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Social deprivation and play in rats
BEHAVIORAL A N D N E U R A L BIOLOGY 3 0 , 197--206 ( 1 9 8 0 )
Social Deprivation and Play in Rats 1 JAAK PANKSEPP
Department of Psychology, Bowling Green State University, Bowling Green, Ohio 43403 AND
WILLIAM W. BEATTY
Department of Psychology, North Dakota State University, Fargo, North Dakota 58102 Social interaction (play fighting) was studied in socially housed and individually housed juvenile rats (18-30 days of age). Pinning (an animal on its back, with the other on top) proved to be a simple measure of play which correlated highly with other measures of playful behavior (solicitive behaviors, following, rough-andtumble play, and together-time measures). Play behaviors were markedly increased by social deprivation and reduced by social satiation. The results suggest that social play is a regulated process which can be easily quantified by the simple and objective measure of pinning behavior.
Although there is a massive descriptive literature on the play behavior of animals (see Aldis, 1975, and American Zoologist, 14, 1974), psychobiological analyses of the phenomenon remain rudimentary. This may be due, in part, to the lack of an efficient behavioral assay for measuring the behavior in a readily available model species. Until recently, continuous observation of animals in the field or their home cages was the most common practice in this area of inquiry. One aim of the present work was to develop a simplified procedure for studying social play in the laboratory rat so that a physiological analysis of underlying processes could be initiated. The other aim was to determine whether play is homeostatically controlled, in that it is responsive to social deprivation and satiation. Social play in rats was initially described by Small (1899), and it has been studied subsequently by several investigators (Mfiller-Schwarze, 1 This research was supported by NIMH Research Scientist Development Award MH00086 to J.P. and NIH Grant HD 12620 to W.W.B. We wish to acknowledge useful discussions of this work with Dr. John Jalowiec and the technical assistance of Rita Weiss and Tony Dodge. 197 0163-1047/80/100197-10502.00/0 Copyright © 1980 by Academic Press, Inc. All rights of reproduction in any form reserved.
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PANKSEPP AND BEATI'Y
1966; Olioff & Stewart, 1978). Using an ethological approach, Poole and Fish (1976) described the sequential interrelationships of 15 differentiable behaviors that are frequently observed during apparent play bouts between rats. Although social play behavior is inherently complex, a simple behavioral assay of play would facilitate the study of underlying biological control mechanisms. A full analysis of all behaviors exhibited during social play is, of course, essential for a thorough understanding of underlying processes, but at the present stage of development in the field, the use of an indicator variable might greatly facilitate further analysis of the phenomenon. In a similar manner, the study of hunger and thirst has been greatly facilitated by the use of food and water intakes as measures, even though it is generally agreed that a microanalysis of all aspects of the behavioral sequences will be needed for a thorough understanding of those processes. On the basis of extensive observation of social play between pairs of rats, "pinning" behavior emerged as the best objective indicator of social play in rats (Panksepp, 1979). As summarized herein, this behavior has now been used to study play between young rats in two independent laboratories. Also, the results document the fact that social deprivation can markedly increase play between pairs of rats. EXPERIMENT 1
When two young rats which have been housed in social isolation are placed together, they rapidly begin to exhibit vigorous social interaction, which is characterized primarily by chasing, pouncing, and wrestling. Although a large number of discrete behaviors occur during these apparent play bouts, most are difficult to categorize and operationalize. However, one behavior that is discrete and easily operationalized is "pinning"--when one animal rolls onto its back with the other animal on top. It is a simple task to count the number of times that a rat ends up in the normally improbable posture of having its dorsal surface to the ground. In the absence of social interaction, this posture is never adopted, whereas it appears repeatedly during play episodes between young rats. In the following experiment, pinning was measured in socially housed and socially isolated rats permitted brief periods of social interaction in a test chamber.
Method Subjects. The animals used were 60 Long-Evans hooded rats (haft of each sex) from six litters (n = 8-12 pups per litter) bred and born at the BGSU laboratory. Until 18 days of age, family groups were housed together in standard, suspended wire cages (24 x 40 x 19 cm). At 18 days of age, half the animals in each litter, counterbalanced across sex, were weaned and rehoused individually in 23 x 10 x 13 c m suspended wire
DEPRIVATION AND PLAY
199
cages. The remaining animals were left in their original home cages without their mothers (group size ranging from four to six pups). Throughout testing, animals had free access to food and water, and temperature was sustained at 72 _ 2°F. Lighting was on a 12/12-hr light/dark schedule, and animals were tested during the second half of the light phase. Apparatus. Testing occurred in a 31 × 31 x 32-cm Lucite test cage situated in a soundproof outer chamber with a 10 x 10-cm observation window. To make the test chamber "comfortable," the floor was covered with about 2 cm of wood shavings, and the only illumination was from a 25-W red light bulb mounted to one side of the test box. Procedure. At 21 days of age, 20 pairs of like-sexed, similarly housed littermates were observed for 5-min periods, and the following behaviors were recorded using digital counters and running-time meters: PinningDefined as either animal lying with its dorsal surface to the ground. Sometimes this occurred briefly when animals were rolling over each other in rough-and-tumble play, and sometimes it was more discrete, lasting for several seconds, often heralding a temporary cessation of social interaction. Social solicitations--This was used as a general category that included all discrete social behaviors emitted other than pinning. The category included anogenital sniffing and investigation of the other animal, social grooming, over-under behavior, pouncing, charging, mounting, and boxing. The presence of any of these behaviors was counted as a single event. Follows--This was counted whenever one animal followed "on the heels" of another animal for at least one length of the chamber. If more than one length of following occurred, each chamber length was scored separately. Together time--Consisted of time (to 0.1 sec per bout) during which animals were within an estimated 2.5 cm of each other, tails excluded. Animals could be indulging in social interaction or simply be proximate. Separations--The frequency with which animals moved more than 2.5 cm from each other. Usually there was little ambiguity in this measure since when animals parted, they moved at least several inches apart. Also, two nonsocial behaviors, self-grooming (in any form) and nibbling of bedding material or feces, were recorded.
