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Habituation of object contact in socially-reared and isolated rats (Rattus norvegicus)
Anim. Behav., 1976, 24, 415-420
HABITUATION OF OBJECT CONTACT IN SOCIALLY-REARED AND ISOLATED RATS (RA TTUS NOR VEGICUS) BY D O R O T H Y EINON & M I C H A E L M O R G A N
The Psychological Laboratory, University of Cambridge, Cambridge CB2 3EB Abstract. Rats reared in social isolation were found to contact fewer novel objects in an open-field than their socially reared litter mates. They also contacted a smaller variety of objects, and contacted them in different ways. Social animals showed more manipulatory behaviour than the isolates, but there were no differences in sniffing. In a second experiment, employing a longer session, it was found that social animals showed more rapid habituation of object contact. This may account for previous claims that isolates show heightened levels of exploration. Social play is an outstanding feature of the development of laboratory rats (Baenninger 1967) and also of wild Rattus norvegicus (Barnett 1963) and Rattus rattus (Ewer 1971). It is usually assumed (e.g. Welker 1961; EiblEibesfeldt 1967) that social play has a functional significance in development, but the nature of this function in the case of the rat is largely unknown. As Barnett (1963, p. 80) noted ' . . . there is a special need for work on the effects on behaviour of social deprivation'. The present paper is a continuation of a previous study of this problem (Morgan 1973) in which it was reported inter alia that social isolation has pronounced effects upon open-field activity in the laboratory rat. It has frequently been claimed that laboratory rats reared in enriched conditions differ in exploratory activity from impoverished rats. However, it is not clear whether the enriched rats are more (Luchins & Forgus 1955; Gill, Reid & Porter 1966) or less (Lore & Levowitz 1966; Syme 1973) exploratory than their impoverished counterparts. There are two major causes of confusion. First, different kinds of 'impoverishment', such as social isolation, and object deprivation, may have very different effects upon adult behaviour (Morgan 1973); and second, different measures of 'exploration' may give entirely different results. For example, socially isolated rats are slow to emerge from a small enclosure into a novel environment, and might be judged on this evidence to be less exploratory: but when placed directly into an open field they are typically more active than social animals (e.g. Lore & Levowitz 1966). Before advancing general conclusions about 'exploration', it is clearly desirable to supplement these findings with more detailed observation of behaviour. The present report is concerned
with yet another aspect of behaviour in a novel situation: the extent to which the animals make contact with objects, and with the kinds of ways in which they contact them. One previous study of object contact (Lore & Levowitz 1966) showed that socially isolated rats spent more time in contact with objects in an open field. It is typical of the confusiov in this area that McCall, Lester & Dolan (1969) failed to find any differences. Neither group of investigators report data about the mode of contact, yet a 'contact' may represent behaviours as various as sniffing and manipulation. The length of time during which the behaviours are permitted to wane may also be an important variable. A previous study of locomotor activity in an open field (Einon, Morgan & Sahakian 1975) has shown that the decrement in activity over time is much less marked in isolates than in socially reared rats. In the present experiments we have specifically looked for qualitative differences in behaviour between the animals, and for possible changes in behaviour over time.
Experiment 1 Methods The subjects were twenty-four socially reared rats (twelve males, twelve females) and twentyfour littermates reared in social isolation (also twelve male and twelve female). The pups were the offspring of pregnant hooded Lister females obtained from Animal Suppliers Ltd. At 17 days of age, the rats were weaned and the isolates were placed individually into plastic, wire-top cages (North Kent Plastics, NKP-M2; 33 • 15 • 13 cm). The social animals were placed in groups of three or four in larger plastic and mesh cages (NKP-RB1 ; 45 • 28 • 22 cm). At 50 days of age all isolates were transferred to the same kind of cages as the social rats, 415
416
ANIMAL
BEHAVIOUR,
viz. NKP-RB1. They continued to be housed in social isolation, but the RB1 cages permitted the animals to view one another, which was not possible in the M2 cages. Since at the time of testing (60 days) the cages of the social and isolated animals were the same size, a confounding feature in these experiments was the amount of space available per rat. However, reasons were given in an earlier paper (Morgan 1973) for thinking that this variable is not of crucial importance; and in a recent study (Morgan, Einon & Nicholas 1975) we have found differences between social and isolated animals when the former were reared in larger cages (NKPGPR4; 56 x 30 x 18 cm) than the isolates. Therefore, in the present paper, we shall refer to the social variable as being probably the more important. Details of the measures taken to protect the weanlings' health in the first few days will be found in Morgan et al. (1975). At 45 days o f age the rats were tested in the open field without objects. The test reported here took place at 60 days of age. The open field measured 76.2 cm x 76.2 cm and was constructed of Bakelite, with a steel-rod floor. The walls were 40 cm high and were covered with a mid-grey oil cloth. The bars of the floor were 0.6 cm in diameter and 0.6 cm apart. The field was lit by a 40-W light placed 50 cm above and to one side of the field. To minimize external cues the experimenter sat behind the light. The open field, illustrated in Plate IV Fig. 1, contained the following objects: a 10-cm plastic flower pot; a small cardboard tube, 9 cm in diameter, 12 cm long; a long Bakelite tube 9 cm in diameter, 25 cm long; the lid of the NKP-M2 mouse cage. All these objects could be entered by the rats; the mouse lid could also be climbed. Other objects that could be climbed were a cylindrical mesh food hopper which was placed upside down, and a food dish. The remaining objects could all be moved: two pieces of crumpled paper, a ball of cotton wool, a whistle from a kettle, a 10-cm diameter plastic ball with a hook on one side, and a small 5-cm diameter ring. The flower pot and the small tube could also be moved by the animals. Objects were placed in specific positions in the open field, (see Plate IV Fig. 1). Animals were placed beside the central food hopper, and remained alone in the field for 7 rain. They were then removed to their home cage. Records were taken for the first 3 min and last 3 min of this period.
