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Individual differences in interspecific aggressiveness: Mouse-killing in rats after isolation
Person. i,,&kf. Din: Vol. 6, No. 4. pp. 479484. Printed in Great Britain. All rights reserved
1985 Copyright
0
0191.8869185 $3.00 + 0.00 1985 Pergamon Press Ltd
INDIVIDUAL DIFFERENCES IN INTERSPECIFIC AGGRESSIVENESS: MOUSE-KILLING IN RATS AFTER ISOLATION ASSUMPCIOMART? and L~tis GARCIA-SEVILLA~ Departmentsof ‘ExperimentalPsychology and Psychophysiology and 2Medical Psychology, Autonomous University of Barcelona, Catalonia, Spain (Receioed
28 August
1984)
Summary-Measures of extraversion and neuroticism in rats are related to aggressive behaviour in two strains of rats. Isolated rats and rats reared together, of the Sprague-Dawley and Wistar strains, were submitted to an aggressiveness test. The results show that isolation generates and/or increases mousekilling behaviour only in Wistar rats which are more emotional (neurotic) than Sprague-Dawley rats. The two strains do not differ significantly in their open-field ambulation (extraversion), although Wistar rats tend to be less ambulatory. Within the Wistar strain, the results showed the same trend, that is, the more emotional and less ambulatory rats (dysthymics) are the ones who became killers after isolation. The Sprague-Dawley strain does not show any significant aggressive behaviour after isolation.
INTRODUCTION
Apart from sex, there are two variables that seem relevant to aggressive behaviour, i.e. extraversion-introversion and neuroticism-stability (Edmunds, 1977). According to Eysenck (1957, 1977) extraverts would show antisocial behauiour, i.e. aggression, more easily than introverts. He also postulates that neuroticism acts as a drive that would reinforce extraverts’ inclination to antisocial behaviour. Some other researchers (Buss, 1960; Edmunds, 1977) have corroborated these observations; however, Frost (1970) found that extraversion did not correlate significantly with aggression variables (other than assertiveness). In animal research, Broadhurst (1957, 1960) starting from the works of Hall (1934, 1936) has validated open-field (OF) defecation in rats as a measure of emotionality, being an analogue of neuroticism in humans (Broadhurst, 1960; Eysenck and Broadhurst, 1964). The OF standardized by Broadhurst (1957) puts the animal in a very stressful situation in order to measure its emotionality. Using a not so frightening OF (lower intensity of sound), ambulation becomes a measure which is independent of defecation and is a good animal index of extraversion (Garcia, 1974; 1984; Marti, 1977). The relation between OF ambulation and the aggression shown by the animals seems clear, but the relation between the latter and the OF defecation is being questioned: Novakova, Flandera and Sandritter (1974) have reported a variety of behavioural differences that could be summarized in terms of their distinction between excitable and non-excitable rats. Thus, killer rats, (excitable type) were found to be less able to habituate exploratory behaviour and to exhibit more horizontal activity in an exploration test. Other authors (Vergnes, Boehrer and Karli, 1974; Thorne, Patterson and Topping, 1975), have reported that killer and non-killer rats do not differ in terms of ambulation in the OF. But Thorne et al. (1975) indicated that the difference in rearing behaviour shown in the OF test could be interpreted as indicating that killers have a greater tendency to explore. On the other hand, Lester (1967) and Lester and Cheses (1968) reported that dominant rats show a greater exploratory trend than submissive ones. Brain and Nowell (1969) demonstrated a significant positive correlation between OF ambulation and the composite Aggression score for isolated male albino mice. We mention these results because mouse-killing behaviour in rats may represent not predatory aggression but something very similar to conspecific attack (Blanchard and Blanchard, 1977). The possibility of an aggressive component, as opposed to a predatory one, in 419
480
ASSUMPCIO
MAwi
and
Lwis
GARCIA~EVILLA
a rat’s attack on mice is further indicated by some reports (Barr, Gibbons and Moyer, 1975). Mouse-killing in rats may be a different aggressive response than inter-male fighting, but the similarity in conditions which initiate these two kinds of aggression suggests that a common mechanism is involved in both. If so, these two behaviours should be correlated. That is, animals that are mouse-killers should also be the most vigorous inter-male fighters (Bowers, 1979). In relation to the measure of defecation, Knutson and Hynan (1973) and Thorne et al. (1975) did not find differences between killer and non-killer rats. But, Bowers (1979) found a correlation between mouse-killing and a conditioned emotional response that suggests that aggressive rats are more emotionally responsive and more fearful than less aggressive rats. This conclusion is supported by Vergnes et al. (1974) who found that mouse-killing rats were more emotional in an OF situation than other rats. Valzelli (1969) also indicated that the greater or lesser susceptibility to become aggressive after a suitable period of isolation is probably linked to the different degree of basic emotionality of the strains considered. On the other hand, the results