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.

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.

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.

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.

Seemingly paradoxical jumping in cataleptic haloperidol-treated rats is triggered by postural instability.

Paradoxically, animals exhibiting haloperidol-induced cataleptic immobility can be induced to leap vigorously, by pushing them forward from behind. It is shown here that such jumping can also be produced by placing them on a board and tilting it tail-end upward until about 50 degrees above horizontal. In both situations, jumps only occurred when the animal's hindlegs began to slip forward, as they lost their postural stability. As alternatives to jumping from the slope, rats turned to face upwards (negative geotaxis), or adopted a spread-eagled posture during head-first downward sliding, with the body and head flattened against the substrate. All 3 responses to the sloping board were present in some undrugged rats. Such rats, and those given low doses of haloperidol (0.5, 1.0 mg/kg), were more likely to turn upwards than to jump or slide. At high doses (7.5, 10.0 mg/kg), they were more likely to slide downward than to turn or jump. Jumping was most likely to occur at an intermediate dose (5 mg/kg), approximately 60 min after injection. We suggest that in the absence of haloperidol, and at low doses, locomotion is dominant over reflexes defending static equilibrium, and hence rats are more likely to turn upwards (which involves stepping). In contrast, at higher doses, locomotion is more fully suppressed, reducing the likelihood of turning. At very high doses of haloperidol and later in the action of the drug, muscle tonus appears to be weakened, reducing the likelihood of jumping. This possibility was supported by the finding that combined injection of the optimal dose of haloperidol and 2 mg/kg diazepam reduced the ability to cling vertically (suggesting weakness of muscle tone). In such rats, jumping from the sloping board was decreased, and active downward sliding was increased. Thus, different factors influence the occurrence of jumping at different doses of haloperidol. However, these are all active defensive responses to postural instability, and hence are similar to the other reflexes used by haloperidol-treated rats to defend against displacement from static stable equilibrium, such as standing immobile, bracing, clinging, and righting. Jumping in response to loss of stability on the sloping board also occasionally occurred in undrugged rats. Unlike jumps by haloperidol-treated rats, those by undrugged animals only occurred when they could be directed to a safe landing place. Thus, if the board faced the edge of the table, so that the jump would carry the animal into space over the edge, undrugged rats either did not jump or jumped off the side of the board onto the table.(ABSTRACT TRUNCATED AT 400 WORDS)

Visual modulation of vestibularly-triggered air-righting in rats involves the superior colliculus.

Vision plays two roles in air-righting, it can trigger air-righting in the absence of the labyrinths, and it can modulate the onset and speed of air-righting depending upon the height of the fall. While the visual cortex is known to be necessary for visual triggering, the neural systems necessary for visual modulation are unclear. In this study, the role of the visual cortex and the superior colliculus in visual modulation by rats was analysed. Rats can visually modulate vestibularly-triggered righting, but not trigger righting visually in the absence of the labyrinths. Adult rats with complete neonatal decortication, and adult rats with more specific ablation of the visual cortex were able to visually modulate air-righting. Ablation of the superior colliculi as well as the visual cortex, or ablation of the superior colliculi alone, resulted in loss of the ability to visually modulate air-righting. It is concluded that the superior colliculus is necessary for visual modulation in rats. It is hypothesized that in cats also, the superior colliculus, not the visual cortex, is necessary for visual modulation.

A behavioral study of the contributions of cells and fibers of passage in the red nucleus of the rat to postural righting, skilled movements, and learning.

Although the red nucleus consists of cells of origin for the rubro-spinal and rubro-olivary tracts, fibers of passage, including those of the superior cerebellar peduncle, which project from the cerebellum to the ventrolateral thalamus, pass through it. This study examined the relative effect of cell vs. fiber damage in the red nucleus on a number of behaviors thought to involve the red nucleus, including a skilled movement of reaching for food with a forelimb, postural righting on a surface and in the air, and learning a place response in a swimming pool test. Rats received unilateral or bilateral red nucleus lesions, using either the relatively cell-specific neurotoxins, ibotenic and quinolinic acid, or non-specific electrolytic anodal lesions. Both neurotoxic lesions effectively eliminated all red nucleus cell bodies, and in some animals they produced small cavities in the red nucleus and/or loss of cells in adjacent structures. Electrolytic lesions destroyed both cells and fibers, leaving a large cavity. The severity of the behavioral deficits were not related to the loss of red nucleus cells and there was a close relation between fiber damage and behavioral impairments on all of the tasks. The results suggest that for a number of behaviors, which have been thought to involve the red nucleus, impairments are more closely associated with fiber damage or damage to structures outside the red nucleus than they are to damage to cells of the red nucleus.

Visual modulation of air righting by rats involves calculation of time-to-impact, but does not require the detection of the looming stimulus of the approaching ground.

