Neonatal interventions differently affect maternal care quality and have sexually dimorphic developmental effects on corticosterone secretion

Abstract

Neonatal handling (H) and maternal separation (MS) both induce changes in maternal care, but the contribution of these changes to the behavioral and neurochemical outcomes of the offspring remains unclear, as studies often find opposite results concerning the frequency of maternal behaviors, particularly in the MS paradigm. In this study, behavior displayed by H, MS and non-handled (NH) Wistar rat dams were observed during the first 10days after birth. A tentative assessment of the quality of maternal care was made, using a previously reported score that reflects behavior fragmentation and inconsistency. Central oxytocin levels and hippocampal synaptic plasticity markers were also evaluated in dams, immediately after litter weaning. In adulthood, male and female offspring were subjected to a contextual stress-induced corticosterone challenge to provide further information on the impact of early interventions on neuroendocrine parameters. We found that while both H and MS interventions induced an increase in the amount of pup-directed behavior, MS dams displayed a more fragmented and inconsistent pattern of care, reflecting poorer maternal care quality. Interestingly, an increase in oxytocin levels was observed only in H dams. While H offspring did not differ from NH, MS males and females showed marked differences in corticosterone secretion compared to controls. Our results suggest that briefly removing the pups from the nest alters maternal care quantity but not quality and increases central oxytocin, while long separations appear to increase low quality maternal care and change neuroendocrine responses in adult offspring in a sex-specific manner.

Neonatal pain and stress disrupts later‐life pavlovian fear conditioning and sensory function in rats: Evidence for a two‐hit model

“…Interestingly, we also did not observe any sex effect on corticosterone levels. In other studies observing neonatal stress manipulations (3 hr maternal separation), marked sex differences have been reported in adulthood corticosterone levels in both basal and acutely stressed rats, with females showing greater corticosterone concentration than males (Couto-Pereira et al, 2016).…”

“…Interestingly, we also did not observe any sex effect on corticosterone levels. In other studies observing neonatal stress manipulations (3 hr maternal separation), marked sex differences have been reported in adulthood corticosterone levels in both basal and acutely stressed rats, with females showing greater corticosterone concentration than males (Couto‐Pereira et al, ). The most obvious explanation as to why we did not observe sex differences is the fact we measured corticosterone levels in prepubescent rats and thus the sex difference had not yet developed.…”

Chronic psychosocial stress during pregnancy affects maternal behavior and neuroendocrine function and modulates hypothalamic CRH and nuclear steroid receptor expression

“…These results are consistent with human data where some of the core features of women suffering from PPD include interrupted patterns of maternal care 60 , lack of child attachment, and depressive mood 61 . Inconsistent maternal care patterns have been hypothesized to result from conflict that arises at the inability of dams to respond to pups' specific needs during active maternal interactions 62 , a process which is thought to depend on the mesolimbic dopaminergic system 63 . CGS dams also exhibit deficits in pup retrieval, a unique element of maternal behavior that relies on goal-directed maternal responses thought to be controlled by neural connections between the medial preoptic area and the mesolimbic dopaminergic system 64 .…”

Experiencing early life maternal separation increases pain sensitivity in adult offspring

“…In this study, we evaluated maternal behavior in order to rule out its influence on alterations in nociceptive responses. Some studies have demonstrated that maternal separation for 3 h per day from PND 1–10 showed an overall increase in the total frequency of licking performed at regular intervals to twice in the dark phase and 3 times in the light phase (Couto‐Pereira et al, 2016). In another study, maternal separation for 4 h per day from PND 1–21 led to a marked increase in licking and arched‐back nursing evaluated on PND 1–12 with 5 observations per day (Pryce et al, 2001).…”