reported by Billingslea (1941), Hall and Klein (1942), Broadhurst (1958) and Ruskin, Davis and De Peralta (1975) indicate that the less emotional rats are the most aggressive. But the results obtained by Brain and Nowell (1969) and Svare and Leshner (1973) on isolated mice indicate a positive correlation between OF defecation and the composite Aggression score. Later, Brain and Nowell (1970) obtained Defecation scores placing the animal into the aggression tank, and there was no demonstrable relationship between defecation and the composite Aggression score. All these contradictory results may indicate some methodological differences, analyses of different types of aggressive behaviour or individual differences in the Ss used. Sex is a very important variable we have to take into account when measuring aggressive behaviour in animals, but we must not forget the role of the type of strain when working with rodents. Seward (1945) Scott and Federicson (1951) and Valzelli (1967, 1971, 1975), have observed that both female mice and female rats, no matter which strain they came from, are not aggressive except during the ‘post-partum’ period, and when deprived of food and water. It seems well-established (review by Brain, 1975) that aggressive behaviour can be induced in laboratory rodents by individual housing, i.e. isolation (Hammour. Goldsmith and Brain, 1982). This method is easy to use, steady in its effects and produces a stable and lasting behaviour pattern (Valzelli, 1971). The objective of the present study is to examine individual differences in the killing behaviour of rats after being isolated, in relation to individual differences in a low-frightening OF, excluding the sex variable in this study. Our expectations are: (1) if OF defecation is a measure of neuroticism in rats, and if neuroticism is related to aggressive behaviour, then social isolation will increase and/or generate killing or aggressive behaviour in the most reactive rats; (2) if OF ambulation is a measure of extraversion, and if extraversion is related to aggressive behaviour, then isolation will increase and/or generate killing or aggressive behaviour in the most ambulatory rats. METHOD
AND PROCEDURE
Subjects Subjects were 66 naive male Sprague-Dawley rats from Charles River Breeding Laboratories and 75 naive male Wistar rats from the Morini Laboratories. They were 90 days old at the beginning of the experiment. Their weight was about 200-300 g, just the weight they have at the time of sexual maturity. The mice used in the aggression test were males of the Swiss strain. All rats were housed in plastic cages of 524 x 274 x 150 mm with ad libitum access to food and water. They had a light and dark circadian rhythm of 12 hr, the temperature was regulated between 22 + 2°C and the humidity between 40 and 60%. OF test This apparatus was similar to that described by Broadhurst (1960). It consists of a circle of 81.5 cm dia and 33.5 cm high. Its floor is made of plywood and has three concentric circles divided
Mouse-killing
into 19 sections a 200 W lamp, Broadhurst one, be heard, which
in rats after isolation
481
marked in pencil having the same area each. The source of light is provided by hanging 120 mm above floor level. To have a less-stressful OF test than the we administered this test in silence. Only the sound of an air-conditioner could rats normally hear in their home-cages.
Aggression test
The measure used was the categorization of the rat’s behaviour confronted by a mouse introduced in its cage, this mouse being an intruder. The categories of Valzelli (1971): muricide, amicable and indifferent were used. As was the method of Svare and Leshner (1973) to measure the aggressive behaviour among mice. The latter was adapted to our Ss as they were rats, not mice. Procedure
Once the Ss were in our laboratory and after 4 days of adaptation, the OF test was administered to each rat. The procedure was similar to that used by Broadhurst (1960): 4 days of testing (at the same hour) and for 2 min/day. The rat was placed in the middle of the OF floor and the number of floor units entered by the animal was scored (i.e. ambulation) and so was the number of faecal boluses (i.e. defecation). Immediately after each testing, the OF was cleaned to prevent any modification in behaviour from the odour of the previous animal. At the end of the fourth OF session, Ss (33 rats of the Sprague-Dawley strain and 54 of the Wistar strain) were housed individually in cages of 524 x 274 x 150 mm and placed in an isolated room to have adequate social deprivation. Control rats (33 of the Sprague-Dawley strain and 21 of the Wistar strain) were housed in cages of the same shape but in groups of 5; so we had three groups of 5 and one of 6 for the 21 control rats of the Wistar strain, and five groups of 5 and two of 4 for the 33 control rats of the Sprague-Dawley strain. The period of isolation was 6 weeks; then the test of aggressivity was administered, for 10 min and on 3 consecutive days. A mouse was introduced into the cage, all the rat’s responses and their frequency were observed-licking, approaching, uncoordinated hyperactivity, picking up, jumping, biting. Control rats had the same treatment after 6 weeks of living together; they were tested individually, removing the rest of the animals and a mouse was introduced into each cage.