24, 2
A record was kept of all objects contacted by the animals, and their mode of contact, using the following classification: (1) Touching by any part of the body except paws and nose; (Usually backing into objects, but including walking over objects without stopping or sniffing.) (2) Nose contact; (3) Paw contact; (4) Entering the object; (5) Climbing; (6) Moving the object. Records were also taken of 'rearing up' onto hind paws. Results The median number of total contacts made by each group of animals, and the median values of each kind of contact, are shown in Table I. An Analysis of Variance carried out on total contacts revealed that rearing condition (social versus isolate) was a significant factor (F---= 46.14; d f = 1, 22; P = 7.97 x 10-7). Sex was not a significant factor ( F = 0.525; d f = 1, 22; P ---- 0.426). In an analysis of variety o f contacts, rearing condition was again a significant factor ( F = 32.4; df-----1, 22; P = 9.9 x 10 -6) and sex was again non-significant (F = 0.018; d f = 1, 22; P = 0.89). An analysis was also undertaken to see if there was a significant difference between the two timesamples in total contacts, with the result that both time-samples (F = 9.5; df-= 1, 66; P = 0.0048) and rearing condition (F = 51.1; df= 1, 22; P = 3-62 x 10-7) emerged as significant main effects. The time-sample effect arises because there were fewer contacts in the second sample than the first. There was no interaction between time-samples and rearing (F = 0.887; df---= 1, 66; P = 0.35), i.e. the social and isolated animals seemed to have habituated at the same rate within the time period of this experiment. Subsequent analysis was carried out by M a n n Whitney U-tests (Siegel 1956) rather than t-tests, because of the considerable inhomogeneity of variance between the samples (which also argues for caution in interpreting the results of the Analysis of Variance). The conservative criterion of 0.02 was chosen to allow for the fact that multiple comparisons were being made (Jones & Fiske 1953). The results of such pair-wise comparisons will be seen in Table I. It was found that social rats 'reared-up' significantly more than isolates. The social rats not only made more contacts, but contacted a greater variety of objects. Social rats contacted more objects with their paws, but there were no significant differences in other modes of contact. Social rats also moved more objects.
EINON & MORGAN: ISOLATION AND OBJECT CONTACT Table 1. Experiment 1: Median Object Contact and Mode of Contact by Socially Reared and Isolated Rats in an Open Field in a 6-Min Sample
Rearing Measure
Social Isolates
Number of object contacts
96
Variety objects contacted
11
Touching Nose contact
6.5
49
Probability (P) < 0-005
7"5
< 0-001
6"0
0.764
21 "5
19
0"680
Paws
7
13
< 0-005
Entering
6
6
0.666
Climbing
9
2-5
< 0-001
Moving
9
1-5
< 0-001
R.earing-up
4
I
< 0-001
The social rats contacted more objects, (z = 3, P = 0-0026) and a greater variety of objects (z = 6, P = 0.00006). There were no significant differences in the number of objects contacted by touching (z = 0.3, P = 0.764), with the nose (z = 0.31, P = 0.680) or in the number of objects entered (z = 0.43, P =0.666). But social rats contacted more objects with the paws (z = 2.83, P-----0.0046), climbed more objects (z = 4, P = 0.00006), and moved more objects (z = 5, P = 0.00006). Discussion
The increased 'rearing-up' of the social animals offers some support to the report by McCall et al. (1969) that social animals are more influenced by external stimuli. The present results do not agree with Lore & Levowitz's (1966) finding that isolated animals contacted more objects than socially-reared animals. On all measures in which one group was superior to the other it was the social animals which showed this superiority. They contacted a greater number and variety of objects, and contacted them in more complex ways. The two groups did not differ in the amount of non-manipulatory contact (touching, entering and nosing objects) but social animals were superior on all measures of manipulatory contact. These results suggest that isolated animals are not more exploratory.