Rats do not visually trigger righting when falling supine in the air. They can, however, use vision to modulate the time of onset of air righting depending upon the height from the ground from which they are dropped. That is, the shorter the height, the quicker they begin to right. The visual cortex has been shown not to be necessary for such modulation; however, such modulation is absent if the superior colliculus is damaged. It is known that the superior colliculus has cells that respond to looming stimuli, and this could be the mechanism for modulation during air righting. In this study, 3 experiments were conducted to test this possibility. The evidence from all 3 suggests that something other than detecting a looming stimulus (i.e., the oncoming ground) is involved in the rats' determination of when to initiate righting. Expt. 1 showed that the ability to modulate the onset of air righting visually is not mature until adulthood (> 80 days). Yet young rats do respond to looming stimuli. Exp. 2 showed that the ability to modulate the onset of air righting requires both eyes. One eye should be sufficient to detect a looming stimulus. Expt. 3 showed that the rats require visual information prior to being dropped, not after, in order to modulate the onset of air righting. If the looming stimulus were the triggering stimulus, then this would be detected after, not before, being dropped. These findings suggest that the rats' ability to calculate the time-to-impact when falling involves a more complex calculation than simply detecting the presence of a looming stimulus.

Visual modulation of vestibularly-triggered air-righting in the rat.

Unlike cats, which can initiate righting in the air either with vestibular or visual input alone, the rat is dependent solely upon the labyrinths to trigger this response. We show, however, that the rat can modulate the onset and speed of its rotation according to the height above the ground from which it is dropped. In the absence of vision, rates initiate rotation with a latency of about 50 ms, irrespective of the height from which they are dropped. With vision, rats can modulate their latency to begin rotation, from about 102 ms at 50 cm, to about 39 ms at 7.5 cm. Similarly, as height of release decreases, the speed of rotation (i.e. degrees/ms) increases. Thus, in rats, even though vision cannot trigger air-righting, it does adaptively modulate this behavior as an allied reflex, increasing the likelihood that the animals will land on their feet.

Recovery from axial apraxia in the lateral hypothalamic labyrinthectomized rat reveals three elements of contact-righting: cephalocaudal dominance, axial rotation, and distal limb action.

In earlier work, we showed that in rats, proprioceptive-tactile information is sufficient for contact-righting on the ground (from lying on one side to prone). Thus, axial rotation, starting with the shoulders and followed by the pelvis, occurs normally in labyrinthectomized animals with eyes occluded. After damage to the lateral hypothalamus, even with labyrinths intact, contact-righting is at first abolished (1-2 days postoperatively), and when it reappears, involves pushing by the hindlegs. Rostrocaudal contact-righting, involving axial rotation, takes 3-4 days to recover. If labyrinthectomy is combined with lateral hypothalamic damage, the deficit is exaggerated and recovery is greatly slowed down, now requiring 2-3 weeks. The present paper shows that during this prolonged period of recovery several transitional forms of righting are present, each produced by a different combination of limb and body axis movements. At first, axial rotation is absent, and righting is achieved only by pushing with the limbs. This is followed by a transitional form in which, even though axial rotation cannot be triggered directly by contact with the ground, it can be triggered indirectly as an allied reflex when the paw places on the ground. Eventually the body axis actively initiates the rotation to proneness (at first, in the pelvis, later in recovery, in the shoulders), with the limbs being carried. Recovery of axial rotation overlaps with the recovery of cephalic dominance, yielding complex intermediate forms of righting.

The impairments in reaching and the movements of compensation in rats with motor cortex lesions: an endpoint, videorecording, and movement notation analysis.

Reaching for food by rats, with the limb contralateral to limb area motor cortex damage, was analyzed using end-point scores, videoanalysis, and Eshkol-Wachmann Movement Notation (EWMN). End point results from groups of rats with small, medium, and large lesions showed reaching success and amount of food grasped per reach decreased with increases in lesion size. Videoanalysis and EWMN showed that the impairments were attributable to: (1) an inability to pronate the paw over the food by abduction of the upper arm, and (2) an inability to supinate the paw at the wrist to orient the food to the mouth. There were no obvious impairments in locating food using olfaction, in positioning the body in order to initiate a reach, or in clasping the digits to grasp food. There were only mild impairments in lifting, aiming, and advancing the limb. In rats with medium and large lesions, loss of pronation and supination were compensated for by a variety of whole body movements. These findings are discussed in reference to neural and behavioral mechanisms underlying recovery of function and the contribution of the motor cortex to skilled movements in the rat and other species.

'Axial apraxia' in labyrinthectomized lateral hypothalamic-damaged rats.

Contact righting, that is, turning from a recumbent position to prone, is abolished for a few days after large electrolytic lesions of the lateral hypothalamus. With recovery, contact righting reappears, but does so in a distinct manner. At first the body is righted by backleg movements, in the absence of any active axial rotation. Later, righting switches from back to front, so that righting begins in the shoulders and then proceeds to the pelvis. Such righting is achieved by axial rotation, that is, the limbs are carried by the torso, rather than vice versa. Labyrinthectomy, when combined with lateral hypothalamic (LH) damage, slows this recovery (now taking as long as 3 weeks), and reveals many intermediate stages of contact-righting. The absence of axial rotation in the early stages of recovery from combined LH damage and labyrinthectomy is compared to the 'axial apraxia' seen in some parkinsonian patients.