RESULTS
There is no significant correlation between ambulation and defecation in the OF test, in both strains of rats (Table 1). The reliability coefficients reported by Broadhurst (1960) are also given in Table 1. Ambulation from Wistar rats (W = 103.9, SD = 42.8) was lower than ambulation from Sprague-Dawley (R = 113.5, SD = 42.8) animals, the difference not being significant [t(139) = - 1.33, NS]. Wistar rats showed a higher level of defecation (r = 14.6, SD = 8.3) than the Sprague-Dawley animals (8 = 11, SD = 7.1), the difference being significant [t(139) = 2.78, P < 0.011. Table 2 indicates the percentage of rats belonging to each category, control and isolated groups of Wistar and Sprague-Dawley strains, and also shows killer (muricide) and non-killer (amicable and indifferent) rats after isolation for both strains. Isolation only produced killer behaviour in the Wistar strain, the difference being significant [x’(l) = 12.21 P < O.OOOS]compared to Table I. Measures (I, SD) taken in the OF, and their inter-correlations reliabilities Wistar Ambulation Defecation I (ambulation+lefecation)
SoranutDawlev
103.9 (42.8) 14.6 (8.3) -0.0216
113.5 (42.8) 11.0(7.1) 0.2515
0.6764 0.4383
0.5191 0.5007
Reliability
Ambulation Defecation
and
AWJMPCIO MARTYand
482
Louis GARCIA~EVILLA
Table 2. Percentages of rats belonging to each category; control and isolated groups of both strains Sprague-Dawley
Wistar Isolated
Control
Table
Isolated
0 73 27
26 63 II
0 62 38
Muricide Amicable Indifferent
Control
0 55 45
3. Pearson correlation between three variables: defecation and aggressive behaviour Wistar Control
Ambulation Defecation
-0.1023 0.031
I
ambulation,
Sprague-Dawley Isolated
Control
Isolated
-0.2944’ 0.2715’
0.0208 0.0421
-0.1084 -0.1891
lP < 0.05.
Table 4. Measurement of aggressive behaviour using the procedure of Svare and Leshner (1973) for the control and experimental groups of both strains (r-values) Wistar
Control Isolated z
Sprague-Dawley
R
SD
R
SD
t
2.1 29.2
1.58 18.43
6 4.1
3.61 2.66
3.9 6.57
-6.51 0.001
P<
0.001 0.001
0.002 2.51
Sprague-Dawley rats. In the Wistar strain the killer rats are not different from the non-killer ones in ambulation, although they tend to appear more defecatory [t(52) = 1.46, P < 0.11. To quantify the aggressive behaviour we gave different scores to the behaviour showed by the rat faced with a mouse, as follows: 0.5 of a point (approaching and licking the mouse), 1 point (uncoordinated hyperactivity and picking up), 2 points (jumping at and biting it). Killer and non-killer rats differed significantly in all these patterns, Table 3 shows the results obtained with a Pearson correlation between aggressive behaviour and the OF measurements: post-isolation, the Wistar strain shows a positive and significant correlation with defecation and a negative one with ambulation. Finally, Table 4 summarizes the results obtained using these scores. In the Sprague-Dawley strain, the control rats have the highest scores, but this trend is inverted as an effect of isolation. DISCUSSION
Defecation and ambulation in the OF test have proved to be reliable and independent measures, as was expected from a low-frightening OF, and in our view (Garcia-Sevilla, 1984) they can be considered as measures of neuroticism (defecation) and of extraversion (ambulation). The socio-environmental isolation to provoke aggression was not effective with the Sprague-Dawley strain, which confirms the results of other investigations (Korn and Moyer, 1968). These differences between strains in post-isolation aggression have been attributed to the different strains’ emotionality (Valzelli and Garattini, 1968). In this sense, our results confirm this expectation, because the strain which proves to be aggressive after isolation, the Wistar strain, is more defecatory in the OF than Sprague-Dawley rats. On the other hand, the Wistar strain, tends (Table 1) to be less ambulatory than the Sprague-Dawley strain. In support of our hypotheses, only the relation between neuroticism (defecation) and postisolation aggressive behaviour appears, both between strains (Table 2) and within the strain affected by isolation, i.e. Wistar (Table 3). Therefore, the more defecatory strain (neurotic) is the one that shows aggression, and within this strain the correlation between defecation and aggressive behaviour is positive and significant. On the other hand, our results in relation to ambulation (extraversion) do not confirm our hypothesis.
Mouse-killing
in rats after
isolation
483
We expected that the more ambulatory rats (extraverts) would more easily become aggressive. But the Wistar strain, the one that turns aggressive, tends to be less ambulatory, and within this strain the correlation between ambulation and aggressive behaviour is negative and significant, just the opposite of what was expected (Table 3). It is as if the critical variable was the magnitude of the aversive situation in the production of aggression through socio-environmental isolation, and this magnitude would affect the dysthymic (neurotic introvert) rats. Among humans there is some evidence that introverted neurotics, with an inadequate personality, when repressed tend to commit murder within the family because they cannot cope with the frustration (Eysenck, 1977). In both cases, familial murderers and mouse-killing rats, there is a build up of frustration and aggression which finally causes the human, or the animal, to perform the aggressive act. A general explanation for our results could be obtained by applying the model of emotional aggression (Buss, 1960). This type of aggression implies a social behaviour, approaching, and a drive, anger. Approaching and exploring would be extravert behaviours and the anger an emotional state, both being necessary to produce emotional aggressive behaviour. Note that control Sprague-Dawley rats are friendly and amicable, according to Valzelli’s classification (Table 2), and more aggressive than control Wistar (Table 4), although Sprague-Dawley control rats cannot be considered truly aggressive as none of them became a killer; in fact, what we obtained was that they approached the mouse (licking, picking up, . . . ), i.e. they showed approaching social behaviours. In fact, social deprivation only produces a slight modification towards indifference in the behaviour shown by the Sprague-Dawley rats. Karli, Vergnes, Eclancher, Schmitt and Chaurand (1972) suggested that there are different motivational states which may express themselves in different kinds of aggressive behaviour. Subsequently, Karli et al. (1974) indicated, in the same sense, that changes in emotional reactivity brought about by early social interactions or by early handling do not necessarily affect all kinds of aggressive behaviour in the same way and it seemed likely to them that low emotional reactivity can reduce the probability that aversively-motivated aggression is elicited, while facilitating the elicitation of an appetitively-motivated aggressive behaviour. Because of this, it is not surprising that in our case, where social isolation (social deprivation) is an aversive situation, the Wistar strain would be the one that shows killing behaviour. It is also within this strain, that a greater tendency to show attack behaviour in rats with higher Defecation scores is observed. The results of Billingslea (1941), Hall and Klein (1942) and Ruskin et al. (1975), which showed a negative correlation between Emotivity and Aggressivity scores, could be explained if we assume that attack displayed by an isolated rat faced with a mouse is an aggressive behaviour different from the attack shown by the rat faced with another rat when the former has not suffered the aversive situation of isolation. Correspondence-All
reprint
requests
should
be addressed
to L. Garcia-Sevilla.