417
The reason for the discrepancy between the present results and those of Lore & Levowitz is not altogether clear, but is probably due to one or more of the procedural differences between the two experiments. In Lore & Levowitzs' experiment animals were exposed to fifteen objects in a box which was less than half the size of the present field. Ten of their objects were small: nuts and bolts, for example. Although Lore & Levowitz measured contact time, number o f objects contacted can be assessed from their data: social animals contacted on average thirty-three objects per session, isolates forty. Considering that sessions were 15 rain long, these figures represent far fewer contacts than were made in our 6-rain experimental sessions, (ninety-six for social animals, forty-nine for isolates). Difference in both session-length and number of contacts suggests that one possible explanation for the lack of agreement between the two experiments might be that isolates habituated more slowly than socially-reared animals. Perhaps in Lore & Levowitzs' 15-min sessions the social animals had time to habituate to the situation, and thus made fewer contacts over the entire session. To investigate this possibility, we carried out a second experiment, in which habituation of object contact was observed over 30 min. Experiment 2 Methods
Rats from six litters, (eighteen females, two males), which had been bred in the laboratory, were weaned at 17 days and assigned to the two rearing conditions employed in the previous experiment. A split-litter design was employed. Social animals were raised in groups of four or five; the single social male animal was housed with three male litter mates. As in the first experiment animals were housed in standard NKP-RB1 cages (45 • 28 x 22 c m ) t h r o u g h o u t the experiment. Object contact was examined when the animals were 60 days old. All animals had previously been exposed to the open field without objects when 45 days old. Rearing conditions were as in the previous experiment. Apparatus and procedure were as in the previous experiment except that the rubber ball was replaced by a small plastic bottle of approximately the same size, and sessions were of 29 min duration. Three 3-min samples were taken: the first 3 rain, 13 to 16 min, and 26 to 29 rain. Animals spent intersample intervals in the open field.
418
ANIMAL
BEHAVIOUR
Results
The number of object contacts made in each of the time samples is shown graphically in Fig. 2, separately for social and isolated rats. Table II presents the modes of contact. It appears that in the first sample, as in experiment 1, social rats made more contacts: but they showed more rapid habituation o f contacting with the result that in the remaining time-samples they made fewer contacts than the isolates. An Analysis of Variance showed that the only significant effects were those of timesamples ( F = 43-8; df= 2, 36; P = 2.2 • 10-10 ) and the rearing condition by time samples interaction ( F = 23.70; df= 2, 36; P = 2 . 7 • 10-7). There was no significant main effect of rearing condition ( F = 2.195; df= 1, 18; P = 0.155). Mann-Whitney U-tests confirmed these effects. The social animals made significantly more contacts in the first time-sample (U = 18; P < 0.02) but significantly fewer in the second sample (U = 17). The difference in the third sample does not meet the criterion of significance we are using (U = 22; P = 0.05).
24,
2
this occurred much more slowly. The difference in the rate of habituation may well explain why Lore & Levowitz (1966) found that isolated animals contacted more objects in their 15-min sample. The finding that isolated animals differ in the rate at which they habituate is in agreement with the finding that these same animals show a slower decline in activity over time in an objectfree open field (Einon, Morgan & Sahakian 1975). The fact that isolated animals are slower to habituate in both a simple and complex environment argues against Zimbardo & Montgomerys' (1957) suggestion that the difference between deprived and enriched animals may be partially a function of the degree of novelty of the exploratory field. The underlying assumption of such a hypothesis is that exploration should be an increasing function of the degree of discrepancy between a familiar standard and a new stimulus up to a point, after which greater magnitudes of discrepancy
Discussion
Initially, the socially reared animals contacted more objects, but the number of contacts they made declined quite rapidly with time. Isolated rats contacted fewer objects initially, and although they showed some decrement with time,
.
.
.
.
.
social isolate
Table H. Experiment 2: Median Object Contact and Mode of Contact by Socially Reared and Isolated Rats in a Open Field in the first 3-Min Sample "o
Rearing Measure
Social Isolates
\,,
2o
Probability (P) o
Number of objects contacted
46
34
< 0'02
Variety objects contacted
11
9
< 0.10
0
< 0,10
Touching
"6 o
0"3
\,
o
\
e~
Nose contact
19
19
< 0.10
Paws
13
6
< 0.05
E
\
Z
Entering
2-5
2
< 0.10
Climbing
7
2
< 0.02
Moving
1.5
1
< 0.10
Rearing-up
3
0
< 0.02
0
I Time
2
3
Sample
Fig. 2. Results of experiment 2: the median object contacts made by socially-reared and isolation-reared rats in three successive 3-rain samples. The rats were in the open field for a total of 29 min. The first time-sample was from the first 3 rain, the second from minutes 13 to 16, and the last from minutes 26 to 29.