Results and Discussion Three days of social isolation markedly increased social interaction. Isolates usually played for the entire observation period whereas vigorous social interaction between socially housed animals was typically less than a third of the observation period. The data, collapsed across sexes (effects of which were not reliable), is summarized in Table 1. Social isolation reliably increased pinning by more than 1000%, social solicitations by 367%, following by 265%, and together time by 300%. Conversely, isolation decreased self-grooming by 54%, nibbling by 78%, and the number of
200
PANKSEPP AND BEATI'Y TABLE 1 Mean (-+SEM) Social Behavior per Session (Expt 1)
Housing condition Isolate Social
Pins
Solicitations
Follows
Together Grooms Nibbles time (sec) Separations
26 (_+2) 2(-+1)*
103 (_+5) 28(_+3)*
15 (_+2) 6(_+1)*
4 (_+8) 1 (_+.5) 9(_+1)* 4(-+1)*
270 (-+3) 8 (-+.5) 88(+_9) * 11 (_+1)*
• p ' s < .001, t tests.
together bouts by 30%, though bout length was, of course, markedly increased by the isolation. In separate tests, interobserver reliability of the pinning measure was .95. The product moment correlation of pinning with the other variables indicated reliable positive relationships with scores of social solicitation (r = .92), following (r = .52), and together time (r = .88). Negative correlations were observed for grooming (r = -.36) and nibbling (r = -.43). In general, the results indicate that pinning may be a useful measure of social play in rats. Not only did the measure clearly differentiate between the apparently vigorous play of socially isolated animals and the desultory play of socially housed animals, but the measure was correlated highly with an overall measure of social activity (i.e., solicitations) as well as general social acts such as following and together time. Of all measures, it showed the largest increment with social deprivation. The face validity of the measure is high in that it appears to be the most prominent discrete behavior to occur in the play episodes that were observed in the present study. Also, since it often appears to terminate a play episode, it is possible that it directly reflects the internal processes which control play. EXPERIMENT 2
To help determine whether the measure of pinning as a measure of social play has general applicability, the following study was conducted to reevaluate the relationship between pinning and other measures of play fighting by a different laboratory using different procedures and a different strain of rat. The only substantive methodological information that was communicated from the Bowling Green Laboratory to the North Dakota State Laboratory was that members of the former believed "pinning" to be a useful indicator variable for measuring play behavior between rats.
Method Subjects. The animals were 22 male and 16 female albino rats. They were the offspring of four mothers purchased from the Holtzman Company, Madison, Wisconsin, that were shipped to the laboratory during the first week of gestation. Upon arrival, the mothers were housed in individual polyethylene breeder cages with free access to food and water.
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201
T h e y lived in these cages until their pups were weaned at 21 days of age. Following weaning the young rats were housed in pairs of the same sex in standard laboratory cages (17.8 x 25.4 × 17.8 cm), except while they were socially isolated. During social isolation periods, the rats were housed singly in similar cages. Food and w a t e r were freely available. The temperature-controlled animal r o o m where the rats were caged was illuminated from 0700 to 1900. Apparatus. The test chamber measured 51 x 32 x 47 cm high. The floor and three of the sides were made of plywood painted flat black; the front wall was m a d e of clear Lucite. Illumination was provided by two 60-W red lamps located 71 cm a b o v e the floor of the test chamber. Social b e h a v i o r was recorded on videotape by means of a closed circuit television system. The illumination was sufficient to produce reasonably clear recordings, but did not a p p e a r to disturb the animals. Procedure. T w o to three days before testing the rats were habituated to the apparatus. During these habituation tests each animal remained in the c h a m b e r alone for 10 rain. Social behavior b e t w e e n pairs of animals of the same sex was studied when the rats were 25-30 days old. Test sessions were 10-rain long and occurred between 1900 and 2100 hr (i.e., within the first 2 hr of the dark period). Each rat was tested twice, once after 24 hr of social isolation and once after social housing. In both conditions the partners during a test were '~strangers" (i.e., animals that had had no social contact with each other since weaning). The order of testing with respect to the isolation conditions was counterbalanced and the two tests were 3 days apart. Since order of testing had no effect on any measure of social behavior, the data were collapsed across this variable yielding 11 male and 8 female pairs under each level of social isolation. The videotape recordings were scored by a rater who was blind to both the sex and isolation condition of the subjects. The rater sat at a console equipped with keys that activated running time meters when depresssed. The total time spent in each of three mutually exclusive categories (chasing, social investigation, and rough-and-tumble play) was measured. The sum of times spent in these activities provides a measure of total social interaction time. The rater also recorded the frequency of pinning, defined as in E x p e r i m e n t 1. Chasing consisted of active pursuit of one rat by the other. Chasing as used in this study is a c o m p o n e n t of following as defined in E x p e r i m e n t 1. Chasing included only the more vigorous episodes of following. Less vigorous following b e h a v i o r was scored as social investigation because it occurred when one animal that had been sniffing the anogenital area of the other animal continued to do so as the other rat m o v e d away. Social Investigation included social sniffing and grooming. Nearly all social sniffing was directed at the anogenital area. Rough-and-tumble play was a c o m p o s i t e of several behaviors including: tail-pulling, boxing, wrestling,