REFERENCES Barr G. A., Gibbons J. L. and Moyer K. E. (1975) The relationship between mouse killing and intraspecific fighting in the albino rat. Behav. Biol. 14(2), 201-208. Billingslea F. Y. (1941) The relationship between emotionality and various other salients of behaviour in the rat. J. cornp. Psychol. 31, 69-77. Blanchard R. J. and Blanchard 0. C. (1977) Aggressive behaviour in the rat. B&u. Biol. 21, 197-224. Bowers D. C. (1979) Mouse-killing, intermale fighting, and conditioned emotional response in rats. Aggressive Behav. 5, 41-49. Brain P. F. (1975) What does individual housing mean to a mouse? Life Sci. 16, 187-200. Brain P. F. and Noweil N. W. (1969) Some behavioural and endocrine relationships in adult male laboratory mice subjected to open field and aggression test. Physiol. Behav. 4, 945-947. Brain P. F. and Nowell N. W. (1970) Activity and defecation related to aggressiveness and adrenal stress response in adult male laboratory mice. Physiol. Behav. 5, 259-261. Broadhurst P. L. (1957) Determinants of emotionality in the rat--I. Situational factors. Br. J. Psychol. 48, I-12. Broadhurst P. L. (1958) Determinants ofemotionality in the rat--III. Strain differences. J. conrp. physiol. Psycho/. 51,55-59. Broadhurst P. L. (1960) Application of biometrical genetics to the inheritance of behaviour. In Experimenfs in Personality: Vol. I, Psycho~enefksarzd Psychopharmacology(Edited by Eysenck H. J.). Rouledge & Kegan Paul, London. ’ Bowers D. C. (1979) Mouse-killing, intermale fighting, and conditioned emotional response in rats. Aggressive Behav. 5, 41-49. Buss A. M. (1960) Psicologia de la Agresidn. Ediciones Troquel, Buenos Aires, Argentina. Denenberg V. H. (1969) Open field behaviour in the rat: what does it mean? Ann. N.Y. Acad. Sci. 159, 852-859.
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MARTi
and Louis GARCIA-SEVILLA
Edmunds S. G. (1977) Extraversion, neuroticism and different aspects of self-reported aggression. J. Person. Assess. 41, 6670. Eysenck H. J. (1957) Drugs and personality--I. Theory and methodology. J. ment. Sci. 103, 119-131. Eysenck H. J. (1977) Crime and Personality, 3rd edn. Routledge & Kegan Paul, London. Eysenck H. J. (Ed.) and Broadhurst P. L. (1964) Introduction. In Experiments in Motivation. Pergamon Press, Oxford. Frost B. P. (1970) A note on extraversion and aggression. Wesrn Psycho\. 1, 11 l-l 12. Garcia-Sevilla L. (1974) Extincio de RFSO, inhibicio i personalitat en rates ma&es Wistar. Unpublished Doctoral Thesis, Autonomous University of Barcelona, Spain. Garcia-Sevilla L. (1984) Extraversion and neuroticism in rats. Person. indiuid. DiB: 5, 51 i-532. Garcia-Sevilla L. and Garau A. (1978) Extraversion y deambulacibn de la rata en el Campo abierto. Reufa lat.-am. Psicol. 10, 21 l-222. Coma M. (1980) Validation de medidas conductuales en el test Campo abierto. Reufa Psicol. gen. apl. 35, 447-455. Hall C. S. (1934) Emotional behaviour in the rat--I. Defecation and urination as measures of individual differences in emotionality. J. camp. physiol. Psycho/. 18, 385-403. Hall C. S. (1936) Emotional behaviour in the rat--III. The relationship between emotionality and ambulatory activity. J. camp. Psycho/. 22, 345-352.