EINON & MORGAN: ISOLATION AND OBJECT-CONTACT will produce less and less exploration. The problem, as with all inverted U-shaped functions, is that it is virtually impossible to make a priori predictions about the degree of novelty that will induce less exploration. Perhaps neither the open field nor the object-filled field represented this degree of novelty for the isolated animals. I t is in any case rather difficult to assess from the present experiment which group of animals is more 'exploratory'. Leaving aside the differences in mode of contact, we have two measures of exploration: number of objects contacted, and the habituation of contact. On the former measure the isolated animals are less exploratory, while on the latter measure they are more exploratory: predictions from a discrepancy hypothesis of exploration, (Zimbardo & Montgomery 1957; Dember & Earl 1957) are unclear in such types of situations. The hypothesis deals mainly with choice behaviour, and has been validated in situations which involve choice. Since it is known that choice measures do not necessarily correlate with measures of vigour (Stanley 1952; Mackintosh 1963) there seems little reason to suppose they are better correlated with activity or rate of habituation. There is obviously no very simple explanation of the various effects produced by isolation: isolates are slower to habituate but clearly are also deficient in other respects. The social animals placed in the object-filled field produced a behavioural strategy that involved the gradual exploration of the whole field. They tended to approach objects, to sniff them, place one paw, sniff and then perhaps climb or move the object. I f they 'accidentally' moved an object they would stop, retreat, then reapproach. The isolated animals tended to walk around objects, tO stop and sniff and then move on: there was nothing very systematic about their behaviour, as we may see from the fact that they manipulated a smaller variety of objects. The majority of the social animals made contact with all objects in the open field. We suggest, therefore, that the differences between socially reared and isolated rats in a novel environment are not profitably described in terms of a simple ' e x p l o r a t i o n ' hypothesis. Rather, the differences seem to depend upon rate of response waning and upon the precise details of the way in which the animals expose themselves to novel stimulation. We have previously described the waning of activity in the open field as 'habituation', on the grounds that there is a recovery after an interval of time
419
outside of the apparatus (Einon, Morgan & Sahakian 1975). In this sense of the word, isolates could be said to show slower 'habituation'. However, as Hinde (1970) points out, a response decrement occurring as a result of repeated or continuous presentation, can only be called habituation 'with certain limitations', and few of the limitations described by Hinde apply to the process observed in the present experiments. We do not know, for example, whether there would be recovery of activity in the social animals if the objects were changed, and, therefore, it cannot be asserted that the response decrement is situation-specific; Thus the suggestion that isolates habituate less readily in a novel situation than social rats should be viewed simply as a rather gross description of a behavioural difference, rather than as a precise suggestion about the mechanism of the difference. It does, however, seem to be of greater value than a description of the isolates as more 'exploratory', since the latter description fails to include changes in behaviour over time, and cannot suggest why different measures of 'exploration' have given such different results. REFERENCES
Baenninger, L. (1967). Comparison of behavioural development in socially isolated and grouped rats. Anita. Behav., 15, 312-323. Barnett, S. A. (1963). A Study in Behaviour: Principles of Ethology and Behavioural Physiology Displayed Mainly in the Rat. London: Methuen.
Dember, W. N. & Earl, R. W. (1957). Analysis of exploratory, manipulative and curiosity behavior. Psychol. Rev., 64, 91-96. Eibl-Eibesfeldt, L (1967). Concepts of Ethology and human behavior. In: Early Behavior: Comparative and Developmental Approaches (Ed. by H. W. Stevenson, E. H. Hess & H. L. Reinegold), pp. 137-141. New York: John Wiley. Einon, D. F., Morgan, M. J. & Sahakian, B. J. (1975). The development of intersession habituation and emergence in socially-reared and isolated rats. Dev. Psychobiol., 8, 553-559. Ewer, R. F. (t971). The biology and behaviour of a freeliving population of black rats (Rattas rattus). Anita. Behav. Monogr., 4, 3, 127-174. Gill, J. H., Reid, L. D. & Porter, P. B. 0966). Effects of restricted rearing on Lashley stand performance. Psychol. Rec., 19, 239-242. Hinde, R. A. (1970). Behavioural habituation. In: Short-term Changes in Neural Activity and Behaviour (Ed. by G. Horn & R. A. Hinde). Cam-
bridge: Cambridge University Press. Jones, L. V. & Fiske, D. W. (1953). Models for testing the significance of combined results. Psychol. Bull., 50, 375-382. Lore, R. K. & Levowitz, A. (1966). Differential rearing and free versus forced exploration. Psychon. Sci., 5, 421-422.
420
ANIMAL
BEHAVIOUR,
Luchins, A. S. & Forgus, R: H. (1955). The effects of differential post-weaning environment on the rigidity of an animal's behavior. J. Genet. PsychoL, 86~ 51-58. Mackintosh, N. J. (1963). Extinction of a discrimination habit as a function of overtraining. J. comp. physioL PsychoL, 56, 842-847. McCall, R. B., Lester, M. L. & Dotan, C. G. (1969). Differential rearing and the exploration of stimuli in the open field. Dev. PsychoL, 1, 750-762. Morgan, M. J. (1973). Effects of post-weaning environment on learning in the rat. Anita. Behav., 21, 429--442. Morgan, M. J., Einon, D. F. & Nicholas, D. (1975). The effects of isolation rearing on behavioural inhibition in the rat. Q. JI. exp. PsychoL, 27, 615-634.
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2
Siegel, S. (1956). Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill. Stanley, W. C. (1952). Extinction as a function of the spacing of extinction trials. J. exp. PsychoL, 43, 249-260. Syme, L. A. (1973). Social isolation at weaning: Some effects on two measures of activity. Anim. Learning Behav., 1, 161-163. Welker, W. I. (1961). An analysis of exploratory and play behavior in animals. In: Functions of Varied Experience (Ed. by D. W. Fiske & S. R.. Maddi). Homewood, Illinois: The Dorsey Press. Zimbardo, P. G. & Montgomery, K. C. (1957). Effects of the 'free environment' rearing upon exploratory activity. PsychoL Rep., 3, 589-594.
(Received 26 March 1975; revised 16 June 1975; MS. number: 1417)
EINON & M O R G A N : ISOLATION AND OBJECT-CONTACT PLATE
IV
Fig. l. Plan view of the open field used in experiments 1 and 2. The position of objects in the field was the same at the start of each session, and the animal was always placed next to the food hopper in the centre of the field. The overall dimensions are 30 • 30 cm.