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PANKSEPP AND BEATFY
pinning, and aggressive grooming. Aggressive grooming differed from social grooming in that it was more intense, almost always directed at the head and neck, and inevitably provoked struggling or squealing from the animal being groomed. This scoring system is similar to one used by Olioff and Stewart (1978), but differs from the system used in Experiment 1. In addition to the difference between chasing and following described above, the measure of social solicitation employed in Experiment 1 includes components of social investigation and rough and tumble play as defined above. In previous studies interrater reliabilities have ranged from .50 to .70 for chasing and .75 and .90 for the other measures. Results Social isolation increased the total amount of time spent in social interaction (F(1, 34) = 31.79, p < .001) (Table 2). After isolation the rats spent much more time in rough-and-tumble play (F(I, 34) = 42.50, p < .001) and chase (F(1, 34) = 16.38, p < .001). The time spent in social investigation declined somewhat, although this effect was not reliable. As in the previous experiment, social isolation increased the frequency of pinning (F(1, 34) = 16.06, p < .001). The effects of social isolation were much the same in male and female pairs; neither the main effect of sex nor the sex by isolation interaction attained significance. Product moment correlations among the various dependent variables are shown in Table 3. Of particular importance is the high and positive correlation between time spent in rough and tumble play and the frequency of pinning. These two measures in turn were highly correlated with time spent in chasing. EXPERIMENT 3
The previous experiments indicate that pinning may be a useful indicator variable for the incidence of social play between rats, as well as that TABLE 2 Mean Social Behavior per Session (Expt 2) Time (sec) spent engaging in Housing condition and sex Isolation Male pairs Female pairs Social Male pairs Female pairs
Total social Rough-andinteraction tumble play Chasing
Social investigation
Pinning (frequency)
270 (± 18) 244 (±12)
146 (_+20) 108 (±25)
37 (___7) 28 (+_10)
87 (_+ 12) 108 (___21)
18 (±5) 16 (±7)
179 (±19) 134 (+16)
26 (±6) 17 (+6)
9 (±2) 8 (+2)
144 (_+ 16) 109 (±7)
0.7 (+_0.4) 0.6 (±0.5)
203
DEPRIVATION AND PLAY TABLE 3 Correlations a m o n g M e a s u r e s
Rough-and-tumble play Chasing Social investigation
Chasing
Social investigation
Pinning
0.82
-0.60 -0.46*
0.89 0.68 -0.63
* p < .05; all other r values are reliable at the .001 level.
social isolation markedly increases play in rats. Previous work on the ability of play deprivation to increase play in other species has yielded equivocal results. Negative results have been obtained with young male deer (Mfiller-Schwarze, 1968) and a trend toward positive results was present in domestic goats (Chepka, 1971). The following experiment was conducted to determine systematically how shorter periods of social isolation and social ~'satiation" would affect play behavior in rats as indexed by a measure of the frequency of pinning. Method
A total of 64 Long-Evans hooded rats from six litters (n = 6-14 pups per litter) bred and born at BGSU were used. Using apparatus and procedures employed in Experiment 1, the play of paired animals was studied beginning at 18 days of age. On the day prior to testing, animals were divided into three groups of 10-11 same-sexed littermate pairs. Animals in one group were placed in isolation 8 hr before testing, and the remaining group was taken for testing directly from the home cage. After this initial test, the 24-hr deprived animals and the socially housed animals were returned to their respective housing conditions. The 8-hr group was distributed equally between the social and isolation conditions. All animals were again tested at 21 and 25 days of age (original pairings maintained). At 27 days of age, the socially housed animals were divided into three groups for deprivation testing. Five pairs were socially deprived for 24 hr, six pairs were assigned to a group which was isolated 8 hr before testing, and five pairs remained socially housed. Conversely, the isolated animals were assigned to corresponding satiety conditions (i.e., returned to their original homes 24, 8, or 1 hr before testing). The measures recorded were the frequency of pins and together time (defined as in Experiment 1). Results
The data (Fig. 1) indicate the systematic manner in which play varied as a function of social deprivation and satiation. At 18 days of age, social isolation reliably increased play (F(2, 16) = 14.2, p < .001) although 8 hr was as effective as 24 hr of deprivation. At 21 and 25 days of age, socially
204
PANKSEPP AND BEATI'Y
4
Depriva!lon
30 25 h- 20
Satiety
Depri vatioiol~n Funct L ~ ~
¢
>- IO
Fun ct ior~
Grouped Animal~
J_
L L
I
i
L I
I
I
0 t
8
24
(MAX.300 )
200 O3 UA h-W~ I FW
[00
i
I
L
0
8
24
DEPRIVATIO(HRS} N 18 Days of A g e
I
I
21 Age
25 DEPRIVATIO OR NSATIATIO(HRS) N (Days)
28
Doy•
of Age
FIG. 1. The effects of social deprivation and satiation on pinning and together time (+SEM) in Experiment 3.