Hall C. S. and Klein S. J. (1942) Individual differences in aggressiveness in rats. J. camp. Psychol. 33, 371. Hammour H., Goldsmith J. F. and Brain P. F. (1982) Effects of sensory communication on development of “isolationinduced” aggression in laboratory mice. Aggressive Behav. 8, 133-136. Harrington G. M. (1972) Strain differences in open field behaviour of the rat. Psychonom. Sci. 9, 285-286. Karli P., Vergnes M., Eclancher F., Schmitt P. and Chaurand J. P. (1972) Role of the amydala in the control of mouse-killing behaviour in the rat. In The Neurobiology of the Amigdalu (Edited by Eleftheriou B. E.), pp. 553-580 Plenum Press, New York. Karh P., Eclencher F., Vergnes M., Chaurand J. P. and Schmitt P. (1974) Emotional responsiveness and interspecific aggressiveness in the rat: interactions between genetic and experiential determinants. In Genetics of Behauiour (Edited by van Abeelen J. H. F.). North-Holland. Amsterdam. Knutson and Hynan (1973)‘Predatory aggression and irritable aggression shock-induced fighting in mouse-killing rats. Phvsiol. Behav. 11. 113-I 15.
Kom J. H. and Moyer K. E. (1968) Behavioral effects of isolation in the rat: the role of sex and time of isolation. J. gener. Psychol. 113, 263-273.
Lester D. (1967) Exploratory behaviour of dominant and submissive rats. Psychonom. Sci. 9, 285286. Lester D. and Cheses K. T. (1968) Effects of deprivation upon aggression in rats. Psycho/. Rep. 22, 1129-I 133. Marti A. (1977) Conducta agressiva en les rates mascles Wistar: Difertncies individuals. Tesi de Llicenciatura, Facultat de Citncies Biologiques, Universitat de Barcelona, Espafia. Novakova V., Flandera V. and Sandritter W. (1974) Aggressive rats: some properties of learning, memory and of the limbic __ system. Pharmac. Biochem. Behav. 2, 129-733.. Ruskin R. S.. Davis G. G. and De Peralta (1975) The relationshin between emotionalitv and dominance in the hooded \ rat. J. gen. psychol. 92, 53-58. Scott J. P. and Fredericson E. (1951) The causes of fighting in mice and rats. Psychol. Zool. 24, 273-309. Seward J. P. (1945) Aggressive behaviour in the rat-4 General characteristics: age and sex differences. J. coma. . Psvchol. . 38, 175-197. ’ -Svare B. B. and Leshner A. I. (1973) Behavioral correlates of intermale aggression and grouping mice. J. camp. physiol. I
Psycho/. 85, 203-210.
Thorne M., Patterson
A. S. and Topping J. S. (1975) Behavioral differences between killer and nonkiller rats. Bull.
psychonom. Sot. 6, 152-154.
Tobeiia A., Garcia-Sevilla L. and Garau A. (1982) Studies on an analogue of extraversion in the rat. Treb. Dept Psicol. Mid., Universitat Autbnoma de Barcelona, Espafia, No. 1. Valzelli L. (1967) Drugs and aggressiveness. Ado. Pharmac. 5, 79-107. Valzelli L. (1969) Aggressive behaviour induced by isolation. In Aggressiue Behauiour (Edited by Garattini S. and Sigg
E. B.). Excerpta-Medica, Amsterdam. Valzelli L. (1971) Aggressivite chez le rat et la souris: Aspects comportamentaux
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Valzelli L. (1975) Personal communication (Sept.). Valzelli L. and Garattini S. (1968) Behavioral changes and 5-hydroxytryptamine
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Vergnes M., Boehrer A. and Karli P. (1974) Interspecific aggressiveness and reactivity in mouse-killing and nonkilling rats: compared effects of olfactory bulb removal and raphe lesions. Aggressiue Behao. 1, I-16. Whimbey A. E. and Denenberg V. H. (1967) Two independent behavioural dimensions in open field performance. J. camp. physiol. Psychol. 63, W-504.
Yates A. J. (1973) Delincuencia, psicopatologia y criminalidad. In Terupiu del Comporfamiento. Ediciones Trillas, Mexico.
1985 Copyright
0
0191.8869185 $3.00 + 0.00 1985 Pergamon Press Ltd
INDIVIDUAL DIFFERENCES IN INTERSPECIFIC AGGRESSIVENESS: MOUSE-KILLING IN RATS AFTER ISOLATION ASSUMPCIOMART? and L~tis GARCIA-SEVILLA~ Departmentsof ‘ExperimentalPsychology and Psychophysiology and 2Medical Psychology, Autonomous University of Barcelona, Catalonia, Spain (Receioed
28 August
1984)
Summary-Measures of extraversion and neuroticism in rats are related to aggressive behaviour in two strains of rats. Isolated rats and rats reared together, of the Sprague-Dawley and Wistar strains, were submitted to an aggressiveness test. The results show that isolation generates and/or increases mousekilling behaviour only in Wistar rats which are more emotional (neurotic) than Sprague-Dawley rats. The two strains do not differ significantly in their open-field ambulation (extraversion), although Wistar rats tend to be less ambulatory. Within the Wistar strain, the results showed the same trend, that is, the more emotional and less ambulatory rats (dysthymics) are the ones who became killers after isolation. The Sprague-Dawley strain does not show any significant aggressive behaviour after isolation.
