Neonatal handling alters the structure of maternal behavior and affects mother–pup bonding

Reis, Adolfo Rodrigues; Azevedo, Márcia Scherem de; Souza, Marcelo Alves de; Lutz, Maiara Lenise; Alves, Márcio Bonesso; Izquierdo, Iván; Cammarota, Martı́n; Silveira, Patrícia Pelufo; Lucion, Aldo Bolten

doi:10.1016/j.bbr.2014.02.036

Cited by 29 publications

(33 citation statements)

References 99 publications

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“…In accordance, behavioral stability has been observed across consecutive litters of the same dam (Champagne et al, 2003). However, as demonstrated here and in other studies (Bodensteiner et al, 2012; Macrí et al, 2004; Pryce et al, 2001; Reis et al, 2014), dams adapt their behavior to meet pups’ demands (Pereira and Ferreira, 2016) and to the environmental conditions. Some adaptations seem to persist to subsequent maternal experiences, even if the source of stress is removed (Wong et al, 2011), implying that a learning component also exists in maternal care (Scanlan et al, 2006).…”

Section: Resultssupporting

confidence: 65%

“…As expected (Champagne et al, 2003;Leon et al, 1978;Reis et al, 2014), maternal care gradually decreased through the days (main effect of day, p < 0.05 for all behaviors analyzed), but no significant interactions between intervention and postpartum day were found (p > 0.05 for all behaviors analyzed; data not shown).…”

Section: Maternal Caresupporting

confidence: 54%

“…In rodents, removing pups from the nest, either for brief (handling) or long periods (maternal separation), increases the frequency of pup-directed behaviors by dams (Bodensteiner et al, 2012;Macrí et al, 2004;Pryce et al, 2001), although some studies present opposite results (Aguggia et al, 2013;Boccia et al, 2007;Reis et al, 2014). It has been proposed that the long-term consequences neonatal interventions have on the offspring, particularly concerning the adaptive programming of the HPA axis by early handling in rodents, result from the changes that this intervention induces on the dams behavior (Cirulli et al, 2003;Denenberg, 1999;Kuhn and Schanberg, 1998;Liu et al, 1997;Meaney et al, 1985).…”

Section: Introductionmentioning

confidence: 99%

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

Couto-Pereira

Ferreira

Lampert

et al. 2016

Intl J of Devlp Neuroscience

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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.

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Section: Resultssupporting

confidence: 65%

Section: Maternal Caresupporting

confidence: 54%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Couto-Pereira

Ferreira

Lampert

et al. 2016

Intl J of Devlp Neuroscience

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“…Models assessing the effects of Day (twelve recording days: PND1-PND12), Time of Day (the 6 time points of observation per day, see above Section 2.3) and Experimental manipulation (daily brief separation vs. no separation from the litter) on maternal behavior have been estimated through generalized estimated equations (GEE) (procedure GENMOD in SAS) according to Reis et al (2014). For all response variables of interest, as initial model we used the model with the 3way interaction between Day, Time of day and Experimental manipulation.…”

Section: Discussionmentioning

confidence: 99%

Rat dams exposed repeatedly to a daily brief separation from the pups exhibit increased maternal behavior, decreased anxiety and altered levels of receptors for estrogens (ERα, ERβ), oxytocin and serotonin (5-HT1A) in their brain

Stamatakis¹,

Kalpachidou²,

Raftogianni³

et al. 2015

Psychoneuroendocrinology

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“…Numerous studies have found differences in maternal behaviors given to handled and unhandled pups, but it is relevant to note that these studies involve observations immediately after reunion with the litter (Denenberg, 1964;Levine, 1975;Lee and Williams, 1974;Liu et al, 1997). The effects of pup handling on maternal care are transient each day (Champagne et al, 2003a;Claessens, Daskalakis, Oitzl, and de Kloet, 2012;Sherrod, Connor, and Meier, 1974) and dissipate as quickly as three hours post-handling (Reis et al, 2014). In our experiments, we intentionally avoided observing the dams and litters within the first three hours after handling to obtain a better impression of how their undisturbed relationship affects development of the offspring, so it is not surprising that we found no differences in total licking bouts between handled and nonhandled litters.…”

Section: Accepted Manuscriptmentioning

confidence: 96%

Associations among within-litter differences in early mothering received and later emotional behaviors, mothering, and cortical tryptophan hydroxylase-2 expression in female laboratory rats

Ragan

Harding

Lonstein

2016

Hormones and Behavior

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This article is part of a Special Issue "Parental Care". The effects of differential maternal care received on offspring phenotype in rodents has been extensively studied between litters, but the consequences of differential mothering within litters on offspring neurobehavioral development have been rarely examined. We here investigated how variability in maternal care received among female rat siblings (measured four times daily on postnatal days 4, 6, 8, and 10) relates to the siblings' later emotional and maternal behaviors. As previously reported, we found that some female pups received up to three times more maternal licking bouts compared to their sisters; this difference was positively correlated with the pups' body weights. The number of maternal licking bouts that females received was negatively correlated with their later neophobic behaviors in an open field during periadolescence, but positively correlated with their anxiety-related behavior in an elevated plus maze during adulthood. Licking received was also positively correlated with females' later likelihood to retrieve pups in a maternal sensitization paradigm. In addition, females' neophobia during adolescence and anxiety-related behavior during adulthood predicted some aspects of both postpartum and sensitized maternal responsiveness. Medial prefrontal cortex expression of tryptophan hydroxylase-2 (TPH2; enzyme necessary for serotonin synthesis) was negatively associated with early maternal licking received. Interestingly, cortical TPH2 was positively associated with the maternal responsiveness of sensitized virgins but negatively associated with it in postpartum females. These results indicate that within-litter differences in maternal care received is an often neglected, but important, contributor to individual differences in offspring socioemotional behaviors as well as to the cortical serotonin neurochemistry that may influence these behaviors.

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Neonatal handling alters the structure of maternal behavior and affects mother–pup bonding

Cited by 29 publications

References 99 publications

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

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

Rat dams exposed repeatedly to a daily brief separation from the pups exhibit increased maternal behavior, decreased anxiety and altered levels of receptors for estrogens (ERα, ERβ), oxytocin and serotonin (5-HT1A) in their brain

Associations among within-litter differences in early mothering received and later emotional behaviors, mothering, and cortical tryptophan hydroxylase-2 expression in female laboratory rats

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