DEPRIVATION AND PLAY
205
deprived animals pinned each other 600-900% more frequently than socially housed animals. At 28 days, social satiation systematically reduced (F(2, 13) = 20.9,p < .001) and deprivation increased (F(2, 13) = l l . 7 , p < .005) pinning and together time (all differences between successive points significant at p < .05 or better, except between play at the 24- and 8-hr satiety conditions). The fact that the deprivation function was much steeper at 28 than 18 days suggests the presence of a maturational factor. GENERAL DISCUSSION The play behavior we observed in these studies was essentially identical to that described by previous investigators (Poole & Fish, 1976; Small, 1899), and the behavior is difficult to describe comprehensively in quantitative terms. The present results indicate that pinning behavior can be used effectively as an indicator measure for quantifying the incidence of play behavior between juvenile rats. All pairs of socially isolated animals, and most of those housed together, exhibited the behavior in brief (5-10 min) observation periods. Pinning correlated highly with other measures of play which are not as easily operationaIized. In Experiment 1 there was a strong and positive correlation between pinning and social solicitation and a weaker relationship with following. In Experiment 2 pinning was strongly and positively related to rough-and-tumble play and chasing but negatively related to social investigation. Most likely these differences in the pattern of correlations among measures arose from different groupings of behaviors within the broad definitional categories. Overall pinning seems to be related most strongly to other measures of rough play or play fighting. Despite many procedural differences between the two laboratories, which may account for the rather marked differences in the absolute level of pinning observed, it is important to note that the effects of social isolation on pinning and other measures of social play were quite comparable. In addition, pinning was positively correlated with other measures of play in both laboratories. There is, of course, some variability in the motor topography of pinning behavior, but in general, the behavior is sufficiently clear-cut as a behavioral act that inexperienced observers can be trained to score the behavior rapidly. The general use of such a measure in play studies would help facilitate comparison of results obtained by different laboratories. Although pinning seems to be the best single dependent variable for measurement of play in rats, it represents only a limited sample of the ongoing behavior. In general, it may be useful to subcategorize play behavior into appetitive and consummatory phases of activity. The former may be represented by following and chasing, while the latter is characterized by rough-and-tumble (wrestling) activity and pinning. From most of our observations, it seems reasonable that pinning may represent a
206
PANKSEPP AND BEATI'Y
major terminal component in individual play bouts between juvenile rats, and if this is so, it could be argued that pinning is an especially reasonable measure of the consummatory phase of social play. Although play behavior between young rats resembles fighting, it is important to emphasize that the animals did not appear "to go at it in earnest." Small (1899) further noted that young rats make "violent assaults upon each other" but with "no sign of anger." In our observations, animals practically never appeared to exhibit sustained defensive attitudes. Thus, an animal that had just been pinned would usually, within the span of a few moments, be the one that was pinning. Although stable dominance relationships do evolve during play, in that one animal, on the average, will end up pinning the other animal about 70% of the time, the "submissive" animal remains socially active (Panksepp, 1979). Thus the type of serious aggression that can be seen in adult animals, in which an intruder rat assumes a sustained defensive attitude, is not seen during juvenile play. The fact that the satiety and deprivation functions of pinning were as systematic as those obtained with feeding and drinking suggests that play is a regulated process. Of course, from the present data, we cannot ascertain whether the modulation of play by isolation was due to its effects specifically on play or to a more general social variable. Regardless, the dat a indicate play has the hallmarks of a regulated process, and a reasonable working assumption is that some aspect of brain neurochemical activity regulates the amount of play exhibited by animals (Panksepp, 1979). In turn, play behavior may reciprocally control the tone of certain brain neurochemical pathways. It would seem that the quantification of rodent play behavior through a simple and unambiguous measure such as pinning can help facilitate quantitative research into the biological underpinnings of this fundamental behavior from which social competence may arise. REFERENCES Aldis, O. (1975). Play Fighting. New York: Academic Press. Chepka, B. D. (1971). A preliminary study of the effect of play deprivation on young goats, Zeitschrift J~r Tierpsychologie, 28, 517-526. Miiller-Schwarze, D. (1967). Experimente zur Triebspezifitiit des S~iugetierspiels. Naturwissenschraften, 53, 137-138. M/iller-Schwarze, D. (1968). Play deprivation in deer. Behaviour, 31, 144-162. Olioff, M., & Stewart, J. (1978). Sex differences in the play behavior of prepubescent rats. Physiology & Behavior, 20, 113-115, Panksepp, J. (1979). The regulation of play: neurochemical controls. Neuroscience Abstracts, 5, 172. Poole, T. B., & Fish, J. (1976). An investigation of individual, age, and sexual differences in the play of Rattus norvegicus (Mamalia: Rodentia). Proceedings of the Royal Society (London), 179, 249-260. Small, W. S. (1899). Notes on the psychic development of the young white rat. American Journal of Psychology, 11, 80-100.
