Role reversal changes during the ontogeny of play fighting in male rats: Attack vs. defense

From weaning until sexual maturity, the rates at which young male rats hold each other supine during play fighting appear to become progressively asymmetrical. These changes have been previously thought to reflect an initial lack of dominance and a later development of dominance-subordinance relationships. In this paper it is shown that pairs of male rats exhibit asymmetries in playful attack and playful defense throughout development. The changes, resulting in greater asymmetry of pinning rates, are shown to result from age-dependent changes in defensive tactics; the relationship, therefore, remains constant while the form of the behavior changes. Furthermore, it is not the animals showing the highest rates of playful attack who become dominant in older ages.     

Neonatal testosterone augmentation increases juvenile play fighting but does not influence the adult dominance relationships of male rats

Neonatal male rats were either injected subcutaneously with testosterone propionate (TP) or oil vehicle. When weaned, each treated pup was paired with an untreated male sibling. The play fighting of TP-and oil-treated rats were compared at the juvenile phase (30–36 days), and in adulthood (84–90 days). In the juvenile phase, the rate of initiating playful attacks was significantly greater for TP-treated rats. Playful defense in response to such attacks did not differ between TP- and oil-treated rats. At the completion of the study, cortical thickness was measured for all the groups of rats. Oil treatment decreased overall cortical thickness relative to untreated pairmates, whereas TP treatment did not. Both oil and TP treatment abolished the asymmetry in hemispheric thickness, which was present in the untreated pairmates. The reversal of at least one of these injectioninduced changes in the cortex by TP provided independent evidence for the effectiveness of the TP treatment. As adults, neither the TP treatment nor the oil treatment influenced which pairmate became dominant. Dominance was judged by which pairmate initiated less playful attacks. Therefore, it is concluded that the early neonatal testosterone surge is not likely to be a factor in influencing the behaviors that lead to adult dominance. In contrast, play fighting is influenced by hormonal events in this early neonatal phase. It thus appears that play fighting and the aggressive systems subserving dominance relationships are differentially controlled. © 1992 Wiley-Liss, Inc.     

Juvenilized play fighting in subordinate male rats

As pairs of male juvenile sibling rats that are housed together become sexually mature, they develop a dominance-subordinance relationship. These dominance relationships appear to be reflected in the play fighting of the pairmates both as juveniles and as young adults, in that the seemingly subordinate partner initiates more playful attacks at both ages. However, as adults, even though it is the subordinate that initiates more playful attacks, it is the subordinate that is pinned on his back by the partner most often. Dominant pairmates were found to switch to defensive patterns typically found in adult males. In contrast, the subordinates, when contacted on the nape, were more likely to retain the juvenile pattern of turning over to supine. Therefore, the subordinate pairmate of an adult pair of male siblings both initiates more playful attacks and defends itself in a more juvenile manner than its dominant partner, and this leads to it being pinned more frequently. This pattern of behavior by subordinate rats is suggested to function as a friendship maintenance mechanism permitting co-existence in multimale colonies.     

Open-field and avoidance behavior after neostriatal lesions in male and female rats.

The behavioral effects of lesions of the anterodorsal or posteroventral parts of the caudate-putamen were studied in adult male and femle rats that were gonadectomized or left untreated prior to brain surgery. Anterodorsal (ADC) lesions consistently impaired acquistion of one-way avoidance behavior and tended to interfere with the development of a two-way avoidance response; comparable effects were observed in gonadectomized and intact animals of both sexes. By contrast, ADC lesions increased activity in the open field only in intact females and increased rearing only in ovariectomized females. Posteroventral caudate (PVC) lesions caused transient aphagia and adipsia in both sexes but did not consistently affect open-field activity or the acquistion of one-way avoidance responses by either sex. These lesions profoundly impaired acquistion of shuttle box avoidance responses by intact males. By contrast, castrated males and intact and ovariectomized females with PVC lesions avoided normally in the shuttle box. The present results suggest that localization of behavioral functions within the striatum differs with the sex of the subject, in part because of activational effects of gonadal hormones.     

