When the individual comes into play: The role of self and the partner in the dyadic play fighting of rats.

Social play in rats is rewarding and important for the development of brain and social skills. There are differences in the amount of play behavior displayed among individuals, with earlier studies suggesting that, despite variation across trials, individual differences tend to be consistent. In the present study, juvenile Lister-hooded rats were paired with a different, unfamiliar same-sex partner on three days and based on the amount of play each individual initiated, it was characterized as a high, medium or low player. Using this categorization, we explored three features related to individual differences. First, we show that by increasing the number of test days from two, as was done in a previous study (Lesscher et al., 2021), to three, characterization was effectively improved. Secondly, while the earlier study only used males, the present study showed that both sexes exhibit a similar pattern of individual differences in the degree of playfulness. Even though low players consistently initiated less play than medium and high players, all rats varied in how much play they initiated from one trial to the next. Thirdly, we assessed two potential mechanisms by which the playfulness of one rat can modify the level of playfulness of the other rat (i.e., emotional contagion vs homeostasis). Analyses of individuals' contribution to the play of dyads suggest that rats consistently adjust their play behavior depending on the behavior displayed by the partner. Since this adjustment can be positive or negative, our data support a homeostatic mechanism, whereby individuals increase or decrease the amount of play they initiate, which results in the experience of an overall stable pattern of play across trials. Future research will investigate the neural bases for individual differences in play and how rats maintain a preferred level of play.

Atypical play experiences in the juvenile period has an impact on the development of the medial prefrontal cortex in both male and female rats.

In rats reared without play, or with limited access to play during the juvenile period, the dendrites of pyramidal neurons of the medial prefrontal cortex (mPFC) exhibit more branching than rats reared with more typical levels of play. This suggests that play is critical for pruning the dendritic arbor of these neurons. However, the rearing paradigms typically used to limit play involve physical separation from a peer or sharing a cage with an adult, causing stress that may disrupt pruning. To limit this potentially confounding source of stress, we used an alternative approach in this study: pairing playful Long Evans rats (LE) with low playing Fischer 344 (F344) rats throughout the juvenile period. We then examined the morphology of medial prefrontal cortex (mPFC) neurons, predicting that pruning should be reduced. LE rats reared with another LE rat had significantly greater pruning of mPFC pyramidal neurons compared to LE rats reared with a F344 partner. Furthermore, in previous studies, only one sex or the other was used, whereas in the present rearing paradigm, both sexes were tested, showing that play influences neuronal pruning in both. The neurons of the play deficient LE rats not only occupied more space, as determined by convex hull analyses, but the dendrites were also longer than in rats with more typical play experiences. Unlike studies using more stressful rearing paradigms, the present effects were limited to the apical dendritic projections, suggesting that the previously reported effects on the basilar dendrites may have resulted from developmental disruptions caused by stress. If correct, the present findings indicate that play experienced over the juvenile period affects how mPFC neurons develop and function.

Who's laughing? Play, tickling and ultrasonic vocalizations in rats.

Social play in rats is a highly rewarding, energetic form of social interaction and important for development of the brain and social skills. The 50 kHz ultrasonic vocalizations (USV) emitted during social play are thought to be an expression of a positive affective state (laughter), which in some situations may also function as communication signals. Heterospecific play, 'tickling' by an experimenter, is thought to simulate conspecific play, and has been used to improve welfare and to study the neurobiology of positive affect. Given that tickling evokes substantial amounts of USV, we investigated whether heterospecific play is simulating conspecific play by comparing USV-behaviour associations in both contexts. If the 50 kHz calls are merely an expression of 'laughter' then the pattern and type of emission in both contexts should be similar. By contrast, as playing with a conspecific involves a two-way exchange of signalling, the additional demands on communication should lead to a different pattern of calling. While calling was prevalent in both types of play, how the different types of 50 kHz calls are used in the two contexts differed markedly. The findings suggest that while conspecific and heterospecific play are positive experiences, tickling is not the equivalent of conspecific play. This article is part of the theme issue 'Cracking the laugh code: laughter through the lens of biology, psychology and neuroscience'.

Measuring Play Fighting in Rats: A Multilayered Approach.

Rough-and-tumble play or play fighting is an important experience in the juvenile period of many species of mammals, as it facilitates the development of social skills, and for some species, play fighting is retained into adulthood as a tool for assessing and managing social relationships. Laboratory rats have been a model species for studying the neurobiology of play fighting and its key developmental and social functions. However, play fighting interactions are complex, involving competition and cooperation; therefore, no single measure to quantify this behavior is able to capture all its facets. Therefore, in this paper, we present a multilayered framework for scoring all the relevant facets of play that can be affected by experimental manipulations and the logic of how to match what is measured with the question being asked. © 2022 Wiley Periodicals LLC.