Social Deprivation and Play in Rats 1 JAAK PANKSEPP
Department of Psychology, Bowling Green State University, Bowling Green, Ohio 43403 AND
WILLIAM W. BEATTY
Department of Psychology, North Dakota State University, Fargo, North Dakota 58102 Social interaction (play fighting) was studied in socially housed and individually housed juvenile rats (18-30 days of age). Pinning (an animal on its back, with the other on top) proved to be a simple measure of play which correlated highly with other measures of playful behavior (solicitive behaviors, following, rough-andtumble play, and together-time measures). Play behaviors were markedly increased by social deprivation and reduced by social satiation. The results suggest that social play is a regulated process which can be easily quantified by the simple and objective measure of pinning behavior.
Although there is a massive descriptive literature on the play behavior of animals (see Aldis, 1975, and American Zoologist, 14, 1974), psychobiological analyses of the phenomenon remain rudimentary. This may be due, in part, to the lack of an efficient behavioral assay for measuring the behavior in a readily available model species. Until recently, continuous observation of animals in the field or their home cages was the most common practice in this area of inquiry. One aim of the present work was to develop a simplified procedure for studying social play in the laboratory rat so that a physiological analysis of underlying processes could be initiated. The other aim was to determine whether play is homeostatically controlled, in that it is responsive to social deprivation and satiation. Social play in rats was initially described by Small (1899), and it has been studied subsequently by several investigators (Mfiller-Schwarze, 1 This research was supported by NIMH Research Scientist Development Award MH00086 to J.P. and NIH Grant HD 12620 to W.W.B. We wish to acknowledge useful discussions of this work with Dr. John Jalowiec and the technical assistance of Rita Weiss and Tony Dodge. 197 0163-1047/80/100197-10502.00/0 Copyright © 1980 by Academic Press, Inc. All rights of reproduction in any form reserved.
198
PANKSEPP AND BEATI'Y
1966; Olioff & Stewart, 1978). Using an ethological approach, Poole and Fish (1976) described the sequential interrelationships of 15 differentiable behaviors that are frequently observed during apparent play bouts between rats. Although social play behavior is inherently complex, a simple behavioral assay of play would facilitate the study of underlying biological control mechanisms. A full analysis of all behaviors exhibited during social play is, of course, essential for a thorough understanding of underlying processes, but at the present stage of development in the field, the use of an indicator variable might greatly facilitate further analysis of the phenomenon. In a similar manner, the study of hunger and thirst has been greatly facilitated by the use of food and water intakes as measures, even though it is generally agreed that a microanalysis of all aspects of the behavioral sequences will be needed for a thorough understanding of those processes. On the basis of extensive observation of social play between pairs of rats, "pinning" behavior emerged as the best objective indicator of social play in rats (Panksepp, 1979). As summarized herein, this behavior has now been used to study play between young rats in two independent laboratories. Also, the results document the fact that social deprivation can markedly increase play between pairs of rats. EXPERIMENT 1
When two young rats which have been housed in social isolation are placed together, they rapidly begin to exhibit vigorous social interaction, which is characterized primarily by chasing, pouncing, and wrestling. Although a large number of discrete behaviors occur during these apparent play bouts, most are difficult to categorize and operationalize. However, one behavior that is discrete and easily operationalized is "pinning"--when one animal rolls onto its back with the other animal on top. It is a simple task to count the number of times that a rat ends up in the normally improbable posture of having its dorsal surface to the ground. In the absence of social interaction, this posture is never adopted, whereas it appears repeatedly during play episodes between young rats. In the following experiment, pinning was measured in socially housed and socially isolated rats permitted brief periods of social interaction in a test chamber.
Method Subjects. The animals used were 60 Long-Evans hooded rats (haft of each sex) from six litters (n = 8-12 pups per litter) bred and born at the BGSU laboratory. Until 18 days of age, family groups were housed together in standard, suspended wire cages (24 x 40 x 19 cm). At 18 days of age, half the animals in each litter, counterbalanced across sex, were weaned and rehoused individually in 23 x 10 x 13 c m suspended wire
DEPRIVATION AND PLAY
199
cages. The remaining animals were left in their original home cages without their mothers (group size ranging from four to six pups). Throughout testing, animals had free access to food and water, and temperature was sustained at 72 _ 2°F. Lighting was on a 12/12-hr light/dark schedule, and animals were tested during the second half of the light phase. Apparatus. Testing occurred in a 31 × 31 x 32-cm Lucite test cage situated in a soundproof outer chamber with a 10 x 10-cm observation window. To make the test chamber "comfortable," the floor was covered with about 2 cm of wood shavings, and the only illumination was from a 25-W red light bulb mounted to one side of the test box. Procedure. At 21 days of age, 20 pairs of like-sexed, similarly housed littermates were observed for 5-min periods, and the following behaviors were recorded using digital counters and running-time meters: PinningDefined as either animal lying with its dorsal surface to the ground. Sometimes this occurred briefly when animals were rolling over each other in rough-and-tumble play, and sometimes it was more discrete, lasting for several seconds, often heralding a temporary cessation of social interaction. Social solicitations--This was used as a general category that included all discrete social behaviors emitted other than pinning. The category included anogenital sniffing and investigation of the other animal, social grooming, over-under behavior, pouncing, charging, mounting, and boxing. The presence of any of these behaviors was counted as a single event. Follows--This was counted whenever one animal followed "on the heels" of another animal for at least one length of the chamber. If more than one length of following occurred, each chamber length was scored separately. Together time--Consisted of time (to 0.1 sec per bout) during which animals were within an estimated 2.5 cm of each other, tails excluded. Animals could be indulging in social interaction or simply be proximate. Separations--The frequency with which animals moved more than 2.5 cm from each other. Usually there was little ambiguity in this measure since when animals parted, they moved at least several inches apart. Also, two nonsocial behaviors, self-grooming (in any form) and nibbling of bedding material or feces, were recorded.