Targets and tactics of agonistic and precopulatory behavior in montane and prairie voles: Their relationship to juvenile play-fighting

Play-fighting by juvenile montane and prairie voles involves attack and defense of the head, neck and shoulders. Since during play animals typically borrow behavior patterns from other functional contexts, two adult behavioral contexts were compared to juvenile play-fighting. These were serious fighting and sexual encounters. During serious fighting in a resident-intruder paradigm, most bites are directed at the rump and lower flanks. During sexual encounters, especially in precopulatory behavior, the head, neck and shoulders are gently contacted. Therefore, play-fighting by juveniles would appear to involve attack and defense of areas of the body contacted in adult precopulatory behavior, not adult fighting. Furthermore, the species-specific differences in juvenile play-fighting were also found to be matched by species-specific differences in precopulatory behavior. In both playful and precopulatory encounters, montane voles contacted the head and used upright defensive behaviors more often than prairie voles. In contrast, prairie voles made mutual contact more often and were more likely to rotate to supine in defense of contact to the nape and head. These findings support our hypothesis that juvenile play-fighting in muroid rodents involves the precocial expression of precopulatory, not agonistic behavior.     

Some subordinates are more equal than others: Play fihgting amongst adult subordinate male rats

Adult male rats living together form dominance relationships, with one dominant and the remainder adopting subordinate roles. In previous studies, it was shown that in adult male pairs, the subordinate rat initiates more playful contacts and retains a more juvenile response to the playful contacts by the dominant. In this experiment, triads were used to examine the play between subordinate males. The subordinates directed fewer playful contacts to each other than to the dominant rat, and there was a symmetrical play relationship between the subordinates. After the dominant was removed from the colony, one subordinate became the dominant. Playful interactions amongst these pairs increased, with the subordiante intiating more playful contacts than the dominant. Furthermore, from a similarly low frequency of juvenile-type response to playful contact to each other when in triads, the subordinate in the dyads increased its frequency of juvenile responses to the dominant partner. This supports the hypothesis that the playful behavior of subordinate male rats towards the dominant is an adaptive response, playful behavior of subordinate male rats towards the dominant is an adaptive response, serving a “friendship maintenance” function. Finally, when in triads, one subordinate was more playful with the dominant than the other subordinate. It was the least playful subordinate that was the most likely to become the dominant. This sugests that within a colony, not all subordinates are the same. © 1993 Wiley-Liss, Inc.     

Influence of dominance on the development of play fighting in pairs of male Syrian golden hamsters (Mesocricetus auratus)

In the highly social rat, male juvenile and adult subordinates initiate more playful contacts with dominant pairmates than vice versa. This study examined the effect of dominance on playful contacts in the relatively asocial golden hamster. Pairs of male hamsters were reared together from weaning, and their play was filmed in the juvenile (28-36 days) and the young adult (60-70 days) stages of development. By the adult stage, it became clear that one pairmate was dominant over the other. The dominant pairmate launched all aggressive attacks (i. e., bites to the lower flanks and rump), and the subordinate pairmate performed all the submissive gesturing (e. g., tail up submissive posture). Playful contact, which in this species involves gentle nibbling of the posterior cheeks, was more frequently launched by the dominant than by the subordinate. This was not only true at the adult stage, but also at the juvenile stage, before dominance-subordination relationships were sharply polarized. Therefore, it would appear that in the relatively asocial hamster, the subordinates tend to avoid playful contact with dominants. This is markedly different to rats, where the subordinates actively seek out and engage dominants in play. This contrast further supports our hypothesis that subordinate male rats use play as a means of maintaining familiarity with dominants. © 1993 Wiley-Liss, Inc.     

Neonatal androgenic stimulation and adult sexual behavior in male and female golden hamsters.

Neonatally and adult castrated male hamsters as well as neonatally androgenized and nonandrogenized female hamsters were tested for both mounting and lordosis behaviors during treatment with either testosterone or ovarian hormones. Neonatal androgenization facilitated mounting behavior in adult animals administered either testosterone or ovarian hormones and suppressed lordosis behavior in adult ovarian-hormone-treated animals. Early androgen effects on the display of lordosis behavior during adult testosterone treatment were complex and varied with the exact timing of perinatal endogenous or exogenous androgenization. Species differences in hormone-behavior relationships and the possible role of perinatal androgenization in the development of rodents' ability to aromatize androgens were discussed.     

