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.

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.

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.

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.

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.

Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play.

Play fighting is the most commonly occurring form of social play in juvenile mammals. Typically, males engage in more play fighting than females, and this difference has been shown to depend on the action of androgens perinatally. It is generally believed that the differences in play fighting between the sexes are quantitative and do not involve qualitative differences in the behavior performed. We show that this is an incorrect characterization of sex difference in play fighting. For example, in laboratory rats, there are at least five different mechanisms that contribute to the observed sex differences in play fighting. These mechanisms involve (I) the motivation to initiate play, (II) the sensory capacity to detect and respond to a play partner, (III) the organization of the motor patterns used to interact with a partner, (IV) age-related changes at puberty in initiating play and in responding to playful contact, and (V) dominance-related changes in adulthood in the pattern of playful interaction. Sex differences in the play fighting of rats are due to an interaction of all of these mechanisms, some of which are sex-typical not play-typical, and involve both quantitative and qualitative differences. This is clearly different from the prevailing view that play fighting is a unitary behavior which is masculinized perinatally. Indeed, even though all five mechanisms are androgenized perinatally, the sensorimotor differences also involve defeminization (i.e. reduction of female-typical qualities). This expanded view of the mechanisms contributing to the sex differences in play fighting has implications for both the analysis of the neural systems involved, and for the functional significance of this activity in childhood and adulthood.

A kinematic analysis of sex-typical movement patterns used during evasive dodging to protect a food item: the role of testicular hormones.

Feeding rats dodge laterally away from a conspecific attempting to steal their food. Dodges by female and male rats differ in their composition of movement. Females pivot around a point more posterior on the longitudinal axis than do males, producing a greater amount of movement of the snout in relation to the pelvis. This experiment examined the role of testicular hormones on these sex-typical movement patterns. Castration at weaning (21 days) does not affect the male-typical pattern. Neonatal testicular hormone manipulation, however, does alter sex-typical patterns of movements. Whereas castration neonatally makes male rats more female-like, injections of neonatal female rats with testosterone propionate make them more male-like. These findings suggest that the organization of sex-typical patterns of dodging involves perinatal action of gonadal hormones. Results are discussed in relation to anatomy, neural structure, and the role of gonadal hormones during development.

Previous experience disrupts atropine-induced stereotyped "trapping" in rats.

Three experiments were conducted to investigate the phenomenon of atropine-induced stereotypic trapping in rats reported by Schallert, De Ryck, and Teitelbaum (1980). The first two showed that such trapping was disrupted by previous experience with the specific trapping task or the test context alone. The third showed that, in response to the test context, specific behaviors were altered in rats experienced with the context. Inexperienced atropine-treated animals moved slowly and showed a strong thigmotaxis to surfaces with the body and particularly the snout. The hindquarters did not cooperate well with the movements of the forequarters. In contrast, atropine-treated animals familiar with the context moved with medium-speed, coordinated movements, were independent of surface contact with body and snout, and the hindquarters cooperated fully with forequarter movements. These reactions of drugged animals were exaggerated forms of those of undrugged animals to the unfamiliar and familiar context, respectively. Thus, atropine enhances the reactions of the rat to both a novel and a familiar environment. The enhanced reactions to a novel environment appear as stereotyped behaviors that trap the animal in particular configurations of surfaces. The enhanced reactions to a familiar environment abolish the stereotypic trapping normally produced by atropine. This pattern of results indicates that it is not atropine per se that leads to trapping. Rather, stereotypic trapping develops as a consequence of an interaction between the adaptive responses of the rat to a novel environment and atropine.

Morphine subtracts subcomponents of haloperidol-isolated postural support reflexes to reveal gradients of their integration.

Although cataleptic rats do not spontaneously orient, scan, or walk, they will cling, stand, right themselves in the air, and resist being displaced from a stable position (Schallert, Whishaw, De Ryck, & Teitelbaum, 1978). Morphine produces a state of immobility in which all reflexes used for stable static support (e.g., standing, righting, clinging, and bracing) appear to be inhibited (De Ryck, Schallert, & Teitelbaum, 1980). Addition of morphine to haloperidol abolished or reduced those reflexes used to defend against slow postural displacements (e.g., bracing) but left intact those used to protect against fast postural displacements (e.g., righting in the air). However, although intact, these responses to fast postural displacements were completely abolished by labyrinthectomy, showing that they were controlled only by vestibular inputs. During recovery from morphine's effects, the responses to slow postural displacements reemerged, revealing fractional subcomponents. Furthermore, the reorganization of the subcomponents proceeded along specific body gradients; for example, bracing and standing reemerged caudorostrally, while at the same time, righting and clinging reemerged rostrocaudally.