Development of righting when falling from a bipedal standing posture: evidence for the dissociation of dynamic and static righting reflexes in rats.

Righting to prone when placed supine on the ground by rats is present at birth, albeit in incomplete form. In contrast, righting in the air when falling from the supine position does not begin to emerge until the end of the first week and is not complete until the end of the third week postnatally. On the ground, the animals have sensory information from proprioceptive-tactile sources, as well as vestibular; in the air, they have only vestibular. Thus, it is possible that the difference between contact righting and air righting is a reflection of the relative difference in the maturation of tactile vs. vestibular mechanisms. In this study, pups were tested by pushing them backwards from a bipedal standing position. Such a context provided proprioceptive-tactile information during the fall. The results showed that the developmental onset and maturation of righting from the bipedal position resembled that of air righting rather than contact righting. This suggests that the difference between air righting and contact righting is not due to differences in sensory inputs, but to differential maturation of neural mechanisms for acceleratory (i.e., falling) vs. stationary (i.e., lying on the ground) forms of righting. That is, the appropriate neural systems are organized for the type of righting, not for the sensory systems used. Even so, some evidence is provided suggesting a developmental dissociation between righting from falling with vestibular information only, and with proprioceptive-tactile information in addition. Therefore, righting systems appear to need two dimensions of classification--one based on sensory systems involved, and the other in terms of the context of righting (i.e., falling vs. stationary).

Pharmacological subtraction of the sensory controls over grasping in rats.

Catecholamine-depletion-induced catalepsy isolates and leaves intact an aggregate of allied reflexes (e.g., righting, standing still, bracing, and clinging) which involve all the body and limb segments in defending stable static equilibrium. Because other movement subsystems (locomotion, orienting, scanning, directed use of mouth or forepaws) are depressed, such animals cling in a vertical position for an abnormally long period of time. As a consequence, grasping reflexes may be studied independently of other responses. Haloperidol, a dopamine antagonist, abolishes visually elicited reaching and grasping, but leaves intact tactile and proprioceptive control of grasping. The grasping of haloperidol-treated rats can be further simplified by the pharmacological removal of the remaining sensory controls. The addition of morphine to haloperidol abolishes tactile grasping, while the addition of diazepam to haloperidol abolishes both tactile and proprioceptive (traction-elicited) grasping. Although visual, tactile, and proprioceptive grasping are abolished by haloperidol-plus-diazepam, some vestibular input to clinging remains: such rats, in response to being held vertically upright in the air, flex their digits with sufficient strength to allow them to cling vertically. The strength of forepaw digit flexion is severely diminished by labyrinthectomy, but the digits of the hindpaws appear to be unaffected. This residual non-labyrinthine digit gripping appears to be induced by proprioceptive inputs from the head, neck and torso in response to the vertical body position. Wrapping an elastic bandage snugly around the head and neck of a labyrinthectomized rat given haloperidol-plus-diazepam further diminishes the strength of forepaw digit flexion, and to a lesser degree hindpaw digit flexion.(ABSTRACT TRUNCATED AT 250 WORDS)

Uses of vision by rats in play fighting and other close-quarter social interactions.

Enucleated juvenile rats were compared to sighted juveniles, and tested over six trials. In some of these trials, the vibrissae were clipped and the test chamber was flooded with white noise. Even though the enucleated rats played, they did so in an atypical manner. They tended to initiate more playful and other social contacts, and were more likely to defend themselves if contacted. When they did defend themselves, they adopted behavior patterns that were more likely to evade the partner's attack. In addition, the enucleated rats were hypersensitive to the partner, being more likely to respond defensively when contacted further from the nape (the main play target). All these changes in play fighting by nonsighted rats suggest that the loss of vision leads to motivational changes in activity and reactivity, and so has an indirect effect on play behavior. In addition, direct evidence is also provided to show that vision is used to orient attacks to the nape. When the vibrissae were closely clipped, the sighted rats continued to make direct attacks on the partner's napes, whereas the nonsighted rats did not. Rather, they first contacted some other part of the partner's body and then oriented to the nape. Another test paradigm was used to determine whether vision is used to trigger defensive responses. The rats were partially food deprived as adults and were filmed in a food wrenching and dodging situation where one rat was given a food pellet and the other allowed to steal it. Measurement of the distance at initiation of the lateral swerve away from the approaching partner (i.e., dodge) showed that when the vibrissae are clipped, the sighted rats continued to initiate dodges at the same distance, whereas the nonsighted rats could not. Therefore, vision appears to have an active role in organizing movement sequences of attack and defense in play fighting and other close-quarter interactions.