Adolescent Neurodevelopment and Psychopathology

Adolescence is a high-risk period for the onset of psychopathology. The occurrence of depression increases markedly in the years following the onset of puberty, and most individuals who are eventually diagnosed with a psychotic disorder show a marked rise in adjustment problems during adolescence. It is well established that puberty involves increases in the secretion of gonadal hormones. More recently, research has shown that stress hormones show a similar normative rise following puberty. Accumulating findings indicate that the postpubescent period is also characterized by significant neurodevelopment; there are changes in brain structure and function that are partially a consequence of hormonal factors. Researchers are now challenged to elucidate the neural mechanisms relating postpubertal neurodevelopment with the elevations in risk for psychopathology that characterize adolescence. One plausible mechanism is the effect of hormones on gene expression. The normal neuromaturational processes observed in adolescence partially reflect the effect of gonadal hormones on the expression of genes that control brain development. Hormone surges following puberty may also trigger the expression of genes that code for brain abnormalities that give rise to mental disorders.     

Learning strategy is influenced by trait anxiety and early rearing conditions in prepubertal male, but not prepubertal female rats

Rodents solve dual-solution tasks that require navigation to a goal by adopting either a hippocampus-dependent place strategy or a striatum-dependent stimulus-response strategy. A variety of factors, including biological sex and emotional status, influence the choice of learning strategy. In these experiments, we investigated the relationship between learning strategy and anxiety level in male and female rats prior to the onset of puberty, before the activational effects of gonadal hormones influence these processes. In the first experiment, prepubertal male rats categorized as high in trait anxiety at 26days of age exhibited a bias toward stimulus-response strategy at 28days of age, whereas age-matched females exhibited no preference in strategy regardless of anxiety level. In the second experiment, male and female rats were separated from their dams for either 15 or 180min per day during the first 2weeks of life and tested on a battery of anxiety and cognitive tasks between 25 and 29days of age. Prolonged maternal separations for 180min were associated with impaired spatial memory on a Y-maze task in both prepubertal males and females. Furthermore, prolonged maternal separations were linked to elevated anxiety and a bias for stimulus-response strategy in prepubertal males but not females. Alternatively, brief separations from dams for 15min were associated with intact spatial memory, lower levels of anxiety, and no preference for either learning strategy in both sexes. These results provide evidence of sex-specific effects of trait anxiety and early maternal separation on the choice of learning strategy used by prepubertal rodents.     

Variations in sex-related cognitive abilities across the menstrual cycle

Sex differences in human cognitive and motor skills may in part be due to organizational or activational effects of sex hormones on the brain. In this study, an extensive battery of cognitive and motor tests was administered to normally cycling women at two phases of the menstrual cycle, in order to detect any hormone-mediated changes in performance. Results confirmed changes across the menstrual cycle on a variety of speeded manual and articulatory measures, and on some nonverbal/spatial tests. The results provide qualified support for the hypothesis that the high levels of gonadal steroids provide qualified support for the hypothesis that the high levels of gonadal steroids present at the luteal phase of the cycle may facilitate skills favoring females, but be detrimental to skills favoring males. The implications of these results for research in the area of human sex differences are discussed.     

Beyond the evil empire: Horseplay and aggression

The dominant mode of studying the antecedents of human aggression in psychology has been to look for these precursors in negative life events, for example, being physically punished, observing models using aggressive means, or experiencing forms of privation or frustration. In contrast, within the ethological literature, certain playful activities, in particular “play fighting,” have been interpreted as crucial precursors of later social activities, both aggressive and nonaggressive. Among humans, horseplay, which may be considered synonymous with play fighting, has only rarely been mentioned in psychological literature and scarcely ever in relation to aggression. Within this study, college students rated the extent to which they had engaged in horseplay and in aggressive acts with same-sex friends and boyfriends or girlfriends over the past 3 years. Analyses indicated that a broad range of playful and aggressive activities was reported by a large proportion of the sample. Results also indicated strong relationships between the tendency to horseplay and to aggress. The relationship was strongest for men with men friends and for women with boyfriends. In general, having steady relationships increased the likelihood that both horseplay and aggressive acts would occur. Weekend alcohol consumption was related to playful activities; heavier use correlated with greater aggressive activities of men with men only. The study suggests that it is useful to broaden the base for conceptualizing aggression to take into account the ways in which playful and friendly activities can facilitate those that are regarded as antisocial and aggressive.     