Einon & Morgan, Anim. Eekav., 24, 2
HABITUATION OF OBJECT CONTACT IN SOCIALLY-REARED AND ISOLATED RATS (RA TTUS NOR VEGICUS) BY D O R O T H Y EINON & M I C H A E L M O R G A N
The Psychological Laboratory, University of Cambridge, Cambridge CB2 3EB Abstract. Rats reared in social isolation were found to contact fewer novel objects in an open-field than their socially reared litter mates. They also contacted a smaller variety of objects, and contacted them in different ways. Social animals showed more manipulatory behaviour than the isolates, but there were no differences in sniffing. In a second experiment, employing a longer session, it was found that social animals showed more rapid habituation of object contact. This may account for previous claims that isolates show heightened levels of exploration. Social play is an outstanding feature of the development of laboratory rats (Baenninger 1967) and also of wild Rattus norvegicus (Barnett 1963) and Rattus rattus (Ewer 1971). It is usually assumed (e.g. Welker 1961; EiblEibesfeldt 1967) that social play has a functional significance in development, but the nature of this function in the case of the rat is largely unknown. As Barnett (1963, p. 80) noted ' . . . there is a special need for work on the effects on behaviour of social deprivation'. The present paper is a continuation of a previous study of this problem (Morgan 1973) in which it was reported inter alia that social isolation has pronounced effects upon open-field activity in the laboratory rat. It has frequently been claimed that laboratory rats reared in enriched conditions differ in exploratory activity from impoverished rats. However, it is not clear whether the enriched rats are more (Luchins & Forgus 1955; Gill, Reid & Porter 1966) or less (Lore & Levowitz 1966; Syme 1973) exploratory than their impoverished counterparts. There are two major causes of confusion. First, different kinds of 'impoverishment', such as social isolation, and object deprivation, may have very different effects upon adult behaviour (Morgan 1973); and second, different measures of 'exploration' may give entirely different results. For example, socially isolated rats are slow to emerge from a small enclosure into a novel environment, and might be judged on this evidence to be less exploratory: but when placed directly into an open field they are typically more active than social animals (e.g. Lore & Levowitz 1966). Before advancing general conclusions about 'exploration', it is clearly desirable to supplement these findings with more detailed observation of behaviour. The present report is concerned
with yet another aspect of behaviour in a novel situation: the extent to which the animals make contact with objects, and with the kinds of ways in which they contact them. One previous study of object contact (Lore & Levowitz 1966) showed that socially isolated rats spent more time in contact with objects in an open field. It is typical of the confusiov in this area that McCall, Lester & Dolan (1969) failed to find any differences. Neither group of investigators report data about the mode of contact, yet a 'contact' may represent behaviours as various as sniffing and manipulation. The length of time during which the behaviours are permitted to wane may also be an important variable. A previous study of locomotor activity in an open field (Einon, Morgan & Sahakian 1975) has shown that the decrement in activity over time is much less marked in isolates than in socially reared rats. In the present experiments we have specifically looked for qualitative differences in behaviour between the animals, and for possible changes in behaviour over time.
Experiment 1 Methods The subjects were twenty-four socially reared rats (twelve males, twelve females) and twentyfour littermates reared in social isolation (also twelve male and twelve female). The pups were the offspring of pregnant hooded Lister females obtained from Animal Suppliers Ltd. At 17 days of age, the rats were weaned and the isolates were placed individually into plastic, wire-top cages (North Kent Plastics, NKP-M2; 33 • 15 • 13 cm). The social animals were placed in groups of three or four in larger plastic and mesh cages (NKP-RB1 ; 45 • 28 • 22 cm). At 50 days of age all isolates were transferred to the same kind of cages as the social rats, 415
416
ANIMAL
BEHAVIOUR,
viz. NKP-RB1. They continued to be housed in social isolation, but the RB1 cages permitted the animals to view one another, which was not possible in the M2 cages. Since at the time of testing (60 days) the cages of the social and isolated animals were the same size, a confounding feature in these experiments was the amount of space available per rat. However, reasons were given in an earlier paper (Morgan 1973) for thinking that this variable is not of crucial importance; and in a recent study (Morgan, Einon & Nicholas 1975) we have found differences between social and isolated animals when the former were reared in larger cages (NKPGPR4; 56 x 30 x 18 cm) than the isolates. Therefore, in the present paper, we shall refer to the social variable as being probably the more important. Details of the measures taken to protect the weanlings' health in the first few days will be found in Morgan et al. (1975). At 45 days o f age the rats were tested in the open field without objects. The test reported here took place at 60 days of age. The open field measured 76.2 cm x 76.2 cm and was constructed of Bakelite, with a steel-rod floor. The walls were 40 cm high and were covered with a mid-grey oil cloth. The bars of the floor were 0.6 cm in diameter and 0.6 cm apart. The field was lit by a 40-W light placed 50 cm above and to one side of the field. To minimize external cues the experimenter sat behind the light. The open field, illustrated in Plate IV Fig. 1, contained the following objects: a 10-cm plastic flower pot; a small cardboard tube, 9 cm in diameter, 12 cm long; a long Bakelite tube 9 cm in diameter, 25 cm long; the lid of the NKP-M2 mouse cage. All these objects could be entered by the rats; the mouse lid could also be climbed. Other objects that could be climbed were a cylindrical mesh food hopper which was placed upside down, and a food dish. The remaining objects could all be moved: two pieces of crumpled paper, a ball of cotton wool, a whistle from a kettle, a 10-cm diameter plastic ball with a hook on one side, and a small 5-cm diameter ring. The flower pot and the small tube could also be moved by the animals. Objects were placed in specific positions in the open field, (see Plate IV Fig. 1). Animals were placed beside the central food hopper, and remained alone in the field for 7 rain. They were then removed to their home cage. Records were taken for the first 3 min and last 3 min of this period.