Escalation of feline predation along a gradient from avoidance through "play" to killing.

In this article, we show that feline predation involves a continuous gradient of activation between defense and attack and that predatory "play" results from an interaction of the two. Benzodiazepines (oxazepam, diazepam) escalated attack toward killing, so that cats that had avoided mice prior to the drug now played with them, cats that had originally played now killed, and cats that killed mice now did so with less preliminary contact. In such shifts, no sharp demarcation between play and predation was evident. Lateral hypothalamic lesions disrupted the escalation of attack. During recovery, attack was escalated once again along the gradient toward killing, but in the absence of both defense and play. A similar result was obtained in intact killers and nonkillers by the application of mild tail pinch. These results suggest that play with prey is a misnomer for predatory behavior that fails to escalate along the gradient between defense and attack. Movement notation analysis revealed that playful movements are adaptive in that they protect the cat from injury.

What do rats find rewarding in play fighting?--an analysis using drug-induced non-playful partners.

Play fighting by juvenile rats involves playful attacks directed at the partner's nape, where successful contact leads to gentle rubbing of the snout into the nape area. In addition, the recipient of such contact may defend the nape by adopting tactics of playful defense. The two most common defensive tactics in the juvenile period are evasion, where the recipient swerves or leaps away and facing defense involving rotation to supine, where the attacker is faced and its further attempts to contact the nape are blocked. An unresolved issue is whether the nape contact itself or defense by the recipient alone or in combination with nape contact, are involved in rewarding play fighting. In this study, drug-induced non-playful partners were used to test the 'motivation' for play fighting when only playful nape contact was possible. In drug-trials compared to baseline and saline trials, both neonatally androgenized females (high players) and control, oil-treated, females (low players), decreased the frequency of launching nape attacks. These results suggest that nape contact alone, in the absence of defense by the recipient, is not sufficient reinforcement for such playful activity, irrespective of the initial playfulness of the subjects. However, while nape attacks decrease, other forms of social contact, such as anogenital investigation and climbing over the partner (i.e., crawl overs), increase in frequency. These results suggest that non-playful partners are not neutral targets for normal rats. Rather, the 'non-normal' behavior of the drugged target may affect the subjects' behavior in such a way as to reduce their playfulness for reasons other than reduced reinforcement for play.

Intrinsic and extrinsic influences on play fighting in rats: effects of dominance, partner's playfulness, temperament and neonatal exposure to testosterone propionate.

Play fighting is a frequent activity of juvenile rats and appears to show marked variability amongst individuals in that some rats play a great deal and others very little. This study attempted to identify some of the factors involved in producing this individual variability. The major influence over an individual's frequency of play as a juvenile was found to be the frequency of play by the partner. That is, play appears to be contagious, in that a high playing animal stimulates its partner to play frequently as well. In male juveniles, but seemingly not in female juveniles, the subsequent adult status of one partner as dominant influences the subordinate-to-be to initiate more playful contacts. In addition to these extrinsic influences, however, there appear to be intrinsic factors that influence whether an individual is a high or low playing animal. One intrinsic factor appears to be 'boldness', so that bolder animals tend to initiate more playful contacts. Higher players tend to be more susceptible to the stereotypy-inducing effects of the dopamine agonist, apomorphine, and tend to be more dependent upon the playful activity of the partner to maintain their own high levels of play. Both of these characteristics are consistent with other studies comparing bold and timid rats. Boldness, however, only seems to influence how much play a rat will exhibit, not how much play it is capable of exhibiting. Neonatal testosterone augmentation increases juvenile play fighting but not apomorphine susceptibility, suggesting that a high player need not be a bold animal. The total frequency of play an individual is capable of initiating appears to depend upon perinatal exposure to androgens. Boldness and the playfulness of the partner appear to modulate the expression of this hormonally set value.

The structure of skilled forelimb reaching in the rat: a proximally driven movement with a single distal rotatory component.