Aggressive behavior in female hamsters: the hormonal basis for fluctuations in female aggressiveness correlated with estrous state

The frequency and sequencing of aggressive behaviors by naive female hamsters change during series of brief encounters, probably because of the lack of stable dominance relations. Such initial encounters seem most representative of interactions likely in free-ranging hamsters and have been emphasized in studies of the hormonal mediation of female aggression. Nonestrous females exhibit intense aggression toward conspecifics of either sex. Estrous females are not aggressive and spend much time in lordosis, indicative of sexual receptivity. The inhibition of fighting on estrous day depends on estrogen and progesterone. Whereas oil-injected adrenalectomized-ovariectomized females fight at high levels, comparable with intact nonestrous females, the combination of 17 beta-estradiol benzoate and progeterone suppresses fighting completely. In contrast, replacement of estradiol, progesterone, or testosterone propionate individually has on consistent effect. Hypophysectomized females also fight at high levels, indicating that pituitary hormones are not required for vigorous aggression. Further, individual anterior pituitary hormones did not produce marked changes in fighting. These results emphasize the roles of estrogen and progesterone in synchronizing aggression with current reproductive state.     

Children's hostile attribution bias is reduced after watching realistic playful fighting, and the effect is mediated by prosocial thoughts

Hostile attribution bias (HAB) has been found to characterize aggressive children. Watching prosocial media has been shown to have positive effects on children, and the general learning model has been used to account for these observations. This study tested the hypotheses derived from this theory that exposure to playful fighting would lead to a reduction in HAB, both immediately and after a 1-day delay, and that this effect would be mediated by positive thoughts. Four studies exposed child participants (N=242) to playful fighting versus neutral behavior primes and then tested their HAB. In two studies, thoughts about playful fighting and about children were assessed and tested as mediators. The main hypotheses were supported. The positive effect of watching playful fighting on HAB was evident immediately but not after 1 day. This effect was mediated by positive thoughts. In line with the general learning model, watching playful fighting reduced HAB in children, and positive thoughts contribute to this effect. This extends the realm of the general learning model and suggests interventions to help children avoid aggression.     

Playful defensive responses in adult male rats depend on the status of the unfamiliar opponent

Adult male rats reared as pairmates from weaning were tested in a neutral arena with both members of another pair (one at a time). The unfamiliar pairs were found to engage in play fighting, although they were more likely to escalate the encounter into serious fighting than were pairs of familiar rats. Based on their within‐home pair behavior, each pairmate was designated as a dominant or a subordinate. When the test encounters between unfamiliar males were analyzed with regard to whether the pairings consisted of two dominants, two subordinates, or a mixed pair, the pattern of play fighting was found to be attenuated. Both dominants and subordinates were more likely to initiate playful encounters, to respond defensively during these encounters, and to do so using adult‐typical tactics of defense when paired with an unfamiliar rat that was dominant in its home cage. The mechanisms by which the home status of unfamiliar male rats can be identified by another male are discussed, particularly with regard to the role that play fighting may serve for this function. It is concluded that the data support the hypothesis that play fighting can be used by adult rats for social testing, which in this case seems to involve ascertaining the opponent's fighting capability. Aggr. Behav. 25:141–152, 1999. © 1999 Wiley‐Liss, Inc.     

The use of the bared-teeth display during play fighting in Tonkean macaques (Macaca tonkeana): sometimes it is all about oneself

Play signals are viewed as important means by which animals inform each other that bites, strikes, and throws that occur during play fighting are indeed playful rather than serious. One such signal is the open mouth play face that is common in primates and many other mammals. Unfortunately, as most play fighting involves biting, it can be ambiguous as to whether any instance of opening the mouth is performed to communicate playful intent or is simply a preparation for biting. In this study, open mouths co-occurring with the bared-teeth display (teeth-baring) in Tonkean macaques were used to assess the context in which facial gestures only relevant for signaling (i.e., teeth-baring is not necessary for biting) are used during play. Two predictions arising from the hypothesis that play signals are used to facilitate playful contact were tested: that the open mouth with teeth-baring should (1) be most frequent preceding contact, and (2) that it should be performed most often when bites are directed at orientations that is visible to the recipient. The data only partially support these predictions. The open mouth with teeth-baring is also frequently used when a monkey withdraws from playful contact. Moreover, it is associated with bites to body targets, such as the rump, that offer little prospect for detection by the recipient; this supports the possibility that play signals may sometimes be emitted not to communicate with the partner but with the performer itself. Thus, play signals serve multiple functions during play fighting.     