24, 2
A record was kept of all objects contacted by the animals, and their mode of contact, using the following classification: (1) Touching by any part of the body except paws and nose; (Usually backing into objects, but including walking over objects without stopping or sniffing.) (2) Nose contact; (3) Paw contact; (4) Entering the object; (5) Climbing; (6) Moving the object. Records were also taken of 'rearing up' onto hind paws. Results The median number of total contacts made by each group of animals, and the median values of each kind of contact, are shown in Table I. An Analysis of Variance carried out on total contacts revealed that rearing condition (social versus isolate) was a significant factor (F---= 46.14; d f = 1, 22; P = 7.97 x 10-7). Sex was not a significant factor ( F = 0.525; d f = 1, 22; P ---- 0.426). In an analysis of variety o f contacts, rearing condition was again a significant factor ( F = 32.4; df-----1, 22; P = 9.9 x 10 -6) and sex was again non-significant (F = 0.018; d f = 1, 22; P = 0.89). An analysis was also undertaken to see if there was a significant difference between the two timesamples in total contacts, with the result that both time-samples (F = 9.5; df-= 1, 66; P = 0.0048) and rearing condition (F = 51.1; df= 1, 22; P = 3-62 x 10-7) emerged as significant main effects. The time-sample effect arises because there were fewer contacts in the second sample than the first. There was no interaction between time-samples and rearing (F = 0.887; df---= 1, 66; P = 0.35), i.e. the social and isolated animals seemed to have habituated at the same rate within the time period of this experiment. Subsequent analysis was carried out by M a n n Whitney U-tests (Siegel 1956) rather than t-tests, because of the considerable inhomogeneity of variance between the samples (which also argues for caution in interpreting the results of the Analysis of Variance). The conservative criterion of 0.02 was chosen to allow for the fact that multiple comparisons were being made (Jones & Fiske 1953). The results of such pair-wise comparisons will be seen in Table I. It was found that social rats 'reared-up' significantly more than isolates. The social rats not only made more contacts, but contacted a greater variety of objects. Social rats contacted more objects with their paws, but there were no significant differences in other modes of contact. Social rats also moved more objects.
EINON & MORGAN: ISOLATION AND OBJECT CONTACT Table 1. Experiment 1: Median Object Contact and Mode of Contact by Socially Reared and Isolated Rats in an Open Field in a 6-Min Sample
Rearing Measure
Social Isolates
Number of object contacts
96
Variety objects contacted
11
Touching Nose contact
6.5
49
Probability (P) < 0-005
7"5
< 0-001
6"0
0.764
21 "5
19
0"680
Paws
7
13
< 0-005
Entering
6
6
0.666
Climbing
9
2-5
< 0-001
Moving
9
1-5
< 0-001
R.earing-up
4
I
< 0-001
The social rats contacted more objects, (z = 3, P = 0-0026) and a greater variety of objects (z = 6, P = 0.00006). There were no significant differences in the number of objects contacted by touching (z = 0.3, P = 0.764), with the nose (z = 0.31, P = 0.680) or in the number of objects entered (z = 0.43, P =0.666). But social rats contacted more objects with the paws (z = 2.83, P-----0.0046), climbed more objects (z = 4, P = 0.00006), and moved more objects (z = 5, P = 0.00006). Discussion
The increased 'rearing-up' of the social animals offers some support to the report by McCall et al. (1969) that social animals are more influenced by external stimuli. The present results do not agree with Lore & Levowitz's (1966) finding that isolated animals contacted more objects than socially-reared animals. On all measures in which one group was superior to the other it was the social animals which showed this superiority. They contacted a greater number and variety of objects, and contacted them in more complex ways. The two groups did not differ in the amount of non-manipulatory contact (touching, entering and nosing objects) but social animals were superior on all measures of manipulatory contact. These results suggest that isolated animals are not more exploratory.
