Play matters: the surprising relationship between juvenile playfulness and anxiety in later life

Besides being recognized as a potential welfare indicator, play behaviour has long been considered to have immediate and/or long-term benefits. In particular, it has been suggested that in play animals learn to cope physically and emotionally with unexpected events. Given that the propensity to play varies greatly between conspecific individuals, such interindividual variability in playfulness may be associated with differences in the animals' future behaviour, a prediction that has rarely been tested. To investigate whether different levels of playfulness in juvenility indeed coincide with behavioural differences in later life, 30 female C57BL/6J mice were subjected to the following series of behavioural observations and tests: (1) quantification of juvenile play behaviour; (2) behavioural testing in paradigms that assess anxiety-like behaviour and exploratory locomotion in an unfamiliar environment; and (3) observation of spontaneous behaviour in the familiar home cage environment. Surprisingly, a high level of juvenile playfulness was predictive of high levels of state anxiety and low levels of exploratory locomotion in later life. While this relationship existed already in adolescence, it became even more prominent in adulthood. By contrast, no substantial differences between playful and less playful mice were found with respect to home cage behaviour. While these findings may reflect better coping abilities in novel and dangerous environments in those mice that played the most during juvenility, they may also argue for the existence of different types of mice. Thus, despite genetic homogeneity and identical housing environments, preferences for either local or global use of space were observed that indicate the emergence of individuality. Concerning animal welfare, our findings suggest that play may constitute a plausible welfare indicator at the population level, but is probably less meaningful for the individual.