Early life stress in fathers improves behavioural flexibility in their offspring

Abstract

Traumatic experiences in childhood can alter behavioural responses and increase the risk for psychopathologies across life, not only in the exposed individuals but also in their progeny. In some conditions, such experiences can however be beneficial and facilitate the appraisal of adverse environments later in life. Here we expose newborn mice to unpredictable maternal separation combined with unpredictable maternal stress (MSUS) for 2 weeks and assess the impact on behaviour in the offspring when adult. We show that MSUS in male mice favours goal-directed behaviours and behavioural flexibility in the adult offspring. This effect is accompanied by epigenetic changes involving histone post-translational modifications at the mineralocorticoid receptor (MR) gene and decreased MR expression in the hippocampus. Mimicking these changes pharmacologically in vivo reproduces the behavioural phenotype. These findings highlight the beneficial impact that early adverse experiences can have in adulthood, and the implication of epigenetic modes of gene regulation.

Potential of Environmental Enrichment to Prevent Transgenerational Effects of Paternal Trauma

“…The present results are in line with this hypothesis because they show that the offspring of males exposed to early trauma can cope better with a challenging situation, similarly to that experienced by their father. Further, they extend previous observations that MSUS animals have improved behavioral flexibility in aversive conditions (Gapp et al, 2014b), suggesting that exposure to early trauma can lead to various forms of resilience.…”

“…Similarly in rodents, successful adaptation after exposure to chronic stress in early life has been observed, and has been associated with changes in the HPA axis (Franklin et al, 2011;Gapp et al, 2014b;Uchida et al, 2011). Thus, the response of individuals exposed to negative experiences in early life can be pathological or adaptive depending on the context, a concept theorized by the match/mismatch hypothesis (Daskalakis et al, 2012).…”

“…For instance, social avoidance is viewed as an active coping behavior that can be manifested by an adult individual after being exposed to traumatic stress in early postnatal life (Franklin et al, 2011) or chronic social defeat in adulthood (Kovalenko et al, 2014). In the case of early traumatic stress, social avoidance has been shown to be accompanied by altered behavioral flexibility, and both are transmitted to the progeny (Franklin et al, 2011;Gapp et al, 2014b). Further, some maladaptive behaviors resulting from early trauma can be modulated by the environment; in particular, they can be reversed by conditions such as environmental enrichment (EE) (Leshem and Schulkin, 2012;Schloesser et al, 2010).…”

Chronic stress impacts the cardiovascular system: animal models and clinical outcomes

“…Ongoing research into animal models of stress and into the clinical outcomes from chronically stressed individuals will improve our understanding of this pervasive disease condition and present us with opportunities to identify biomarkers that will not only improve diagnostic accuracy but will also allow for the improved monitoring of responses to therapeutic management strategies. On the other hand, recent data suggesting a beneficial heritable aspect of stress make this puzzle even more complicated (101).…”

Stressed-out dads can (metabolically) stress their kids

“…Moreover, it has also been established that paternal experiences could affect behavior in the resulting offspring (Gapp et al, 2014a(Gapp et al, , 2014bDias and Ressler, 2014). These results are likely to be relevant for human disease, since intergenerational effects of paternal information on the growth of their future offspring have been observed in two general populations (Pembrey et al, 2006).…”