of visits suggests that the difference between HR and LR rats is in the response for a change (novelty seeking): the 2 groups differed in the number of visits and not in the duration of visits which reflects a response to a change (imposed novelty). This can be related to the classical distinction between inquisitive and inspective exploration (Berlyne, 1960).
* * *
LR
HR
_@
_L
LR
HR
Fig. 3. Exploration in a 16-arm radial maze. Number of visits in the arms (A) and mean duration of one visit (in set) (B) for HR and LR rats, The measures were recorded during a 15 min session. Statistical significances: number of visits, ***P < 0.001; mean duration of one visit (in set), lP < 0.05.
Behavioral responses to novelty in rats
417
350
300 2 ;
250
& z
200
z z
150
z; 2 cl
100
1 *
x
50
0.5
i
0 LR
-I
HR
LR
HR
Fig. 4. Exploration in the dark-light emergence test. Latency to emerge (in set) (A) and number of emergences (B) from dark to brightly illuminated compartment by HR and LR rats. The measures represented are the first 5min of one 10 min session. Statistical significances: latency to emerge ***P < 0.001, number of emergences during the first 5 min, **P i 0.01.
In the 16-arm radial maze, HR rats entered more arms and visited more novel arms that did the LR rats. Moreover, the visits were shorter for the HR animals. This was assumed to be the cause rather than the consequence of the larger number of visits made by these animals since they made no more visits than the LR animals in the familiar arms of the Y-maze. In the 16-arm maze, HR rats tended to investigate more novel places, perhaps due to a more rapid decrease in the stimulating properties of novelty. This is reminiscent of the increased boredom susceptibility of human high-sensation seekers. The HR rats behaved as if they needed to be permanently aroused by a high level of novelty. In the dark-light emergence test, the HR rats visited the illuminated compartment more rapidly and more frequently in the initial period of the test than did the LR rats. However, the number of visits during the entire testing period did not differ between the two groups, indicating that the behavior of HR rats was not the result of a general locomotor hyperactivity. Thus, HR rats showed an increased approach to an environment generally considered as aversive in rats. Taken together, the results of the three behavioral tests demonstrate the existence of individual differences in behavioral responses of rats when faced with different novel environments. Some rats, defined as high-responders, exhibit a strong tendency to seek novelty and “stressful” situations. These behavioral characteristics may be analogous to certain factors found in human high-sensation seekers. Moreover, as in humans in which sensation-seeking is one of the few personality traits that declines with age, we have found that the behavioral characteristics of HR rats is observed in 6-month-old rats but not in 24-month-old rats (unpublished data). Other studies carried out in our laboratory, have shown that HR and LR rats, in addition to their behavioral differences, also differ in certain neurochemical and neuroendocrinological characteristics. In comparison to LR rats, HR animals have an enhanced dopaminergic activity in the nucleus accumbens both under basal conditions (Piazza, Rouge-Pont, Deminiere, Kharouby, Le Moal & Simon, 1991b) or following a tail-pinch stress (Rouge-Pont, Piazza, Kharouby, Le Moal & Simon, in press). This is of interest in view of results consistently implicating these dopaminergic neurons in the response to novelty (Taghzouti, Simon, Louilot, Herman & Le Meal, 1985; Pierce, Crawford, Nonneman, Mattingly & Bardo, 1990) and in drug taking behaviors (Koob, 1992; Le Moal & Simon, 1991). Furthermore, HR and LR rats differ in reactivity of the hypothalamo-pituitary-adrenal axis. HR animals exposed to a novel environment (the same as in this
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study) have a prolonged secretion of corticosterone (Piazza, Maccari, Deminiere, Le Meal, Mormede & Simon, 1991a). Moreover, we have shown that rats self-administer corticosterone, and that HR rats are more sensitive to the reinforcing properties of this hormone (Piazza, Deroche, Deminiere, Maccari, Le Moal & Simon, submitted). Taken together, these findings may have a bearing on the sensation-seeking trait since a key feature of the exposure to novel and/or “aversive” situations is activation of the hypothalamo-pituitary-adrenal axis. This in turn leads to enhanced secretion of corticosterone in rats and cortisol in man. Thus, it can be speculated that HR rats (and high-sensation seekers) may seek novelty and stressful situations for the reinforcing properties of corticosteroids. Whatever the biological basis of high-sensation seeking may be, our findings indicate that a differential psychobiological approach in animals may be useful. Clearly, more experiments are needed to characterize the behavior of HR rats more completely before claiming that a sensation-seeking like trait can be found in rats. Acknowledgemenrs-We thank M. Kharouby and J. M. Claustrat for their technical by grants from INSERM, Universitt de Bordeaux II, Conseil Regional d’Aquitaine
assistance. This work was supported and Fondation de France.
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