Are agonistic behavior patterns signals or combat tactics - or does it matter? Targets as organizing principles of fighting.

During competitive interactions, such as fighting and predation, animals perform various actions, some of which are easy to characterize and label, some of which are reliably repeated. Such 'behavior patterns' are often the measures of choice when comparing across species and experimental contexts. However, as Bob Blanchard and others have pointed out, such measurements can be misleading as in competitive interactions in which the animals compete for some advantage, often the biting or otherwise contacting a particular target on the opponent's body. In this context, the animals' behavior is better analyzed in terms of the tactics of attack and defense deployed by the combatants to gain or avoid contact with those targets. Several examples are shown to reveal that this is an important distinction as simply scoring predefined behavior patterns can obscure the dynamic context in which the actions are performed. This can lead to confounding species and experimental differences and the mislabeling of combat actions as communicatory signals.

Are 50-kHz calls used as play signals in the playful interactions of rats? I. Evidence from the timing and context of their use.

During playful interactions, rats emit increased levels of 50-kHz vocalizations. It is possible that these vocalizations are used as play signals that promote and maintain playful contact. The study investigated this possibility. It was predicted that if these vocalizations are used as play signals, they should be more prevalent (1) before an attack, (2) in attacks leading to wrestling, and (3) in males compared to females, as males play more roughly. Moreover, given that there are at least 15 different subtypes of 50-kHz calls, it is possible that different calls are used in different contexts. Therefore, our prediction (4) was that different subtypes would be used for initiating and terminating playful contact. Pairs of same-sex juveniles were tested so that video recordings of their play and audio recordings of their vocalizations were synchronized. 50-kHz vocalizations occur more often before an attack and in male pairs. Specific calls were associated with specific types of behaviors and these associations differed between male and female rats. However, calls were not more frequent in attacks leading to wrestling than in attacks leading to withdrawal. The data provide qualified support for the hypothesis that 50-kHz vocalizations function as play signals.

Juvenile play experience does not affect nicotine sensitization and voluntary consumption of nicotine in adult rats.

Juvenile play experiences promote behavioral flexibility in rats. If other early positive experiences, such as tactile stimulation, are given prior to exposure to psychostimulants, the behavioral response to the drug is attenuated. The objective of the present study was to determine if the experience of juvenile play behavior would attenuate the response to nicotine. Two experiments were conducted: (1) behavioral sensitization to nicotine exposure, and (2) voluntary consumption of nicotine. For both experiments, rats were reared either with three same-sex peers (play group) or one adult (no play group) during their juvenile period. Then, as adults, half of each group was exposed to repeated injections of nicotine and the other half to saline. Prior play experience had no effect on behavioral sensitization or on voluntary consumption of nicotine. It remains to be determined whether juvenile experience with play influences the rewarding properties of nicotine in social contexts as adults.

Juvenile play experience primes neurons in the medial prefrontal cortex to be more responsive to later experiences.

Juvenile play behavior in rats promotes later behavioral flexibility and appears to do so by modifying the neural systems that regulate the animal's response to unexpected challenges. For example, the experience of play has been shown to prune the dendritic arbor of the cells in the medial prefrontal cortex (mPFC), part of the brain's executive control system. The objective of the present study was to determine if the play-induced changes in the mPFC promotes greater plasticity to experiences later in life. In order to test this possibility, exposure to nicotine was used as the secondary experience given later in life, as it has been shown to produce later changes to the morphology of mPFC pyramidal neurons. Animals were either paired with three same-sex peers (play condition) or one adult (no play condition) during their juvenile period. As young adults, half of the rats from each condition were exposed to repeated injections of nicotine and the other half to injections of saline. The neural plasticity of the mPFC was measured by changes in length and branching of dendrites. Neural changes induced separately by play and by nicotine were consistent with previously published findings. The novel finding was that the cells in the mPFC exhibit a greater response to exposure to nicotine if the rats first had play experience. These findings suggest that juvenile play experiences enhance the plasticity of some neural systems.

Reducing stability of support structure for a target does not alter reach kinematics among younger adults.

