Effects of neonatal handling on playfulness by means of reversal of the desire to play in rats (Rattus norvegicus).

Abstract

In the present study the authors sought to establish whether the range of effects of neonatal handling stimulation (H), that is, brief daily periods of infant isolation, could be extended to the domain of social motivation. With this aim, the authors studied the innate motivation to engage in rough-and-tumble play (R&T) in adolescent rats (Rattus norvegicus) by means of a reversal design, in which half of the rats were first housed in isolation (Days 1-3), and then in company (Days 4-6), while the other half followed the reverse sequence of housing conditions. Results showed in a clear-cut manner that H fuelled playfulness, as measured by pin and dorsal contact episodes, with (relative) independence of trait-based differences in fearful behavior between handled and nonhandled rats. Given that the different levels of the rat's social brain are apparently sensitive to tactile stimulation in infancy, the authors propose that the vibrant R&T reported here could reflect an enduring alteration of genetically based, motivational systems underlying playfulness and, perhaps, positive social emotions like joy.

Infantile experience and play motivation

“…As shown in Aguilar et al (2009), early handling had modest effects on dorsal contacts, with H rats outperforming their NH counterparts only the first day of testing in Parts 2 and 5, an effect that dissipated thereafter as a result of gradual diminution of this behavior in H rats. This pattern of results in conjunction with the increments in pin frequency observed with time of isolation appears to indicate that H rats tended to make dorsal contacts more frequently than NH controls when not engaged vigorously in reciprocal pinning.…”

“…The treatment of early handling was the same as in Aguilar et al (2002Aguilar et al ( , 2009, performed twice daily (morning and evening) from postnatal Day 1 to Day 18. Briefly, it consisted of placing the pups individually in plastic cages (42 × 26 × 18 cm) for a total period of 10 min, each pup being gently handled by the experimenter from the head to the tail with his forefinger for 5 s (one stroke per second).…”

“…Pins are currently considered "a hallmark of high-quality R&T" (Knutson, Panksepp, & Pruitt, 1996, p. 305) and, together with dorsal contacts, a robust index of play motivation (Burghardt, 2005;Panksepp, 1998;Panksepp et al, 1984;Pellis & Pellis, 1998;Thor & Holloway, 1984b), although additional evasion maneuvers coexist (Pellis & McKenna, 1992Pellis & Pellis, 1987. Recent experiments indicate that early handling-brief periods of infant-mother separation known for making rats less prone to stress by epigenetic brain changes (Anisman, Zaharia, Meaney, & Merali, 1998;Daly, 1973;Levine, 1957Levine, , 2005Levine, Haltmeyer, Karas, & Denenberg, 1967;Macrì & Würbel, 2006;Zhang & Meaney, 2010)-appears to increase the amount of R&T in different strains of rats (Aguilar, Caramés, & Espinet, 2009;Siviy & Harrison, 2008), although it is still unclear which motivational mechanism accounts for such an effect. One possible interpretation is that an aversive emotional state related to higher hypothalamic-pituitary-adrenal (HPA) responses to stress partially suppresses R&T in nonhandled (NH) rats, handled (H) rats being less affected and thus indirectly more playful.…”

“…Testing took place in the light phase of the light-dark cycle, between 10:30 and 20:30, in a counterbalanced manner regarding the treatment (H/NH), the housing conditions (social/individual), and the sex (male/female) of the couples, during a 5-min period following the same procedural routines used in Aguilar et al (2009). Inter-rater reliability correlations for pins, dorsal contacts, and time spent together were r = .97, .87 and .94 respectively (all p values < .001).…”

Mild environmental intervention in mother-infant interactions reduces social play behavior in rats.

“…However, in both cases, the pups were subjected to high-licking mothers because handling induces a burst in licking behavior (de Azevedo et al, 2010). A previous study (Aguilar, Caramés, & Espinet, 2009) showed that neonatal handling may increase the frequency of pinning behavior, provided that the animals were previously socially isolated. In that specific situation of social deprivation, handled rats showed increased social play behavior instead of the decrease described herein.…”