417
The reason for the discrepancy between the present results and those of Lore & Levowitz is not altogether clear, but is probably due to one or more of the procedural differences between the two experiments. In Lore & Levowitzs' experiment animals were exposed to fifteen objects in a box which was less than half the size of the present field. Ten of their objects were small: nuts and bolts, for example. Although Lore & Levowitz measured contact time, number o f objects contacted can be assessed from their data: social animals contacted on average thirty-three objects per session, isolates forty. Considering that sessions were 15 rain long, these figures represent far fewer contacts than were made in our 6-rain experimental sessions, (ninety-six for social animals, forty-nine for isolates). Difference in both session-length and number of contacts suggests that one possible explanation for the lack of agreement between the two experiments might be that isolates habituated more slowly than socially-reared animals. Perhaps in Lore & Levowitzs' 15-min sessions the social animals had time to habituate to the situation, and thus made fewer contacts over the entire session. To investigate this possibility, we carried out a second experiment, in which habituation of object contact was observed over 30 min. Experiment 2 Methods
Rats from six litters, (eighteen females, two males), which had been bred in the laboratory, were weaned at 17 days and assigned to the two rearing conditions employed in the previous experiment. A split-litter design was employed. Social animals were raised in groups of four or five; the single social male animal was housed with three male litter mates. As in the first experiment animals were housed in standard NKP-RB1 cages (45 • 28 x 22 c m ) t h r o u g h o u t the experiment. Object contact was examined when the animals were 60 days old. All animals had previously been exposed to the open field without objects when 45 days old. Rearing conditions were as in the previous experiment. Apparatus and procedure were as in the previous experiment except that the rubber ball was replaced by a small plastic bottle of approximately the same size, and sessions were of 29 min duration. Three 3-min samples were taken: the first 3 rain, 13 to 16 min, and 26 to 29 rain. Animals spent intersample intervals in the open field.
418
ANIMAL
BEHAVIOUR
Results
The number of object contacts made in each of the time samples is shown graphically in Fig. 2, separately for social and isolated rats. Table II presents the modes of contact. It appears that in the first sample, as in experiment 1, social rats made more contacts: but they showed more rapid habituation o f contacting with the result that in the remaining time-samples they made fewer contacts than the isolates. An Analysis of Variance showed that the only significant effects were those of timesamples ( F = 43-8; df= 2, 36; P = 2.2 • 10-10 ) and the rearing condition by time samples interaction ( F = 23.70; df= 2, 36; P = 2 . 7 • 10-7). There was no significant main effect of rearing condition ( F = 2.195; df= 1, 18; P = 0.155). Mann-Whitney U-tests confirmed these effects. The social animals made significantly more contacts in the first time-sample (U = 18; P < 0.02) but significantly fewer in the second sample (U = 17). The difference in the third sample does not meet the criterion of significance we are using (U = 22; P = 0.05).
24,
2
this occurred much more slowly. The difference in the rate of habituation may well explain why Lore & Levowitz (1966) found that isolated animals contacted more objects in their 15-min sample. The finding that isolated animals differ in the rate at which they habituate is in agreement with the finding that these same animals show a slower decline in activity over time in an objectfree open field (Einon, Morgan & Sahakian 1975). The fact that isolated animals are slower to habituate in both a simple and complex environment argues against Zimbardo & Montgomerys' (1957) suggestion that the difference between deprived and enriched animals may be partially a function of the degree of novelty of the exploratory field. The underlying assumption of such a hypothesis is that exploration should be an increasing function of the degree of discrepancy between a familiar standard and a new stimulus up to a point, after which greater magnitudes of discrepancy
Discussion
Initially, the socially reared animals contacted more objects, but the number of contacts they made declined quite rapidly with time. Isolated rats contacted fewer objects initially, and although they showed some decrement with time,
.
.
.
.
.
social isolate
Table H. Experiment 2: Median Object Contact and Mode of Contact by Socially Reared and Isolated Rats in a Open Field in the first 3-Min Sample "o
Rearing Measure
Social Isolates
\,,
2o
Probability (P) o
Number of objects contacted
46
34
< 0'02
Variety objects contacted
11
9
< 0.10
0
< 0,10
Touching
"6 o
0"3
\,
o
\
e~
Nose contact
19
19
< 0.10
Paws
13
6
< 0.05
E
\
Z
Entering
2-5
2
< 0.10
Climbing
7
2
< 0.02
Moving
1.5
1
< 0.10
Rearing-up
3
0
< 0.02
0
I Time
2
3
Sample
Fig. 2. Results of experiment 2: the median object contacts made by socially-reared and isolation-reared rats in three successive 3-rain samples. The rats were in the open field for a total of 29 min. The first time-sample was from the first 3 rain, the second from minutes 13 to 16, and the last from minutes 26 to 29.