Results and Discussion Three days of social isolation markedly increased social interaction. Isolates usually played for the entire observation period whereas vigorous social interaction between socially housed animals was typically less than a third of the observation period. The data, collapsed across sexes (effects of which were not reliable), is summarized in Table 1. Social isolation reliably increased pinning by more than 1000%, social solicitations by 367%, following by 265%, and together time by 300%. Conversely, isolation decreased self-grooming by 54%, nibbling by 78%, and the number of
200
PANKSEPP AND BEATI'Y TABLE 1 Mean (-+SEM) Social Behavior per Session (Expt 1)
Housing condition Isolate Social
Pins
Solicitations
Follows
Together Grooms Nibbles time (sec) Separations
26 (_+2) 2(-+1)*
103 (_+5) 28(_+3)*
15 (_+2) 6(_+1)*
4 (_+8) 1 (_+.5) 9(_+1)* 4(-+1)*
270 (-+3) 8 (-+.5) 88(+_9) * 11 (_+1)*
• p ' s < .001, t tests.
together bouts by 30%, though bout length was, of course, markedly increased by the isolation. In separate tests, interobserver reliability of the pinning measure was .95. The product moment correlation of pinning with the other variables indicated reliable positive relationships with scores of social solicitation (r = .92), following (r = .52), and together time (r = .88). Negative correlations were observed for grooming (r = -.36) and nibbling (r = -.43). In general, the results indicate that pinning may be a useful measure of social play in rats. Not only did the measure clearly differentiate between the apparently vigorous play of socially isolated animals and the desultory play of socially housed animals, but the measure was correlated highly with an overall measure of social activity (i.e., solicitations) as well as general social acts such as following and together time. Of all measures, it showed the largest increment with social deprivation. The face validity of the measure is high in that it appears to be the most prominent discrete behavior to occur in the play episodes that were observed in the present study. Also, since it often appears to terminate a play episode, it is possible that it directly reflects the internal processes which control play. EXPERIMENT 2
To help determine whether the measure of pinning as a measure of social play has general applicability, the following study was conducted to reevaluate the relationship between pinning and other measures of play fighting by a different laboratory using different procedures and a different strain of rat. The only substantive methodological information that was communicated from the Bowling Green Laboratory to the North Dakota State Laboratory was that members of the former believed "pinning" to be a useful indicator variable for measuring play behavior between rats.
Method Subjects. The animals were 22 male and 16 female albino rats. They were the offspring of four mothers purchased from the Holtzman Company, Madison, Wisconsin, that were shipped to the laboratory during the first week of gestation. Upon arrival, the mothers were housed in individual polyethylene breeder cages with free access to food and water.
