The Role of the Cortex in Play Fighting by Rats: Developmental and Evolutionary Implications

Abstract

Play is a distinctive behavior of young mammals, especially mammals with a well-developed forebrain. For this reason it is thought that there may be a relation between forebrain evolution and highly elaborated play behavior. This study investigated the contribution of the cortex to play behavior by comparing play in control and neonatally decorticated rats (Rattus norvegicus). Play fighting in rats involves the combination of attack by one rat and defense by the recipient, with pinning arising when specific patterns of defense are used. Whether paired with another decorticate or with an intact pairmate, decorticates attacked pairmates as frequently as did intacts, and they were just as likely to defend against playful attacks as were intacts. Where decorticates differed from intacts was on a measure of pinning, in which one rat stands over a supine partner, decorticate rats displayed a reduction of 50% relative to control rats during the juvenile stage in which play is most pronounced (days 25 to 40). Juvenile decorticate rats adopted types of defensive responses which were less likely to result in the pinning configuration. Thus, a reduced pinning frequency reflects an altered pattern of defense, not a reduced level of play fighting. Rather, the decorticate patterns of defense were typical of those defensive responses displayed by adult rats. That is, decorticate juveniles exhibit a precociously mature pattern of playful defense. As intact controls mature, they come to resemble the decorticates in their defensive responses, and hence the difference in pinning frequency between decorticate and intact pairs diminishes. This suggests that the cortex may inhibit the escalation of defense in juveniles and thus promote prolonged ventral-ventral contact during play fighting. The results further suggest that the cortex is involved in the development of adult behavioral skills by facilitating juvenile play.

Deficient Social and Play Behavior in Juvenile and Adult Rats after Neonatal Cortical Lesion: Effects of Chronic Pubertal Cannabinoid Treatment

“…Play behavior: Beside the frequency of play behaviors (pins, attacks, and defensive behavior) (Pellis et al, 1992;Pellis and McKenna, 1995;, the percentage of defensive behavior depending upon the number of attacks received was also evaluated (see Defense). We further analyzed the percentage of pins for an animal, initiated by its own complete rotation and also the probability to respond upon an attack.…”

“…Surprisingly, it was found that neonatally decorticated rodents still engage in play fights as juveniles (Panksepp et al, 1994;Pellis et al, 1992). These findings indicate that an intact cortex is not necessary for rats to engage in social play and, therefore, cannot be involved in the motivation of social play behavior (Pellis et al, 1992). However, decorticated rats showed a significant reduction in pinning, a common position in play fights in which one rat stands over a supine partner.…”

“…Since play fighting is most obvious in mammals, it was suggested that social play is positively correlated with encephalization (Fagen, 1981) and depends upon distinct specializations of the mammalian brain such as a highly evolved neocortex (Panksepp et al, 1994). Surprisingly, it was found that neonatally decorticated rodents still engage in play fights as juveniles (Panksepp et al, 1994;Pellis et al, 1992). These findings indicate that an intact cortex is not necessary for rats to engage in social play and, therefore, cannot be involved in the motivation of social play behavior (Pellis et al, 1992).…”

“…However, decorticated rats showed a significant reduction in pinning, a common position in play fights in which one rat stands over a supine partner. By itself, pinning is an insufficient measure for investigating the mechanisms of an altered frequency of social play, since most pins arise from combined action of two play partners, where one attacks and the other adopts a particular defensive position (Pellis et al, 1992). A thorough study by Pellis et al (1992) showed that the reduced pinning frequency in decorticated rats reflects an altered pattern of defense, rather than a reduction in play fighting.…”

Optogenetic Examination of Prefrontal-Amygdala Synaptic Development

“…The transition from infancy to adulthood marks the ontogenesis of fundamental behavioral processes, such as threat learning (Rudy, 1993;Richardson et al, 2000;Akers et al, 2012;Deal et al, 2016), social interaction (Panksepp, 1981;Vanderschuren et al, 1997), and aggression (Pellis et al, 1992;Pellis and Pasztor, 1999). On the other hand, this period is also characterized by a peak incidence of the majority of psychiatric disorders (Kessler et al, 2005).…”