EINON & MORGAN: ISOLATION AND OBJECT-CONTACT will produce less and less exploration. The problem, as with all inverted U-shaped functions, is that it is virtually impossible to make a priori predictions about the degree of novelty that will induce less exploration. Perhaps neither the open field nor the object-filled field represented this degree of novelty for the isolated animals. I t is in any case rather difficult to assess from the present experiment which group of animals is more 'exploratory'. Leaving aside the differences in mode of contact, we have two measures of exploration: number of objects contacted, and the habituation of contact. On the former measure the isolated animals are less exploratory, while on the latter measure they are more exploratory: predictions from a discrepancy hypothesis of exploration, (Zimbardo & Montgomery 1957; Dember & Earl 1957) are unclear in such types of situations. The hypothesis deals mainly with choice behaviour, and has been validated in situations which involve choice. Since it is known that choice measures do not necessarily correlate with measures of vigour (Stanley 1952; Mackintosh 1963) there seems little reason to suppose they are better correlated with activity or rate of habituation. There is obviously no very simple explanation of the various effects produced by isolation: isolates are slower to habituate but clearly are also deficient in other respects. The social animals placed in the object-filled field produced a behavioural strategy that involved the gradual exploration of the whole field. They tended to approach objects, to sniff them, place one paw, sniff and then perhaps climb or move the object. I f they 'accidentally' moved an object they would stop, retreat, then reapproach. The isolated animals tended to walk around objects, tO stop and sniff and then move on: there was nothing very systematic about their behaviour, as we may see from the fact that they manipulated a smaller variety of objects. The majority of the social animals made contact with all objects in the open field. We suggest, therefore, that the differences between socially reared and isolated rats in a novel environment are not profitably described in terms of a simple ' e x p l o r a t i o n ' hypothesis. Rather, the differences seem to depend upon rate of response waning and upon the precise details of the way in which the animals expose themselves to novel stimulation. We have previously described the waning of activity in the open field as 'habituation', on the grounds that there is a recovery after an interval of time
419
outside of the apparatus (Einon, Morgan & Sahakian 1975). In this sense of the word, isolates could be said to show slower 'habituation'. However, as Hinde (1970) points out, a response decrement occurring as a result of repeated or continuous presentation, can only be called habituation 'with certain limitations', and few of the limitations described by Hinde apply to the process observed in the present experiments. We do not know, for example, whether there would be recovery of activity in the social animals if the objects were changed, and, therefore, it cannot be asserted that the response decrement is situation-specific; Thus the suggestion that isolates habituate less readily in a novel situation than social rats should be viewed simply as a rather gross description of a behavioural difference, rather than as a precise suggestion about the mechanism of the difference. It does, however, seem to be of greater value than a description of the isolates as more 'exploratory', since the latter description fails to include changes in behaviour over time, and cannot suggest why different measures of 'exploration' have given such different results. REFERENCES
Baenninger, L. (1967). Comparison of behavioural development in socially isolated and grouped rats. Anita. Behav., 15, 312-323. Barnett, S. A. (1963). A Study in Behaviour: Principles of Ethology and Behavioural Physiology Displayed Mainly in the Rat. London: Methuen.
Dember, W. N. & Earl, R. W. (1957). Analysis of exploratory, manipulative and curiosity behavior. Psychol. Rev., 64, 91-96. Eibl-Eibesfeldt, L (1967). Concepts of Ethology and human behavior. In: Early Behavior: Comparative and Developmental Approaches (Ed. by H. W. Stevenson, E. H. Hess & H. L. Reinegold), pp. 137-141. New York: John Wiley. Einon, D. F., Morgan, M. J. & Sahakian, B. J. (1975). The development of intersession habituation and emergence in socially-reared and isolated rats. Dev. Psychobiol., 8, 553-559. Ewer, R. F. (t971). The biology and behaviour of a freeliving population of black rats (Rattas rattus). Anita. Behav. Monogr., 4, 3, 127-174. Gill, J. H., Reid, L. D. & Porter, P. B. 0966). Effects of restricted rearing on Lashley stand performance. Psychol. Rec., 19, 239-242. Hinde, R. A. (1970). Behavioural habituation. In: Short-term Changes in Neural Activity and Behaviour (Ed. by G. Horn & R. A. Hinde). Cam-
bridge: Cambridge University Press. Jones, L. V. & Fiske, D. W. (1953). Models for testing the significance of combined results. Psychol. Bull., 50, 375-382. Lore, R. K. & Levowitz, A. (1966). Differential rearing and free versus forced exploration. Psychon. Sci., 5, 421-422.
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Luchins, A. S. & Forgus, R: H. (1955). The effects of differential post-weaning environment on the rigidity of an animal's behavior. J. Genet. PsychoL, 86~ 51-58. Mackintosh, N. J. (1963). Extinction of a discrimination habit as a function of overtraining. J. comp. physioL PsychoL, 56, 842-847. McCall, R. B., Lester, M. L. & Dotan, C. G. (1969). Differential rearing and the exploration of stimuli in the open field. Dev. PsychoL, 1, 750-762. Morgan, M. J. (1973). Effects of post-weaning environment on learning in the rat. Anita. Behav., 21, 429--442. Morgan, M. J., Einon, D. F. & Nicholas, D. (1975). The effects of isolation rearing on behavioural inhibition in the rat. Q. JI. exp. PsychoL, 27, 615-634.
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Siegel, S. (1956). Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill. Stanley, W. C. (1952). Extinction as a function of the spacing of extinction trials. J. exp. PsychoL, 43, 249-260. Syme, L. A. (1973). Social isolation at weaning: Some effects on two measures of activity. Anim. Learning Behav., 1, 161-163. Welker, W. I. (1961). An analysis of exploratory and play behavior in animals. In: Functions of Varied Experience (Ed. by D. W. Fiske & S. R.. Maddi). Homewood, Illinois: The Dorsey Press. Zimbardo, P. G. & Montgomery, K. C. (1957). Effects of the 'free environment' rearing upon exploratory activity. PsychoL Rep., 3, 589-594.
(Received 26 March 1975; revised 16 June 1975; MS. number: 1417)
EINON & M O R G A N : ISOLATION AND OBJECT-CONTACT PLATE
IV
Fig. l. Plan view of the open field used in experiments 1 and 2. The position of objects in the field was the same at the start of each session, and the animal was always placed next to the food hopper in the centre of the field. The overall dimensions are 30 • 30 cm.
Einon & Morgan, Anim. Eekav., 24, 2