The movements of rats trained to reach through an aperture for food pellets, located on a shelf, were videorecorded and filmed from lateral and ventral perspectives for analysis using Eshkol-Wachman Movement Notation (EWMN). Reaching was subdivided into phases of locating the food and advancing the limb to grasp the food, bringing the food to the mouth, and returning to the starting position. Further analysis of the movements comprising these acts revealed a number of novel findings. (1) Most of the first phase of the movement is produced proximally, with the limb lifted, aimed, and advanced from the shoulder. (2) After the limb is lifted from the substrate to initiate reaching, it is carried to a parasagittal position so that the long axis of the forearm is aligned along the midline of the body. This aspect of the movement 'aims' the limb toward the target. (3) The digits are opened as the limb is advanced from the aiming position toward the food. As the paw approaches the food, pronation of the palm is accomplished by abduction of the upper arm. (4) As the limb is retracted, the digits are closed to grasp the food. As retraction ends, the paw is supinated by a rotatory movement at the wrist. This is the only distal rotatory movement. (5) The position taken by the second forelimb, as it is adducted to aid in holding the food pellet for eating, resembles the 'aiming' posture. The results are discussed in reference to the kinematics, neural control, and the evolutionary origins of reaching in the rat and other animals. Additionally, the results provide a framework for analysis of changes in movements produced by physiological manipulations.

Air righting without the cervical righting reflex in adult rats.

The current explanation of air righting in animals is that when falling supine in the air, labyrinthine stimulation triggers head rotation. The head rotation involves neck rotation which, via the cervical righting reflex, triggers rotation of the body. (In cats and monkeys, when the labyrinths are absent, visual stimulation when falling supine can also trigger this righting sequence.) In the present paper, a descriptive analysis of air righting in the rat shows that the shoulders rotate, carrying the unmoving head and neck passively along. Thus, for this species, labyrinthine input appears to trigger shoulder rotation directly, independently of the cervical righting reflex. This suggests that at least two physiological mechanisms exist for labyrinthine control of head rotation during air righting, one via the neck and the other via the shoulder girdle.

Labyrinthine and other supraspinal inhibitory controls over head-and-body ventroflexion.

The vestibular head righting reflex can be demonstrated by holding an adult rat vertically downward, so that the snout points downward. In this situation, the animal dorsiflexes its head and neck, bringing the head towards its normal orientation in space. Bilateral labyrinthectomy not only blocks this response, but releases an actively maintained ventroflexion of the head and neck. Bilateral electrolytic lesions of the lateral hypothalamus (LH) exaggerate such ventroflexion in labyrinthectomized rats. By themselves, LH lesions had no such effect. Therefore, it is argued that there are vestibular and supraspinal inhibitory mechanisms which, in the intact adult animal, keep this ventroflexion response in check. In addition, when the rats were held with their heads down, and with gentle paw contact with the ground, they did not ventroflex. However, they ventroflexed immediately upon releasing this paw contact. These observations suggest that there are tactile mechanisms which can also inhibit this exaggerated ventroflexion released by labyrinthectomy.

Haloperidol exaggerates proprioceptive-tactile support reflexes and diminishes vestibular dominance over them.

Rats made immobile and cataleptic by haloperidol, a dopamine receptor blocker, maintain their static stable equilibrium by employing a variety of allied postural support reflexes. Under some test conditions, competition between such reflexes occurs, and in haloperidol-treated rats, unlike undrugged controls, proprioceptive-tactile stimuli appear to be dominant over vestibular stimuli. We investigated this relationship in rats by testing their air-righting with and without simultaneous contact of the tail on a wooden platform. The rats were lightly held in a supine position by the shoulders and pelvis, with or without tail contact on a small wooden platform 47 cm above the ground. Undrugged rats showed the normal pattern of righting which involves axial rotation with cephalocaudal recruitment whether the tail is contacting the platform or not. Upon release, the haloperidol-treated rats (2.5 mg/kg) gripped the platform with their tail, which interfered with the air-righting reflex. This demonstrates that in haloperidol-treated rats, the dominance of tactile-proprioceptive postural support reflexes over those triggered vestibularly.

Labyrinthine and visual involvement in the dorsal immobility response of adult rats.

The dorsal immobility response (DIR) is typically seen in the infants of many altricial mammalian species. Lifting the animal into the air by the nape of the neck is the primary releasing stimulus. Functionally, this response appears to facilitate carrying of the infants by the adults. When grasped by the nape and lifted into the air, adult rats will also exhibit the DIR. In this paper, the role of the labyrinths in the DIR of adult male rats was examined. Vestibular stimulation produced by vertical circular acceleration increased the duration of the DIR, while labyrinthectomy greatly diminished the DIR. In rats with intact labyrinths, visual occlusion greatly potentiated the DIR, whereas, in labyrinthectomized rats, visual occlusion had little effect. These data indicate that the vestibular system plays a major role in mediating the DIR of adult rats. The retention of the DIR into adulthood and the possible increased role of the labyrinths in the control of the adult DIR, are discussed with respect to the possible role of the DIR as an anti-predator mechanism.