Investigation into the reach-to-grasp movement has indicated that this movement sequence is composed of two distinct movement components, independently influenced by the characteristics of the target. It remains undetermined whether properties other than those conveyed by the target also influence the strategy used to complete the task successfully. Here, we explored whether characteristics of the support structure influence reaching kinematics among younger adults. The purpose of the study was to assess whether support structure stability affected movement kinematics of the transport phase. Subjects were required to reach for a full glass of water on a stable or an unstable support structure. Kinematic measures of interest included transport time, peak transport velocity, peak transport acceleration, and timing of kinematic peaks. Analysis showed that reducing the stability of the support structure did not significantly affect any of the measures of interest. The results imply that stability of support structure does not influence transport kinematics among younger adults.

Accelerated nervous system development contributes to behavioral efficiency in the laboratory mouse: a behavioral review and theoretical proposal.

The emergence of the laboratory mouse as a favored species for genetic research has posed a number of problems for scientists interested in the reflection of genetic influences in mouse behavior. It is commonly thought that rat behavior, which has been studied more extensively than mouse behavior, could be easily generalized to mice. In this article, a number of categories of behavior displayed by the mouse (motor, spatial, defensive, social) are reviewed and contrasted with the same categories of behavior displayed by the rat. The comparison suggests that mouse behavior is simpler and more dependent upon elementary actions than the behavior of the rat. We suggest that the behavioral simplification in the mouse adapts it for a different ecological niche than that occupied by the rat. We propose that this simplification may be mediated by accelerated brain maturation during development. We further propose that this developmental acceleration in the mouse renders it less dependent upon complex social behavior and plastic nervous system changes associated with learning than the rat. This difference poses problems for the development of relevant methods of behavioral analysis and interpretation. Since the mouse's biological adaptations will be reflected in laboratory behavior, suggestions are made for behavioral approaches to the study and interpretation of mouse behavior.

Do big-brained animals play more? Comparative analyses of play and relative brain size in mammals.

It has been hypothesized that play is more likely to be present in larger brained species. We tested this hypothesis in mammals using independent contrasts, a method that controls for phylogenetic relatedness. Comparisons across 15 orders revealed that the prevalence and complexity of play was significantly correlated with brain size, with larger brained orders having more playful species. Three orders, Rodentia, Marsupialia, and Primates, were used for within-order comparisons among species and, where possible, among families. The comparisons were not significant for rodents or primates, and those for marsupials yielded inconsistent results. Therefore, although a strong relationship is present at the highest taxonomic level of comparison, it diminishes or evaporates at lower level comparisons.

Sex differences in catalepsy: evidence for hormone-dependent postural mechanisms in haloperidol-treated rats.

Catalepsy, a symptom of Parkinson's disease and related disorders can be produced in rats and other laboratory animals by the blockade of nigrostriatal dopamine using dopaminergic antagonists such as haloperidol. When haloperidol-induced cataleptic rats are placed facing downward on an inclined plane, they will brace against the resulting downward force by pushing backwards, and if they lose postural stability, or their position on the inclined plane, they will jump forward. Females, however, jump from the inclined plane at a significantly lower angle than do males. Frame-by-frame analysis of the jumping sequences revealed that females and males use a different combination of postural adjustments to maintain their position on the inclined plane prior to jumping. Furthermore, gonadal hormone manipulations at birth and in adulthood reveal that these sex differences in postural adjustments are dependent on the organizational effects of gonadal hormones in the perinatal period. These results provide evidence for sex differences in postural support mechanisms and suggest that the sex of subjects, or their hormonal state, must be considered when studying the behavioral aspects of neurological disorders such as Parkinson's disease which include a postural component.

Comparative analyses of the role of postnatal development on the expression of play fighting.

Whether it is that animals are young so that they can play, or whether it is that they play because they are young, play should be more prevalent in species that have a greater degree of postnatal development. This hypothesis is tested by comparative analyses within two mammalian orders (primates and muroid rodents) using independent contrasts. This technique can account for the relative degree of relatedness among the species. For both orders, the complexity or prevalence of play fighting is compared to the degree of prenatal development (neonatal weight/adult weight). In addition, the prevalence of play in primates is compared to prenatal brain development (neonatal brain weight/adult brain weight). Significant negative regressions show that 30% of the variance in the distribution of play in the rodents is accounted for by the degree of prenatal development of body size, and 60% of the variance in play in the primates is accounted for by prenatal brain growth. The findings are thus consistent with the prediction. Species with a greater proportion of their growth occurring postnatally play more and have more complex play than do species with more of their growth occurring prenatally.

Brain size is not correlated with forelimb dexterity in fissiped carnivores (Carnivora): A comparative test of the principle of proper mass.