INTRODUCTION
Apart from sex, there are two variables that seem relevant to aggressive behaviour, i.e. extraversion-introversion and neuroticism-stability (Edmunds, 1977). According to Eysenck (1957, 1977) extraverts would show antisocial behauiour, i.e. aggression, more easily than introverts. He also postulates that neuroticism acts as a drive that would reinforce extraverts’ inclination to antisocial behaviour. Some other researchers (Buss, 1960; Edmunds, 1977) have corroborated these observations; however, Frost (1970) found that extraversion did not correlate significantly with aggression variables (other than assertiveness). In animal research, Broadhurst (1957, 1960) starting from the works of Hall (1934, 1936) has validated open-field (OF) defecation in rats as a measure of emotionality, being an analogue of neuroticism in humans (Broadhurst, 1960; Eysenck and Broadhurst, 1964). The OF standardized by Broadhurst (1957) puts the animal in a very stressful situation in order to measure its emotionality. Using a not so frightening OF (lower intensity of sound), ambulation becomes a measure which is independent of defecation and is a good animal index of extraversion (Garcia, 1974; 1984; Marti, 1977). The relation between OF ambulation and the aggression shown by the animals seems clear, but the relation between the latter and the OF defecation is being questioned: Novakova, Flandera and Sandritter (1974) have reported a variety of behavioural differences that could be summarized in terms of their distinction between excitable and non-excitable rats. Thus, killer rats, (excitable type) were found to be less able to habituate exploratory behaviour and to exhibit more horizontal activity in an exploration test. Other authors (Vergnes, Boehrer and Karli, 1974; Thorne, Patterson and Topping, 1975), have reported that killer and non-killer rats do not differ in terms of ambulation in the OF. But Thorne et al. (1975) indicated that the difference in rearing behaviour shown in the OF test could be interpreted as indicating that killers have a greater tendency to explore. On the other hand, Lester (1967) and Lester and Cheses (1968) reported that dominant rats show a greater exploratory trend than submissive ones. Brain and Nowell (1969) demonstrated a significant positive correlation between OF ambulation and the composite Aggression score for isolated male albino mice. We mention these results because mouse-killing behaviour in rats may represent not predatory aggression but something very similar to conspecific attack (Blanchard and Blanchard, 1977). The possibility of an aggressive component, as opposed to a predatory one, in 419
480
ASSUMPCIO
MAwi
and
Lwis
GARCIA~EVILLA
a rat’s attack on mice is further indicated by some reports (Barr, Gibbons and Moyer, 1975). Mouse-killing in rats may be a different aggressive response than inter-male fighting, but the similarity in conditions which initiate these two kinds of aggression suggests that a common mechanism is involved in both. If so, these two behaviours should be correlated. That is, animals that are mouse-killers should also be the most vigorous inter-male fighters (Bowers, 1979). In relation to the measure of defecation, Knutson and Hynan (1973) and Thorne et al. (1975) did not find differences between killer and non-killer rats. But, Bowers (1979) found a correlation between mouse-killing and a conditioned emotional response that suggests that aggressive rats are more emotionally responsive and more fearful than less aggressive rats. This conclusion is supported by Vergnes et al. (1974) who found that mouse-killing rats were more emotional in an OF situation than other rats. Valzelli (1969) also indicated that the greater or lesser susceptibility to become aggressive after a suitable period of isolation is probably linked to the different degree of basic emotionality of the strains considered. On the other hand, the results reported by Billingslea (1941), Hall and Klein (1942), Broadhurst (1958) and Ruskin, Davis and De Peralta (1975) indicate that the less emotional rats are the most aggressive. But the results obtained by Brain and Nowell (1969) and Svare and Leshner (1973) on isolated mice indicate a positive correlation between OF defecation and the composite Aggression score. Later, Brain and Nowell (1970) obtained Defecation scores placing the animal into the aggression tank, and there was no demonstrable relationship between defecation and the composite Aggression score. All these contradictory results may indicate some methodological differences, analyses of different types of aggressive behaviour or individual differences in the Ss used. Sex is a very important variable we have to take into account when measuring aggressive behaviour in animals, but we must not forget the role of the type of strain when working with rodents. Seward (1945) Scott and Federicson (1951) and Valzelli (1967, 1971, 1975), have observed that both female mice and female rats, no matter which strain they came from, are not aggressive except during the ‘post-partum’ period, and when deprived of food and water. It seems well-established (review by Brain, 1975) that aggressive behaviour can be induced in laboratory rodents by individual housing, i.e. isolation (Hammour. Goldsmith and Brain, 1982). This method is easy to use, steady in its effects and produces a stable and lasting behaviour pattern (Valzelli, 1971). The objective of the present study is to examine individual differences in the killing behaviour of rats after being isolated, in relation to individual differences in a low-frightening OF, excluding the sex variable in this study. Our expectations are: (1) if OF defecation is a measure of neuroticism in rats, and if neuroticism is related to aggressive behaviour, then social isolation will increase and/or generate killing or aggressive behaviour in the most reactive rats; (2) if OF ambulation is a measure of extraversion, and if extraversion is related to aggressive behaviour, then isolation will increase and/or generate killing or aggressive behaviour in the most ambulatory rats. METHOD
AND PROCEDURE
Subjects Subjects were 66 naive male Sprague-Dawley rats from Charles River Breeding Laboratories and 75 naive male Wistar rats from the Morini Laboratories. They were 90 days old at the beginning of the experiment. Their weight was about 200-300 g, just the weight they have at the time of sexual maturity. The mice used in the aggression test were males of the Swiss strain. All rats were housed in plastic cages of 524 x 274 x 150 mm with ad libitum access to food and water. They had a light and dark circadian rhythm of 12 hr, the temperature was regulated between 22 + 2°C and the humidity between 40 and 60%. OF test This apparatus was similar to that described by Broadhurst (1960). It consists of a circle of 81.5 cm dia and 33.5 cm high. Its floor is made of plywood and has three concentric circles divided
Mouse-killing
into 19 sections a 200 W lamp, Broadhurst one, be heard, which
in rats after isolation
481
marked in pencil having the same area each. The source of light is provided by hanging 120 mm above floor level. To have a less-stressful OF test than the we administered this test in silence. Only the sound of an air-conditioner could rats normally hear in their home-cages.