DEPRIVATION AND PLAY
201
T h e y lived in these cages until their pups were weaned at 21 days of age. Following weaning the young rats were housed in pairs of the same sex in standard laboratory cages (17.8 x 25.4 × 17.8 cm), except while they were socially isolated. During social isolation periods, the rats were housed singly in similar cages. Food and w a t e r were freely available. The temperature-controlled animal r o o m where the rats were caged was illuminated from 0700 to 1900. Apparatus. The test chamber measured 51 x 32 x 47 cm high. The floor and three of the sides were made of plywood painted flat black; the front wall was m a d e of clear Lucite. Illumination was provided by two 60-W red lamps located 71 cm a b o v e the floor of the test chamber. Social b e h a v i o r was recorded on videotape by means of a closed circuit television system. The illumination was sufficient to produce reasonably clear recordings, but did not a p p e a r to disturb the animals. Procedure. T w o to three days before testing the rats were habituated to the apparatus. During these habituation tests each animal remained in the c h a m b e r alone for 10 rain. Social behavior b e t w e e n pairs of animals of the same sex was studied when the rats were 25-30 days old. Test sessions were 10-rain long and occurred between 1900 and 2100 hr (i.e., within the first 2 hr of the dark period). Each rat was tested twice, once after 24 hr of social isolation and once after social housing. In both conditions the partners during a test were '~strangers" (i.e., animals that had had no social contact with each other since weaning). The order of testing with respect to the isolation conditions was counterbalanced and the two tests were 3 days apart. Since order of testing had no effect on any measure of social behavior, the data were collapsed across this variable yielding 11 male and 8 female pairs under each level of social isolation. The videotape recordings were scored by a rater who was blind to both the sex and isolation condition of the subjects. The rater sat at a console equipped with keys that activated running time meters when depresssed. The total time spent in each of three mutually exclusive categories (chasing, social investigation, and rough-and-tumble play) was measured. The sum of times spent in these activities provides a measure of total social interaction time. The rater also recorded the frequency of pinning, defined as in E x p e r i m e n t 1. Chasing consisted of active pursuit of one rat by the other. Chasing as used in this study is a c o m p o n e n t of following as defined in E x p e r i m e n t 1. Chasing included only the more vigorous episodes of following. Less vigorous following b e h a v i o r was scored as social investigation because it occurred when one animal that had been sniffing the anogenital area of the other animal continued to do so as the other rat m o v e d away. Social Investigation included social sniffing and grooming. Nearly all social sniffing was directed at the anogenital area. Rough-and-tumble play was a c o m p o s i t e of several behaviors including: tail-pulling, boxing, wrestling,
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pinning, and aggressive grooming. Aggressive grooming differed from social grooming in that it was more intense, almost always directed at the head and neck, and inevitably provoked struggling or squealing from the animal being groomed. This scoring system is similar to one used by Olioff and Stewart (1978), but differs from the system used in Experiment 1. In addition to the difference between chasing and following described above, the measure of social solicitation employed in Experiment 1 includes components of social investigation and rough and tumble play as defined above. In previous studies interrater reliabilities have ranged from .50 to .70 for chasing and .75 and .90 for the other measures. Results Social isolation increased the total amount of time spent in social interaction (F(1, 34) = 31.79, p < .001) (Table 2). After isolation the rats spent much more time in rough-and-tumble play (F(I, 34) = 42.50, p < .001) and chase (F(1, 34) = 16.38, p < .001). The time spent in social investigation declined somewhat, although this effect was not reliable. As in the previous experiment, social isolation increased the frequency of pinning (F(1, 34) = 16.06, p < .001). The effects of social isolation were much the same in male and female pairs; neither the main effect of sex nor the sex by isolation interaction attained significance. Product moment correlations among the various dependent variables are shown in Table 3. Of particular importance is the high and positive correlation between time spent in rough and tumble play and the frequency of pinning. These two measures in turn were highly correlated with time spent in chasing. EXPERIMENT 3
The previous experiments indicate that pinning may be a useful indicator variable for the incidence of social play between rats, as well as that TABLE 2 Mean Social Behavior per Session (Expt 2) Time (sec) spent engaging in Housing condition and sex Isolation Male pairs Female pairs Social Male pairs Female pairs
Total social Rough-andinteraction tumble play Chasing
Social investigation
Pinning (frequency)
270 (± 18) 244 (±12)
146 (_+20) 108 (±25)
37 (___7) 28 (+_10)
87 (_+ 12) 108 (___21)
18 (±5) 16 (±7)
179 (±19) 134 (+16)
26 (±6) 17 (+6)
9 (±2) 8 (+2)
144 (_+ 16) 109 (±7)
0.7 (+_0.4) 0.6 (±0.5)
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DEPRIVATION AND PLAY TABLE 3 Correlations a m o n g M e a s u r e s
Rough-and-tumble play Chasing Social investigation
Chasing
Social investigation
Pinning
0.82
-0.60 -0.46*
0.89 0.68 -0.63
* p < .05; all other r values are reliable at the .001 level.
social isolation markedly increases play in rats. Previous work on the ability of play deprivation to increase play in other species has yielded equivocal results. Negative results have been obtained with young male deer (Mfiller-Schwarze, 1968) and a trend toward positive results was present in domestic goats (Chepka, 1971). The following experiment was conducted to determine systematically how shorter periods of social isolation and social ~'satiation" would affect play behavior in rats as indexed by a measure of the frequency of pinning. Method
A total of 64 Long-Evans hooded rats from six litters (n = 6-14 pups per litter) bred and born at BGSU were used. Using apparatus and procedures employed in Experiment 1, the play of paired animals was studied beginning at 18 days of age. On the day prior to testing, animals were divided into three groups of 10-11 same-sexed littermate pairs. Animals in one group were placed in isolation 8 hr before testing, and the remaining group was taken for testing directly from the home cage. After this initial test, the 24-hr deprived animals and the socially housed animals were returned to their respective housing conditions. The 8-hr group was distributed equally between the social and isolation conditions. All animals were again tested at 21 and 25 days of age (original pairings maintained). At 27 days of age, the socially housed animals were divided into three groups for deprivation testing. Five pairs were socially deprived for 24 hr, six pairs were assigned to a group which was isolated 8 hr before testing, and five pairs remained socially housed. Conversely, the isolated animals were assigned to corresponding satiety conditions (i.e., returned to their original homes 24, 8, or 1 hr before testing). The measures recorded were the frequency of pins and together time (defined as in Experiment 1). Results
The data (Fig. 1) indicate the systematic manner in which play varied as a function of social deprivation and satiation. At 18 days of age, social isolation reliably increased play (F(2, 16) = 14.2, p < .001) although 8 hr was as effective as 24 hr of deprivation. At 21 and 25 days of age, socially
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DEPRIVATIO(HRS} N 18 Days of A g e
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25 DEPRIVATIO OR NSATIATIO(HRS) N (Days)
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FIG. 1. The effects of social deprivation and satiation on pinning and together time (+SEM) in Experiment 3.