To test the hypothesis that brain size and forelimb dexterity are positively correlated, the relative brain size of 41 species of fissiped (terrestrial) carnivores (Order: Carnivora) was examined with respect to their forelimb use during feeding. With the use of a newly derived dexterity index, the forelimb dexterity executed by each of the species was calculated as a single, continuous variable which was then regressed against the residuals of brain size. To account for confounding effects of phylogenetic inertia, the analysis was performed with independent contrasts analysis using a speciational model of evolutionary change (i.e. equal branch lengths). The results suggest that relative brain size and isocortex size are not correlated with the dexterity of the proximal or distal segments or a combination of the two (total forelimb dexterity). The presence of species with widely different brain sizes and similar dexterities, and vice versa, suggests that an increase in the amount of neural substrate might not be necessary for the production of finely coordinated forelimb movements. It is suggested that this outcome is representative of the plasticity of both mammalian brain size and behavior and that variations in brain size and forelimb dexterity could be linked to disparate ecological and phylogenetic factors which act in concert to promote or constrain neural development and behavior in different species.

The development of a sex-differentiated defensive motor pattern in rats: A possible role for juvenile experience.

When protecting a food item held in the forepaws, rats will dodge laterally away from an approaching conspecific. Both males and females dodge, but do so differently, with females pivoting around the pelvis and males pivoting around the midbody. While females tend to end the dodge with their rumps opposing the other rat's midbody, males typically oppose the head. In this study, two developmental factors were investigated for their role in the genesis of this sex-differentiated motor pattern: (a) Dodging by males and females was analyzed before and after puberty to ascertain whether the differential pattern of movement was associated with the pubertal change in pelvic morphology, and (b) Dodging by adult males and females that had been raised without social interaction from weaning was analyzed to ascertain whether experience in the juvenile phase of development was necessary. In both studies, males and females performed the sex-typical version of the dodging motor pattern regardless of age or test condition. However, orienting to the head of the opponent was disrupted in males reared in social isolation, a feature of dodging that developed between weaning and puberty. Therefore, the evidence is consistent with the view that while the sexual differentiation of the motor organization of dodging develops without the need for experience, the males' ability to direct this motor pattern with the correct orientation towards the opponent requires some prepubertal experience.

Is digital dexterity really related to corticospinal projections?: a re-analysis of the Heffner and Masterton data set using modern comparative statistics.

Using a data set of 69 different mammalian species, Heffner and Masterton propose that the longer and deeper the fibres of the corticospinal tract, the greater an animal's digital dexterity. Because of the effects that phylogeny may have upon the extant phenotype of a given species, however, data from a wide range of species can rarely be considered to represent fully independent data points. Using modern comparative statistics, which incorporate phylogenetic information, we reanalysed their data set such that the assumption of independence was not violated. If Heffner and Masterton's hypothesis is correct, then one would expect evidence of strong correlated evolution between corticospinal tract anatomy and digital dexterity once the effects of the phylogenetic relationships between the species in the data set have been removed. The results show that a distinct bias in the number of primate species sampled by Heffner and Masterton significantly affected their findings. Furthermore, once phylogeny has been taken into account, only the length of the corticospinal tract fibres showed a significant relationship with two out of the four behaviours analysed, digital dexterity and hand-eye coordination. Based upon our results we recommend the use of modern comparative statistics for synthesising neural structure and behaviour, rather than examining structure function relationships in an ahistorical context. It is also evident that there is a need for data on the length and depth of the corticospinal fibres for a greater range of species so that the relationship between the corticospinal tract structure and motor behaviour for mammals as a whole can be more readily interpreted.

The developmental onset of a rudimentary form of play fighting in C57 mice.

Play fighting in its most elaborate form involves nonagonistic wrestling between pairmates, where one partner grabs, holds, bites, or otherwise contacts the other. Such play occurs in the absence of the functional consequences associated with serious fighting (e.g., resource acquisition or protection). Typically, the biting, nosing, or grooming contact during play fighting is directed at specific body targets. House mice have been classified as a species that lacks such play, even though play fighting is present in closely related species such as the rat. In this study, six litters of C57 mice were observed daily from the week before weaning until the week after weaning (15-30 days postnatally). Thirty-min videotaped records were collected daily for each litter. Consistent with other studies, over 85% of all play involved locomotor play, and most of the social play involved noncontact locomotion (86%). However, a rudimentary pattern of the "attack and defense" typical of play fighting was found to occur, albeit at a low frequency (2% of all play). Most playful attacks involved snout contact with the partner's rump, but evidence is provided that suggests that this rump contact may be transitory, with the nape area being the primary target for play. Most of the playful attacks elicited playful defense (97%), which in all cases involved the defender evading such contact by leaping or running away, or by dodging laterally away from the attacker. Therefore, there appears to be directed playful attacks in this species, with defense limited to evasion. Defensive tactics leading to wrestling were never observed. That is, play fighting in mice involves only a small subset of what other species, such as rats, exhibit. Nonetheless, the basic components of attack and defense are present in mice.

Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses.

Play fighting is a commonly reported form of play in the young of many mammals. Most of the studies on the neurobehavioral mechanisms regulating this behavior have focused on the laboratory rat. The rationale for doing so has been primarily on practical grounds. This paper seeks to answer the question. "How good is the rat as a model of mammalian play fighting?" A review of the detailed structure of play fighting in rats and other mammals reveals that play fighting is not a unitary activity, but rather has distinct components with each having distinct regulatory mechanisms. The rat is typical of many other mammals for some features of play fighting, but not others. Therefore, two conclusions are drawn from this review. First, given that play fighting is a composite category of behavior, questions regarding its underlying neurobehavioral mechanisms need to be narrowly constructed, so as to deal with highly specific mechanisms. For example, what mechanism regulates the pubertal decline in play fighting? Second, the rat is shown to be a good model species for the study of some features of play fighting, but it cannot be assumed to represent an "average" mammal for all features.

Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species.

Order Rodentia comprises a vast portion of mammalian species (1814 species), which occupy extremely diverse habitats requiring very distinct motor specializations (e.g. burrowing, hopping, climbing, flying and swimming). Although early classification of paw use ability suggests rodents are impoverished relative to primates and make little use of their paws, there have been no systematic investigations of paw use in rodents. The present study was undertaken to describe limb/paw movements in a variety of common rodents. The movements used for handling sunflower seeds and other foods were videorecorded and analyzed in the guinea pig (Cavia porcellus), Mongolian gerbil (Meriones unguiculatus), Syrian hamster (Mesocricetus auratus), laboratory mouse (Mus musculus), laboratory rat (Rattus norvegicus), gray squirrel (Sciurus carolinensis), red squirrel (Tamiasciurus hudsonicus), Richardson's ground squirrel (Spermophilus richardsonni), prairie dog (Cynomus parvidens), and Canadian beaver (Castor americanus). The results suggested five order-common movements of food handling: (1) locating food by sniffing, (2) grasping food by mouth, (3) sitting back on the haunches to eat, (4) grasping the food using an elbow-in movement, and (5) manipulate the food with the digits. Different species displayed species-typical specializations including (1) bilateral grasping with the paws (gerbil), (2) unilateral grasping with a paw (beaver), (3) unilateral holding (ground squirrels), (4) various grip and digit postures (all species), (5) unilateral object removal from the mouth (gerbil), (6) bilateral thumb holding (squirrels), and (7) simultaneous holding/manipulation of two objects (squirrels). Only the guinea pig did not handle food with its paws, suggesting its behavior is regressive. The existence of a core pattern of paw and digit use in rodents suggests that skilled limb and paw movements originate at least with the common ancestors of the rodent, and likely the common ancestor to rodent and primate lineages, while species-typical movements suggest specialization/regression of limb use has occurred in a number of mammalian orders.

Mechanisms underlying the absence of the pubertal shift in the playful defense of female rats.

Due to the action of testicular hormones in the perinatal period, juvenile male rats engage in more play fighting than juvenile females. Also, following puberty, males, but not females, switch to using adultlike defensive tactics more frequently during play. This change in play is also due to the action of testicular hormones perinatally. In this study, two experiments were conducted to determine if the pubertal transition in defense could be induced in females. For Experiment 1, male and female cagemates were tested before and after puberty with familiar and unfamiliar partners. Even when playfully interacting with subadult males, females did not increase the use of the adultlike defensive tactics. For Experiment 2, neonatal females were either injected with testosterone propionate (TP) or ovariectomized (OVX), and again tested before and after puberty. While the TP-treated females had higher frequencies of play fighting, they did not change their pattern of defense following puberty. The OVX females exhibited the lower frequency of play fighting typical of females, but changed their pattern of defense with increased age. Thus, it appears that the pattern of pubertal change in playful defense typical of males is inhibited by ovarian hormones. The mechanisms by which ovarian hormones could exert this effect on developing females are discussed.