Aggression test
The measure used was the categorization of the rat’s behaviour confronted by a mouse introduced in its cage, this mouse being an intruder. The categories of Valzelli (1971): muricide, amicable and indifferent were used. As was the method of Svare and Leshner (1973) to measure the aggressive behaviour among mice. The latter was adapted to our Ss as they were rats, not mice. Procedure
Once the Ss were in our laboratory and after 4 days of adaptation, the OF test was administered to each rat. The procedure was similar to that used by Broadhurst (1960): 4 days of testing (at the same hour) and for 2 min/day. The rat was placed in the middle of the OF floor and the number of floor units entered by the animal was scored (i.e. ambulation) and so was the number of faecal boluses (i.e. defecation). Immediately after each testing, the OF was cleaned to prevent any modification in behaviour from the odour of the previous animal. At the end of the fourth OF session, Ss (33 rats of the Sprague-Dawley strain and 54 of the Wistar strain) were housed individually in cages of 524 x 274 x 150 mm and placed in an isolated room to have adequate social deprivation. Control rats (33 of the Sprague-Dawley strain and 21 of the Wistar strain) were housed in cages of the same shape but in groups of 5; so we had three groups of 5 and one of 6 for the 21 control rats of the Wistar strain, and five groups of 5 and two of 4 for the 33 control rats of the Sprague-Dawley strain. The period of isolation was 6 weeks; then the test of aggressivity was administered, for 10 min and on 3 consecutive days. A mouse was introduced into the cage, all the rat’s responses and their frequency were observed-licking, approaching, uncoordinated hyperactivity, picking up, jumping, biting. Control rats had the same treatment after 6 weeks of living together; they were tested individually, removing the rest of the animals and a mouse was introduced into each cage.
RESULTS
There is no significant correlation between ambulation and defecation in the OF test, in both strains of rats (Table 1). The reliability coefficients reported by Broadhurst (1960) are also given in Table 1. Ambulation from Wistar rats (W = 103.9, SD = 42.8) was lower than ambulation from Sprague-Dawley (R = 113.5, SD = 42.8) animals, the difference not being significant [t(139) = - 1.33, NS]. Wistar rats showed a higher level of defecation (r = 14.6, SD = 8.3) than the Sprague-Dawley animals (8 = 11, SD = 7.1), the difference being significant [t(139) = 2.78, P < 0.011. Table 2 indicates the percentage of rats belonging to each category, control and isolated groups of Wistar and Sprague-Dawley strains, and also shows killer (muricide) and non-killer (amicable and indifferent) rats after isolation for both strains. Isolation only produced killer behaviour in the Wistar strain, the difference being significant [x’(l) = 12.21 P < O.OOOS]compared to Table I. Measures (I, SD) taken in the OF, and their inter-correlations reliabilities Wistar Ambulation Defecation I (ambulation+lefecation)
SoranutDawlev
103.9 (42.8) 14.6 (8.3) -0.0216
113.5 (42.8) 11.0(7.1) 0.2515
0.6764 0.4383
0.5191 0.5007
Reliability
Ambulation Defecation
and
AWJMPCIO MARTYand
482
Louis GARCIA~EVILLA
Table 2. Percentages of rats belonging to each category; control and isolated groups of both strains Sprague-Dawley
Wistar Isolated
Control
Table
Isolated
0 73 27
26 63 II
0 62 38
Muricide Amicable Indifferent
Control
0 55 45
3. Pearson correlation between three variables: defecation and aggressive behaviour Wistar Control
Ambulation Defecation
-0.1023 0.031
I
ambulation,
Sprague-Dawley Isolated
Control
Isolated
-0.2944’ 0.2715’
0.0208 0.0421
-0.1084 -0.1891
lP < 0.05.