Targets,tactics, and the open mouth face during play fighting in three species of primates

The play fighting of many mammals involves the nonserious use of behavior patterns derived from serious fighting. A major question of theoretical importance has been that of how, given this overlap in patterns of behavior, the animals can distinguish between playful and nonplayful intent. One proposed solution is that animals use play signals to inform each other about the playful intent of their actions. The most widely reported play signal amongst primates is the open mouth play face. The manner in which this so-called signal functions is based on correlational evidence, with most reports simply noting its presence or absence in a given species. This study involved a detailed video-based analysis of the occurrence of open mouths during the play fighting of three species of primates. One captive troop each of ring-tailed lemurs, black-handed spider monkeys, and patas monkeys was used. By examining all open mouths in the context of the species-typical style of play fighting, several conclusions were empirically verified. 1) Most open mouths occur as a functionally necessary precursor for biting. 2) Some open mouths occur as a defensive threat which deters further contact. 3) The residual open mouths which may function as contact promoting play signals, constituted about 20–25% of all open mouths by the lemurs and patas monkeys, but less than 5% for spider monkeys. These species differences appeared to arise from two causes. Firstly, the spider monkeys used another signal, the head shake, in situations where lemurs and patas monkeys used open mouths. Secondly, the style of play fighting greatly influenced the frequency and duration of open mouths. This was most marked in the face-to-face combat style of patas monkeys. These findings show that comparative studies of the occurrence and function of play signals need to take into account species-typical styles of playful combat. Aggr. Behav. 23:41–57, 1997. © 1997 Wiley-Liss, Inc.     

Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus

Play-fighting is often difficult to differentiate from inhibited or immature serious fighting because both may utilize many of the same behavior patterns. In the rat the two behaviors involve different targets of attack. During play-fighting, snout or oral contact is directed at the opponent's nape of the neck, whereas during serious fighting, male residents mostly direct their bites at the intruder's rump. Although similar to those used in serious fighting, the behavior patterns used during play-fighting are modified to achieve the different targets of attack. Even though the tactics of attack and defense appear more adult-like with increasing age, the playful targets persist well into adulthood.     

Agonistic versus amicable targets of attack and defense: Consequences for the origin,function, and descriptive classification of play-fighting

Play-fighting appears to involve the behavior patterns of attack and defense otherwise seen in serious fighting. The degree of similarity, however, depends on the body targets attacked and defended during these forms of fighting. For many taxa, including diverse mammalian families and some birds, the same targets are attacked and defended during both play-fighting and serious fighting. However, for several species of muroid rodents, the targets of play-fighting are not the same as those of serious fighting. In these cases, the tactics of attack and defense are also different. It is argued that for these muroid species the playful targets have arisen from amicable behavior (e.g., social investigation, greeting, allogrooming) rather than, as appears to be the case in so many other taxa, from agonistic behavior. These data strongly suggest that “play-fighting” has evolved from different precursors in different taxa and thus has multiple origins. Furthermore, these data have an important bearing on the universal applicability of many of the suggested functions of play-fighting and also on how such behavior is to be described and classified.     

Stress-induced progesterone secretion and progesterone receptor immunoreactivity in the paraventricular nucleus are modulated by pubertal development in male rats

Male rats show a differential adrenocortical response to stress before and after pubertal development, such that prepubertal animals have a more prolonged stress-induced corticosterone response compared to adults. Whether pubertal maturation affects other adrenocortical responses to stress is currently unknown. To address this question, we assessed stress-induced progesterone secretion in both intact and gonadectomized prepubertal (28 days of age) and adult (77 days of age) male rats either before or after exposure to a 30 min session of restraint stress. We found that prepubertal males show a greater and more prolonged stress-induced progesterone response compared to adults. We also found a similar effect in castrated prepubertal and adult males, indicating the differential stress-induced progesterone response is not gonadal in origin. We also examined progesterone receptor (PR) levels by immunohistochemistry in the paraventricular nucleus (PVN) of the hypothalamus, a key regulatory nucleus of the hypothalamic-pituitary-adrenal (HPA) axis, and found lower PR protein expression in the PVN of prepubertal compared to adult males. These data indicate that in addition to corticosterone, stress-induced adrenocortical progesterone levels are differentially affected by pubertal maturation. Furthermore, these data raise the possibility of different progesterone sensitivity of the PVN before and after puberty. The significance of this differential response is presently unknown. However, given the pleiotropic effects of progesterone on male physiology and behaviour, it is likely that the disparate post-stress exposure to progesterone affects the prepubertal and adult male differently.