DEPRIVATION AND PLAY
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deprived animals pinned each other 600-900% more frequently than socially housed animals. At 28 days, social satiation systematically reduced (F(2, 13) = 20.9,p < .001) and deprivation increased (F(2, 13) = l l . 7 , p < .005) pinning and together time (all differences between successive points significant at p < .05 or better, except between play at the 24- and 8-hr satiety conditions). The fact that the deprivation function was much steeper at 28 than 18 days suggests the presence of a maturational factor. GENERAL DISCUSSION The play behavior we observed in these studies was essentially identical to that described by previous investigators (Poole & Fish, 1976; Small, 1899), and the behavior is difficult to describe comprehensively in quantitative terms. The present results indicate that pinning behavior can be used effectively as an indicator measure for quantifying the incidence of play behavior between juvenile rats. All pairs of socially isolated animals, and most of those housed together, exhibited the behavior in brief (5-10 min) observation periods. Pinning correlated highly with other measures of play which are not as easily operationaIized. In Experiment 1 there was a strong and positive correlation between pinning and social solicitation and a weaker relationship with following. In Experiment 2 pinning was strongly and positively related to rough-and-tumble play and chasing but negatively related to social investigation. Most likely these differences in the pattern of correlations among measures arose from different groupings of behaviors within the broad definitional categories. Overall pinning seems to be related most strongly to other measures of rough play or play fighting. Despite many procedural differences between the two laboratories, which may account for the rather marked differences in the absolute level of pinning observed, it is important to note that the effects of social isolation on pinning and other measures of social play were quite comparable. In addition, pinning was positively correlated with other measures of play in both laboratories. There is, of course, some variability in the motor topography of pinning behavior, but in general, the behavior is sufficiently clear-cut as a behavioral act that inexperienced observers can be trained to score the behavior rapidly. The general use of such a measure in play studies would help facilitate comparison of results obtained by different laboratories. Although pinning seems to be the best single dependent variable for measurement of play in rats, it represents only a limited sample of the ongoing behavior. In general, it may be useful to subcategorize play behavior into appetitive and consummatory phases of activity. The former may be represented by following and chasing, while the latter is characterized by rough-and-tumble (wrestling) activity and pinning. From most of our observations, it seems reasonable that pinning may represent a
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major terminal component in individual play bouts between juvenile rats, and if this is so, it could be argued that pinning is an especially reasonable measure of the consummatory phase of social play. Although play behavior between young rats resembles fighting, it is important to emphasize that the animals did not appear "to go at it in earnest." Small (1899) further noted that young rats make "violent assaults upon each other" but with "no sign of anger." In our observations, animals practically never appeared to exhibit sustained defensive attitudes. Thus, an animal that had just been pinned would usually, within the span of a few moments, be the one that was pinning. Although stable dominance relationships do evolve during play, in that one animal, on the average, will end up pinning the other animal about 70% of the time, the "submissive" animal remains socially active (Panksepp, 1979). Thus the type of serious aggression that can be seen in adult animals, in which an intruder rat assumes a sustained defensive attitude, is not seen during juvenile play. The fact that the satiety and deprivation functions of pinning were as systematic as those obtained with feeding and drinking suggests that play is a regulated process. Of course, from the present data, we cannot ascertain whether the modulation of play by isolation was due to its effects specifically on play or to a more general social variable. Regardless, the dat a indicate play has the hallmarks of a regulated process, and a reasonable working assumption is that some aspect of brain neurochemical activity regulates the amount of play exhibited by animals (Panksepp, 1979). In turn, play behavior may reciprocally control the tone of certain brain neurochemical pathways. It would seem that the quantification of rodent play behavior through a simple and unambiguous measure such as pinning can help facilitate quantitative research into the biological underpinnings of this fundamental behavior from which social competence may arise. REFERENCES Aldis, O. (1975). Play Fighting. New York: Academic Press. Chepka, B. D. (1971). A preliminary study of the effect of play deprivation on young goats, Zeitschrift J~r Tierpsychologie, 28, 517-526. Miiller-Schwarze, D. (1967). Experimente zur Triebspezifitiit des S~iugetierspiels. Naturwissenschraften, 53, 137-138. M/iller-Schwarze, D. (1968). Play deprivation in deer. Behaviour, 31, 144-162. Olioff, M., & Stewart, J. (1978). Sex differences in the play behavior of prepubescent rats. Physiology & Behavior, 20, 113-115, Panksepp, J. (1979). The regulation of play: neurochemical controls. Neuroscience Abstracts, 5, 172. Poole, T. B., & Fish, J. (1976). An investigation of individual, age, and sexual differences in the play of Rattus norvegicus (Mamalia: Rodentia). Proceedings of the Royal Society (London), 179, 249-260. Small, W. S. (1899). Notes on the psychic development of the young white rat. American Journal of Psychology, 11, 80-100.