Table 4. Measurement of aggressive behaviour using the procedure of Svare and Leshner (1973) for the control and experimental groups of both strains (r-values) Wistar
Control Isolated z
Sprague-Dawley
R
SD
R
SD
t
2.1 29.2
1.58 18.43
6 4.1
3.61 2.66
3.9 6.57
-6.51 0.001
P<
0.001 0.001
0.002 2.51
Sprague-Dawley rats. In the Wistar strain the killer rats are not different from the non-killer ones in ambulation, although they tend to appear more defecatory [t(52) = 1.46, P < 0.11. To quantify the aggressive behaviour we gave different scores to the behaviour showed by the rat faced with a mouse, as follows: 0.5 of a point (approaching and licking the mouse), 1 point (uncoordinated hyperactivity and picking up), 2 points (jumping at and biting it). Killer and non-killer rats differed significantly in all these patterns, Table 3 shows the results obtained with a Pearson correlation between aggressive behaviour and the OF measurements: post-isolation, the Wistar strain shows a positive and significant correlation with defecation and a negative one with ambulation. Finally, Table 4 summarizes the results obtained using these scores. In the Sprague-Dawley strain, the control rats have the highest scores, but this trend is inverted as an effect of isolation. DISCUSSION
Defecation and ambulation in the OF test have proved to be reliable and independent measures, as was expected from a low-frightening OF, and in our view (Garcia-Sevilla, 1984) they can be considered as measures of neuroticism (defecation) and of extraversion (ambulation). The socio-environmental isolation to provoke aggression was not effective with the Sprague-Dawley strain, which confirms the results of other investigations (Korn and Moyer, 1968). These differences between strains in post-isolation aggression have been attributed to the different strains’ emotionality (Valzelli and Garattini, 1968). In this sense, our results confirm this expectation, because the strain which proves to be aggressive after isolation, the Wistar strain, is more defecatory in the OF than Sprague-Dawley rats. On the other hand, the Wistar strain, tends (Table 1) to be less ambulatory than the Sprague-Dawley strain. In support of our hypotheses, only the relation between neuroticism (defecation) and postisolation aggressive behaviour appears, both between strains (Table 2) and within the strain affected by isolation, i.e. Wistar (Table 3). Therefore, the more defecatory strain (neurotic) is the one that shows aggression, and within this strain the correlation between defecation and aggressive behaviour is positive and significant. On the other hand, our results in relation to ambulation (extraversion) do not confirm our hypothesis.
Mouse-killing
in rats after
isolation
483
We expected that the more ambulatory rats (extraverts) would more easily become aggressive. But the Wistar strain, the one that turns aggressive, tends to be less ambulatory, and within this strain the correlation between ambulation and aggressive behaviour is negative and significant, just the opposite of what was expected (Table 3). It is as if the critical variable was the magnitude of the aversive situation in the production of aggression through socio-environmental isolation, and this magnitude would affect the dysthymic (neurotic introvert) rats. Among humans there is some evidence that introverted neurotics, with an inadequate personality, when repressed tend to commit murder within the family because they cannot cope with the frustration (Eysenck, 1977). In both cases, familial murderers and mouse-killing rats, there is a build up of frustration and aggression which finally causes the human, or the animal, to perform the aggressive act. A general explanation for our results could be obtained by applying the model of emotional aggression (Buss, 1960). This type of aggression implies a social behaviour, approaching, and a drive, anger. Approaching and exploring would be extravert behaviours and the anger an emotional state, both being necessary to produce emotional aggressive behaviour. Note that control Sprague-Dawley rats are friendly and amicable, according to Valzelli’s classification (Table 2), and more aggressive than control Wistar (Table 4), although Sprague-Dawley control rats cannot be considered truly aggressive as none of them became a killer; in fact, what we obtained was that they approached the mouse (licking, picking up, . . . ), i.e. they showed approaching social behaviours. In fact, social deprivation only produces a slight modification towards indifference in the behaviour shown by the Sprague-Dawley rats. Karli, Vergnes, Eclancher, Schmitt and Chaurand (1972) suggested that there are different motivational states which may express themselves in different kinds of aggressive behaviour. Subsequently, Karli et al. (1974) indicated, in the same sense, that changes in emotional reactivity brought about by early social interactions or by early handling do not necessarily affect all kinds of aggressive behaviour in the same way and it seemed likely to them that low emotional reactivity can reduce the probability that aversively-motivated aggression is elicited, while facilitating the elicitation of an appetitively-motivated aggressive behaviour. Because of this, it is not surprising that in our case, where social isolation (social deprivation) is an aversive situation, the Wistar strain would be the one that shows killing behaviour. It is also within this strain, that a greater tendency to show attack behaviour in rats with higher Defecation scores is observed. The results of Billingslea (1941), Hall and Klein (1942) and Ruskin et al. (1975), which showed a negative correlation between Emotivity and Aggressivity scores, could be explained if we assume that attack displayed by an isolated rat faced with a mouse is an aggressive behaviour different from the attack shown by the rat faced with another rat when the former has not suffered the aversive situation of isolation. Correspondence-All
reprint
requests
should
be addressed
to L. Garcia-Sevilla.
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